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Organizational Properties of the Pericentriolar Material

  • David Comartin
  • Laurence Pelletier
Chapter

Abstract

The centrosome is the major microtubule-organizing centre of animal cells. It participates in a number of crucial cellular functions including cell motility, intracellular transport, mitotic spindle assembly/positioning and cilia formation. Centrosome is composed of pair of ninefold symmetric centrioles surrounded by pericentriolar material, or PCM. PCM organization undergoes a series of dramatic changes in its organization and function as cells progress through the cell cycle. Indeed, the rather small interphase centrosome increases dramatically in size and microtubule nucleation capacity from interphase to mitosis, a process referred to as centrosome maturation. Until very recently, the PCM was thought to be largely amorphous. However, it has been elegantly demonstrated in several super-resolution studies that the PCM is highly organized and that the higher-order organizational properties are conserved from flies to humans. In this book chapter, we review current knowledge on the organization and composition of PCM in both interphase and mitosis and discuss how the centrosome landscape is altered through post-translational modifications, mainly mitotic phosphorylation, during centrosome maturation.

Keywords

Mitotic Spindle Asymmetric Cell Division Microtubule Nucleation Mother Centriole Centriole Duplication 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Arquint C, Nigg EA (2014) STIL microcephaly mutations interfere with APC/C-mediated degradation and cause centriole amplification. Curr Biol 24:351–360. doi: 10.1016/j.cub.2013.12.016 PubMedCrossRefGoogle Scholar
  2. Bärenz F, Mayilo D, Gruss OJ (2011) Centriolar satellites: busy orbits around the centrosome. Eur J Cell Biol 90:983–989. doi: 10.1016/j.ejcb.2011.07.007 PubMedCrossRefGoogle Scholar
  3. Barenz F, Inoue D, Yokoyama H, Tegha-Dunghu J, Freiss S, Draeger S, Mayilo D, Cado I, Merker S, Klinger M, Hoeckendorf B, Pilz S, Hupfeld K, Steinbeisser H, Lorenz H, Ruppert T, Wittbrodt J, Gruss OJ (2013) The centriolar satellite protein SSX2IP promotes centrosome maturation. J Cell Biol 202:81–95. doi: 10.1083/jcb.201302122 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barr FA, Silljé HHW, Nigg EA (2004) Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5:429–441. doi: 10.1038/nrm1401 PubMedCrossRefGoogle Scholar
  5. Bond J, Roberts E, Springell K, Lizarraga S, Scott S, Higgins J, Hampshire DJ, Morrison EE, Leal GF, Silva EO, Costa SMR, Baralle D, Raponi M, Karbani G, Rashid Y, Jafri H, Bennett C, Corry P, Walsh CA, Woods CG (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37:353–355. doi: 10.1038/ng1539 PubMedCrossRefGoogle Scholar
  6. Bouckson-Castaing V, Moudjou M, Ferguson DJ, Mucklow S, Belkaid Y, Milon G, Crocker PR (1996) Molecular characterisation of ninein, a new coiled-coil protein of the centrosome. J Cell Sci 109:179–190PubMedGoogle Scholar
  7. Buchman JJ, Tseng H-C, Zhou Y, Frank CL, Xie Z, Tsai L-H (2010) Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex. Neuron 66:386–402. doi: 10.1016/j.neuron.2010.03.036 PubMedCrossRefGoogle Scholar
  8. Casenghi M (2005) Phosphorylation of Nlp by Plk1 negatively regulates its dynein-dynactin-dependent targeting to the centrosome. J Cell Sci 118:5101–5108. doi: 10.1242/jcs.02622 PubMedCrossRefGoogle Scholar
  9. Casenghi M, Meraldi P, Weinhart U, Duncan PI, Körner R, Nigg EA (2003) Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev Cell 5:113–125PubMedCrossRefGoogle Scholar
  10. Ching YP, Qi Z, Wang JH (2000) Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 242:285–294PubMedCrossRefGoogle Scholar
  11. Comartin D, Gupta GD, Fussner E, Coyaud É, Hasegan M, Archinti M, Cheung SWT, Pinchev D, Lawo S, Raught B, Bazett-Jones DP, Lüders J, Pelletier L (2013) CEP120 and SPICE1 Cooperate with CPAP in centriole elongation. Curr Biol 23:1360–1366. doi: 10.1016/j.cub.2013.06.002 PubMedCrossRefGoogle Scholar
  12. Conduit PT (2013) The dominant force of Centrobin in centrosome asymmetry. Nat Cell Biol 15:235–237PubMedCrossRefGoogle Scholar
