Microtubules in Non-conventional Yeasts

  • Hiromi MaekawaEmail author
  • Douglas R. DrummondEmail author


Microtubules polymerise from tubulin proteins and play a significant role in the growth and proliferation of eukaryotic cells. In yeasts, most studies on microtubules and tubulins have utilised the budding yeast Saccharomyces cerevisiae and fission yeast Schizosaccharomyces pombe model systems. However, more recently interest in the microtubules of other non-conventional yeast and fungal species has increased, both for investigation of biological processes such as fungal evolution and for applications such as developing antifungal drugs. We review the microtubule cytoskeleton and its role in yeast and fungal cellular processes in vivo and the tubulin proteins found in yeast cells and their study in vitro, together with the recent advances in cryoEM leading to detailed molecular structures of yeast microtubules. We examine what is known about the microtubule cytoskeleton in non-conventional yeasts and highlight the significant differences, as well as many conserved aspects, in their microtubule biology compared to the two model yeasts. Finally, we discuss the potential role of microtubules as drug targets for treatment of yeast and fungal infections.


microtubule tubulin cytoskeleton yeast SPB MTOC 



We thank Dr. A. Neuner and Dr. M. Yamaguchi for providing electron micrographs.


  1. Adachi Y, Toda T, Niwa O, Yanagida M (1986) Differential expressions of essential and nonessential alpha-tubulin genes in Schizosaccharomyces pombe. Mol Cell Biol 6:2168–2178PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adames NR, Cooper JA (2000) Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J Cell Biol 149:863–874PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adams IR, Kilmartin JV (1999) Localization of core spindle pole body (SPB) components during SPB duplication in Saccharomyces cerevisiae. J Cell Biol 145:809–823PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aire TA (2005) Short-term effects of carbendazim on the gross and microscopic features of the testes of Japanese quails (Coturnix coturnix japonica). Anat Embryol 210:43–49PubMedCrossRefGoogle Scholar
  5. Akhmanova A, Steinmetz MO (2015) Control of microtubule organization and dynamics: two ends in the limelight. Nat Rev Mol Cell Biol 16:711–726PubMedCrossRefGoogle Scholar
  6. Al-Bassam J, Kim H, Flor-Parra I, Lal N, Velji H, Chang F (2012) Fission yeast Alp14 is a dose-dependent plus end-tracking microtubule polymerase. Mol Biol Cell 23:2878–2890PubMedPubMedCentralCrossRefGoogle Scholar
  7. Alberti-Segui C, Dietrich F, Altmann-Jöhl R, Hoepfner D, Philippsen P (2001) Cytoplasmic dynein is required to oppose the force that moves nuclei towards the hyphal tip in the filamentous ascomycete Ashbya gossypii. J Cell Sci 114:975–986PubMedGoogle Scholar
  8. Al-Ebaisat HS (2011) Synthesis and biological activities of some benzimidazoles derivatives. J Appl Sci Environ Manag 15:451–454Google Scholar
  9. Alfa CE, Hyams JS (1991) Microtubules in the fission yeast Schizosaccharomyces pombe contain only the tyrosinated form of alpha-tubulin. Cell Motil Cytoskeleton 18:86–93PubMedCrossRefGoogle Scholar
  10. Alonso MC, Drummond DR, Kain S, Hoeng J, Amos L, Cross RA (2007) An ATP gate controls tubulin binding by the tethered head of kinesin-1. Science 316:120–123PubMedPubMedCentralCrossRefGoogle Scholar
  11. Alonso A, Greenlee M, Matts J, Kline J, Davis KJ, Miller RK (2015) Emerging roles of sumoylation in the regulation of actin, microtubules, intermediate filaments, and septins. Cytoskeleton (Hoboken) 72:305–339CrossRefGoogle Scholar
  12. Alushin GM, Lander GC, Kellogg EH, Zhang R, Baker D, Nogales E (2014) High-resolution microtubule structures reveal the structural transitions in αβ-tubulin upon GTP hydrolysis. Cell 157:1117–1129PubMedPubMedCentralCrossRefGoogle Scholar
  13. Anders A, Lourenço PCC, Sawin KE (2006) Noncore components of the fission yeast gamma-tubulin complex. Mol Biol Cell 17:5075–5093PubMedPubMedCentralCrossRefGoogle Scholar
  14. Arellano-Santoyo H, Geyer EA, Stokasimov E, Chen GY, Su X, Hancock W, Rice LM, Pellman D (2017) A tubulin binding switch underlies Kip3/Kinesin-8 Depolymerase activity. Dev Cell 42:37–51.e8PubMedPubMedCentralCrossRefGoogle Scholar
  15. Atherton J, Jiang K, Stangier MM, Luo Y, Hua S, Houben K, van Hooff JJE, Joseph AP, Scarabelli G, Grant BJ, Roberts AJ, Topf M, Steinmetz MO, Baldus M, Moores CA, Akhmanova A (2017) A structural model for microtubule minus-end recognition and protection by CAMSAP proteins. Nat Struct Mol Biol 24:931–943PubMedPubMedCentralCrossRefGoogle Scholar
  16. Atherton J, Stouffer M, Francis F, Moores CA (2018) Microtubule architecture in vitro and in cells revealed by cryo-electron tomography. Acta Crystallogr D Struct Biol 74:572–584PubMedPubMedCentralCrossRefGoogle Scholar
  17. Ayhan-Kilcigil G, Tuncbilek M, Altanlar N, Goker H (1999) Synthesis and antimicrobial activity of some new benzimidazole carboxylates and carboxamides. Farmaco 54:562–565PubMedCrossRefGoogle Scholar
  18. Badin-Larçon AC, Boscheron C, Soleilhac JM, Piel M, Mann C, Denarier E, Fourest-Lieuvin A, Lafanechère L, Bornens M, Job D (2004) Suppression of nuclear oscillations in Saccharomyces cerevisiae expressing Glu tubulin. Proc Natl Acad Sci U S A 101:5577–5582PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bahtz R, Seidler J, Arnold M, Haselmann-Weiss U, Antony C, Lehmann WD, Hoffmann I (2012) GCP6 is a substrate of Plk4 and required for centriole duplication. J Cell Sci 125:486–496PubMedCrossRefGoogle Scholar
  20. Bansal Y, Silakari O (2012) The therapeutic journey of benzimidazoles: a review. Bioorg Med Chem 20:6208–6236PubMedCrossRefGoogle Scholar
  21. Banuett F (1995) Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet 29:179–208PubMedCrossRefGoogle Scholar
  22. Banuett F, Quintanilla RH, Reynaga-Peña CG (2008) The machinery for cell polarity, cell morphogenesis, and the cytoskeleton in the Basidiomycete fungus Ustilago maydis-a survey of the genome sequence. Fungal Genet Biol 45(Suppl 1):S3–S14PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bao XX, Spanos C, Kojidani T, Lynch EM, Rappsilber J, Hiraoka Y, Haraguchi T, Sawin KE (2018) Exportin Crm1 is repurposed as a docking protein to generate microtubule organizing centers at the nuclear pore. elife 7:1195CrossRefGoogle Scholar
  24. Barnes G, Louie KA, Botstein D (1992) Yeast proteins associated with microtubules in vitro and in vivo. Mol Biol Cell 3:29–47PubMedPubMedCentralCrossRefGoogle Scholar
  25. Barrett JG, Manning BD, Snyder M (2000) The Kar3p kinesin-related protein forms a novel heterodimeric structure with its associated protein Cik1p. Mol Biol Cell 11:2373–2385PubMedPubMedCentralCrossRefGoogle Scholar
  26. Barton RC, Gull K (1992) Isolation, characterization, and genetic analysis of monosomic, aneuploid mutants of Candida albicans. Mol Microbiol 6:171–177PubMedCrossRefGoogle Scholar
  27. Bassetti M, Righi E, Montravers P, Cornely OA (2018) What has changed in the treatment of invasive candidiasis? A look at the past 10 years and ahead. J Antimicrob Chemother 73:i14–i25PubMedPubMedCentralCrossRefGoogle Scholar
  28. Bates D, Eastman A (2016) Microtubule destabilizing agents: far more than just anti-mitotic anti-cancer drugs. Br J Clin Pharmacol 83:255–268PubMedPubMedCentralCrossRefGoogle Scholar
  29. Bauer J, Kinast S, Burger-Kentischer A, Finkelmeier D, Kleymann G, Rayyan WA, Schroppel K, Singh A, Jung G, Wiesmuller KH, Rupp S, Eickhoff H (2011) High-throughput-screening-based identification and structure-activity relationship characterization defined (S)-2-(1-aminoisobutyl)-1-(3-chlorobenzyl)benzimidazole as a highly antimycotic agent nontoxic to cell lines. J Med Chem 54:6993–6997PubMedCrossRefGoogle Scholar
  30. Behrens R, Nurse P (2002) Roles of fission yeast tea1p in the localization of polarity factors and in organizing the microtubular cytoskeleton. J Cell Biol 157:783–793PubMedPubMedCentralCrossRefGoogle Scholar
  31. Bellocq C, Andrey-Tornare I, Paunier Doret AM, Maeder B, Paturle L, Job D, Haiech J, Edelstein SJ (1992) Purification of assembly-competent tubulin from Saccharomyces cerevisiae. Eur J Biochem 210:343–349PubMedCrossRefGoogle Scholar
  32. Bennett RJ, Miller MG, Chua PR, Maxon ME, Johnson AD (2005) Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene. Mol Microbiol 55:1046–1059PubMedCrossRefGoogle Scholar
  33. Bergman ZJ, Wong J, Drubin DG, Barnes G (2018) Microtubule dynamics regulation reconstituted in budding yeast lysates. J Cell Sci 132:jcs219386PubMedCrossRefGoogle Scholar
  34. Bieling P, Laan L, Schek H, Munteanu EL, Sandblad L, Dogterom M, Brunner D, Surrey T (2007) Reconstitution of a microtubule plus-end tracking system in vitro. Nature 450:1100–1105PubMedCrossRefGoogle Scholar
  35. Bode CJ, Gupta ML, Reiff EA, Suprenant KA, Georg GI, Himes RH (2002) Epothilone and paclitaxel: unexpected differences in promoting the assembly and stabilization of yeast microtubules. Biochemistry 41:3870–3874PubMedCrossRefGoogle Scholar
  36. Bode CJ, Gupta ML, Suprenant KA, Himes RH (2003) The two alpha-tubulin isotypes in budding yeast have opposing effects on microtubule dynamics in vitro. EMBO Rep 4:94–99PubMedPubMedCentralCrossRefGoogle Scholar
  37. Bond JF, Fridovich-Keil JL, Pillus L, Mulligan RC, Solomon F (1986) A chicken-yeast chimeric beta-tubulin protein is incorporated into mouse microtubules in vivo. Cell 44:461–468PubMedCrossRefGoogle Scholar
  38. Bouissou A, Vérollet C, Sousa A, Sampaio P, Wright M, Sunkel CE, Merdes A, Raynaud-Messina B (2009) {gamma}-Tubulin ring complexes regulate microtubule plus end dynamics. J Cell Biol 187:327–334PubMedPubMedCentralCrossRefGoogle Scholar
  39. Brachat A, Kilmartin JV, Wach A, Philippsen P (1998) Saccharomyces cerevisiae cells with defective spindle pole body outer plaques accomplish nuclear migration via half-bridge-organized microtubules. Mol Biol Cell 9:977–991PubMedPubMedCentralCrossRefGoogle Scholar
  40. Braun M, Drummond DR, Cross RA, McAinsh AD (2009) The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATP-dependent sorting mechanism. Nat Cell Biol 11:724–730PubMedCrossRefGoogle Scholar
  41. Britto M, Goulet A, Rizvi S, von Loeffelholz O, Moores CA, Cross RA (2016) Schizosaccharomyces pombe kinesin-5 switches direction using a steric blocking mechanism. Proc Natl Acad Sci U S A 113:E7483–E7489PubMedPubMedCentralCrossRefGoogle Scholar
  42. Brouhard GJ (2015) Dynamic instability 30 years later: complexities in microtubule growth and catastrophe. Mol Biol Cell 26:1207–1210PubMedPubMedCentralCrossRefGoogle Scholar
  43. Brouhard GJ, Rice LM (2018) Microtubule dynamics: an interplay of biochemistry and mechanics. Nat Rev Mol Cell Biol 19:451–463PubMedPubMedCentralCrossRefGoogle Scholar
  44. Brown GD, Denning DW, Gow NAR, Levitz SM, Netea MG, White TC (2012) Hidden killers: human fungal infections. Sci Trans Med 4:165rv13CrossRefGoogle Scholar
  45. Browning H, Hayles J, Mata J, Aveline L, Nurse P, McIntosh JR (2000) Tea2p is a kinesin-like protein required to generate polarized growth in fission yeast. J Cell Biol 151:15–28PubMedPubMedCentralCrossRefGoogle Scholar
  46. Browning H, Hackney DD, Nurse P (2003) Targeted movement of cell end factors in fission yeast. Nat Cell Biol 5:812–818PubMedCrossRefGoogle Scholar
  47. Brunner D, Nurse P (2000) CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102:695–704PubMedCrossRefGoogle Scholar
  48. Burke D, Gasdaska P, Hartwell L (1989) Dominant effects of tubulin overexpression in Saccharomyces cerevisiae. Mol Cell Biol 9:1049–1059PubMedPubMedCentralCrossRefGoogle Scholar
  49. Busch KE, Hayles J, Nurse P, Brunner D (2004) Tea2p kinesin is involved in spatial microtubule organization by transporting tip1p on microtubules. Dev Cell 6:831–843PubMedCrossRefGoogle Scholar
  50. Cabanas R, Castella G, Abarca ML, Bragulat MR, Cabanes FJ (2009) Thiabendazole resistance and mutations in the beta-tubulin gene of Penicillium expansum strains isolated from apples and pears with blue mold decay. FEMS Microbiol Lett 297:189–195PubMedCrossRefGoogle Scholar
