Advertisement

pp 1-30 | Cite as

α- and β-1,3-Glucan Synthesis and Remodeling

  • Johannes WagenerEmail author
  • Kristina Striegler
  • Nikola Wagener
Chapter
  • 18 Downloads
Part of the Current Topics in Microbiology and Immunology book series

Abstract

Glucans are characteristic and major constituents of fungal cell walls. Depending on the species, different glucan polysaccharides can be found. These differ in the linkage of the d-glucose monomers which can be either in α- or β-conformation and form 1,3, 1,4 or 1,6 O-glycosidic bonds. The linkages and polymer lengths define the physical properties of the glucan macromolecules, which may form a scaffold for other cell wall structures and influence the rigidity and elasticity of the wall. β-1,3-glucan is essential for the viability of many fungal pathogens. Therefore, the β-1,3-glucan synthase complex represents an excellent and primary target structure for antifungal drugs. Fungal cell wall β-glucan is also an important pathogen-associated molecular pattern (PAMP). To hide from innate immunity, many fungal pathogens depend on the synthesis of cell wall α-glucan, which functions as a stealth molecule to mask the β-glucans itself or links other masking structures to the cell wall. Here, we review the current knowledge about the biosynthetic machineries that synthesize β-1,3-glucan, β-1,6-glucan, and α-1,3-glucan. We summarize the discovery of the synthases, major regulatory traits, and the impact of glucan synthesis deficiencies on the fungal organisms. Despite all efforts, many aspects of glucan synthesis remain yet unresolved, keeping research directed toward cell wall biogenesis an exciting and continuously challenging topic.

References

  1. Aimanianda V, Clavaud C, Simenel C, Fontaine T, Delepierre M, Latgé J-P (2009) Cell wall beta-(1,6)-glucan of Saccharomyces cerevisiae: structural characterization and in situ synthesis. J Biol Chem 284:13401–13412Google Scholar
  2. Aimanianda V, Simenel C, Garnaud C, Clavaud C, Tada R, Barbin L, Mouyna I, Heddergott C, Popolo L, Ohya Y et al (2017) The dual activity responsible for the elongation and branching of β-(1,3)-glucan in the fungal cell wall. MBio 8Google Scholar
  3. Al-Aidroos K, Bussey H (1978) Chromosomal mutants of Saccharomyces cerevisiae affecting the cell wall binding site for killer factor. Can J Microbiol 24:228–237Google Scholar
  4. Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37:420–423Google Scholar
  5. Almyroudis NG, Sutton DA, Fothergill AW, Rinaldi MG, Kusne S (2007) In vitro susceptibilities of 217 clinical isolates of zygomycetes to conventional and new antifungal agents. Antimicrob Agents Chemother 51:2587–2590Google Scholar
  6. Arellano M, Durán A, Pérez P (1996) Rho 1 GTPase activates the (1-3)beta-d-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15:4584–4591Google Scholar
  7. Beauvais A, Bruneau JM, Mol PC, Buitrago MJ, Legrand R, Latgé JP (2001) Glucan synthase complex of Aspergillus fumigatus. J Bacteriol 183:2273–2279Google Scholar
  8. Beauvais A, Maubon D, Park S, Morelle W, Tanguy M, Huerre M, Perlin DS, Latgé JP (2005) Two alpha(1-3) glucan synthases with different functions in Aspergillus fumigatus. Appl Environ Microbiol 71:1531–1538Google Scholar
  9. Beauvais A, Bozza S, Kniemeyer O, Formosa C, Formosa C, Balloy V, Henry C, Roberson RW, Dague E, Chignard M et al (2013) Deletion of the α-(1,3)-glucan synthase genes induces a restructuring of the conidial cell wall responsible for the avirulence of Aspergillus fumigatus. PLoS Pathog 9:e1003716Google Scholar
  10. Beyda ND, Liao G, Endres BT, Lewis RE, Garey KW (2015) Innate inflammatory response and immunopharmacologic activity of micafungin, caspofungin, and voriconazole against wild-type and FKS mutant Candida glabrata isolates. Antimicrob Agents Chemother 59:5405–5412Google Scholar
  11. Bohn JA, BeMiller JN (1995) (1→3)-β-d-glucans as biological response modifiers: a review of structure-functional activity relationships. Carbohyd Polym 28:3–14Google Scholar
  12. Boone C, Sommer SS, Hensel A, Bussey H (1990) Yeast KRE genes provide evidence for a pathway of cell wall beta-glucan assembly. J Cell Biol 110:1833–1843Google Scholar
  13. Breinig F, Tipper DJ, Schmitt MJ (2002) Kre1p, the plasma membrane receptor for the yeast K1 viral toxin. Cell 108:395–405Google Scholar
  14. Breinig F, Schleinkofer K, Schmitt MJ (2004) Yeast Kre1p is GPI-anchored and involved in both cell wall assembly and architecture. Microbiology (Reading, Engl.) 150:3209–3218Google Scholar