  13. Conduit PT, Raff JW (2010) Cnn dynamics drive centrosome size asymmetry to ensure daughter centriole retention in Drosophila neuroblasts. Curr Biol 20:2187–2192. doi: 10.1016/j.cub.2010.11.055 PubMedCrossRefGoogle Scholar
  14. Conduit PT, Brunk K, Dobbelaere J, Dix CI, Lucas EP, Raff JW (2010) Centrioles regulate centrosome size by controlling the rate of Cnn incorporation into the PCM. Curr Biol 20:2178–2186. doi: 10.1016/j.cub.2010.11.011 PubMedCrossRefGoogle Scholar
  15. Conduit PT, Feng Z, Richens JH, Baumbach J, Wainman A, Bakshi SD, Dobbelaere J, Johnson S, Lea SM, Raff JW (2014a) The centrosome-specific phosphorylation of Cnn by polo/Plk1 drives Cnn scaffold assembly and centrosome maturation. Dev Cell 28:659–669. doi: 10.1016/j.devcel.2014.02.013 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Conduit PT, Richens JH, Wainman A, Holder J, Vicente CC, Pratt MB, Dix CI, Novak ZA, Dobbie IM, Schermelleh L, Others (2014b) A molecular mechanism of mitotic centrosome assembly in Drosophila. eLife 3, e03399PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cottee MA, Muschalik N, Wong YL, Johnson CM, Johnson S, Andreeva A, Oegema K, Lea SM, Raff JW, van Breugel M (2013) Crystal structures of the CPAP/STIL complex reveal its role in centriole assembly and human microcephaly. Elife 2Google Scholar
  18. Dammermann A (2002) Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255–266. doi: 10.1083/jcb.200204023 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dauber A, LaFranchi SH, Maliga Z, Lui JC, Moon JE, McDeed C, Henke K, Zonana J, Kingman GA, Pers TH, Baron J, Rosenfeld RG, Hirschhorn JN, Harris MP, Hwa V (2012) Novel microcephalic primordial Dwarfism disorder associated with variants in the centrosomal protein ninein. J Clin Endocrinol Metab 97:E2140–E2151. doi: 10.1210/jc.2012-2150 PubMedPubMedCentralCrossRefGoogle Scholar
  20. David-Pfeuty T, Erickson HP, Pantaloni D (1977) Guanosinetriphosphatase activity of tubulin associated with microtubule assembly. Proc Natl Acad Sci 74:5372–5376PubMedPubMedCentralCrossRefGoogle Scholar
  21. de Bruijn DRH, dos Santos NR, Kater-Baats E, Thijssen J, van den Berk L, Stap J, Balemans M, Schepens M, Merkx G, Geurts van Kessel A (2002) The cancer-related protein SSX2 interacts with the human homologue of a Ras-like GTPase interactor, RAB3IP, and a novel nuclear protein, SSX2IP. Genes. Chromosomes Cancer 34:285–298. doi: 10.1002/gcc.10073 CrossRefGoogle Scholar
  22. Delaval B, Doxsey SJ (2010) Pericentrin in cellular function and disease. J Cell Biol 188:181–190. doi: 10.1083/jcb.200908114 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Delgehyr N (2005) Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J Cell Sci 118:1565–1575. doi: 10.1242/jcs.02302 PubMedCrossRefGoogle Scholar
  24. Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13:83–117PubMedCrossRefGoogle Scholar
  25. Dictenberg JB, Zimmerman W, Sparks CA, Young A, Vidair C, Zheng Y, Carrington W, Fay FS, Doxsey SJ (1998) Pericentrin and γ-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J Cell Biol 141:163–174PubMedPubMedCentralCrossRefGoogle Scholar
  26. Doxsey SJ, Stein P, Evans L, Calarco PD, Kirshner M (1994) Pericentrin, A highly conserved centrosome protein involved in microtuuble organization. Cell 76:639–650PubMedCrossRefGoogle Scholar
  27. Elia AEH (2003) Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299:1228–1231. doi: 10.1126/science.1079079 PubMedCrossRefGoogle Scholar
  28. Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, Hoepker K, Mohammad D, Cantley LC, Smerdon SJ, Yaffe MB (2003) The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115:83–95PubMedCrossRefGoogle Scholar
  29. Firat-Karalar EN, Rauniyar N, Yates JR, Stearns T (2014) Proximity interactions among centrosome components identify regulators of centriole duplication. Curr Biol 24:664–670. doi: 10.1016/j.cub.2014.01.067 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Fong K-W, Choi Y-K, Rattner JB, Qi RZ (2008) CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the γ-tubulin ring complex. Mol Biol Cell 19:115–125PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fong K-W, Hau S-Y, Kho Y-S, Jia Y, He L, Qi RZ (2009) Interaction of CDK5RAP2 with EB1 to track growing microtubule tips and to regulate microtubule dynamics. Mol Biol Cell 20:3660–3670PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fu J, Glover DM (2012) Structured illumination of the interface between centriole and peri-centriolar material. Open Biol 2:120104-12117. doi: 10.1098/rsob.120104