  51. Carazo-Salas RE, Antony C, Nurse P (2005) The kinesin Klp2 mediates polarization of interphase microtubules in fission yeast. Science 309:297–300PubMedCrossRefGoogle Scholar
  52. Caron JM, Vega LR, Fleming J, Bishop R, Solomon F (2001) Single site alpha-tubulin mutation affects astral microtubules and nuclear positioning during anaphase in Saccharomyces cerevisiae: possible role for palmitoylation of alpha-tubulin. Mol Biol Cell 12:2672–2687PubMedPubMedCentralCrossRefGoogle Scholar
  53. Cavanaugh AM, Jaspersen SL (2017) Big lessons from little yeast: budding and fission yeast centrosome structure, duplication, and function. Annu Rev Genet 51:361–383PubMedCrossRefGoogle Scholar
  54. Chaaban S, Brouhard GJ (2017) A microtubule bestiary: structural diversity in tubulin polymers. Mol Biol Cell 28:2924–2931PubMedPubMedCentralCrossRefGoogle Scholar
  55. Chacón MR, Delivani P, Tolić IM (2016) Meiotic nuclear oscillations are necessary to avoid excessive chromosome associations. CellReports 17:1632–1645Google Scholar
  56. Chandrika NT, Shrestha SK, Ngo HX, Garneau-Tsodikova S (2016) Synthesis and investigation of novel benzimidazole derivatives as antifungal agents. Bioorg Med Chem 24:3680–3686PubMedPubMedCentralCrossRefGoogle Scholar
  57. Chang F, Martin SG (2009) Shaping fission yeast with microtubules. Cold Spring Harb Perspect Biol 1:a001347–a001347PubMedPubMedCentralCrossRefGoogle Scholar
  58. Chen Y, Zhou MG (2009) Characterization of Fusarium graminearum isolates resistant to both carbendazim and a new fungicide JS399-19. Phytopathology 99:441–446PubMedCrossRefGoogle Scholar
  59. Chen XP, Yin H, Huffaker TC (1998) The yeast spindle pole body component Spc72p interacts with Stu2p and is required for proper microtubule assembly. J Cell Biol 141:1169–1179PubMedPubMedCentralCrossRefGoogle Scholar
  60. Chen CJ, Yu JJ, Bi CW, Zhang YN, Xu JQ, Wang JX, Zhou MG (2009) Mutations in a beta-tubulin confer resistance of Gibberella zeae to benzimidazole fungicides. Phytopathology 99:1403–1411PubMedCrossRefGoogle Scholar
  61. Chen Z, Gao T, Liang S, Liu K, Zhou M, Chen C (2014) Molecular mechanism of resistance of Fusarium fujikuroi to benzimidazole fungicides. FEMS Microbiol Lett 357:77–84PubMedCrossRefGoogle Scholar
  62. Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, Yanagida M, Hiraoka Y (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273PubMedCrossRefGoogle Scholar
  63. Chiou J-G, Balasubramanian MK, Lew DJ (2017) Cell polarity in yeast. Annu Rev Cell Dev Biol 33:77–101PubMedPubMedCentralCrossRefGoogle Scholar
  64. Cimolai N, Gill MJ, Church D (1987) Saccharomyces cerevisiae fungemia: case report and review of the literature. Diagn Microbiol Infect Dis 8:113–117PubMedCrossRefGoogle Scholar
  65. Clayton L, Pogson CI, Gull K (1979) Microtubule proteins in the yeast, Saccharomyces cerevisiae. FEBS Lett 106:67–70PubMedCrossRefGoogle Scholar
  66. Clement MJ, Rathinasamy K, Adjadj E, Toma F, Curmi PA, Panda D (2008) Benomyl and colchicine synergistically inhibit cell proliferation and mitosis: evidence of distinct binding sites for these agents in tubulin. Biochemistry 47:13016–13025PubMedCrossRefGoogle Scholar
  67. Corsello SM, Bittker JA, Liu Z, Gould J, McCarren P, Hirschman JE, Johnston SE, Vrcic A, Wong B, Khan M (2017) The drug repurposing hub: a next-generation drug library and information resource. Nat Med 23:405PubMedPubMedCentralCrossRefGoogle Scholar
  68. Cota RR, Teixidó-Travesa N, Ezquerra A, Eibes S, Lacasa C, Roig J, Lüders J (2017) MZT1 regulates microtubule nucleation by linking γTuRC assembly to adapter-mediated targeting and activation. J Cell Sci 130:406–419PubMedCrossRefGoogle Scholar
  69. Cross RA (2019) Microtubule lattice plasticity. Curr Opin Cell Biol 56:88–93PubMedCrossRefGoogle Scholar
  70. Cruz MC, Edlind T (1997) Beta-Tubulin genes and the basis for benzimidazole sensitivity of the opportunistic fungus Cryptococcus neoformans. Microbiology 143:2003–2008PubMedCrossRefGoogle Scholar
  71. Cruz MC, Bartlett MS, Edlind TD (1994) In vitro susceptibility of the opportunistic fungus Cryptococcus neoformans to anthelmintic benzimidazoles. Antimicrob Agents Chemother 38:378–380PubMedPubMedCentralCrossRefGoogle Scholar
  72. Daga RR, Yonetani A, Chang F (2006) Asymmetric microtubule pushing forces in nuclear centering. Curr Biol 16:1544–1550PubMedCrossRefGoogle Scholar
  73. Daly S, Yacoub A, Dundon W, Mastromei G, Islam K, Lorenzetti R (1997) Isolation and characterization of a gene encoding alpha-tubulin from Candida albicans. Gene 187:151–158PubMedCrossRefGoogle Scholar
  74. David M, Gabriel M, Kopecká M (2007) Cytoskeletal structures, ultrastructural characteristics and the capsule of the basidiomycetous yeast Cryptococcus laurentii. Antonie Van Leeuwenhoek 92:29–36PubMedCrossRefGoogle Scholar
  75. Davidse LC (1986) Benzimidazole fungicides: mechanism of action and biological impact. Annu Rev Phytopathol 24:43–65CrossRefGoogle Scholar
  76. Davidson RM, Hanson LE (2006) Analysis of b-tubulin gene fragments from Benzimidazole-sensitive and –tolerant Cercospora beticola. J Phytopathol 154:321–328CrossRefGoogle Scholar
  77. Davis A, Sage CR, Wilson L, Farrell KW (1993) Purification and biochemical characterization of tubulin from the budding yeast Saccharomyces cerevisiae. Biochemistry 32:8823–8835PubMedCrossRefGoogle Scholar
  78. Davis A, Sage CR, Dougherty CA, Farrell KW (1994) Microtubule dynamics modulated by guanosine triphosphate hydrolysis activity of beta-tubulin. Science 264:839–842PubMedCrossRefGoogle Scholar
  79. Delgehyr N, Lopes CSJ, Moir CA, Huisman SM, Segal M (2008) Dissecting the involvement of formins in Bud6p-mediated cortical capture of microtubules in S. cerevisiae. J Cell Sci 121:3803–3814PubMedCrossRefGoogle Scholar
  80. des Georges A, Katsuki M, Drummond DR, Osei M, Cross RA, Amos LA (2008) Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice. Nat Struct Mol Biol 15:1102–1108PubMedPubMedCentralCrossRefGoogle Scholar
  81. Devereux M, McCann M, Shea DO, Kelly R, Egan D, Deegan C, Kavanagh K, McKee V, Finn G (2004) Synthesis, antimicrobial activity and chemotherapeutic potential of inorganic derivatives of 2-(4′-thiazolyl)benzimidazole[thiabendazole]: X-ray crystal structures of [Cu(TBZH)2Cl]Cl.H2O.EtOH and TBZH2NO3 (TBZH=thiabendazole). J Inorg Biochem 98:1023–1031PubMedCrossRefGoogle Scholar
  82. Dhani DK, Goult BT, George GM, Rogerson DT, Bitton DA, Miller CJ, Schwabe JWR, Tanaka K (2013) Mzt1/Tam4, a fission yeast MOZART1 homologue, is an essential component of the γ-tubulin complex and directly interacts with GCP3(Alp6). Mol Biol Cell 24:3337–3349PubMedPubMedCentralCrossRefGoogle Scholar
  83. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pöhlmann R, Luedi P, Choi S, Wing RA, Flavier A, Gaffney TD, Philippsen P (2004) The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304:304–307PubMedCrossRefGoogle Scholar
  84. Ding R, McDonald KL, McIntosh JR (1993) Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J Cell Biol 120:141–151PubMedCrossRefGoogle Scholar
  85. Ding R, West RR, Morphew DM, Oakley BR, McIntosh JR (1997) The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol Biol Cell 8:1461–1479PubMedPubMedCentralCrossRefGoogle Scholar
  86. Ding D-Q, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6:329–341PubMedCrossRefGoogle Scholar
  87. Ding Y, Li Y, Li Z, Zhang J, Lu C, Wang H, Shen Y, Du L (2016) Alteramide B is a microtubule antagonist of inhibiting Candida albicans. Biochim Biophys Acta 1860:2097–2106PubMedPubMedCentralCrossRefGoogle Scholar
  88. Dorleans A, Knossow M, Gigant B (2007) Studying drug-tubulin interactions by X-ray crystallography. Methods Mol Med 137:235–243PubMedCrossRefGoogle Scholar
  89. Dostal V, Libusova L (2014) Microtubule drugs: action, selectivity, and resistance across the kingdoms of life. Protoplasma 251:991–1005PubMedCrossRefGoogle Scholar
  90. Dougherty CA, Himes RH, Wilson L, Farrell KW (1998) Detection of GTP and Pi in wild-type and mutated yeast microtubules: implications for the role of the GTP/GDP-Pi cap in microtubule dynamics. Biochemistry 37:10861–10865PubMedCrossRefGoogle Scholar
  91. Downing KH, Nogales E (2010) Cryoelectron microscopy applications in the study of tubulin structure, microtubule architecture, dynamics and assemblies, and interaction of microtubules with motors. Methods Enzymol 483:121–142PubMedPubMedCentralCrossRefGoogle Scholar
  92. Drummond DR, Cross RA (2000) Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr Biol 10:766–775PubMedCrossRefGoogle Scholar
  93. Drummond DR, Kain S, Newcombe A, Hoey C, Katsuki M, Cross RA (2011) Purification of tubulin from the fission yeast Schizosaccharomyces pombe. Methods Mol Biol 777:29–55PubMedCrossRefGoogle Scholar
  94. Duan D, Hnatchuk DJ, Brenner J, Davis D, Allingham JS (2012) Crystal structure of the Kar3-like kinesin motor domain from the filamentous fungus Ashbya gossypii. Proteins 80:1016–1027PubMedCrossRefGoogle Scholar
  95. Duellberg C, Cade NI, Holmes D, Surrey T (2016) The size of the EB cap determines instantaneous microtubule stability. elife 5:e13470PubMedPubMedCentralCrossRefGoogle Scholar
  96. Edamatsu M (2014) Bidirectional motility of the fission yeast kinesin-5, Cut7. Biochem Biophys Res Commun 446:231–234PubMedCrossRefGoogle Scholar
  97. Edzuka T, Yamada L, Kanamaru K, Sawada H, Goshima G (2014) Identification of the augmin complex in the filamentous fungus Aspergillus nidulans. PLoS One 9:e101471PubMedPubMedCentralCrossRefGoogle Scholar
  98. Efimov VP, Zhang J, Xiang X (2006) CLIP-170 homologue and NUDE play overlapping roles in NUDF localization in Aspergillus nidulans. Mol Biol Cell 17:2021–2034PubMedPubMedCentralCrossRefGoogle Scholar
  99. Egan MJ, McClintock MA, Reck-Peterson SL (2012) Microtubule-based transport in filamentous fungi. Curr Opin Microbiol 15:637–645PubMedPubMedCentralCrossRefGoogle Scholar
  100. El-Gohary NS, Shaaban MI (2017) Synthesis, antimicrobial, antiquorum-sensing and antitumor activities of new benzimidazole analogs. Eur J Med Chem 137:439–449PubMedCrossRefGoogle Scholar
  101. Enke C, Zekert N, Veith D, Schaaf C, Konzack S, Fischer R (2007) Aspergillus nidulans Dis1/XMAP215 protein AlpA localizes to spindle pole bodies and microtubule plus ends and contributes to growth directionality. Eukaryot Cell 6:555–562PubMedPubMedCentralCrossRefGoogle Scholar
  102. Farache D, Emorine L, Haren L, Merdes A (2018) Assembly and regulation of γ-tubulin complexes. Open Biol 8:170266PubMedPubMedCentralCrossRefGoogle Scholar
  103. Farkasovsky M, Küntzel H (2001) Cortical Num1p interacts with the dynein intermediate chain Pac11p and cytoplasmic microtubules in budding yeast. J Cell Biol 152:251–262PubMedPubMedCentralCrossRefGoogle Scholar
  104. Fedyanina OS, Book AJ, Grishchuk EL (2009) Tubulin heterodimers remain functional for one cell cycle after the inactivation of tubulin-folding cofactor D in fission yeast cells. Yeast 26:235–247PubMedPubMedCentralCrossRefGoogle Scholar
  105. Feierbach B, Verde F, Chang F (2004) Regulation of a formin complex by the microtubule plus end protein tea1p. J Cell Biol 165:697–707PubMedPubMedCentralCrossRefGoogle Scholar
  106. Fink G, Steinberg G (2006) Dynein-dependent motility of microtubules and nucleation sites supports polarization of the tubulin array in the fungus Ustilago maydis. Mol Biol Cell 17:3242–3253PubMedPubMedCentralCrossRefGoogle Scholar
  107. Finley KR, Berman J (2005) Microtubules in Candida albicans hyphae drive nuclear dynamics and connect cell cycle progression to morphogenesis. Eukaryot Cell 4:1697–1711PubMedPubMedCentralCrossRefGoogle Scholar
  108. Finley KR, Bouchonville KJ, Quick A, Berman J (2008) Dynein-dependent nuclear dynamics affect morphogenesis in Candida albicans by means of the Bub2p spindle checkpoint. J Cell Sci 121:466–476PubMedCrossRefGoogle Scholar
  109. Fischer R, Timberlake WE (1995) Aspergillus nidulans apsA (anucleate primary sterigmata) encodes a coiled-coil protein required for nuclear positioning and completion of asexual development. J Cell Biol 128:485–498PubMedCrossRefGoogle Scholar