  15. Brown JL, Kossaczka Z, Jiang B, Bussey H (1993) A mutational analysis of killer toxin resistance in Saccharomyces cerevisiae identifies new genes involved in cell wall (1→6)-beta-glucan synthesis. Genetics 133:837–849Google Scholar
  16. Bull AT (1970) Chemical composition of wild-type and mutant Aspergillus nidulans cell walls. The nature of polysaccharide and melanin constituents. J Gen Microbiol 63:75–94Google Scholar
  17. Calonge TM, Nakano K, Arellano M, Arai R, Katayama S, Toda T, Mabuchi I, Perez P (2000) Schizosaccharomyces pombe rho2p GTPase regulates cell wall alpha-glucan biosynthesis through the protein kinase pck2p. Mol Biol Cell 11:4393–4401Google Scholar
  18. Camacho E, Sepulveda VE, Goldman WE, San-Blas G, Niño-Vega GA (2012) Expression of Paracoccidioides brasiliensis AMY1 in a Histoplasma capsulatum amy1 mutant, relates an α-(1,4)-amylase to cell wall α-(1,3)-glucan synthesis. PLoS ONE 7:e50201Google Scholar
  19. Castro C, Ribas JC, Valdivieso MH, Varona R, del Rey F, Duran A (1995) Papulacandin B resistance in budding and fission yeasts: isolation and characterization of a gene involved in (1,3)beta-d-glucan synthesis in Saccharomyces cerevisiae. J Bacteriol 177:5732–5739Google Scholar
  20. Chen T, Jackson JW, Tams RN, Davis SE, Sparer TE, Reynolds TB (2019a) Exposure of Candida albicans β (1,3)-glucan is promoted by activation of the Cek1 pathway. PLoS Genet 15:e1007892Google Scholar
  21. Chen T, Wagner AS, Tams RN, Eyer JE, Kauffman SJ, Gann ER, Fernandez EJ, Reynolds TB (2019b) Lrg1 regulates β (1,3)-glucan masking in Candida albicans through the Cek1 MAP kinase pathway. MBio 10Google Scholar
  22. Choma A, Wiater A, Komaniecka I, Paduch R, Pleszczyńska M, Szczodrak J (2013) Chemical characterization of a water insoluble (1→3)-α-d-glucan from an alkaline extract of Aspergillus wentii. Carbohydr Polym 91:603–608Google Scholar
  23. Cortés JCG, Ishiguro J, Durán A, Ribas JC (2002) Localization of the (1,3)beta-d-glucan synthase catalytic subunit homologue Bgs1p/Cps1p from fission yeast suggests that it is involved in septation, polarized growth, mating, spore wall formation and spore germination. J Cell Sci 115:4081–4096Google Scholar
  24. Cortés JCG, Carnero E, Ishiguro J, Sánchez Y, Durán A, Ribas JC (2005) The novel fission yeast (1,3)beta-d-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth. J Cell Sci 118:157–174Google Scholar
  25. Cortés JCG, Konomi M, Martins IM, Muñoz J, Moreno MB, Osumi M, Durán A, Ribas JC (2007) The (1,3)beta-d-glucan synthase subunit Bgs1p is responsible for the fission yeast primary septum formation. Mol Microbiol 65:201–217Google Scholar
  26. Cramer RA, Perfect BZ, Pinchai N, Park S, Perlin DS, Asfaw YG, Heitman J, Perfect JR, Steinbach WJ (2008) Calcineurin target CrzA regulates conidial germination, hyphal growth, and pathogenesis of Aspergillus fumigatus. Eukaryot Cell 7:1085–1097Google Scholar
  27. Damveld RA, vanKuyk PA, Arentshorst M, Klis FM, van den Hondel CAMJJ, Ram AFJ (2005a) Expression of agsA, one of five 1,3-alpha-d-glucan synthase-encoding genes in Aspergillus niger, is induced in response to cell wall stress. Fungal Genet Biol 42:165–177Google Scholar
  28. Damveld RA, Arentshorst M, Franken A, vanKuyk PA, Klis FM, van den Hondel CAMJJ, Ram AFJ (2005b) The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol Microbiol 58:305–319Google Scholar
  29. Davis MR, Donnelley MA, Thompson GR (2019) Ibrexafungerp: a novel oral glucan synthase inhibitor. Med MycolGoogle Scholar
  30. Denning DW (2003) Echinocandin antifungal drugs. Lancet 362:1142–1151Google Scholar
  31. Dichtl K, Helmschrott C, Dirr F, Wagener J (2012) Deciphering cell wall integrity signalling in Aspergillus fumigatus: identification and functional characterization of cell wall stress sensors and relevant Rho GTPases. Mol Microbiol 83:506–519Google Scholar
  32. Dichtl K, Samantaray S, Aimanianda V, Zhu Z, Prévost M-C, Latgé J-P, Ebel F, Wagener J (2015) Aspergillus fumigatus devoid of cell wall β-1,3-glucan is viable, massively sheds galactomannan and is killed by septum formation inhibitors. Mol Microbiol 95:458–471Google Scholar
  33. Dichtl K, Samantaray S, Wagener J (2016) Cell wall integrity signalling in human pathogenic fungi. Cell Microbiol 18:1228–1238Google Scholar
  34. Douglas CM (2001) Fungal beta(1,3)-d-glucan synthesis. Med Mycol 39(Suppl 1):55–66Google Scholar
  35. Douglas CM, Foor F, Marrinan JA, Morin N, Nielsen JB, Dahl AM, Mazur P, Baginsky W, Li W, el-Sherbeini M (1994) The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-beta-d-glucan synthase. Proc Natl Acad Sci USA 91:12907–12911Google Scholar