  33. Gillingham AK, Munro S (2000) The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep 1:524–529PubMedPubMedCentralCrossRefGoogle Scholar
  34. Golsteyn RM, Schultz SJ, Bartek J, Ziemiecki A, Ried T, Nigg EA (1994) Cell cycle analysis and chromosomal localization of human Plk1, a putative homologue of the mitotic kinases Drosophila polo and Saccharomyces cerevisiae Cdc5. J Cell Sci 107:1509–1517PubMedGoogle Scholar
  35. Golsteyn RM, Mundt KE, Fry AM, Nigg EA (1995) Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. J Cell Biol 129:1617–1628PubMedCrossRefGoogle Scholar
  36. Gomez-Ferreria MA, Rath U, Buster DW, Chanda SK, Caldwell JS, Rines DR, Sharp DJ (2007) Human Cep192 is required for mitotic centrosome and spindle assembly. Curr Biol 17:1960–1966. doi: 10.1016/j.cub.2007.10.019 PubMedCrossRefGoogle Scholar
  37. Gomez-Ferreria MA, Bashkurov M, Helbig AO, Larsen B, Pawson T, Gingras A-C, Pelletier L (2012) Novel NEDD1 phosphorylation sites regulate -tubulin binding and mitotic spindle assembly. J Cell Sci 125:3745–3751. doi: 10.1242/jcs.105130 PubMedCrossRefGoogle Scholar
  38. Gönczy P (2012) Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 13:425–435. doi: 10.1038/nrm3373 PubMedCrossRefGoogle Scholar
  39. Gopalakrishnan J, Mennella V, Blachon S, Zhai B, Smith AH, Megraw TL, Nicastro D, Gygi SP, Agard DA, Avidor-Reiss T (2011) Sas-4 provides a scaffold for cytoplasmic complexes and tethers them in a centrosome. Nat Commun 2:359. doi: 10.1038/ncomms1367 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gopalakrishnan J, Frederick Chim Y-C, Ha A, Basiri ML, Lerit DA, Rusan NM, Avidor-Reiss T (2012) Tubulin nucleotide status controls Sas-4-dependent pericentriolar material recruitment. Nat Cell Biol 14:865–873. doi: 10.1038/ncb2527 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gould RR, Borisy GR (1977) The pericentriolar material in Chinese hamster ovary cells nucleates microtubule formation. J Cell Biol 73:601–615PubMedPubMedCentralCrossRefGoogle Scholar
  42. Griffith E, Walker S, Martin C-A, Vagnarelli P, Stiff T, Vernay B, Sanna NA, Saggar A, Hamel B, Earnshaw WC, Jeggo PA, Jackson AP, O’Driscoll M (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat Genet 40:232–236. doi: 10.1038/ng.2007.80 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gudi R, Zou C, Li J, Gao Q (2011) Centrobin-tubulin interaction is required for centriole elongation and stability. J Cell Biol 193:711–725. doi: 10.1083/jcb.201006135 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Gudi R, Zou C, Dhar J, Gao Q, Vasu C (2014) Centrobin-centrosomal protein 4.1-associated protein (CPAP) interaction promotes CPAP localization to the centrioles during centriole duplication. J Biol Chem 289:15166–15178. doi: 10.1074/jbc.M113.531152 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Guernsey DL, Jiang H, Hussin J, Arnold M, Bouyakdan K, Perry S, Babineau-Sturk T, Beis J, Dumas N, Evans SC, Ferguson M, Matsuoka M, Macgillivray C, Nightingale M, Patry L, Rideout AL, Thomas A, Orr A, Hoffmann I, Michaud JL, Awadalla P, Meek DC, Ludman M, Samuels ME (2010) Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4. Am J Hum Genet 87:40–51. doi: 10.1016/j.ajhg.2010.06.003 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Guichard P, Hachet V, Majubu N, Neves A, Demurtas D, Olieric N, Fluckiger I, Yamada A, Kihara K, Nishida Y, Moriya S, Steinmetz MO, Hongoh Y, Gönczy P (2013) Native architecture of the centriole proximal region reveals features underlying its 9-fold radial symmetry. Curr Biol 23:1620–1628. doi: 10.1016/j.cub.2013.06.061 PubMedCrossRefGoogle Scholar
  47. Gustafsson MG (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198:82–87PubMedCrossRefGoogle Scholar
  48. Habedanck R, Stierhof Y-D, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7:1140–1146. doi: 10.1038/ncb1320 PubMedCrossRefGoogle Scholar