  110. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194PubMedCrossRefGoogle Scholar
  111. Fisher MC, Hawkins NJ, Sanglard D, Gurr SJ (2018) Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science 360:739–742PubMedCrossRefGoogle Scholar
  112. Flor-Parra I, Iglesias-Romero AB, Chang F (2018) The XMAP215 Ortholog Alp14 promotes microtubule nucleation in fission Yeast. Curr Biol: CB 28:1681–1691.e4PubMedCrossRefGoogle Scholar
  113. Flory MR, Morphew M, Joseph JD, Means AR, Davis TN (2002) Pcp1p, an Spc110p-related calmodulin target at the centrosome of the fission yeast Schizosaccharomyces pombe. Cell Growth Differ: The Mol Biol J Am Assoc Cancer Res 13:47–58Google Scholar
  114. Fong KK, Zelter A, Graczyk B, Hoyt JM, Riffle M, Johnson R, MacCoss MJ, Davis TN (2018) Novel phosphorylation states of the yeast spindle pole body. Biology open 7:bio033647PubMedPubMedCentralCrossRefGoogle Scholar
  115. Foster KE, Burland TG, Gull K (1987) A mutant beta-tubulin confers resistance to the action of benzimidazole-carbamate microtubule inhibitors both in vivo and in vitro. Eur J Biochem 163:449–455PubMedCrossRefGoogle Scholar
  116. Freitag M (2016) The kinetochore interaction network (KIN) of ascomycetes. Mycologia 108:485–505PubMedPubMedCentralCrossRefGoogle Scholar
  117. Friedman DB, Sundberg HA, Huang EY, Davis TN (1996) The 110-kD spindle pole body component of Saccharomyces cerevisiae is a phosphoprotein that is modified in a cell cycle-dependent manner. J Cell Biol 132:903–914PubMedCrossRefGoogle Scholar
  118. Friedman DB, Kern JW, Huneycutt BJ, Vinh DB, Crawford DK, Steiner E, Scheiltz D, Yates J, Resing KA, Ahn NG, Winey M, Davis TN (2001) Yeast Mps1p phosphorylates the spindle pole component Spc110p in the N-terminal domain. J Biol Chem 276:17958–17967PubMedPubMedCentralCrossRefGoogle Scholar
  119. Fujita A, Vardy L, Garcia MA, Toda T (2002) A fourth component of the fission yeast gamma-tubulin complex, Alp16, is required for cytoplasmic microtubule integrity and becomes indispensable when gamma-tubulin function is compromised. Mol Biol Cell 13:2360–2373PubMedPubMedCentralCrossRefGoogle Scholar
  120. Fujita I, Yamashita A, Yamamoto M (2015) Dynactin and Num1 cooperate to establish the cortical anchoring of cytoplasmic dynein in S. pombe. J Cell Sci 128:1555–1567PubMedCrossRefGoogle Scholar
  121. Gaba M, Mohan C (2016) Development of drugs based on imidazole and benzimidazole bioactive heterocycles: recent advances and future directions. Med Chem Res 25:173–210CrossRefGoogle Scholar
  122. Gandhi SR, Gierliński M, Mino A, Tanaka K, Kitamura E, Clayton L, Tanaka TU (2011) Kinetochore-dependent microtubule rescue ensures their efficient and sustained interactions in early mitosis. Dev Cell 21:920–933PubMedPubMedCentralCrossRefGoogle Scholar
  123. Gardner MK, Bouck DC, Paliulis LV, Meehl JB, O’Toole ET, Haase J, Soubry A, Joglekar AP, Winey M, Salmon ED, Bloom K, Odde DJ (2008) Chromosome congression by Kinesin-5 motor-mediated disassembly of longer kinetochore microtubules. Cell 135:894–906PubMedPubMedCentralCrossRefGoogle Scholar
  124. Geerts S, Gryseels B (2000) Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev 13:207–222PubMedPubMedCentralCrossRefGoogle Scholar
  125. Gell C, Friel CT, Borgonovo B, Drechsel DN, Hyman AA, Howard J (2011) Purification of tubulin from porcine brain. Methods Mol Biol 777:15–28PubMedCrossRefGoogle Scholar
  126. Gerson-Gurwitz A, Thiede C, Movshovich N, Fridman V, Podolskaya M, Danieli T, Lakämper S, Klopfenstein DR, Schmidt CF, Gheber L (2011) Directionality of individual kinesin-5 Cin8 motors is modulated by loop 8, ionic strength and microtubule geometry. EMBO J 30:4942–4954PubMedPubMedCentralCrossRefGoogle Scholar
  127. Geyer EA, Burns A, Lalonde BA, Ye X, Piedra FA, Huffaker TC, Rice LM (2015) A mutation uncouples the tubulin conformational and GTPase cycles, revealing allosteric control of microtubule dynamics. elife 4:e10113PubMedPubMedCentralCrossRefGoogle Scholar
  128. Geymonat M, Segal M (2017) Intrinsic and extrinsic determinants linking spindle pole fate, spindle polarity, and asymmetric cell division in the budding Yeast S. cerevisiae. Results Probl Cell Differ 61:49–82PubMedCrossRefGoogle Scholar
  129. Ghosh PN, Fisher MC, Bates KA (2018) Diagnosing emerging fungal threats: a one health perspective. Front Genet 9:article376CrossRefGoogle Scholar
  130. Giannakakou P, Gussio R, Nogales E, Downing KH, Zaharevitz D, Bollbuck B, Poy G, Sackett D, Nicolaou KC, Fojo T (2000) A common pharmacophore for epothilone and taxanes: molecular basis for drug resistance conferred by tubulin mutations in human cancer cells. Proc Natl Acad Sci U S A 97:2904–2909PubMedPubMedCentralCrossRefGoogle Scholar
  131. Gibeaux R, Lang C, Politi AZ, Jaspersen SL, Philippsen P, Antony C (2012) Electron tomography of the microtubule cytoskeleton in multinucleated hyphae of Ashbya gossypii. J Cell Sci 125:5830–5839PubMedCrossRefGoogle Scholar
  132. Gibeaux R, Politi AZ, Nédélec F, Antony C, Knop M (2013) Spindle pole body-anchored Kar3 drives the nucleus along microtubules from another nucleus in preparation for nuclear fusion during yeast karyogamy. Genes Dev 27:335–349PubMedPubMedCentralCrossRefGoogle Scholar
  133. Gibeaux R, Politi AZ, Philippsen P, Nédélec F (2017) Mechanism of nuclear movements in a multinucleated cell. Mol Biol Cell 28:645–660PubMedPubMedCentralCrossRefGoogle Scholar
  134. Gladfelter AS, Hungerbuehler AK, Philippsen P (2006) Asynchronous nuclear division cycles in multinucleated cells. J Cell Biol 172:347–362PubMedPubMedCentralCrossRefGoogle Scholar
  135. Goker H, Tuncbilek M, Ayhan G, Altanlar N (1998) Synthesis of some new benzimidazolecarboxamides and evaluation of their antimicrobial activity. Farmaco 53:415–420PubMedCrossRefGoogle Scholar
  136. Goodson HV, Jonasson EM (2018) Microtubules and microtubule-associated proteins. Cold Spring Harb Perspect Biol 10:a022608PubMedCrossRefGoogle Scholar
  137. Grava S, Keller M, Voegeli S, Seger S, Lang C, Philippsen P (2011) Clustering of nuclei in multinucleated hyphae is prevented by dynein-driven bidirectional nuclear movements and microtubule growth control in Ashbya gossypii. Eukaryot Cell 10:902–915PubMedPubMedCentralCrossRefGoogle Scholar
  138. Graziano BR, DuPage AG, Michelot A, Breitsprecher D, Moseley JB, Sagot I, Blanchoin L, Goode BL (2011) Mechanism and cellular function of Bud6 as an actin nucleation-promoting factor. Mol Biol Cell 22:4016–4028PubMedPubMedCentralCrossRefGoogle Scholar
  139. Grishchuk EL, McIntosh JR (1999) Sto1p, a fission yeast protein similar to tubulin folding cofactor E, plays an essential role in mitotic microtubule assembly. J Cell Sci 112:1979–1988PubMedGoogle Scholar
  140. Gruneberg U, Campbell K, Simpson C, Grindlay J, Schiebel E (2000) Nud1p links astral microtubule organization and the control of exit from mitosis. EMBO J 19:6475–6488PubMedPubMedCentralCrossRefGoogle Scholar
  141. Guesdon A, Bazile F, Buey RM, Mohan R, Monier S, Garcia RR, Angevin M, Heichette C, Wieneke R, Tampe R, Duchesne L, Akhmanova A, Steinmetz MO, Chretien D (2016) EB1 interacts with outwardly curved and straight regions of the microtubule lattice. Nat Cell Biol 18:1102–1108PubMedCrossRefGoogle Scholar
  142. Gunzelmann J, Ruthnick D, Lin TC, Zhang W, Neuner A, Jakle U, Schiebel E (2018) The microtubule polymerase Stu2 promotes oligomerization of the gamma-TuSC for cytoplasmic microtubule nucleation. elife 7:934CrossRefGoogle Scholar
  143. Gupta ML Jr, Bode CJ, Thrower DA, Pearson CG, Suprenant KA, Bloom KS, Himes RH (2002) Beta-tubulin C354 mutations that severely decrease microtubule dynamics do not prevent nuclear migration in yeast. Mol Biol Cell 13:2919–2932PubMedPubMedCentralCrossRefGoogle Scholar
  144. Gupta ML Jr, Bode CJ, Georg GI, Himes RH (2003) Understanding tubulin-Taxol interactions: mutations that impart Taxol binding to yeast tubulin. Proc Natl Acad Sci U S A 100:6394–6397PubMedPubMedCentralCrossRefGoogle Scholar
  145. Gupta K, Bishop J, Peck A, Brown J, Wilson L, Panda D (2004) Antimitotic antifungal compound benomyl inhibits brain microtubule polymerization and dynamics and cancer cell proliferation at mitosis, by binding to a novel site in tubulin. Biochemistry 43:6645–6655PubMedCrossRefGoogle Scholar
  146. H_örrmansdorfer S, Bauer J (2000) Yeast infections in veterinary medicine. In: Ernst JF, Schmidt A (eds) Dimorphism in human pathogenic and apathogenic yeasts. Karger, BaselGoogle Scholar
  147. Haag C, Steuten B, Feldbrugge M (2015) Membrane-coupled mRNA trafficking in Fungi. Annu Rev Microbiol 69:265–281PubMedCrossRefGoogle Scholar
  148. Hagan IM (1998) The fission yeast microtubule cytoskeleton. J Cell Sci 111:1603–1612PubMedGoogle Scholar
  149. Hagan I, Yanagida M (1990) Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature 347:563–566PubMedCrossRefGoogle Scholar
  150. Han G, Liu B, Zhang J, Zuo W, Morris NR, Xiang X (2001) The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr Biol 11:719–724PubMedCrossRefGoogle Scholar
  151. Han ZJ, Feng YH, Gu BH, Li YM, Chen H (2018) The post-translational modification, SUMOylation, and cancer (review). Int J Oncol 52:1081–1094PubMedPubMedCentralGoogle Scholar
  152. Hara M, Fukagawa T (2018) Kinetochore assembly and disassembly during mitotic entry and exit. Curr Opin Cell Biol 52:73–81PubMedCrossRefGoogle Scholar
  153. Haren L, Remy M-H, Bazin I, Callebaut I, Wright M, Merdes A (2006) NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 172:505–515PubMedPubMedCentralCrossRefGoogle Scholar
  154. Heil-Chapdelaine RA, Oberle JR, Cooper JA (2000) The cortical protein Num1p is essential for dynein-dependent interactions of microtubules with the cortex. J Cell Biol 151:1337–1344PubMedPubMedCentralCrossRefGoogle Scholar
  155. Hentrich C, Surrey T (2010) Microtubule organization by the antagonistic mitotic motors kinesin-5 and kinesin-14. J Cell Biol 189:465–480PubMedPubMedCentralCrossRefGoogle Scholar
  156. Hepperla AJ, Willey PT, Coombes CE, Schuster BM, Gerami-Nejad M, McClellan M, Mukherjee S, Fox J, Winey M, Odde DJ, O’Toole E, Gardner MK (2014) Minus-end-directed Kinesin-14 motors align antiparallel microtubules to control metaphase spindle length. Dev Cell 31:61–72PubMedPubMedCentralCrossRefGoogle Scholar
  157. Hiller G, Weber K (1978) Radioimmunoassay for tubulin: a quantitative comparison of the tubulin content of different established tissue culture cells and tissues. Cell 14:795–804PubMedCrossRefPubMedCentralGoogle Scholar
  158. Hiraoka Y, Toda T, Yanagida M (1984) The NDA3 gene of fission yeast encodes beta-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 39:349–358PubMedCrossRefPubMedCentralGoogle Scholar
  159. Hirschi S, Letscher-Bru V, Pottecher J, Lannes B, Jeung MY, Degot T, Santelmo N, Sabou AM, Herbrecht R, Kessler R (2012) Disseminated Trichosporon mycotoxinivorans, Aspergillus fumigatus, and Scedosporium apiospermum coinfection after lung and liver transplantation in a cystic fibrosis patient. J Clin Microbiol 50:4168–4170PubMedPubMedCentralCrossRefGoogle Scholar
  160. Hoepfner D, Schaerer F, Brachat A, Wach A, Philippsen P (2002) Reorientation of mispositioned spindles in short astral microtubule mutant spc72Delta is dependent on spindle pole body outer plaque and Kar3 motor protein. Mol Biol Cell 13:1366–1380PubMedPubMedCentralCrossRefGoogle Scholar
  161. Hollomon DW (2010) New fungicide modes of action strengthen disease control strategies. Outlooks on Pest Management June:1–5Google Scholar
  162. Honda Y, Tsuchiya K, Sumiyoshi E, Haruta N, Sugimoto A (2017) Tubulin isotype substitution revealed that isotype combination modulates microtubule dynamics in C. elegans embryos. J Cell Sci 130:1652–1661PubMedCrossRefPubMedCentralGoogle Scholar
  163. Höög JL, Antony C (2007) Whole-cell investigation of microtubule cytoskeleton architecture by electron tomography. Methods Cell Biol 79:145–167PubMedCrossRefGoogle Scholar
  164. Hoog JL, Schwartz C, Noon AT, O’Toole ET, Mastronarde DN, McIntosh JR, Antony C (2007) Organization of interphase microtubules in fission yeast analyzed by electron tomography. Dev Cell 12:349–361PubMedCrossRefGoogle Scholar