  36. Douglas CM, D’Ippolito JA, Shei GJ, Meinz M, Onishi J, Marrinan JA, Li W, Abruzzo GK, Flattery A, Bartizal K et al (1997) Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-d-glucan synthase inhibitors. Antimicrob Agents Chemother 41:2471–2479Google Scholar
  37. Drgonová J, Drgon T, Tanaka K, Kollár R, Chen GC, Ford RA, Chan CS, Takai Y, Cabib E (1996) Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272:277–279Google Scholar
  38. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432Google Scholar
  39. el-Sherbeini M, Clemas JA (1995) Nikkomycin Z supersensitivity of an echinocandin-resistant mutant of Saccharomyces cerevisiae. Antimicrob Agents Chemother 39:200–207Google Scholar
  40. Eng WK, Faucette L, McLaughlin MM, Cafferkey R, Koltin Y, Morris RA, Young PR, Johnson RK, Livi GP (1994) The yeast FKS1 gene encodes a novel membrane protein, mutations in which confer FK506 and cyclosporin A hypersensitivity and calcineurin-dependent growth. Gene 151:61–71Google Scholar
  41. Fiedler MR, Lorenz A, Nitsche BM, van den Hondel CA, Ram AF, Meyer V (2014) The capacity of Aspergillus niger to sense and respond to cell wall stress requires at least three transcription factors: RlmA. MsnA and CrzA. Fungal Biol Biotechnol 1:5Google Scholar
  42. Fleet GH, Manners DJ (1976) Isolation and composition of an alkali-soluble glucan from the cell walls of Saccharomyces cerevisiae. J Gen Microbiol 94:180–192Google Scholar
  43. Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, Lemoine J, Vorgias CE, Diaquin M, Latgé JP (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275:27594–27607Google Scholar
  44. Fontaine T, Beauvais A, Loussert C, Thevenard B, Fulgsang CC, Ohno N, Clavaud C, Prevost M-C, Latgé J-P (2010) Cell wall alpha1-3glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet Biol 47:707–712Google Scholar
  45. Fortwendel JR, Juvvadi PR, Pinchai N, Perfect BZ, Alspaugh JA, Perfect JR, Steinbach WJ (2009) Differential effects of inhibiting chitin and 1,3-{beta}-d-glucan synthesis in ras and calcineurin mutants of Aspergillus fumigatus. Antimicrob Agents Chemother 53:476–482Google Scholar
  46. Frost DJ, Brandt K, Capobianco J, Goldman R (1994) Characterization of (1,3)-beta-glucan synthase in Candida albicans: microsomal assay from the yeast or mycelial morphological forms and a permeabilized whole-cell assay. Microbiology (Reading, Engl.) 140 (Pt 9):2239–2246Google Scholar
  47. Fujikawa T, Sakaguchi A, Nishizawa Y, Kouzai Y, Minami E, Yano S, Koga H, Meshi T, Nishimura M (2012) Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog 8:e1002882Google Scholar
  48. Fujioka T, Mizutani O, Furukawa K, Sato N, Yoshimi A, Yamagata Y, Nakajima T, Abe K (2007) MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukaryot Cell 6:1497–1510Google Scholar
  49. García I, Tajadura V, Martín V, Toda T, Sánchez Y (2006) Synthesis of alpha-glucans in fission yeast spores is carried out by three alpha-glucan synthase paralogues, Mok12p, Mok13p and Mok14p. Mol Microbiol 59:836–853Google Scholar
  50. García Cortés JC, Ramos M, Osumi M, Pérez P, Ribas JC (2016) The cell biology of fission yeast septation. Microbiol Mol Biol Rev 80:779–791Google Scholar
  51. Garrett-Engele P, Moilanen B, Cyert MS (1995) Calcineurin, the Ca2+/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar H(+)-ATPase. Mol Cell Biol 15:4103–4114Google Scholar
  52. Gastebois A, Clavaud C, Aimanianda V, Latgé J-P (2009) Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol 4:583–595Google Scholar
  53. Geurtsen J, Chedammi S, Mesters J, Cot M, Driessen NN, Sambou T, Kakutani R, Ummels R, Maaskant J, Takata H et al (2009) Identification of mycobacterial alpha-glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation. J Immunol 183:5221–5231Google Scholar
  54. Goyal S, Castrillón-Betancur JC, Klaile E, Slevogt H (2018) The interaction of human pathogenic fungi With C-type lectin receptors. Front Immunol 9:1261Google Scholar
  55. Grün CH, Hochstenbach F, Humbel BM, Verkleij AJ, Sietsma JH, Klis FM, Kamerling JP, Vliegenthart JFG (2005) The structure of cell wall alpha-glucan from fission yeast. Glycobiology 15:245–257Google Scholar
  56. Guerriero G, Silvestrini L, Legay S, Maixner F, Sulyok M, Hausman J-F, Strauss J (2017) Deletion of the celA gene in Aspergillus nidulans triggers overexpression of secondary metabolite biosynthetic genes. Sci Rep 7:5978Google Scholar
  57. Hagen S, Marx F, Ram AF, Meyer V (2007) The antifungal protein AFP from Aspergillus giganteus inhibits chitin synthesis in sensitive fungi. Appl Environ Microbiol 73:2128–2134Google Scholar