  49. Haren L (2006) NEDD1-dependent recruitment of the -tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 172:505–515. doi: 10.1083/jcb.200510028 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Haren L, Stearns T, Lüders J (2009) Plk1-dependent recruitment of γ-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS One 4, e5976. doi: 10.1371/journal.pone.0005976 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hatzopoulos GN, Erat MC, Cutts E, Rogala KB, Slater LM, Stansfeld PJ, Vakonakis I (2013) Structural analysis of the G-box domain of the microcephaly protein CPAP suggests a role in centriole architecture. Structure 21:2069–2077. doi: 10.1016/j.str.2013.08.019 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hori A, Ikebe C, Tada M, Toda T (2014) Msd1/SSX2IP-dependent microtubule anchorage ensures spindle orientation and primary cilia formation. EMBO Rep. doi: 10.1002/embr.201337929 PubMedPubMedCentralGoogle Scholar
  53. Hsu W-B, Hung L-Y, Tang C-JC, Su C-L, Chang Y, Tang TK (2008) Functional characterization of the microtubule-binding and -destabilizing domains of CPAP and d-SAS-4. Exp Cell Res 314:2591–2602. doi: 10.1016/j.yexcr.2008.05.012 PubMedCrossRefGoogle Scholar
  54. Huang B, Bates M, Zhuang X (2009) Super-resolution fluorescence microscopy. Annu Rev Biochem 78:993–1016. doi: 10.1146/annurev.biochem.77.061906.092014 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Huang B, Babcock H, Zhuang X (2010) Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143:1047–1058. doi: 10.1016/j.cell.2010.12.002 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hung L-Y, Tang C-JC, Tang TK (2000) Protein 4.1 R-135 interacts with a novel centrosomal protein (CPAP) which is associated with the gamma -tubulin complex. Mol Cell Biol 20:7813–7825. doi: 10.1128/MCB.20.20.7813-7825.2000 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Jang Y-J, Lin C-Y, Ma S, Erikson RL (2002) Functional studies on the role of the C-terminal domain of mammalian polo-like kinase. Proc Natl Acad Sci 99:1984–1989PubMedPubMedCentralCrossRefGoogle Scholar
  58. Januschke J, Reina J, Llamazares S, Bertran T, Rossi F, Roig J, Gonzalez C (2013) Centrobin controls mother–daughter centriole asymmetry in Drosophila neuroblasts. Nat Cell Biol 15:241–248. doi: 10.1038/ncb2671 PubMedCrossRefGoogle Scholar
  59. Jeffery JM, Urquhart AJ, Subramaniam VN, Parton RG, Khanna KK (2010) Centrobin regulates the assembly of functional mitotic spindles. Oncogene 29:2649–2658PubMedCrossRefGoogle Scholar
  60. Jeong Y, Lee J, Kim K, Yoo JC, Rhee K (2007) Characterization of NIP2/centrobin, a novel substrate of Nek2, and its potential role in microtubule stabilization. J Cell Sci 120:2106–2116. doi: 10.1242/jcs.03458 PubMedCrossRefGoogle Scholar
  61. Joukov V, De Nicolo A, Rodriguez A, Walter JC, Livingston DM (2010) Centrosomal protein of 192 kDa (Cep192) promotes centrosome-driven spindle assembly by engaging in organelle-specific Aurora A activation. Proc Natl Acad Sci 107:21022–21027. doi: 10.1073/pnas.1014664107 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Joukov V, Walter JC, De Nicolo A (2014) The Cep192-organized aurora A-Plk1 cascade is essential for centrosome cycle and bipolar spindle assembly. Mol Cell 55:578–591. doi: 10.1016/j.molcel.2014.06.016 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kaindl AM (2014) Autosomal recessive primary microcephalies (MCPH). Eur J Paediatr Neurol 18:547–548. doi: 10.1016/j.ejpn.2014.03.010 PubMedCrossRefGoogle Scholar
  64. Keryer G, Di Fiore B, Celati C, Lechtreck KF, Mogensen M, Delouvée A, Lavia P, Bornens M, Tassin A-M (2003a) Part of Ran is associated with AKAP450 at the centrosome: involvement in microtubule-organizing activity. Mol Biol Cell 14:4260–4271PubMedPubMedCentralCrossRefGoogle Scholar
  65. Keryer G, Witczak O, Delouvée A, Kemmner WA, Rouillard D, Taskén K, Bornens M (2003b) Dissociating the centrosomal matrix protein AKAP450 from centrioles impairs centriole duplication and cell cycle progression. Mol Biol Cell 14:2436–2446PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kim T-S, Park J-E, Shukla A, Choi S, Murugan RN, Lee JH, Ahn M, Rhee K, Bang JK, Kim BY, Loncarek J, Erikson RL, Lee KS (2013) Hierarchical recruitment of Plk4 and regulation of centriole biogenesis by two centrosomal scaffolds, Cep192 and Cep152. Proc Natl Acad Sci 110:E4849–E4857. doi: 10.1073/pnas.1319656110 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kirkham M, Müller-Reichert T, Oegema K, Grill S, Hyman AA (2003) SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112:575–587PubMedCrossRefGoogle Scholar