  165. Hoog JL, Huisman SM, Sebo-Lemke Z, Sandblad L, McIntosh JR, Antony C, Brunner D (2011) Electron tomography reveals a flared morphology on growing microtubule ends. J Cell Sci 124:693–698PubMedPubMedCentralCrossRefGoogle Scholar
  166. Horio T, Oakley BR (1994) Human gamma-tubulin functions in fission yeast. J Cell Biol 126:1465–1473PubMedCrossRefGoogle Scholar
  167. Horio T, Oakley BR (2003) Expression of Arabidopsis gamma-tubulin in fission yeast reveals conserved and novel functions of gamma-tubulin. Plant Physiol 133:1926–1934PubMedPubMedCentralCrossRefGoogle Scholar
  168. Horio T, Oakley BR (2005) The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Mol Biol Cell 16:918–926PubMedPubMedCentralCrossRefGoogle Scholar
  169. Horio T, Uzawa S, Jung MK, Oakley BR, Tanaka K, Yanagida M (1991) The fission yeast gamma-tubulin is essential for mitosis and is localized at microtubule organizing centers. J Cell Sci 99:693–700PubMedGoogle Scholar
  170. Horio T, Kimura N, Basaki A, Tanaka Y, Noguchi T, Akashi T, Tanaka K (2002) Molecular and structural characterization of the spindle pole bodies in the fission yeast Schizosaccharomyces japonicus var japonicus. Yeast 19:1335–1350PubMedCrossRefGoogle Scholar
  171. Howes SC, Geyer EA, LaFrance B, Zhang R, Kellogg EH, Westermann S, Rice LM, Nogales E (2017) Structural differences between yeast and mammalian microtubules revealed by cryo-EM. J Cell Biol 216:2669–2677PubMedPubMedCentralGoogle Scholar
  172. Howes SC, Geyer EA, LaFrance B, Zhang R, Kellogg EH, Westermann S, Rice LM, Nogales E (2018) Structural and functional differences between porcine brain and budding yeast microtubules. Cell Cycle 17:278–287PubMedPubMedCentralCrossRefGoogle Scholar
  173. Huffaker TC, Hoyt MA, Botstein D (1987) Genetic analysis of the yeast cytoskeleton. Annu Rev Genet 21:259–284PubMedCrossRefGoogle Scholar
  174. Huisman SM, Bales OAM, Bertrand M, Smeets MFMA, Reed SI, Segal M (2004) Differential contribution of Bud6p and Kar9p to microtubule capture and spindle orientation in S. cerevisiae. J Cell Biol 167:231–244PubMedPubMedCentralCrossRefGoogle Scholar
  175. Hussmann F, Drummond DR, Peet DR, Martin DS, Cross RA (2016) Alp7/TACC-Alp14/TOG generates long-lived, fast-growing MTs by an unconventional mechanism. Sci Rep 6:20653PubMedPubMedCentralCrossRefGoogle Scholar
  176. Hwang E, Kusch J, Barral Y, Huffaker TC (2003) Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables. J Cell Biol 161:483–488PubMedPubMedCentralCrossRefGoogle Scholar
  177. Hyman AA, Salser S, Drechsel DN, Unwin N, Mitchison TJ (1992) Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP. Mol Biol Cell 3:1155–1167PubMedPubMedCentralCrossRefGoogle Scholar
  178. Ilan Y (2018) Microtubules: from understanding their dynamics to using them as potential therapeutic targets. J Cell Physiol 234:7923–7937PubMedCrossRefGoogle Scholar
  179. Ishitsuka Y, Savage N, Li Y, Bergs A, Grün N, Kohler D, Donnelly R, Nienhaus GU, Fischer R, Takeshita N (2015) Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth. Sci Adv 1:e1500947PubMedPubMedCentralCrossRefGoogle Scholar
  180. Izumi N, Fumoto K, Izumi S, Kikuchi A (2008) GSK-3beta regulates proper mitotic spindle formation in cooperation with a component of the gamma-tubulin ring complex, GCP5. J Biol Chem 283:12981–12991PubMedCrossRefGoogle Scholar
  181. Jaeger LH, Carvalho-Costa FA (2017) Status of benzimidazole resistance in intestinal nematode populations of livestock in Brazil: a systematic review. BMC Vet Res 13:358PubMedPubMedCentralCrossRefGoogle Scholar
  182. Janeczko M, Kazimierczuk Z, Orzeszko A, Niewiadomy A, Krol E, Szyszka R, Maslyk M (2016) In search of the antimicrobial potential of Benzimidazole derivatives. Pol J Microbiol 65:359–364PubMedCrossRefGoogle Scholar
  183. Jang MH, Kim J, Kalme S, Han JW, Yoo HS, Koo BS, Kim SK, Yoon MY (2008) Cloning, purification, and polymerization of Capsicum annuum recombinant alpha and beta tubulin. Biosci Biotechnol Biochem 72:1048–1055PubMedCrossRefGoogle Scholar
  184. Janson ME, Setty TG, Paoletti A, Tran PT (2005) Efficient formation of bipolar microtubule bundles requires microtubule-bound gamma-tubulin complexes. J Cell Biol 169:297–308PubMedPubMedCentralCrossRefGoogle Scholar
  185. Joffe LS, Schneider R, Lopes W, Azevedo R, Staats CC, Kmetzsch L, Schrank A, Del Poeta M, Vainstein MH, Rodrigues ML (2017) The anti-helminthic compound Mebendazole has multiple antifungal effects against Cryptococcus neoformans. Front Microbiol 8:535PubMedPubMedCentralCrossRefGoogle Scholar
  186. Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, Berman J, He X, Salmon ED, Bloom KS (2008) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181:587–594PubMedPubMedCentralCrossRefGoogle Scholar
  187. Johnson V, Ayaz P, Huddleston P, Rice LM (2011) Design, overexpression, and purification of polymerization-blocked yeast alphabeta-tubulin mutants. Biochemistry 50:8636–8644PubMedCrossRefGoogle Scholar
  188. Joshi M, Duan D, Drew D, Jia Z, Davis D, Campbell RL, Allingham JS (2013) Kar3Vik1 mechanochemistry is inhibited by mutation or deletion of the C terminus of the Vik1 subunit. J Biol Chem 288:36957–36970PubMedPubMedCentralCrossRefGoogle Scholar
  189. Jung MK, Oakley BR (1990) Identification of an amino acid substitution in the benA, beta-tubulin gene of Aspergillus nidulans that confers thiabendazole resistance and benomyl supersensitivity. Cell Motil Cytoskeleton 17:87–94PubMedCrossRefGoogle Scholar
  190. Jung MK, Wilder IB, Oakley BR (1992) Amino acid alterations in the benA (beta-tubulin) gene of Aspergillus nidulans that confer benomyl resistance. Cell Motil Cytoskeleton 22:170–174PubMedCrossRefGoogle Scholar
  191. Kaplancikli ZA, Levent S, Osmaniye D, Saglik BN, Cevik UA, Cavusoglu BK, Ozkay Y, Ilgin S (2017) Synthesis and Anticandidal activity evaluation of new Benzimidazole-Thiazole derivatives. Molecules 22:2051PubMedCentralCrossRefPubMedGoogle Scholar
  192. Kapoor TM, Mayer TU, Coughlin ML, Mitchison TJ (2000) Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J Cell Biol 150:975–988PubMedPubMedCentralCrossRefGoogle Scholar
  193. Katsuki M, Drummond DR, Osei M, Cross RA (2009) Mal3 masks catastrophe events in Schizosaccharomyces pombe microtubules by inhibiting shrinkage and promoting rescue. J Biol Chem 284:29246–29250PubMedPubMedCentralCrossRefGoogle Scholar
  194. Katsuki M, Drummond DR, Cross RA (2014) Ectopic A-lattice seams destabilize microtubules. Nat Commun 5:3094PubMedPubMedCentralCrossRefGoogle Scholar
  195. Katz W, Weinstein B, Solomon F (1990) Regulation of tubulin levels and microtubule assembly in Saccharomyces cerevisiae: consequences of altered tubulin gene copy number. Mol Cell Biol 10:5286–5294PubMedPubMedCentralCrossRefGoogle Scholar
  196. Keeling PJ (2003) Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol 38:298–309PubMedCrossRefGoogle Scholar
  197. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617–624PubMedCrossRefGoogle Scholar
  198. Khabnadideh S, Rezaei Z, Pakshir K, Zomorodian K, Ghafari N (2012) Synthesis and antifungal activity of benzimidazole, benzotriazole and aminothiazole derivatives. Res Pharm Sci 7:65–72PubMedPubMedCentralGoogle Scholar
  199. Kharazi M, Ahmadi B, Makimur K, Farhang A, Kianipour S, Motamedi M, Mirhendi H (2018) Characterization of beta-tubulin DNA sequences within Candida parapsilosis complex. Curr Med Mycol 4:24–29PubMedPubMedCentralCrossRefGoogle Scholar
  200. Khodiyar VK, Maltais LJ, Ruef BJ, Sneddon KM, Smith JR, Shimoyama M, Cabral F, Dumontet C, Dutcher SK, Harvey RJ, Lafanechère L, Murray JM, Nogales E, Piquemal D, Stanchi F, Povey S, Lovering RC (2007) A revised nomenclature for the human and rodent alpha-tubulin gene family. Genomics 90:285–289PubMedCrossRefGoogle Scholar
  201. Kilmartin JV (1981) Purification of yeast tubulin by self-assembly in vitro. Biochemistry 20:3629–3633PubMedCrossRefGoogle Scholar
  202. Kilmartin JV, Goh PY (1996) Spc110p: assembly properties and role in the connection of nuclear microtubules to the yeast spindle pole body. EMBO J 15:4592–4602PubMedPubMedCentralCrossRefGoogle Scholar
  203. Klimesova V, Koci J, Pour M, Stachel J, Waisser K, Kaustova J (2002) Synthesis and preliminary evaluation of benzimidazole derivatives as antimicrobial agents. Eur J Med Chem 37:409–418PubMedCrossRefGoogle Scholar
  204. Knop M, Schiebel E (1997) Spc98p and Spc97p of the yeast gamma-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO J 16:6985–6995PubMedPubMedCentralCrossRefGoogle Scholar
  205. Knop M, Schiebel E (1998) Receptors determine the cellular localization of a gamma-tubulin complex and thereby the site of microtubule formation. EMBO J 17:3952–3967PubMedPubMedCentralCrossRefGoogle Scholar
  206. Koenraadt H, Somerville SC, Jones AL (1992) Characterization of mutations in the beta-tubulin gene of benomyl-resistant field strains of Venturia inaequalis and other plant pathogenic fungi. Phytopathology 82:1348–1354CrossRefGoogle Scholar
  207. Kollman JM, Polka JK, Zelter A, Davis TN, Agard DA (2010) Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 466:879–882PubMedPubMedCentralCrossRefGoogle Scholar
  208. Kollman JM, Greenberg CH, Li S, Moritz M, Zelter A, Fong KK, Fernandez JJ, Sali A, Kilmartin J, Davis TN, Agard DA (2015) Ring closure activates yeast γTuRC for species-specific microtubule nucleation. Nat Struct Mol Biol 22:132–137PubMedPubMedCentralCrossRefGoogle Scholar
  209. Konzack S, Rischitor PE, Enke C, Fischer R (2005) The role of the kinesin motor KipA in microtubule organization and polarized growth of Aspergillus nidulans. Mol Biol Cell 16:497–506PubMedPubMedCentralCrossRefGoogle Scholar
  210. Koo BS, Kalme S, Yeo SH, Lee SJ, Yoon MY (2009) Molecular cloning and biochemical characterization of alpha- and beta-tubulin from potato plants (Solanum tuberosum L.). Plant Physiol Biochem 47:761–768PubMedCrossRefGoogle Scholar
  211. Kopecka M (2016) Microtubules and actin cytoskeleton of Cryptococcus neoformans as targets for anticancer agents to potentiate a novel approach for new antifungals. Chemotherapy 61:117–121PubMedCrossRefGoogle Scholar
  212. Kopecka M, Gabriel M (2009) Microtubules and actin cytoskeleton of potentially pathogenic basidiomycetous yeast as targets for antifungals. Chemotherapy 55:278–286PubMedCrossRefGoogle Scholar
  213. Kopecka M, Gabriel M, Takeo K, Yamaguchi M, Svoboda A, Ohkusu M, Hata K, Yoshida S (2001) Microtubules and actin cytoskeleton in Cryptococcus neoformans compared with ascomycetous budding and fission yeasts. Eur J Cell Biol 80:303–311PubMedCrossRefGoogle Scholar
  214. Kosco KA, Pearson CG, Maddox PS, Wang PJ, Adams IR, Salmon ED, Bloom K, Huffaker TC (2001) Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol Biol Cell 12:2870–2880PubMedPubMedCentralCrossRefGoogle Scholar
  215. Kowal J, Wyrobisz A, Nosal P, Kucharski M, Kaczor U, Skalska M, Sendor P (2016) Benzimidazole resistance in the ovine Haemonchus contortus from southern Poland - coproscopical and molecular findings. Ann Parasitol 62:119–123PubMedGoogle Scholar
  216. Kurihara LJ, Beh CT, Latterich M, Schekman R, Rose MD (1994) Nuclear congression and membrane fusion: two distinct events in the yeast karyogamy pathway. J Cell Biol 126:911–923PubMedCrossRefGoogle Scholar
  217. Kurischko C, Swoboda RK (2000) Cytoskeletal proteins and morphogenesis in Candida albicans and Yarrowia lipolytica. In: Ernst JF, Schmidt A (eds) Dimorphism in human pathogenic and apathogenic yeasts. Karger, BaselGoogle Scholar
  218. Lacefield S, Solomon F (2003) A novel step in beta-tubulin folding is important for heterodimer formation in Saccharomyces cerevisiae. Genetics 165:531–541PubMedPubMedCentralGoogle Scholar
  219. Lacefield S, Magendantz M, Solomon F (2006) Consequences of defective tubulin folding on heterodimer levels, mitosis and spindle morphology in Saccharomyces cerevisiae. Genetics 173:635–646PubMedPubMedCentralCrossRefGoogle Scholar
  220. Lai J, Koh CH, Tjota M, Pieuchot L, Raman V, Chandrababu KB, Yang D, Wong L, Jedd G (2012) Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity. Proc Natl Acad Sci U S A 109:15781–15786PubMedPubMedCentralCrossRefGoogle Scholar