  58. He X, Li S, Kaminskyj SGW (2014) Characterization of Aspergillus nidulans α-glucan synthesis: roles for two synthases and two amylases. Mol Microbiol 91:579–595Google Scholar
  59. Henry C, Latgé J-P, Beauvais A (2012) α1,3 glucans are dispensable in Aspergillus fumigatus. Eukaryot Cell 11:26–29Google Scholar
  60. Hochstenbach F, Klis FM, van den Ende H, van Donselaar E, Peters PJ, Klausner RD (1998) Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc Natl Acad Sci USA 95:9161–9166Google Scholar
  61. Hogan LH, Klein BS (1994) Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62:3543–3546Google Scholar
  62. Horisberger M, Lewis BA, Smith F (1972) Structure of a (1 leads to 3)-d-glucan (pseudonigeran) of Aspergillus niger NNRL 326 cell wall. Carbohydr Res 23:183–188Google Scholar
  63. Inoue SB, Takewaki N, Takasuka T, Mio T, Adachi M, Fujii Y, Miyamoto C, Arisawa M, Furuichi Y, Watanabe T (1995) Characterization and gene cloning of 1,3-beta-d-glucan synthase from Saccharomyces cerevisiae. Eur J Biochem 231:845–854Google Scholar
  64. Ishihara S, Hirata A, Nogami S, Beauvais A, Latge J-P, Ohya Y (2007) Homologous subunits of 1,3-beta-glucan synthase are important for spore wall assembly in Saccharomyces cerevisiae. Eukaryot Cell 6:143–156Google Scholar
  65. Johnson ME, Edlind TD (2012) Topological and mutational analysis of Saccharomyces cerevisiae Fks1. Eukaryot Cell 11:952–960Google Scholar
  66. Johnson ME, Katiyar SK, Edlind TD (2011) New Fks hot spot for acquired echinocandin resistance in Saccharomyces cerevisiae and its contribution to intrinsic resistance of Scedosporium species. Antimicrob Agents Chemother 55:3774–3781Google Scholar
  67. Kanetsuna F, Carbonell LM, Moreno RE, Rodriguez J (1969) Cell wall composition of the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol 97:1036–1041Google Scholar
  68. Kang X, Kirui A, Muszyński A, Widanage MCD, Chen A, Azadi P, Wang P, Mentink-Vigier F, Wang T (2018) Molecular architecture of fungal cell walls revealed by solid-state NMR. Nat Commun 9:2747Google Scholar
  69. Kanno T, Takekawa D, Miyakawa Y (2015) Analysis of the essentiality of ROM2 genes in the pathogenic yeasts Candida glabrata and Candida albicans using temperature-sensitive mutants. J Appl Microbiol 118:851–863Google Scholar
  70. Kapteyn JC, Montijn RC, Dijkgraaf GJ, Van den Ende H, Klis FM (1995) Covalent association of beta-1,3-glucan with beta-1,6-glucosylated mannoproteins in cell walls of Candida albicans. J Bacteriol 177:3788–3792Google Scholar
  71. Kapteyn JC, Montijn RC, Vink E, de la Cruz J, Llobell A, Douwes JE, Shimoi H, Lipke PN, Klis FM (1996) Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. Glycobiology 6:337–345Google Scholar
  72. Kapteyn JC, Ram AF, Groos EM, Kollar R, Montijn RC, Van Den Ende H, Llobell A, Cabib E, Klis FM (1997) Altered extent of cross-linking of beta1,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall beta1,3-glucan content. J Bacteriol 179:6279–6284Google Scholar
  73. Katayama S, Hirata D, Arellano M, Pérez P, Toda T (1999) Fission yeast alpha-glucan synthase Mok1 requires the actin cytoskeleton to localize the sites of growth and plays an essential role in cell morphogenesis downstream of protein kinase C function. J Cell Biol 144:1173–1186Google Scholar
  74. Katayama T, Ohta A, Horiuchi H (2015) Protein kinase C regulates the expression of cell wall-related genes in RlmA-dependent and independent manners in Aspergillus nidulans. Biosci Biotechnol Biochem 79:321–330Google Scholar
  75. Katiyar SK, Alastruey-Izquierdo A, Healey KR, Johnson ME, Perlin DS, Edlind TD (2012) Fks1 and Fks2 are functionally redundant but differentially regulated in Candida glabrata: implications for echinocandin resistance. Antimicrob Agents Chemother 56:6304–6309Google Scholar
  76. Kim K-Y, Levin DE (2010) Transcriptional reporters for genes activated by cell wall stress through a non-catalytic mechanism involving Mpk1 and SBF. Yeast 27:541–548Google Scholar
  77. Kim K-Y, Levin DE (2011) Mpk1 MAPK association with the Paf1 complex blocks Sen1-mediated premature transcription termination. Cell 144:745–756Google Scholar
  78. Kim H, Melén K, von Heijne G (2003) Topology models for 37 Saccharomyces cerevisiae membrane proteins based on C-terminal reporter fusions and predictions. J Biol Chem 278:10208–10213Google Scholar
  79. Klis FM (1994) Review: cell wall assembly in yeast. Yeast 10:851–869Google Scholar