  68. Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, Bortfeld M, Erat MC, Flückiger I, Gönczy P, Steinmetz MO (2011) Structural basis of the 9-fold symmetry of centrioles. Cell 144:364–375. doi: 10.1016/j.cell.2011.01.008 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof Y-D, Nigg EA (2007) Plk4-induced centriole biogenesis in human cells. Dev Cell 13:190–202. doi: 10.1016/j.devcel.2007.07.002 PubMedCrossRefGoogle Scholar
  70. Kobayashi T (1975) Dephosphorylation of tubulin-bound Gaunosine triphosphate during microtubule assembly. J Biochem (Tokyo) 77:1193–1197Google Scholar
  71. Kodani A, Salomé Sirerol‐Piquer M, Seol A, Manuel Garcia‐Verdugo J, Reiter JF (2013) Kif3a interacts with Dynactin subunit p150Glued to organize centriole subdistal appendages. EMBO J 32:597–607. doi: 10.1038/emboj.2013.3 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Korzeniewski N, Cuevas R, Duensing A, Duensing S (2010) Daughter centriole elongation is controlled by proteolysis. Mol Biol Cell 21:3942–3951PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kraemer N, Issa L, Hauck SCR, Mani S, Ninnemann O, Kaindl AM (2011) What’s the hype about CDK5RAP2? Cell Mol Life Sci 68:1719–1736. doi: 10.1007/s00018-011-0635-4 PubMedCrossRefGoogle Scholar
  74. Kubo A (2003) Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J Cell Sci 116:919–928. doi: 10.1242/jcs.00282 PubMedCrossRefGoogle Scholar
  75. Kubo A, Sasaki H, Yuba-Kubo A, Tsukita S, Shiina N, Centriolar Satellites Molecular Characterization (1999) Atp-dependent movement toward centrioles and possible involvement in ciliogenesis. J Cell Biol 147:969–980PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kumar A, Girimaji SC, Duvvari MR, Blanton SH (2009) Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly. Am J Hum Genet 84:286–290. doi: 10.1016/j.ajhg.2009.01.017 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lane HA, Nigg EA (1996) Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J Cell Biol 135:1701–1713PubMedCrossRefGoogle Scholar
  78. Lawo S, Bashkurov M, Mullin M, Ferreria MG, Kittler R, Habermann B, Tagliaferro A, Poser I, Hutchins JRA, Hegemann B, Pinchev D, Buchholz F, Peters J-M, Hyman AA, Gingras A-C, Pelletier L (2009) HAUS, the 8-subunit human augmin complex, regulates centrosome and spindle integrity. Curr Biol 19:816–826. doi: 10.1016/j.cub.2009.04.033 PubMedCrossRefGoogle Scholar
  79. Lawo S, Hasegan M, Gupta GD, Pelletier L (2012) Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat Cell Biol 14:1148–1158. doi: 10.1038/ncb2591 PubMedCrossRefGoogle Scholar
  80. Leal GF, Roberts E, Silva EO, Costa SMR, Hampshire DJ, Woods CG (2003) A novel locus for autosomal recessive primary microcephaly (MCPH6) maps to 13q12. 2. J Med Genet 40:540–542PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lee S, Rhee K (2010) CEP215 is involved in the dynein-dependent accumulation of pericentriolar matrix proteins for spindle pole formation. Cell Cycle 9:774–783PubMedGoogle Scholar
  82. Lee K, Rhee K (2011) PLK1 phosphorylation of pericentrin initiates centrosome maturation at the onset of mitosis. J Cell Biol 195:1093–1101. doi: 10.1083/jcb.201106093 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lee J, Jeong Y, Jeong S, Rhee K (2010) Centrobin/NIP2 is a microtubule stabilizer whose activity is enhanced by PLK1 phosphorylation during mitosis. J Biol Chem 285:25476–25484. doi: 10.1074/jbc.M109.099127 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Leidel S, Gönczy P (2003) SAS-4 is essential for centrosome duplication in C. elegans and is recruited to daughter centrioles once per cell cycle. Dev Cell 4:431–439PubMedCrossRefGoogle Scholar
  85. Lerit DA, Rusan NM (2013) PLP inhibits the activity of interphase centrosomes to ensure their proper segregation in stem cells. J Cell Biol 202:1013–1022. doi: 10.1083/jcb.201303141 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Li Q, Hansen D, Killilea A, Joshi HC, Palazzo RE, Balczon R (2001) Kendrin/pericentrin-B, a centrosome protein with homology to pericentrin that complexes with PCM-1. J Cell Sci 114:797–809PubMedGoogle Scholar