  221. Lammers LG, Markus SM (2015) The dynein cortical anchor Num1 activates dynein motility by relieving Pac1/LIS1-mediated inhibition. J Cell Biol 211:309–322PubMedPubMedCentralCrossRefGoogle Scholar
  222. Lang C, Grava S, van den Hoorn T, Trimble R, Philippsen P, Jaspersen SL (2010a) Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of Ashbya gossypii. Mol Biol Cell 21:18–28PubMedPubMedCentralCrossRefGoogle Scholar
  223. Lang C, Grava S, Finlayson M, Trimble R, Philippsen P, Jaspersen SL (2010b) Structural mutants of the spindle pole body cause distinct alteration of cytoplasmic microtubules and nuclear dynamics in multinucleated hyphae. Mol Biol Cell 21:753–766PubMedPubMedCentralCrossRefGoogle Scholar
  224. Laryea D, Gullbo J, Isaksson A, Larsson R, Nygren P (2010) Characterization of the cytotoxic properties of the benzimidazole fungicides, benomyl and carbendazim, in human tumour cell lines and primary cultures of patient tumour cells. Anti-Cancer Drugs 21:33–42PubMedCrossRefGoogle Scholar
  225. Leandro-García LJ, Leskelä S, Landa I, Montero-Conde C, López-Jiménez E, Letón R, Cascón A, Robledo M, Rodríguez-Antona C (2010) Tumoral and tissue-specific expression of the major human beta-tubulin isotypes. Cytoskeleton (Hoboken) 67:214–223CrossRefGoogle Scholar
  226. Lecland N, Lüders J (2014) The dynamics of microtubule minus ends in the human mitotic spindle. Nat Publ Group 16:770–778Google Scholar
  227. Lee SC, Heitman J (2012) Function of Cryptococcus neoformans KAR7 (SEC66) in karyogamy during unisexual and opposite-sex mating. Eukaryot Cell 11:783–794PubMedPubMedCentralCrossRefGoogle Scholar
  228. Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, Bach J, Gredt M, Chapeland F (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag Sci 58:876–888PubMedCrossRefGoogle Scholar
  229. Li Z, Nielsen K (2017) Morphology changes in human fungal pathogens upon interaction with the host. J Fungi (Basel) 3:66CrossRefGoogle Scholar
  230. Li J, Katiyar SK, Edlind TD (1996) Site-directed mutagenesis of Saccharomyces cerevisiae beta-tubulin: interaction between residue 167 and benzimidazole compounds. FEBS Lett 385:7–10PubMedCrossRefGoogle Scholar
  231. Li CR, Wang Y-M, De Zheng X, Liang HY, Tang JCW, Wang Y (2005) The formin family protein CaBni1p has a role in cell polarity control during both yeast and hyphal growth in Candida albicans. J Cell Sci 118:2637–2648PubMedCrossRefGoogle Scholar
  232. Liakopoulos D, Kusch J, Grava S, Vogel J, Barral Y (2003) Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell 112:561–574PubMedCrossRefGoogle Scholar
  233. Lim J, Miller MG (1997) The role of the benomyl metabolite carbendazim in benomyl-induced testicular toxicity. Toxicol Appl Pharmacol 142:401–410PubMedCrossRefGoogle Scholar
  234. Lin TC, Gombos L, Neuner A, Sebastian D, Olsen JV, Hrle A, Benda C, Schiebel E (2011) Phosphorylation of the yeast γ-tubulin Tub4 regulates microtubule function. PLoS One 6:e19700PubMedPubMedCentralCrossRefGoogle Scholar
  235. Lin TC, Neuner A, Schlosser YT, Scharf AN, Weber L, Schiebel E (2014) Cell-cycle dependent phosphorylation of yeast pericentrin regulates γ-TuSC-mediated microtubule nucleation. elife 3:e02208PubMedPubMedCentralCrossRefGoogle Scholar
  236. Lin C, Schuster M, Guimaraes SC, Ashwin P, Schrader M, Metz J, Hacker C, Gurr SJ, Steinberg G (2016a) Active diffusion and microtubule-based transport oppose myosin forces to position organelles in cells. Nat Commun 7:11814PubMedPubMedCentralCrossRefGoogle Scholar
  237. Lin TC, Neuner A, Flemming D, Liu P, Chinen T, Jakle U, Arkowitz R, Schiebel E (2016b) MOZART1 and gamma-tubulin complex receptors are both required to turn gamma-TuSC into an active microtubule nucleation template. J Cell Biol 215:823–840PubMedPubMedCentralCrossRefGoogle Scholar
  238. Linder S, Schliwa M, Kube-Granderath E (1998) Expression of Reticulomyxa filosa alpha- and beta-tubulins in Escherichia coli yields soluble and partially correctly folded material. Gene 212:87–94PubMedCrossRefGoogle Scholar
  239. Liu K, Pan X, Han Y, Tang F, Yu Y (2012) Estimating the toxicity of the weak base carbendazim to the earthworm (Eisenia fetida) using in situ pore water concentrations in different soils. Sci Total Environ 438:26–32PubMedCrossRefGoogle Scholar
  240. Liu Y, Chen X, Jiang J, Hamada MS, Yin Y, Ma Z (2014) Detection and dynamics of different carbendazim-resistance conferring β-tubulin variants of Gibberella zeae collected from infected wheat heads and rice stubble in China. Pest Manag Sci 70:1228–1236PubMedCrossRefGoogle Scholar
  241. Liu C, Yao J, Yin J, Xue J, Zhang H (2018) Recombinant α- and β-tubulin from Echinococcus granulosus: expression, purification and polymerization. Parasite 25:62PubMedPubMedCentralCrossRefGoogle Scholar
  242. Lopez-Fanarraga M, Avila J, Guasch A, Coll M, Zabala JC (2001) Review: postchaperonin tubulin folding cofactors and their role in microtubule dynamics. J Struct Biol 135:219–229PubMedCrossRefGoogle Scholar
  243. Lüders J (2018) XMAP215 joins microtubule nucleation team. Nat Publ Group 20:508–510Google Scholar
  244. Lüders J, Patel UK, Stearns T (2006) GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat Cell Biol 8:137–147PubMedCrossRefGoogle Scholar
  245. Ludueña RF (1998) Multiple forms of tubulin: different gene products and covalent modifications. Int Rev Cytol 178:207–275PubMedCrossRefGoogle Scholar
  246. Lynch EM, Groocock LM, Borek WE, Sawin KE (2014) Activation of the γ-tubulin complex by the Mto1/2 complex. Curr Biol 24:896–903PubMedPubMedCentralCrossRefGoogle Scholar
  247. Ma Z, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot 24:853–863CrossRefGoogle Scholar
  248. MacDonald LM, Armson A, Thompson RC, Reynoldson JA (2001) Expression of Giardia duodenalis beta-tubulin as a soluble protein in Escherichia coli. Protein Expr Purif 22:25–30PubMedCrossRefGoogle Scholar
  249. MacDonald LM, Armson A, Thompson RC, Reynoldson JA (2003) Characterization of factors favoring the expression of soluble protozoan tubulin proteins in Escherichia coli. Protein Expr Purif 29:117–122PubMedCrossRefGoogle Scholar
  250. Maddox PS, Bloom KS, Salmon ED (2000) The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae. Nat Cell Biol 2:36–41PubMedPubMedCentralCrossRefGoogle Scholar
  251. Maekawa H, Schiebel E (2004) Cdk1-Clb4 controls the interaction of astral microtubule plus ends with subdomains of the daughter cell cortex. Genes Dev 18:1709–1724PubMedPubMedCentralCrossRefGoogle Scholar
  252. Maekawa H, Usui T, Knop M, Schiebel E (2003) Yeast Cdk1 translocates to the plus end of cytoplasmic microtubules to regulate bud cortex interactions. EMBO J 22:438–449PubMedPubMedCentralCrossRefGoogle Scholar
  253. Maekawa H, Neuner A, Rüthnick D, Schiebel E, Pereira G, Kaneko Y (2017) Polo-like kinase Cdc5 regulates Spc72 recruitment to spindle pole body in the methylotrophic yeast Ogataea polymorpha. elife 6:e24340PubMedPubMedCentralCrossRefGoogle Scholar
  254. Majumdar S, Kim T, Chen Z, Munyoki S, Tso SC, Brautigam CA, Rice LM (2018) An isolated CLASP TOG domain suppresses microtubule catastrophe and promotes rescue. Mol Biol Cell 29:1359–1375PubMedPubMedCentralCrossRefGoogle Scholar
  255. Manck R, Ishitsuka Y, Herrero S, Takeshita N, Nienhaus GU, Fischer R (2015) Genetic evidence for a microtubule-capture mechanism during polarised growth of Aspergillus nidulans. J Cell Sci 128:3569–3582PubMedCrossRefGoogle Scholar
  256. Manka SW, Moores CA (2018) Microtubule structure by cryo-EM: snapshots of dynamic instability. Essays Biochem 62:737–751PubMedPubMedCentralCrossRefGoogle Scholar
  257. Manning BD, Barrett JG, Wallace JA, Granok H, Snyder M (1999) Differential regulation of the Kar3p kinesin-related protein by two associated proteins, Cik1p and Vik1p. J Cell Biol 144:1219–1233PubMedPubMedCentralCrossRefGoogle Scholar
  258. Martin R, Walther A, Wendland J (2004) Deletion of the dynein heavy-chain gene DYN1 leads to aberrant nuclear positioning and defective hyphal development in Candida albicans. Eukaryot Cell 3:1574–1588PubMedPubMedCentralCrossRefGoogle Scholar
  259. Martin SG, McDonald WH, Yates JR, Chang F (2005) Tea4p links microtubule plus ends with the formin for 3p in the establishment of cell polarity. Dev Cell 8:479–491PubMedCrossRefGoogle Scholar
  260. Masuda H, Toda T (2016) Synergistic role of fission yeast Alp16GCP6 and Mzt1MOZART1 in γ-tubulin complex recruitment to mitotic spindle pole bodies and spindle assembly. Mol Biol Cell 27:1753–1763PubMedPubMedCentralCrossRefGoogle Scholar
  261. Masuda H, Mori R, Yukawa M, Toda T (2013) Fission yeast MOZART1/Mzt1 is an essential γ-tubulin complex component required for complex recruitment to the microtubule organizing center, but not its assembly. Mol Biol Cell 24:2894–2906PubMedPubMedCentralCrossRefGoogle Scholar
  262. Mata J, Nurse P (1997) tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 89:939–949PubMedCrossRefGoogle Scholar
  263. McCoy KM, Tubman ES, Claas A, Tank D, Clancy SA, O’Toole ET, Berman J, Odde DJ (2015) Physical limits on kinesin-5-mediated chromosome congression in the smallest mitotic spindles. Mol Biol Cell 26:3999–4014PubMedPubMedCentralCrossRefGoogle Scholar
  264. McDonald KL, O’Toole ET, Mastronarde DN, McIntosh JR (1992) Kinetochore microtubules in PTK cells. J Cell Biol 118:369–383PubMedCrossRefGoogle Scholar
  265. McIntosh JR, O’Toole E, Morgan G, Austin J, Ulyanov E, Ataullakhanov F, Gudimchuk N (2018) Microtubules grow by the addition of bent guanosine triphosphate tubulin to the tips of curved protofilaments. J Cell Biol 217:2691–2708PubMedPubMedCentralCrossRefGoogle Scholar
  266. Meadows JC, Messin LJ, Kamnev A, Lancaster TC, Balasubramanian MK, Cross RA, Millar JB (2018) Opposing kinesin complexes queue at plus tips to ensure microtubule catastrophe at cell ends. EMBO Rep 19:e46196PubMedPubMedCentralCrossRefGoogle Scholar
  267. Meluh PB, Rose MD (1990) KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell 60:1029–1041PubMedCrossRefGoogle Scholar
  268. Mieck C, Molodtsov MI, Drzewicka K, van der Vaart B, Litos G, Schmauss G, Vaziri A, Westermann S (2015) Non-catalytic motor domains enable processive movement and functional diversification of the kinesin-14 Kar3. elife 4:1161CrossRefGoogle Scholar
  269. Miller RK, Rose MD (1998) Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. J Cell Biol 140:377–390PubMedPubMedCentralCrossRefGoogle Scholar
  270. Miller RK, Matheos D, Rose MD (1999) The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J Cell Biol 144:963–975PubMedPubMedCentralCrossRefGoogle Scholar
  271. Minoura I, Hachikubo Y, Yamakita Y, Takazaki H, Ayukawa R, Uchimura S, Muto E (2013) Overexpression, purification, and functional analysis of recombinant human tubulin dimer. FEBS Lett 587:3450–3455PubMedCrossRefGoogle Scholar
  272. Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242PubMedCrossRefGoogle Scholar
  273. Mochizuki T (1998) Three-dimensional reconstruction of mitotic cells of Cryptococcus neoformans based on serial section electron microscopy. Jpn J Med Mycol 39:123–127CrossRefGoogle Scholar
  274. Moore JK, Cooper JA (2010) Coordinating mitosis with cell polarity: molecular motors at the cell cortex. Semin Cell Dev Biol 21:283–289PubMedPubMedCentralCrossRefGoogle Scholar
  275. Mori R, Toda T (2013) The dual role of fission yeast Tbc1/cofactor C orchestrates microtubule homeostasis in tubulin folding and acts as a GAP for GTPase Alp41/Arl2. Mol Biol Cell 24:1713–24, S1PubMedPubMedCentralCrossRefGoogle Scholar
  276. Moseley JB, Sagot I, Manning AL, Xu Y, Eck MJ, Pellman D, Goode BL (2004) A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol Biol Cell 15:896–907PubMedPubMedCentralCrossRefGoogle Scholar
  277. Mouriño-Pérez RR, Roberson RW, Bartnicki-Garcia S (2006) Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa. Fungal Genet Biol 43:389–400PubMedCrossRefPubMedCentralGoogle Scholar
  278. Mouriño-Pérez RR, Linacre-Rojas LP, Román-Gavilanes AI, Lew TK, Callejas-Negrete OA, Roberson RW, Freitag M (2013) MTB-3, a microtubule plus-end tracking protein (+TIP) of Neurospora crassa. PLoS One 8:e70655PubMedPubMedCentralCrossRefGoogle Scholar