  80. Klis FM, Boorsma A, De Groot PWJ (2006) Cell wall construction in Saccharomyces cerevisiae. Yeast 23:185–202Google Scholar
  81. Kollár R, Petráková E, Ashwell G, Robbins PW, Cabib E (1995) Architecture of the yeast cell wall. The linkage between chitin and beta(1→3)-glucan. J Biol Chem 270:1170–1178Google Scholar
  82. Kontoyiannis DP, Lewis RE, Osherov N, Albert ND, May GS (2003) Combination of caspofungin with inhibitors of the calcineurin pathway attenuates growth in vitro in Aspergillus species. J Antimicrob Chemother 51:313–316Google Scholar
  83. Kopecká M, Kreger DR (1986) Assembly of microfibrils in vivo and in vitro from (1≫3)-beta-d-glucan synthesized by protoplasts of Saccharomyces cerevisiae. Arch Microbiol 143:387–395Google Scholar
  84. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580Google Scholar
  85. Kwon MJ, Arentshorst M, Roos ED, van den Hondel CAMJJ, Meyer V, Ram AFJ (2011) Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol Microbiol 79:1151–1167Google Scholar
  86. Lamaris GA, Lewis RE, Chamilos G, May GS, Safdar A, Walsh TJ, Raad II, Kontoyiannis DP (2008) Caspofungin-mediated beta-glucan unmasking and enhancement of human polymorphonuclear neutrophil activity against Aspergillus and non-Aspergillus hyphae. J Infect Dis 198:186–192Google Scholar
  87. Laroche C, Michaud P (2007) New developments and prospective applications for beta (1,3) glucans. Recent Pat Biotechnol 1:59–73Google Scholar
  88. Latgé J-P (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66:279–290Google Scholar
  89. Latgé J-P (2010) Tasting the fungal cell wall. Cell Microbiol 12:863–872Google Scholar
  90. Legentil L, Paris F, Ballet C, Trouvelot S, Daire X, Vetvicka V, Ferrières V (2015) Molecular interactions of β-(1→3)-glucans with their receptors. Molecules 20:9745–9766Google Scholar
  91. Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70:317–343Google Scholar
  92. Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69:262–291Google Scholar
  93. Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189:1145–1175Google Scholar
  94. Liu J, Wang H, McCollum D, Balasubramanian MK (1999) Drc1p/Cps1p, a 1,3-beta-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe. Genetics 153:1193–1203Google Scholar
  95. Liu J, Tang X, Wang H, Balasubramanian M (2000) Bgs2p, a 1,3-beta-glucan synthase subunit, is essential for maturation of ascospore wall in Schizosaccharomyces pombe. FEBS Lett 478:105–108Google Scholar
  96. Liu J, Tang X, Wang H, Oliferenko S, Balasubramanian MK (2002) The localization of the integral membrane protein Cps1p to the cell division site is dependent on the actomyosin ring and the septation-inducing network in Schizosaccharomyces pombe. Mol Biol Cell 13:989–1000Google Scholar
  97. Liu S, Hou Y, Liu W, Lu C, Wang W, Sun S (2015) Components of the calcium-calcineurin signaling pathway in fungal cells and their potential as antifungal targets. Eukaryot Cell 14:324–334Google Scholar
  98. Loiko V, Wagener J (2017) The paradoxical effect of echinocandins in Aspergillus fumigatus relies on recovery of the β-1,3-glucan synthase Fks1. Antimicrob, Agents Chemother, p 61Google Scholar
  99. López-Romero E, Ruiz-Herrera J (1978) Properties of beta-glucan synthetase from Saccharomyces cerevisiae. Antonie Van Leeuwenhoek 44:329–339Google Scholar
  100. Maddi A, Free SJ (2010) α-1,6-Mannosylation of N-linked oligosaccharide present on cell wall proteins is required for their incorporation into the cell wall in the filamentous fungus Neurospora crassa. Eukaryot Cell 9:1766–1775Google Scholar
  101. Magnelli P, Cipollo JF, Abeijon C (2002) A refined method for the determination of Saccharomyces cerevisiae cell wall composition and beta-1,6-glucan fine structure. Anal Biochem 301:136–150Google Scholar
  102. Magnelli PE, Cipollo JF, Robbins PW (2005) A glucanase-driven fractionation allows redefinition of Schizosaccharomyces pombe cell wall composition and structure: assignment of diglucan. Anal Biochem 336:202–212Google Scholar
  103. Manners DJ, Meyer MT (1977) The molecular structures of some glucans from the cell walls of Schizosaccharomyces pombe. Carbohyd Res 57:189–203Google Scholar
  104. Manners DJ, Masson AJ, Patterson JC (1973) The structure of a beta-(1 leads to 3)-d-glucan from yeast cell walls. Biochem J 135:19–30Google Scholar
  105. Marion CL, Rappleye CA, Engle JT, Goldman WE (2006) An alpha-(1,4)-amylase is essential for alpha-(1,3)-glucan production and virulence in Histoplasma capsulatum. Mol Microbiol 62:970–983Google Scholar