  87. Lin Y-C, Chang C-W, Hsu W-B, Tang C-JC, Lin Y-N, Chou E-J, Wu C-T, Tang TK (2013) Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J 32:1141–1154Google Scholar
  88. Lin Y-N, Wu C-T, Lin Y-C, Hsu W-B, Tang C-JC, Chang C-W, Tang TK (2013b) CEP120 interacts with CPAP and positively regulates centriole elongation. J Cell Biol 202:211–219. doi: 10.1083/jcb.201212060 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lin T, 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, e02208PubMedPubMedCentralGoogle Scholar
  90. Löffler H, Fechter A, Liu FY, Poppelreuther S, Krämer A (2012) DNA damage-induced centrosome amplification occurs via excessive formation of centriolar satellites. Oncogene 32:2963–2972PubMedCrossRefGoogle Scholar
  91. Lüders J, Stearns T (2007) Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8:161–167PubMedCrossRefGoogle Scholar
  92. Lüders J, Patel UK, Stearns T (2006) GCP-WD is a γ-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat Cell Biol 8:137–147. doi: 10.1038/ncb1349 PubMedCrossRefGoogle Scholar
  93. Mahjoub MR, Xie Z, Stearns T (2010) Cep120 is asymmetrically localized to the daughter centriole and is essential for centriole assembly. J Cell Biol 191:331–346. doi: 10.1083/jcb.201003009 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Megraw TL (2002) The centrosome is a dynamic structure that ejects PCM flares. J Cell Sci 115:4707–4718. doi: 10.1242/jcs.00134 PubMedCrossRefGoogle Scholar
  95. Mennella V, Keszthelyi B, McDonald KL, Chhun B, Kan F, Rogers GC, Huang B, Agard DA (2012) Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 14:1159–1168. doi: 10.1038/ncb2597 PubMedPubMedCentralCrossRefGoogle Scholar
  96. Miyoshi K, Asanuma M, Miyazaki I, Diaz-Corrales FJ, Katayama T, Tohyama M, Ogawa N (2004) DISC1 localizes to the centrosome by binding to kendrin. Biochem Biophys Res Commun 317:1195–1199. doi: 10.1016/j.bbrc.2004.03.163 PubMedCrossRefGoogle Scholar
  97. Mogensen MM, Malik A, Piel M, Bouckson-Castaing V, Bornens M (2000) Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J Cell Sci 113:3013–3023PubMedGoogle Scholar
  98. Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441:1068–1074. doi: 10.1038/nature04956 PubMedCrossRefGoogle Scholar
  99. Moynihan L, Jackson AP, Roberts E, Karbani G, Lewis I, Corry P, Turner G, Mueller RF, Lench NJ, Woods CG (2000) A third novel locus for primary autosomal recessive microcephaly maps to chromosome 9q34. Am J Hum Genet 66:724–727PubMedPubMedCentralCrossRefGoogle Scholar
  100. Nagase T, Kikuno R, Nakayama M, Hirosawa M, Ohara O (2000) Prediction of the coding sequences of unidentified human genes. XVIII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res 7:271–281CrossRefGoogle Scholar
  101. O’Rourke BP, Gomez-Ferreria MA, Berk RH, Hackl AMU, Nicholas MP, O’Rourke SC, Pelletier L, Sharp DJ (2014) Cep192 controls the balance of centrosome and non-centrosomal microtubules during interphase. PLoS One 9, e101001. doi: 10.1371/journal.pone.0101001 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Oshimori N, Ohsugi M, Yamamoto T (2006) The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity. Nat Cell Biol 8:1095–1101. doi: 10.1038/ncb1474 PubMedCrossRefGoogle Scholar
  103. Oshimori N, Li X, Ohsugi M, Yamamoto T (2009) Cep72 regulates the localization of key centrosomal proteins and proper bipolar spindle formation. EMBO J 28:2066–2076PubMedPubMedCentralCrossRefGoogle Scholar
  104. Ou YY, Mack GJ, Zhang M, Rattner JB (2002) CEP110 and ninein are located in a specific domain of the centrosome associated with centrosome maturation. J Cell Sci 115:1825–1835PubMedGoogle Scholar
  105. Ou Y, Zhang M, Rattner JB (2004) The centrosome: the centriole-PCM coalition. Cell Motil Cytoskeleton 57:1–7PubMedCrossRefGoogle Scholar
  106. Pelletier L, O’Toole E, Schwager A, Hyman AA, Müller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444:619–623. doi: 10.1038/nature05318 PubMedCrossRefGoogle Scholar
  107. Petronczki M, Lénárt P, Peters J-M (2008) Polo on the rise—from mitotic entry to cytokinesis with Plk1. Dev Cell 14:646–659. doi: 10.1016/j.devcel.2008.04.014 PubMedCrossRefGoogle Scholar