  279. Mouriño-Pérez RR, Riquelme M, Callejas-Negrete OA, Galván-Mendoza JI (2016) Microtubules and associated molecular motors in Neurospora crassa. Mycologia 108:515–527PubMedCrossRefPubMedCentralGoogle Scholar
  280. Muller EG, Snydsman BE, Novik I, Hailey DW, Gestaut DR, Niemann CA, O’Toole ET, Giddings TH, Sundin BA, Davis TN (2005) The organization of the core proteins of the yeast spindle pole body. Mol Biol Cell 16:3341–3352PubMedPubMedCentralCrossRefGoogle Scholar
  281. Munguia B, Teixeira R, Veroli V, Melian E, Saldana J, Minteguiaga M, Senorale M, Marin M, Dominguez L (2017) Purification of native M. vogae and H. contortus tubulin by TOG affinity chromatography. Exp Parasitol 182:37–44PubMedCrossRefPubMedCentralGoogle Scholar
  282. Mustyatsa VV, Boyakhchyan AV, Ataullakhanov FI, Gudimchuk NB (2017) EB-family proteins: functions and microtubule interaction mechanisms. Biochemistry (Mosc) 82:791–802CrossRefGoogle Scholar
  283. Neff NF, Thomas JH, Grisafi P, Botstein D (1983) Isolation of the beta-tubulin gene from yeast and demonstration of its essential function in vivo. Cell 33:211–219PubMedCrossRefGoogle Scholar
  284. Nguyen T, Vinh DB, Crawford DK, Davis TN (1998) A genetic analysis of interactions with Spc110p reveals distinct functions of Spc97p and Spc98p, components of the yeast gamma-tubulin complex. Mol Biol Cell 9:2201–2216PubMedPubMedCentralCrossRefGoogle Scholar
  285. Niessing D, Jansen RP, Pohlmann T, Feldbrugge M (2018) mRNA transport in fungal top models. Wiley Interdiscip Rev RNA 9:e1453CrossRefGoogle Scholar
  286. Nieuwenhuis J, Brummelkamp TR (2018) The tubulin Detyrosination cycle: function and enzymes. Trends Cell Biol 29:80–92PubMedCrossRefGoogle Scholar
  287. Niki H (2014) Schizosaccharomyces japonicus: the fission yeast is a fusion of yeast and hyphae. Yeast 31:83–90PubMedCrossRefGoogle Scholar
  288. Nixon GL, McEntee L, Johnson A, Farrington N, Whalley S, Livermore J, Natal C, Washbourn G, Bibby J, Berry N, Lestner J, Truong M, Owen A, Lalloo D, Charles I, Hope W (2018) Repurposing and reformulation of the Antiparasitic agent Flubendazole for treatment of Cryptococcal meningoencephalitis, a neglected fungal disease. Antimicrob Agents Chemother 62:e01909–e01917PubMedPubMedCentralCrossRefGoogle Scholar
  289. Nogales E (2015) An electron microscopy journey in the study of microtubule structure and dynamics. Protein Sci 24:1912–1919PubMedPubMedCentralCrossRefGoogle Scholar
  290. Oakley CE, Oakley BR (1989) Identification of gamma-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338:662–664PubMedCrossRefGoogle Scholar
  291. Oakley BR, Paolillo V, Zheng Y (2015) γ-Tubulin complexes in microtubule nucleation and beyond. Mol Biol Cell 26:2957–2962PubMedPubMedCentralCrossRefGoogle Scholar
  292. Olmsted ZT, Riehlman TD, Branca CN, Colliver AG, Cruz LO, Paluh JL (2013) Kinesin-14 Pkl1 targets γ-tubulin for release from the γ-tubulin ring complex (γ-TuRC). Cell Cycle 12:842–848PubMedPubMedCentralCrossRefGoogle Scholar
  293. Olmsted ZT, Colliver AG, Riehlman TD, Paluh JL (2014) Kinesin-14 and kinesin-5 antagonistically regulate microtubule nucleation by γ-TuRC in yeast and human cells. Nat Commun 5:5339PubMedPubMedCentralCrossRefGoogle Scholar
  294. Oren I, Temiz O, Yalcin I, Sener E, Altanlar N (1999) Synthesis and antimicrobial activity of some novel 2,5- and/or 6-substituted benzoxazole and benzimidazole derivatives. Eur J Pharm Sci 7:153–160PubMedCrossRefGoogle Scholar
  295. O’Toole ET, Winey M, McIntosh JR (1999) High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell 10:2017–2031PubMedPubMedCentralCrossRefGoogle Scholar
  296. Oxberry ME, Geary TG, Winterrowd CA, Prichard RK (2001) Individual expression of recombinant alpha- and beta-tubulin from Haemonchus contortus: polymerization and drug effects. Protein Expr Purif 21:30–39PubMedCrossRefGoogle Scholar
  297. Ozdemir I, Temelli N, Gunal S, Demir S (2010) Gold(I) complexes of N-heterocyclic carbene ligands containing benzimidazole: synthesis and antimicrobial activity. Molecules 15:2203–2210PubMedPubMedCentralCrossRefGoogle Scholar
  298. Ozkay Y, Tunali Y, Karaca H, Isikdag I (2011) Antimicrobial activity of a new series of benzimidazole derivatives. Arch Pharm Res 34:1427–1435PubMedCrossRefGoogle Scholar
  299. Palmer RE, Sullivan DS, Huffaker T, Koshland D (1992) Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 119:583–593PubMedCrossRefGoogle Scholar
  300. Panse VG, Hardeland U, Werner T, Kuster B, Hurt E (2004) A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 279:41346–41351PubMedCrossRefGoogle Scholar
  301. Parker AL, Teo WS, Pandzic E, Vicente JJ, McCarroll JA, Wordeman L, Kavallaris M (2018) Beta-tubulin carboxy-terminal tails exhibit isotype-specific effects on microtubule dynamics in human gene-edited cells. Life Sci Alliance 1:e201800059PubMedPubMedCentralCrossRefGoogle Scholar
  302. Peñalva MA, Zhang J, Xiang X, Pantazopoulou A (2017) Transport of fungal RAB11 secretory vesicles involves myosin-5, dynein/dynactin/p25, and kinesin-1 and is independent of kinesin-3. Mol Biol Cell 28:947–961PubMedPubMedCentralCrossRefGoogle Scholar
  303. Pereira G, Knop M, Schiebel E (1998) Spc98p directs the yeast gamma-tubulin complex into the nucleus and is subject to cell cycle-dependent phosphorylation on the nuclear side of the spindle pole body. Mol Biol Cell 9:775–793PubMedPubMedCentralCrossRefGoogle Scholar
  304. Pereira G, Grueneberg U, Knop M, Schiebel E (1999) Interaction of the yeast gamma-tubulin complex-binding protein Spc72p with Kar1p is essential for microtubule function during karyogamy. EMBO J 18:4180–4195PubMedPubMedCentralCrossRefGoogle Scholar
  305. Pettit RK, Woyke T, Pon S, Cichacz ZA, Pettit GR, Herald CL (2005) In vitro and in vivo antifungal activities of the marine sponge constituent spongistatin. Med Mycol 43:453–463PubMedCrossRefGoogle Scholar
  306. Pisano C, Battistoni A, Antoccia A, Degrassi F, Tanzarella C (2000) Changes in microtubule organization after exposure to a benzimidazole derivative in Chinese hamster cells. Mutagenesis 15:507–515PubMedCrossRefGoogle Scholar
  307. Plamann M, Minke PF, Tinsley JH, Bruno KS (1994) Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J Cell Biol 127:139–149PubMedCrossRefGoogle Scholar
  308. Popchock AR, Tseng K-F, Wang P, Karplus PA, Xiang X, Qiu W (2017) The mitotic kinesin-14 KlpA contains a context-dependent directionality switch. Nat Commun 8:13999PubMedPubMedCentralCrossRefGoogle Scholar
  309. Pruyne D, Legesse-Miller A, Gao L, Dong Y, Bretscher A (2004) Mechanisms of polarized growth and organelle segregation in yeast. Annu Rev Cell Dev Biol 20:559–591PubMedCrossRefGoogle Scholar
  310. Qiu J, Huang T, Xu J, Bi C, Chen C, Zhou M (2012) Beta-Tubulins in Gibberella zeae: their characterization and contribution to carbendazim resistance. Pest Manag Sci 68:1191–1198PubMedCrossRefGoogle Scholar
  311. Qiu R, Zhang J, Xiang X (2018) p25 of the dynactin complex plays a dual role in cargo binding and dynactin regulation. J Biol Chem 293:15606–15619PubMedCrossRefGoogle Scholar
  312. Radcliffe PA, Hirata D, Vardy L, Toda T (1999) Functional dissection and hierarchy of tubulin-folding cofactor homologues in fission yeast [In Process Citation]. Mol Biol Cell 10:2987–3001PubMedPubMedCentralCrossRefGoogle Scholar
  313. Radcliffe PA, Garcia MA, Toda T (2000) The cofactor-dependent pathways for alpha- and beta-tubulins in microtubule biogenesis are functionally different in fission yeast. Genetics 156:93–103PubMedPubMedCentralGoogle Scholar
  314. Richards KL, Anders KR, Nogales E, Schwartz K, Downing KH, Botstein D (2000) Structure-function relationships in yeast tubulins. Mol Biol Cell 11:1887–1903PubMedPubMedCentralCrossRefGoogle Scholar
  315. Riquelme M, Fischer R, Bartnicki-García S (2003) Apical growth and mitosis are independent processes in Aspergillus nidulans. Protoplasma 222:211–215PubMedCrossRefGoogle Scholar
  316. Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B, Castro-Longoria E, Free SJ, Fleissner A, Freitag M, Lew RR, Mouriño-Pérez R, Plamann M, Rasmussen C, Richthammer C, Roberson RW, Sanchez-Leon E, Seiler S, Watters MK (2011) Architecture and development of the Neurospora crassa hypha – a model cell for polarized growth. Fungal Biol 115:446–474PubMedCrossRefGoogle Scholar
  317. Riquelme M, Aguirre J, Bartnicki-Garcia S, Braus GH, Feldbrügge M, Fleig U, Hansberg W, Herrera-Estrella A, Kämper J, Kück U, Mouriño-Pérez RR, Takeshita N, Fischer R (2018) Fungal morphogenesis, from the polarized growth of hyphae to complex reproduction and infection structures. Microbiol Mol Biol Rev 82:e00068–e00017PubMedPubMedCentralCrossRefGoogle Scholar
  318. Rischitor PE, Konzack S, Fischer R (2004) The Kip3-like kinesin KipB moves along microtubules and determines spindle position during synchronized mitoses in Aspergillus nidulans hyphae. Eukaryot Cell 3:632–645PubMedPubMedCentralCrossRefGoogle Scholar
  319. Roll-Mecak A (2018) How cells exploit tubulin diversity to build functional cellular microtubule mosaics. Curr Opin Cell Biol 56:102–108PubMedCrossRefGoogle Scholar
  320. Rombke J, Garcia MV, Scheffczyk A (2007) Effects of the fungicide benomyl on earthworms in laboratory tests under tropical and temperate conditions. Arch Environ Contam Toxicol 53:590–598PubMedCrossRefGoogle Scholar
  321. Roostalu J, Surrey T (2017) Microtubule nucleation: beyond the template. Nat Rev Mol Cell Biol 18:702–710PubMedCrossRefGoogle Scholar
  322. Roostalu J, Hentrich C, Bieling P, Telley IA, Schiebel E, Surrey T (2011) Directional switching of the kinesin Cin8 through motor coupling. Science 332:94–99PubMedCrossRefGoogle Scholar
  323. Roostalu J, Cade NI, Surrey T (2015) Complementary activities of TPX2 and chTOG constitute an efficient importin-regulated microtubule nucleation module. Nat Publ Group 17:1422–1434Google Scholar
  324. Rosenberg JA, Tomlin GC, McDonald WH, Snydsman BE, Muller EG, Yates JR, Gould KL (2006) Ppc89 links multiple proteins, including the septation initiation network, to the core of the fission yeast spindle-pole body. Mol Biol Cell 17:3793–3805PubMedPubMedCentralCrossRefGoogle Scholar
  325. Rosselló CA, Lindström L, Eklund G, Corvaisier M, Kristensson MA (2018) γ-Tubulinγ-tubulin interactions as the basis for the formation of a meshwork. Int J Mol Sci 19:3245PubMedCentralCrossRefPubMedGoogle Scholar
  326. Rout MP, Kilmartin JV (1990) Components of the yeast spindle and spindle pole body. J Cell Biol 111:1913–1927PubMedCrossRefGoogle Scholar
  327. Routh MM, Raut JS, Karuppayil SM (2011) Dual properties of anticancer agents: an exploratory study on the in vitro anti-Candida properties of thirty drugs. Chemotherapy 57:372–380PubMedCrossRefGoogle Scholar
  328. Rüthnick D, Schiebel E (2016) Duplication of the yeast spindle pole body once per cell cycle. Mol Cell Biol 36:1324–1331PubMedPubMedCentralCrossRefGoogle Scholar
  329. Sadoul K, Khochbin S (2016) The growing landscape of tubulin acetylation: lysine 40 and many more. Biochem J 473:1859–1868PubMedCrossRefGoogle Scholar
  330. Sage CR, Davis AS, Dougherty CA, Sullivan K, Farrell KW (1995) Beta-Tubulin mutation suppresses microtubule dynamics in vitro and slows mitosis in vivo. Cell Motil Cytoskeleton 30:285–300PubMedCrossRefGoogle Scholar
  331. Sagolla MJ, Uzawa S, Cande WZ (2003) Individual microtubule dynamics contribute to the function of mitotic and cytoplasmic arrays in fission yeast. J Cell Sci 116:4891–4903PubMedCrossRefGoogle Scholar
  332. Saito TT, Okuzaki D, Nojima H (2006) Mcp5, a meiotic cell cortex protein, is required for nuclear movement mediated by dynein and microtubules in fission yeast. J Cell Biol 173:27–33PubMedPubMedCentralCrossRefGoogle Scholar
  333. Salogiannis J, Reck-Peterson SL (2017) Hitchhiking: a non-canonical mode of microtubule-based transport. Trends Cell Biol 27:141–150PubMedCrossRefGoogle Scholar
  334. Samejima I, Miller VJ, Groocock LM, Sawin KE (2008) Two distinct regions of Mto1 are required for normal microtubule nucleation and efficient association with the gamma-tubulin complex in vivo. J Cell Sci 121:3971–3980PubMedPubMedCentralCrossRefGoogle Scholar