  106. Martín V, García B, Carnero E, Durán A, Sánchez Y (2003) Bgs3p, a putative 1,3-beta-glucan synthase subunit, is required for cell wall assembly in Schizosaccharomyces pombe. Eukaryot Cell 2:159–169Google Scholar
  107. Martinac B, Zhu H, Kubalski A, Zhou XL, Culbertson M, Bussey H, Kung C (1990) Yeast K1 killer toxin forms ion channels in sensitive yeast spheroplasts and in artificial liposomes. Proc Natl Acad Sci USA 87:6228–6232Google Scholar
  108. Mazur P, Baginsky W (1996) In vitro activity of 1,3-beta-d-glucan synthase requires the GTP-binding protein Rho1. J Biol Chem 271:14604–14609Google Scholar
  109. Mazur P, Morin N, Baginsky W, el-Sherbeini M, Clemas JA, Nielsen JB, Foor F (1995) Differential expression and function of two homologous subunits of yeast 1,3-beta-d-glucan synthase. Mol Cell Biol 15:5671–5681Google Scholar
  110. Meaden P, Hill K, Wagner J, Slipetz D, Sommer SS, Bussey H (1990) The yeast KRE5 gene encodes a probable endoplasmic reticulum protein required for (1—6)-beta-d-glucan synthesis and normal cell growth. Mol Cell Biol 10:3013–3019Google Scholar
  111. Mélida H, Sain D, Stajich JE, Bulone V (2015) Deciphering the uniqueness of Mucoromycotina cell walls by combining biochemical and phylogenomic approaches. Environ Microbiol 17:1649–1662Google Scholar
  112. Meyer V, Damveld RA, Arentshorst M, Stahl U, van den Hondel CAMJJ, Ram AFJ (2007) Survival in the presence of antifungals: genome-wide expression profiling of Aspergillus niger in response to sublethal concentrations of caspofungin and fenpropimorph. J Biol Chem 282:32935–32948Google Scholar
  113. Mio T, Adachi-Shimizu M, Tachibana Y, Tabuchi H, Inoue SB, Yabe T, Yamada-Okabe T, Arisawa M, Watanabe T, Yamada-Okabe H (1997) Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSC1/FKS1 and its involvement in beta-1,3-glucan synthesis. J Bacteriol 179:4096–4105Google Scholar
  114. Miyazawa K, Yoshimi A, Kasahara S, Sugahara A, Koizumi A, Yano S, Kimura S, Iwata T, Sano M, Abe K (2018) Molecular mass and localization of α-1,3-glucan in cell wall control the degree of hyphal aggregation in liquid culture of Aspergillus nidulans. Front Microbiol 9:2623Google Scholar
  115. Montijn RC, Vink E, Müller WH, Verkleij AJ, Van Den Ende H, Henrissat B, Klis FM (1999) Localization of synthesis of beta1,6-glucan in Saccharomyces cerevisiae. J Bacteriol 181:7414–7420Google Scholar
  116. Morris GJ, Winters L, Coulson GE, Clarke KJ (1986) Effect of osmotic stress on the ultrastructure and viability of the yeast Saccharomyces cerevisiae. J Gen Microbiol 132:2023–2034Google Scholar
  117. Mouyna I, Monod M, Fontaine T, Henrissat B, Léchenne B, Latgé JP (2000) Identification of the catalytic residues of the first family of beta(1-3)glucanosyltransferases identified in fungi. Biochem J 347(Pt 3):741–747Google Scholar
  118. Nuoffer C, Jenö P, Conzelmann A, Riezman H (1991) Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiae GAS1 protein to the plasma membrane. Mol Cell Biol 11:27–37Google Scholar
  119. Okada H, Abe M, Asakawa-Minemura M, Hirata A, Qadota H, Morishita K, Ohnuki S, Nogami S, Ohya Y (2010) Multiple functional domains of the yeast l,3-beta-glucan synthase subunit Fks1p revealed by quantitative phenotypic analysis of temperature-sensitive mutants. Genetics 184:1013–1024Google Scholar
  120. Onishi J, Meinz M, Thompson J, Curotto J, Dreikorn S, Rosenbach M, Douglas C, Abruzzo G, Flattery A, Kong L et al (2000) Discovery of novel antifungal (1,3)-beta-d-glucan synthase inhibitors. Antimicrob Agents Chemother 44:368–377Google Scholar
  121. Onishi M, Ko N, Nishihama R, Pringle JR (2013) Distinct roles of Rho1, Cdc42, and Cyk3 in septum formation and abscission during yeast cytokinesis. J Cell Biol 202:311–329Google Scholar
  122. Pagé N, Gérard-Vincent M, Ménard P, Beaulieu M, Azuma M, Dijkgraaf GJP, Li H, Marcoux J, Nguyen T, Dowse T et al (2003) A Saccharomyces cerevisiae genome-wide mutant screen for altered sensitivity to K1 killer toxin. Genetics 163:875–894Google Scholar
  123. Parent SA, Nielsen JB, Morin N, Chrebet G, Ramadan N, Dahl AM, Hsu MJ, Bostian KA, Foor F (1993) Calcineurin-dependent growth of an FK506- and CsA-hypersensitive mutant of Saccharomyces cerevisiae. J Gen Microbiol 139:2973–2984Google Scholar
  124. Park J, Hulsman M, Arentshorst M, Breeman M, Alazi E, Lagendijk EL, Rocha MC, Malavazi I, Nitsche BM, van den Hondel CAMJJ et al (2016) Transcriptomic and molecular genetic analysis of the cell wall salvage response of Aspergillus niger to the absence of galactofuranose synthesis. Cell Microbiol 18:1268–1284Google Scholar