  108. Piehl M, Tulu US, Wadsworth P, Cassimeris L (2004) Centrosome maturation: measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc Natl Acad Sci U S A 101:1584–1588PubMedPubMedCentralCrossRefGoogle Scholar
  109. Prosser SL, Straatman KR, Fry AM (2009) Molecular dissection of the centrosome overduplication pathway in S-phase-arrested cells. Mol Cell Biol 29:1760–1773. doi: 10.1128/MCB.01124-08 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Puklowski A, Homsi Y, Keller D, May M, Chauhan S, Kossatz U, Grünwald V, Kubicka S, Pich A, Manns MP, Hoffmann I, Gönczy P, Malek NP (2011) The SCF–FBXW5 E3-ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nat Cell Biol 13:1004–1009. doi: 10.1038/ncb2282 PubMedCrossRefGoogle Scholar
  111. Qian Y-W, Erikson E, Maller JL (1999) Mitotic effects of a constitutively active mutant of the Xenopus polo-like kinase Plx1. Mol Cell Biol 19:8625–8632PubMedPubMedCentralCrossRefGoogle Scholar
  112. Rapley J, Baxter JE, Blot J, Wattam SL, Casenghi M, Meraldi P, Nigg EA, Fry AM (2005) Coordinate regulation of the mother centriole component Nlp by Nek2 and Plk1 protein kinases. Mol Cell Biol 25:1309–1324. doi: 10.1128/MCB.25.4.1309-1324.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rauch A, Thiel CT, Schindler D, Wick U, Crow YJ, Ekici AB, van Essen AJ, Goecke TO, Al-Gazali L, Chrzanowska KH, Zweier C, Brunner HG, Becker K, Curry CJ, Dallapiccola B, Devriendt K, Dorfler A, Kinning E, Megarbane A, Meinecke P, Semple RK, Spranger S, Toutain A, Trembath RC, Voss E, Wilson L, Hennekam R, de Zegher F, Dorr H-G, Reis A (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319:816–819. doi: 10.1126/science.1151174 PubMedCrossRefGoogle Scholar
  114. Reina J, Gonzalez C (2014) When fate follows age: unequal centrosomes in asymmetric cell division. Philos Trans R Soc B Biol Sci 369:20130466–20130466. doi: 10.1098/rstb.2013.0466
  115. Rivero S, Cardenas J, Bornens M, Rios RM (2009) Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 28:1016–1028PubMedPubMedCentralCrossRefGoogle Scholar
  116. Schermelleh L, Heintzmann R, Leonhardt H (2010) A guide to super-resolution fluorescence microscopy. J Cell Biol 190:165–175. doi: 10.1083/jcb.201002018 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Schmidt PH, Dransfield DT, Claudio JO, Hawley RG, Trotter KW, Milgram SL, Goldenring JR (1999) AKAP350, a multiply spliced protein kinase A-anchoring protein associated with centrosomes. J Biol Chem 274:3055–3066. doi: 10.1074/jbc.274.5.3055 PubMedCrossRefGoogle Scholar
  118. Sdelci S, Schütz M, Pinyol R, Bertran MT, Regué L, Caelles C, Vernos I, Roig J (2012) Nek9 phosphorylation of NEDD1/GCP-WD contributes to Plk1 control of γ-tubulin recruitment to the mitotic centrosome. Curr Biol 22:1516–1523. doi: 10.1016/j.cub.2012.06.027 PubMedCrossRefGoogle Scholar
  119. Seki A, Coppinger JA, Du H, Jang C-Y, Yates JR, Fang G (2008a) Plk1- and -TrCP-dependent degradation of Bora controls mitotic progression. J Cell Biol 181:65–78. doi: 10.1083/jcb.200712027 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Seki A, Coppinger JA, Jang C-Y, Yates JR, Fang G (2008b) Bora and the kinase aurora A cooperatively activate the kinase Plk1 and control mitotic entry. Science 320:1655–1658. doi: 10.1126/science.1157425 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Shimanovskaya E, Viscardi V, Lesigang J, Lettman MM, Qiao R, Svergun DI, Round A, Oegema K, Dong G (2014) Structure of the C. elegans ZYG-1 cryptic polo box suggests a conserved mechanism for centriolar docking of Plk4 kinases. Structure 22:1090–1104. doi: 10.1016/j.str.2014.05.009 PubMedPubMedCentralCrossRefGoogle Scholar
  122. Shiratsuchi G, Takaoka K, Ashikawa T, Hamada H, Kitagawa D (2014) RBM14 prevents assembly of centriolar protein complexes and maintains mitotic spindle integrity. EMBO J. doi: 10.15252/embj.201488979 PubMedPubMedCentralGoogle Scholar
  123. Sillibourne JE, Milne DM, Takahashi M, Ono Y, Meek DW (2002) Centrosomal anchoring of the protein kinase CK1δ mediated by attachment to the large, coiled-coil scaffolding protein CG-NAP/AKAP450. J Mol Biol 322:785–797. doi: 10.1016/S0022-2836(02)00857-4 PubMedCrossRefGoogle Scholar