  335. Samejima I, Miller VJ, Rincon SA, Sawin KE (2010) Fission yeast Mto1 regulates diversity of cytoplasmic microtubule organizing centers. Curr Biol 20:1959–1965PubMedPubMedCentralCrossRefGoogle Scholar
  336. Sampson K, Heath IB (2005) The dynamic behaviour of microtubules and their contributions to hyphal tip growth in Aspergillus nidulans. Microbiology 151:1543–1555PubMedCrossRefGoogle Scholar
  337. Sanchez AD, Feldman JL (2016) Microtubule-organizing centers: from the centrosome to non-centrosomal sites. Curr Opin Cell Biol 44:93–101PubMedPubMedCentralCrossRefGoogle Scholar
  338. Sanchez-Perez I, Renwick SJ, Crawley K, Karig I, Buck V, Meadows JC, Franco-Sanchez A, Fleig U, Toda T, Millar JBA (2005) The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J 24:2931–2943PubMedPubMedCentralCrossRefGoogle Scholar
  339. Saunders WS, Hoyt MA (1992) Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell 70:451–458PubMedCrossRefGoogle Scholar
  340. Sawin KE, Tran PT (2006) Cytoplasmic microtubule organization in fission yeast. Yeast 23:1001–1014PubMedPubMedCentralCrossRefGoogle Scholar
  341. Sawin KE, Lourenço PCC, Snaith HA (2004) Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr Biol 14:763–775PubMedCrossRefGoogle Scholar
  342. Schaerer F, Morgan G, Winey M, Philippsen P (2001) Cnm67p is a spacer protein of the Saccharomyces cerevisiae spindle pole body outer plaque. Mol Biol Cell 12:2519–2533PubMedPubMedCentralCrossRefGoogle Scholar
  343. Schatz PJ, Solomon F, Botstein D (1986a) Genetically essential and nonessential alpha-tubulin genes specify functionally interchangeable proteins. Mol Cell Biol 6:3722–3733PubMedPubMedCentralCrossRefGoogle Scholar
  344. Schatz PJ, Pillus L, Grisafi P, Solomon F, Botstein D (1986b) Two functional alpha-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins. Mol Cell Biol 6:3711–3721PubMedPubMedCentralCrossRefGoogle Scholar
  345. Schatz PJ, Georges GE, Solomon F, Botstein D (1987) Insertions of up to 17 amino acids into a region of alpha-tubulin do not disrupt function in vivo. Mol Cell Biol 7:3799–3805PubMedPubMedCentralCrossRefGoogle Scholar
  346. Scheffler K, Minnes R, Fraisier V, Paoletti A, Tran PT (2015) Microtubule minus end motors kinesin-14 and dynein drive nuclear congression in parallel pathways. J Cell Biol 209:47–58PubMedPubMedCentralCrossRefGoogle Scholar
  347. Schmidt A (2000) Yeast infections in humans with special emphasis on Malassezia furfur and infections caused by “rare” yeast species. In: Ernst JF, Schmidt A (eds) Dimorphism in human pathogenic and apathogenic yeasts. Karger, Basel, pp 36–53CrossRefGoogle Scholar
  348. Schoch CL, Aist JR, Yoder OC, Gillian Turgeon B (2003) A complete inventory of fungal kinesins in representative filamentous ascomycetes. Fungal Genet Biol 39:1–15PubMedCrossRefGoogle Scholar
  349. Schramm C, Elliott S, Shevchenko A, Schiebel E (2000) The Bbp1p-Mps2p complex connects the SPB to the nuclear envelope and is essential for SPB duplication. EMBO J 19:421–433PubMedPubMedCentralCrossRefGoogle Scholar
  350. Schuster M, Kilaru S, Fink G, Collemare J, Roger Y, Steinberg G (2011) Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array. Mol Biol Cell 22:3645–3657PubMedPubMedCentralCrossRefGoogle Scholar
  351. Schuster M, Treitschke S, Kilaru S, Molloy J, Harmer NJ, Steinberg G (2012) Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J 31:214–227PubMedCrossRefGoogle Scholar
  352. Schweiggert J, Stevermann L, Panigada D, Kammerer D, Liakopoulos D (2016) Regulation of a spindle positioning factor at kinetochores by SUMO-targeted ubiquitin ligases. Dev Cell 36:415–427PubMedCrossRefGoogle Scholar
  353. Segal M, Clarke DJ, Maddox P, Salmon ED, Bloom K, Reed SI (2000) Coordinated spindle assembly and orientation requires Clb5p-dependent kinase in budding yeast. J Cell Biol 148:441–452PubMedPubMedCentralCrossRefGoogle Scholar
  354. Segal M, Bloom K, Reed SI (2002) Kar9p-independent microtubule capture at Bud6p cortical sites primes spindle polarity before bud emergence in Saccharomyces cerevisiae. Mol Biol Cell 13:4141–4155PubMedPubMedCentralCrossRefGoogle Scholar
  355. Seidel C, Moreno-Velásquez SD, Riquelme M, Fischer R (2013) Neurospora crassa NKIN2, a kinesin-3 motor, transports early endosomes and is required for polarized growth. Eukaryot Cell 12:1020–1032PubMedPubMedCentralCrossRefGoogle Scholar
  356. Shapira O, Goldstein A, Al-Bassam J, Gheber L (2017) A potential physiological role for bi-directional motility and motor clustering of mitotic kinesin-5 Cin8 in yeast mitosis. J Cell Sci 130:725–734PubMedPubMedCentralCrossRefGoogle Scholar
  357. Shaw SL, Yeh E, Maddox P, Salmon ED, Bloom K (1997) Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J Cell Biol 139:985–994PubMedPubMedCentralCrossRefGoogle Scholar
  358. She Z-Y, Yang W-X (2017) Molecular mechanisms of kinesin-14 motors in spindle assembly and chromosome segregation. J Cell Sci 130:2097–2110PubMedCrossRefGoogle Scholar
  359. Sheeman B, Carvalho P, Sagot I, Geiser J, Kho D, Hoyt MA, Pellman D (2003) Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning. Curr Biol 13:364–372PubMedCrossRefGoogle Scholar
  360. Shen J, Li T, Niu X, Liu W, Zheng S, Wang J, Wang F, Cao X, Yao X, Zheng F, Fu C (2019) The J-domain co-chaperone Rsp1 interacts with Mto1 to organize non-centrosomal microtubule assembly. Mol Biol Cell 30:256–267PubMedPubMedCentralCrossRefGoogle Scholar
  361. Silva WP, Soares RBA, Jesuino RSA, Izacc SMS, Felipe MSS, Soares CMA (2001) Expression of alpha tubulin during the dimorphic transition of Paracoccidioides brasiliensis. Med Mycol 39:457–462PubMedCrossRefGoogle Scholar
  362. Simanis V (2015) Pombe’s thirteen - control of fission yeast cell division by the septation initiation network. J Cell Sci 128:1465–1474PubMedCrossRefGoogle Scholar
  363. Sipiczki M (2000) Where does fission yeast sit on the tree of life. Genome Biol 1:REVIEWS1011PubMedPubMedCentralCrossRefGoogle Scholar
  364. Sirajuddin M, Rice LM, Vale RD (2014) Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat Cell Biol 16:335–344PubMedPubMedCentralCrossRefGoogle Scholar
  365. Smith HA, Gorman JW, Koltin Y, Gorman JA (1990) Functional expression of the Candida albicans beta-tubulin gene in Saccharomyces cerevisiae. Gene 90:115–123PubMedCrossRefGoogle Scholar
  366. Song Y, Brady ST (2015) Post-translational modifications of tubulin: pathways to functional diversity of microtubules. Trends Cell Biol 25:125–136PubMedCrossRefGoogle Scholar
  367. Sorour J, Larink O (2001) Toxic effects of benomyl on the ultrastructure during spermatogenesis of the earthworm Eisenia fetida. Ecotoxicol Environ Saf 50:180–188PubMedCrossRefGoogle Scholar
  368. Souès S, Adams IR (1998) SPC72: a spindle pole component required for spindle orientation in the yeast Saccharomyces cerevisiae. J Cell Sci 111:2809–2818PubMedGoogle Scholar
  369. Spang A, Geissler S, Grein K, Schiebel E (1996) Gamma-Tubulin-like Tub4p of Saccharomyces cerevisiae is associated with the spindle pole body substructures that organize microtubules and is required for mitotic spindle formation. J Cell Biol 134:429–441PubMedCrossRefGoogle Scholar
  370. Sproul LR, Anderson DJ, Mackey AT, Saunders WS, Gilbert SP (2005) Cik1 targets the minus-end kinesin depolymerase kar3 to microtubule plus ends. Curr Biol 15:1420–1427PubMedPubMedCentralCrossRefGoogle Scholar
  371. Steinberg G, Fuchs U (2004) The role of microtubules in cellular organization and endocytosis in the plant pathogen Ustilago maydis. J Microsc 214:114–123PubMedCrossRefGoogle Scholar
  372. Steinberg G, Schuster M, Theisen U, Kilaru S, Forge A, Martin-Urdiroz M (2012) Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport. J Cell Biol 198:343–355PubMedPubMedCentralCrossRefGoogle Scholar
  373. Stewart AJ, Salazar T, Welles EG (2008) Systemic and pulmonary fungal infections. Compendium on Continuing Education for the Practicing Veterinarian Equine Edition 3:260–272Google Scholar
  374. Stojkovic M, Zwahlen M, Teggi A, Vutova K, Cretu CM, Virdone R, Nicolaidou P, Cobanoglu N, Junghanss T (2009) Treatment response of cystic echinococcosis to benzimidazoles: a systematic review. PLoS Negl Trop Dis 3:e524PubMedPubMedCentralCrossRefGoogle Scholar
  375. Straube A, Brill M, Oakley BR, Horio T, Steinberg G (2003) Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol Biol Cell 14:642–657PubMedPubMedCentralCrossRefGoogle Scholar
  376. Stringer A, Wright MA (1976) The toxicity of benomyl and some related 2-substituted benzimidazoles to the earthworm Lumbricus terrestris. Pestic Sci 7:459–464CrossRefGoogle Scholar
  377. Suelmann R, Sievers N, Fischer R (1997) Nuclear traffic in fungal hyphae: in vivo study of nuclear migration and positioning in Aspergillus nidulans. Mol Microbiol 25:757–769PubMedCrossRefGoogle Scholar
  378. Syrovatkina V, Tran PT (2015) Loss of kinesin-14 results in aneuploidy via kinesin-5-dependent microtubule protrusions leading to chromosome cut. Nat Commun 6:7322PubMedPubMedCentralCrossRefGoogle Scholar
  379. Takeshita N, Higashitsuji Y, Konzack S, Fischer R (2008) Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 19:339–351PubMedPubMedCentralCrossRefGoogle Scholar
  380. Takeshita N, Mania D, Herrero S, Ishitsuka Y, Nienhaus GU, Podolski M, Howard J, Fischer R (2013) The cell-end marker TeaA and the microtubule polymerase AlpA contribute to microtubule guidance at the hyphal tip cortex of Aspergillus nidulans to provide polarity maintenance. J Cell Sci 126:5400–5411PubMedCrossRefGoogle Scholar
  381. Takeshita N, Manck R, Grün N, de Vega SH, Fischer R (2014) Interdependence of the actin and the microtubule cytoskeleton during fungal growth. Curr Opin Microbiol 20:34–41PubMedCrossRefGoogle Scholar
  382. Tanaka K, Kanbe T (1986) Mitosis in the fission yeast Schizosaccharomyces pombe as revealed by freeze-substitution electron microscopy. J Cell Sci 80:253–268PubMedGoogle Scholar
  383. Tang X, Punch JJ, Lee W-L (2009) A CAAX motif can compensate for the PH domain of Num1 for cortical dynein attachment. Cell Cycle 8:3182–3190PubMedPubMedCentralCrossRefGoogle Scholar
  384. Tatebe H, Shimada K, Uzawa S, Morigasaki S, Shiozaki K (2005) Wsh3/Tea4 is a novel cell-end factor essential for bipolar distribution of Tea1 and protects cell polarity under environmental stress in S. pombe. Curr Biol 15:1006–1015PubMedCrossRefGoogle Scholar
  385. Tay YD, Leda M, Goryachev AB, Sawin KE (2018) Local and global Cdc42 guanine nucleotide exchange factors for fission yeast cell polarity are coordinated by microtubules and the Tea1-Tea4-Pom1 axis. J Cell Sci 131:jcs216580PubMedPubMedCentralCrossRefGoogle Scholar
  386. Ten Hoopen R, Cepeda-García C, Fernández-Arruti R, Juanes MA, Delgehyr N, Segal M (2012) Mechanism for astral microtubule capture by cortical Bud6p priming spindle polarity in S. cerevisiae. Curr Biol 22:1075–1083PubMedCrossRefGoogle Scholar
  387. Thakur J, Sanyal K (2011) The essentiality of the fungus-specific Dam1 complex is correlated with a one-kinetochore-one-microtubule interaction present throughout the cell cycle, independent of the nature of a centromere. Eukaryot Cell 10:1295–1305PubMedPubMedCentralCrossRefGoogle Scholar
  388. Thawani A, Kadzik RS, Petry S (2018) XMAP215 is a microtubule nucleation factor that functions synergistically with the γ-tubulin ring complex. Nat Publ Group 20:575–585Google Scholar
  389. Thomas GE, Renjith MR, Manna TK (2017) Kinetochore-microtubule interactions in chromosome segregation: lessons from yeast and mammalian cells. Biochem J 474:3559–3577PubMedCrossRefGoogle Scholar
  390. Ti SC, Alushin GM, Kapoor TM (2018) Human beta-tubulin isotypes can regulate microtubule protofilament number and stability. Dev Cell 47:175PubMedCrossRefGoogle Scholar
  391. Toda T, Adachi Y, Hiraoka Y, Yanagida M (1984) Identification of the pleiotropic cell division cycle gene NDA2 as one of two different alpha-tubulin genes in Schizosaccharomyces pombe. Cell 37:233–242PubMedCrossRefGoogle Scholar
  392. Tovey CA, Conduit PT (2018) Microtubule nucleation by γ-tubulin complexes and beyond. Essays Biochem 91:EBC20180028Google Scholar