  125. Paulson JC, Colley KJ (1989) Glycosyltransferases. Structure, localization, and control of cell type-specific glycosylation. J Biol Chem 264:17615–17618Google Scholar
  126. Pereira M, Felipe MS, Brígido MM, Soares CM, Azevedo MO (2000) Molecular cloning and characterization of a glucan synthase gene from the human pathogenic fungus Paracoccidioides brasiliensis. Yeast 16:451–462Google Scholar
  127. Pérez P, Cansado J (2010) Cell integrity signaling and response to stress in fission yeast. Curr Protein Pept Sci 11:680–692Google Scholar
  128. Perlin DS (2015) Mechanisms of echinocandin antifungal drug resistance. Ann NY Acad Sci 1354:1–11Google Scholar
  129. Qadota H, Python CP, Inoue SB, Arisawa M, Anraku Y, Zheng Y, Watanabe T, Levin DE, Ohya Y (1996) Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-beta-glucan synthase. Science 272:279–281Google Scholar
  130. Quigley DR, Selitrennikoff CP (1987) β-Linked disaccharides stimulate, but do not act as primer for, β (1–3) glucan synthase activity of Neurospora crassa. Curr Microbiol 15:181–184Google Scholar
  131. Ram AF, Brekelmans SS, Oehlen LJ, Klis FM (1995) Identification of two cell cycle regulated genes affecting the beta 1,3-glucan content of cell walls in Saccharomyces cerevisiae. FEBS Lett 358:165–170Google Scholar
  132. Rappleye CA, Engle JT, Goldman WE (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53:153–165Google Scholar
  133. Rappleye CA, Eissenberg LG, Goldman WE (2007) Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Natl Acad Sci USA 104:1366–1370Google Scholar
  134. Rees DA, Scott W (1971) Polysaccharide conformation. Part VI. Computer model-building for linear and branched pyranoglycans. Correlations with biological function. Preliminary assessment of inter-residue forces in aqueous solution. Further interpretation of optical rotation in terms of chain conformation. J Chem Soc B: Phys Org 469–479Google Scholar
  135. Reese AJ, Doering TL (2003) Cell wall alpha-1,3-glucan is required to anchor the Cryptococcus neoformans capsule. Mol Microbiol 50:1401–1409Google Scholar
  136. Reese AJ, Yoneda A, Breger JA, Beauvais A, Liu H, Griffith CL, Bose I, Kim M-J, Skau C, Yang S et al (2007) Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol Microbiol 63:1385–1398Google Scholar
  137. Richthammer C, Enseleit M, Sanchez-Leon E, März S, Heilig Y, Riquelme M, Seiler S (2012) RHO1 and RHO2 share partially overlapping functions in the regulation of cell wall integrity and hyphal polarity in Neurospora crassa. Mol Microbiol 85:716–733Google Scholar
  138. Rocha MC, Fabri JHTM, Franco de Godoy K, Alves de Castro P, Hori JI, Ferreira da Cunha A, Arentshorst M, Ram AFJ, van den Hondel CAMJJ, Goldman GH et al (2016) Aspergillus fumigatus MADS-box transcription factor rlmA is required for regulation of the cell wall integrity and virulence. G3 (Bethesda) 6:2983–3002Google Scholar
  139. Rodicio R, Buchwald U, Schmitz H-P, Heinisch JJ (2008) Dissecting sensor functions in cell wall integrity signaling in Kluyveromyces lactis. Fungal Genet Biol 45:422–435Google Scholar
  140. Roemer T, Bussey H (1991) Yeast beta-glucan synthesis: KRE6 encodes a predicted type II membrane protein required for glucan synthesis in vivo and for glucan synthase activity in vitro. Proc Natl Acad Sci USA 88:11295–11299Google Scholar
  141. Roemer T, Delaney S, Bussey H (1993) SKN1 and KRE6 define a pair of functional homologs encoding putative membrane proteins involved in beta-glucan synthesis. Mol Cell Biol 13:4039–4048Google Scholar
  142. Roemer T, Paravicini G, Payton MA, Bussey H (1994) Characterization of the yeast (1→6)-beta-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly. J Cell Biol 127:567–579Google Scholar
  143. Ruiz-Herrera J, Elorza MV, Valentín E, Sentandreu R (2006) Molecular organization of the cell wall of Candida albicans and its relation to pathogenicity. FEMS Yeast Res 6:14–29Google Scholar
  144. Samantaray S, Neubauer M, Helmschrott C, Wagener J (2013) Role of the guanine nucleotide exchange factor Rom2 in cell wall integrity maintenance of Aspergillus fumigatus. Eukaryot Cell 12:288–298Google Scholar
  145. Samar D, Kieler JB, Klutts JS (2015) Identification and deletion of Tft1, a predicted glycosyltransferase necessary for cell wall β-1,3;1,4-glucan synthesis in Aspergillus fumigatus. PLoS ONE 10:e0117336Google Scholar
  146. San-Blas G, Vernet D (1977) Induction of the synthesis of cell wall alpha-1,3-glucan in the yeastlike form of Paracoccidioides brasiliensis strain IVIC Pb9 by fetal calf serum. Infect Immun 15:897–902Google Scholar
  147. San-Blas G, Ordaz D, Yegres FJ (1978) Histoplasma capsulatum: chemical variability of the yeast cell wall. Sabouraudia 16:279–284Google Scholar
  148. Sánchez-León E, Riquelme M (2015) Live imaging of β-1,3-glucan synthase FKS-1 in Neurospora crassa hyphae. Fungal Genet Biol 82:104–107Google Scholar
  149. Schimoler-O’Rourke R, Renault S, Mo W, Selitrennikoff CP (2003) Neurospora crassa FKS protein binds to the (1,3)beta-glucan synthase substrate, UDP-glucose. Curr Microbiol 46:408–412Google Scholar
  150. Schoffelmeer EA, Klis FM, Sietsma JH, Cornelissen BJ (1999) The cell wall of Fusarium oxysporum. Fungal Genet Biol 27:275–282Google Scholar
  151. Shahinian S, Bussey H (2000) Beta-1,6-glucan synthesis in Saccharomyces cerevisiae. Mol Microbiol 35:477–489Google Scholar
  152. Shematek EM, Cabib E (1980) Biosynthesis of the yeast cell wall. II. Regulation of beta-(1 leads to 3)glucan synthetase by ATP and GTP. J Biol Chem 255:895–902Google Scholar
  153. Shematek EM, Braatz JA, Cabib E (1980) Biosynthesis of the yeast cell wall. I. Preparation and properties of beta-(1 leads to 3)glucan synthetase. J Biol Chem 255:888–894Google Scholar
  154. Sorais F, Barreto L, Leal JA, Bernabé M, San-Blas G, Niño-Vega GA (2010) Cell wall glucan synthases and GTPases in Paracoccidioides brasiliensis. Med Mycol 48:35–47Google Scholar
  155. Stathopoulos AM, Cyert MS (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev 11:3432–3444Google Scholar
  156. Steinbach WJ, Cramer RA, Perfect BZ, Henn C, Nielsen K, Heitman J, Perfect JR (2007) Calcineurin inhibition or mutation enhances cell wall inhibitors against Aspergillus fumigatus. Antimicrob Agents Chemother 51:2979–2981Google Scholar
  157. Stevens DA, Ichinomiya M, Koshi Y, Horiuchi H (2006) Escape of Candida from caspofungin inhibition at concentrations above the MIC (paradoxical effect) accomplished by increased cell wall chitin; evidence for beta-1,6-glucan synthesis inhibition by caspofungin. Antimicrob Agents Chemother 50:3160–3161Google Scholar
  158. Suwunnakorn S, Wakabayashi H, Kordalewska M, Perlin DS, Rustchenko E (2018) FKS2 and FKS3 genes of opportunistic human pathogen Candida albicans influence echinocandin susceptibility. Antimicrob, Agents Chemother, p 62Google Scholar
  159. Thompson JR, Douglas CM, Li W, Jue CK, Pramanik B, Yuan X, Rude TH, Toffaletti DL, Perfect JR, Kurtz M (1999) A glucan synthase FKS1 homolog in Cryptococcus neoformans is single copy and encodes an essential function. J Bacteriol 181:444–453Google Scholar
  160. Valsecchi I, Dupres V, Michel J-P, Duchateau M, Matondo M, Chamilos G, Saveanu C, Guijarro JI, Aimanianda V, Lafont F et al (2019) The puzzling construction of the conidial outer layer of Aspergillus fumigatus. Cell Microbiol 21:e12994Google Scholar
  161. Villar-Tajadura MA, Coll PM, Madrid M, Cansado J, Santos B, Pérez P (2008) Rga2 is a Rho2 GAP that regulates morphogenesis and cell integrity in S. pombe. Mol Microbiol 70:867–881Google Scholar
  162. Vitale RG, de Hoog GS, Schwarz P, Dannaoui E, Deng S, Machouart M, Voigt K, van de Sande WWJ, Dolatabadi S, Meis JF et al (2012) Antifungal susceptibility and phylogeny of opportunistic members of the order mucorales. J Clin Microbiol 50:66–75Google Scholar
  163. Vos A, Dekker N, Distel B, Leunissen JAM, Hochstenbach F (2007) Role of the synthase domain of Ags1p in cell wall alpha-glucan biosynthesis in fission yeast. J Biol Chem 282:18969–18979Google Scholar
  164. Wagener J, Loiko V (2017) Recent insights into the paradoxical effect of echinocandins. J Fungi (Basel) 4Google Scholar
  165. Walker LA, Munro CA, de Bruijn I, Lenardon MD, McKinnon A, Gow NAR (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4:e1000040Google Scholar
  166. Wheeler RT, Kombe D, Agarwala SD, Fink GR (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4:e1000227Google Scholar
  167. Yoshimi A, Sano M, Inaba A, Kokubun Y, Fujioka T, Mizutani O, Hagiwara D, Fujikawa T, Nishimura M, Yano S et al (2013) Functional analysis of the α-1,3-glucan synthase genes agsA and agsB in Aspergillus nidulans: agsB is the major α-1,3-glucan synthase in this fungus. PLoS ONE 8:e54893Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Johannes Wagener
    • 1
    • 2
    Email author
  • Kristina Striegler
    • 1
  • Nikola Wagener
    • 3
  1. 1.Institut Für Hygiene Und Mikrobiologie, University of WürzburgWürzburgGermany
  2. 2.National Reference Center for Invasive Fungal Infections (NRZMyk)JenaGermany
  3. 3.Department of Cell Biology, Medical FacultyUniversity of MunichMartinsriedGermany

Personalised recommendations