  393. Tran PT, Marsh L, Doye V, Inoué S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411PubMedPubMedCentralCrossRefGoogle Scholar
  394. Troxell CL, Sweezy MA, West RR, Reed KD, Carson BD, Pidoux AL, Cande WZ, McIntosh JR (2001) pkl1(+)and klp2(+): two kinesins of the Kar3 subfamily in fission yeast perform different functions in both mitosis and meiosis. Mol Biol Cell 12:3476–3488PubMedPubMedCentralCrossRefGoogle Scholar
  395. Tuncbilek M, Kiper T, Altanlar N (2009) Synthesis and in vitro antimicrobial activity of some novel substituted benzimidazole derivatives having potent activity against MRSA. Eur J Med Chem 44:1024–1033PubMedCrossRefPubMedCentralGoogle Scholar
  396. Uchida M, Mouriño-Pérez RR, Freitag M, Bartnicki-Garcia S, Roberson RW (2008) Microtubule dynamics and the role of molecular motors in Neurospora crassa. Fungal Genet Biol 45:683–692PubMedCrossRefPubMedCentralGoogle Scholar
  397. Uchimura S, Oguchi Y, Katsuki M, Usui T, Osada H, Nikawa J, Ishiwata S, Muto E (2006) Identification of a strong binding site for kinesin on the microtubule using mutant analysis of tubulin. EMBO J 25:5932–5941PubMedPubMedCentralCrossRefGoogle Scholar
  398. Uchimura S, Oguchi Y, Hachikubo Y, Ishiwata S, Muto E (2010) Key residues on microtubule responsible for activation of kinesin ATPase. EMBO J 29:1167–1175PubMedPubMedCentralCrossRefGoogle Scholar
  399. Uchimura S, Fujii T, Takazaki H, Ayukawa R, Nishikawa Y, Minoura I, Hachikubo Y, Kurisu G, Sutoh K, Kon T, Namba K, Muto E (2015) A flipped ion pair at the dynein-microtubule interface is critical for dynein motility and ATPase activation. J Cell Biol 208:211–222PubMedPubMedCentralCrossRefGoogle Scholar
  400. Umesono K, Toda T, Hayashi S, Yanagida M (1983) Cell division cycle genes nda2 and nda3 of the fission yeast Schizosaccharomyces pombe control microtubular organization and sensitivity to anti-mitotic benzimidazole compounds. J Mol Biol 168:271–284PubMedCrossRefGoogle Scholar
  401. Usui T, Maekawa H, Pereira G, Schiebel E (2003) The XMAP215 homologue Stu2 at yeast spindle pole bodies regulates microtubule dynamics and anchorage. EMBO J 22:4779–4793PubMedPubMedCentralCrossRefGoogle Scholar
  402. Vela-Corcia D, Romero D, de Vicente A, Perez-Garcia A (2018) Analysis of beta-tubulin-carbendazim interaction reveals that binding site for MBC fungicides does not include residues involved in fungicide resistance. Sci Rep 8:7161PubMedPubMedCentralCrossRefGoogle Scholar
  403. Vemu A, Atherton J, Spector JO, Moores CA, Roll-Mecak A (2017) Tubulin isoform composition tunes microtubule dynamics. Mol Biol Cell 28:3564–3572PubMedPubMedCentralCrossRefGoogle Scholar
  404. Venkatram S, Tasto JJ, Feoktistova A, Jennings JL, Link AJ, Gould KL (2004) Identification and characterization of two novel proteins affecting fission yeast gamma-tubulin complex function. Mol Biol Cell 15:2287–2301PubMedPubMedCentralCrossRefGoogle Scholar
  405. Venkatram S, Jennings JL, Link A, Gould KL (2005) Mto2p, a novel fission yeast protein required for cytoplasmic microtubule organization and anchoring of the cytokinetic actin ring. Mol Biol Cell 16:3052–3063PubMedPubMedCentralCrossRefGoogle Scholar
  406. Vogel J, Drapkin B, Oomen J, Beach D, Bloom K, Snyder M (2001) Phosphorylation of gamma-tubulin regulates microtubule organization in budding yeast. Dev Cell 1:621–631PubMedCrossRefGoogle Scholar
  407. von Loeffelholz O, Venables NA, Drummond DR, Katsuki M, Cross R, Moores CA (2017) Nucleotide- and Mal3-dependent changes in fission yeast microtubules suggest a structural plasticity view of dynamics. Nat Commun 8:2110CrossRefGoogle Scholar
  408. von Loeffelholz O, Pena A, Drummond DR, Cross R, Moores CA (2019) 4.5Å Cryo-EM structure of yeast Kinesin-5-microtubule complex reveals a distinct binding footprint and mechanism of drug resistance. J Mol Biol 431:864–872CrossRefGoogle Scholar
  409. Walker RA, O’Brien ET, Pryer NK, Soboeiro MF, Voter WA, Erickson HP, Salmon ED (1988) Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol 107:1437–1448PubMedCrossRefGoogle Scholar
  410. Wasserstrom L, Lengeler KB, Walther A, Wendland J (2013) Molecular determinants of sporulation in Ashbya gossypii. Genetics 195:87–99PubMedPubMedCentralCrossRefGoogle Scholar
  411. Wedlich-Söldner R, Straube A, Friedrich MW, Steinberg G (2002) A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J 21:2946–2957PubMedPubMedCentralCrossRefGoogle Scholar
  412. Weinstein B, Solomon F (1990) Phenotypic consequences of tubulin overproduction in Saccharomyces cerevisiae: differences between alpha-tubulin and beta-tubulin. Mol Cell Biol 10:5295–5304PubMedPubMedCentralCrossRefGoogle Scholar
  413. Westermann S, Avila-Sakar A, Wang H-W, Niederstrasser H, Wong J, Drubin DG, Nogales E, Barnes G (2005) Formation of a dynamic kinetochore- microtubule interface through assembly of the Dam1 ring complex. Mol Cell 17:277–290PubMedCrossRefGoogle Scholar
  414. Widlund PO, Podolski M, Reber S, Alper J, Storch M, Hyman AA, Howard J, Drechsel DN (2012) One-step purification of assembly-competent tubulin from diverse eukaryotic sources. Mol Biol Cell 23:4393–4401PubMedPubMedCentralCrossRefGoogle Scholar
  415. Winey M, Bloom K (2012) Mitotic spindle form and function. Genetics 190:1197–1224PubMedPubMedCentralCrossRefGoogle Scholar
  416. Winey M, Mamay CL, O’Toole ET, Mastronarde DN, Giddings TH, McDonald KL, McIntosh JR (1995) Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J Cell Biol 129:1601–1615PubMedCrossRefGoogle Scholar
  417. Wloga D, Joachimiak E, Fabczak H (2017) Tubulin post-translational modifications and microtubule dynamics. Int J Mol Sci 18:2207PubMedCentralCrossRefPubMedGoogle Scholar
  418. Wohlschlegel JA, Johnson ES, Reed SI, Yates JR (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 279:45662–45668PubMedCrossRefGoogle Scholar
  419. Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713PubMedCrossRefGoogle Scholar
  420. Wolff J (2009) Plasma membrane tubulin. Biochim Biophys Acta 1788:1415–1433PubMedCrossRefGoogle Scholar
  421. Woodruff JB, Ferreira Gomes B, Widlund PO, Mahamid J, Honigmann A, Hyman AA (2017) The centrosome is a selective condensate that nucleates microtubules by concentrating tubulin. Cell 169:1066–1077PubMedCrossRefGoogle Scholar
  422. Woyke T, Pettit GR, Winkelmann G, Pettit RK (2001) In vitro activities and postantifungal effects of the potent dolastatin 10 derivative auristatin PHE. Antimicrob Agents Chemother 45:3580–3584PubMedPubMedCentralCrossRefGoogle Scholar
  423. Xiang X (2018) Nuclear movement in fungi. Semin Cell Dev Biol 82:3–16PubMedCrossRefGoogle Scholar
  424. Xiang X, Fischer R (2004) Nuclear migration and positioning in filamentous fungi. Fungal Genet Biol 41:411–419PubMedCrossRefGoogle Scholar
  425. Xiang X, Beckwith SM, Morris NR (1994) Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc Natl Acad Sci 91:2100–2104PubMedCrossRefGoogle Scholar
  426. Xiang X, Roghi C, Morris NR (1995) Characterization and localization of the cytoplasmic dynein heavy chain in Aspergillus nidulans. Proc Natl Acad Sci 92:9890–9894PubMedCrossRefGoogle Scholar
  427. Xiang X, Han G, Winkelmann DA, Zuo W, Morris NR (2000) Dynamics of cytoplasmic dynein in living cells and the effect of a mutation in the dynactin complex actin-related protein Arp1. Curr Biol 10:603–606PubMedCrossRefGoogle Scholar
  428. Xiong Y, Oakley BR (2009) In vivo analysis of the functions of gamma-tubulin-complex proteins. J Cell Sci 122:4218–4227PubMedPubMedCentralCrossRefGoogle Scholar
  429. Xu D, Jiang B, Ketela T, Lemieux S, Veillette K, Martel N, Davison J, Sillaots S, Trosok S, Bachewich C, Bussey H, Youngman P, Roemer T (2007) Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathog 3:e92PubMedPubMedCentralCrossRefGoogle Scholar
  430. Yamaguchi M, Biswas SK, Suzuki Y, Furukawa H, Sameshima M, Takeo K (2002) The spindle pole body duplicates in early G1 phase in the pathogenic yeast Exophiala dermatitidis: an ultrastructural study. Exp Cell Res 279:71–79PubMedCrossRefGoogle Scholar
  431. Yamaguchi M, Biswas SK, Ohkusu M, Takeo K (2009) Dynamics of the spindle pole body of the pathogenic yeast Cryptococcus neoformans examined by freeze-substitution electron microscopy. FEMS Microbiol Lett 296:257–265PubMedCrossRefGoogle Scholar
  432. Yamamoto M (1980) Genetic analysis of resistant mutants to antimitotic benzimidazole compounds in Schizosaccharomyces pombe. Mol Gen Genet 180:231–234PubMedCrossRefGoogle Scholar
  433. Yamamoto A, Hiraoka Y (2003) Cytoplasmic dynein in fungi: insights from nuclear migration. J Cell Sci 116:4501–4512PubMedCrossRefGoogle Scholar
  434. Yamashita A, Yamamoto M (2006) Fission yeast Num1p is a cortical factor anchoring dynein and is essential for the horse-tail nuclear movement during meiotic prophase. Genetics 173:1187–1196PubMedPubMedCentralCrossRefGoogle Scholar
  435. Yanagida M (1987) Yeast tubulin genes. Microbiol Sci 4:115–118PubMedGoogle Scholar
  436. Yao X, Zhang J, Zhou H, Wang E, Xiang X (2012) In vivo roles of the basic domain of dynactin p150 in microtubule plus-end tracking and dynein function. Traffic (Copenhagen, Denmark) 13:375–387CrossRefGoogle Scholar
  437. Yenjerla M, Cox C, Wilson L, Jordan MA (2009) Carbendazim inhibits cancer cell proliferation by suppressing microtubule dynamics. J Pharmacol Exp Ther 328:390–398PubMedCrossRefGoogle Scholar
  438. Yin H, Pruyne D, Huffaker TC, Bretscher A (2000) Myosin V orientates the mitotic spindle in yeast. Nature 406:1013–1015PubMedCrossRefGoogle Scholar
  439. Yokoyama K, Kaji H, Nishimura K, Miyaji M (1990) The role of microfilaments and microtubules in apical growth and dimorphism of Candida albicans. J Gen Microbiol 136:1067–1075PubMedCrossRefGoogle Scholar
  440. Yoon Y, Oakley BR (1995) Purification and characterization of assembly-competent tubulin from Aspergillus nidulans. Biochemistry 34:6373–6381PubMedCrossRefGoogle Scholar
  441. Yu I, Garnham CP, Roll-Mecak A (2015) Writing and Reading the tubulin code. J Biol Chem 290:17163–17172PubMedPubMedCentralCrossRefGoogle Scholar
  442. Zekert N, Fischer R (2009) The Aspergillus nidulans kinesin-3 UncA motor moves vesicles along a subpopulation of microtubules. Mol Biol Cell 20:673–684PubMedPubMedCentralCrossRefGoogle Scholar
  443. Zekert N, Veith D, Fischer R (2010) Interaction of the Aspergillus nidulans microtubule-organizing center (MTOC) component ApsB with gamma-tubulin and evidence for a role of a subclass of peroxisomes in the formation of septal MTOCs. Eukaryot Cell 9:795–805PubMedPubMedCentralCrossRefGoogle Scholar
  444. Zhang J, Li S, Fischer R, Xiang X (2003) Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol Biol Cell 14:1479–1488PubMedPubMedCentralCrossRefGoogle Scholar
  445. Zhang R, Alushin GM, Brown A, Nogales E (2015) Mechanistic origin of microtubule dynamic instability and its modulation by EB proteins. Cell 162:849–859PubMedPubMedCentralCrossRefGoogle Scholar
  446. Zhang Y, Gao X, Manck R, Schmid M, Osmani AH, Osmani SA, Takeshita N, Fischer R (2017) Microtubule-organizing centers of Aspergillus nidulans are anchored at septa by a disordered protein. Mol Microbiol 106:285–303PubMedCrossRefGoogle Scholar
  447. Zhang R, LaFrance B, Nogales E (2018) Separating the effects of nucleotide and EB binding on microtubule structure. Proc Natl Acad Sci U S A 115:E6191–E6200PubMedPubMedCentralCrossRefGoogle Scholar
  448. Zhao Z, Liu H, Luo Y, Zhou S, An L, Wang C, Jin Q, Zhou M, Xu J-R (2014) Molecular evolution and functional divergence of tubulin superfamily in the fungal tree of life. Sci Rep 4:6746PubMedPubMedCentralCrossRefGoogle Scholar
  449. Zuelke KA, Perreault SD (1995) Carbendazim (MBC) disrupts oocyte spindle function and induces aneuploidy in hamsters exposed during fertilization (meiosis II). Mol Reprod Dev 42:200–209PubMedCrossRefGoogle Scholar
  450. Zwetsloot AJ, Tut G, Straube A (2018) Measuring microtubule dynamics. Essays Biochem 62(6):725–735PubMedPubMedCentralCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Faculty of AgricultureKyushu UniversityFukuokaJapan

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