  124. Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA (2012) 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open 1:965–976. doi: 10.1242/bio.20122337 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Sonnen KF, Gabryjonczyk A-M, Anselm E, Stierhof Y-D, Nigg EA (2013) Human Cep192 and Cep152 cooperate in Plk4 recruitment and centriole duplication. J Cell Sci 126:3223–3233. doi: 10.1242/jcs.129502 PubMedCrossRefGoogle Scholar
  126. Soung N-K, Kang YH, Kim K, Kamijo K, Yoon H, Seong Y-S, Kuo Y-L, Miki T, Kim SR, Kuriyama R, Giam C-Z, Ahn CH, Lee KS (2006) Requirement of hCenexin for proper mitotic functions of polo-like kinase 1 at the centrosomes. Mol Cell Biol 26:8316–8335. doi: 10.1128/MCB.00671-06 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Soung N-K, Park J-E, Yu L-R, Lee KH, Lee J-M, Bang JK, Veenstra TD, Rhee K, Lee KS (2009) Plk1-dependent and -independent roles of an ODF2 splice variant, hCenexin1, at the centrosome of somatic cells. Dev Cell 16:539–550. doi: 10.1016/j.devcel.2009.02.004 PubMedPubMedCentralCrossRefGoogle Scholar
  128. Takahashi M, Shibata H, Shimakawa M, Miyamoto M, Mukai H, Ono Y (1999) Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the Golgi apparatus. J Biol Chem 274:17267–17274. doi: 10.1074/jbc.274.24.17267 PubMedCrossRefGoogle Scholar
  129. Takahashi M, Yamagiwa A, Nishimura T, Mukai H, Ono Y (2002) Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring γ-tubulin ring complex. Mol Biol Cell 13:3235–3245PubMedPubMedCentralCrossRefGoogle Scholar
  130. Tang C-JC, Lin S-Y, Hsu W-B, Lin Y-N, Wu C-T, Lin Y-C, Chang C-W, Wu K-S, Tang TK (2011) The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J 30:4790–4804PubMedPubMedCentralCrossRefGoogle Scholar
  131. Telzer BR, Rosenbaum JL (1979) Cell cycle-dependent, in vitro assembly of microtubules onto pericentriolar material of HeLa cells. J Cell Biol 81:484–497PubMedCrossRefGoogle Scholar
  132. Tollenaere MAX, Mailand N, Bekker-Jensen S (2015) Centriolar satellites: key mediators of centrosome functions. Cell Mol Life Sci 72:11–23. doi: 10.1007/s00018-014-1711-3 PubMedCrossRefGoogle Scholar
  133. van Breugel M, Hirono M, Andreeva A, Yanagisawa H-a, Yamaguchi S, Nakazawa Y, Morgner N, Petrovich M, Ebong I-O, Robinson CV, Johnson CM, Veprintsev D, Zuber B (2011) Structures of SAS-6 suggest its organization in centrioles. Science 331:1196–1199. doi: 10.1126/science.1199325
  134. Wang Y, Zhan Q (2007) Cell cycle-dependent expression of centrosomal ninein-like protein in human cells is regulated by the anaphase-promoting complex. J Biol Chem 282:17712–17719. doi: 10.1074/jbc.M701350200 PubMedCrossRefGoogle Scholar
  135. Wang X, Tsai J-W, Imai JH, Lian W-N, Vallee RB, Shi S-H (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461:947–955. doi: 10.1038/nature08435 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Wang Z, Wu T, Shi L, Zhang L, Zheng W, Qu JY, Niu R, Qi RZ (2010) Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex. J Biol Chem 285:22658–22665. doi: 10.1074/jbc.M110.105965 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Witczak O, Sk\a alhegg BS, Keryer G, Bornens M, Taskén K, Jahnsen T, Ørstavik S (1999) Cloning and characterization of a cDNA encoding an A-kinase anchoring protein located in the centrosome, AKAP450. EMBO J 18:1858–1868Google Scholar
  138. Xie Z, Moy LY, Sanada K, Zhou Y, Buchman JJ, Tsai L-H (2007) Cep120 and TACCs control interkinetic nuclear migration and the neural progenitor pool. Neuron 56:79–93. doi: 10.1016/j.neuron.2007.08.026 PubMedPubMedCentralCrossRefGoogle Scholar
  139. Yamanaka M, Smith NI, Fujita K (2014) Introduction to super-resolution microscopy. Microscopy 63:177–192. doi: 10.1093/jmicro/dfu007 PubMedCrossRefGoogle Scholar
  140. Zhang X, Chen Q, Feng J, Hou J, Yang F, Liu J, Jiang Q, Zhang C (2009a) Sequential phosphorylation of Nedd1 by Cdk1 and Plk1 is required for targeting of the TuRC to the centrosome. J Cell Sci 122:2240–2251. doi: 10.1242/jcs.042747 PubMedCrossRefGoogle Scholar
  141. Zhang X, Liu D, Lv S, Wang H, Zhong X, Liu B, Wang B, Liao J, Li J, Pfeifer GP, Others (2009b) CDK5RAP2 is required for spindle checkpoint function. Cell Cycle 8:1206–1216PubMedPubMedCentralCrossRefGoogle Scholar
  142. Zhao X, Jin S, Song Y, Zhan Q (2010) Cdc2/cyclin B1 regulates centrosomal Nlp proteolysis and subcellular localization. Cancer Biol Ther 10:945–952. doi: 10.4161/cbt.10.9.13368 PubMedCrossRefGoogle Scholar
  143. Zhu F, Lawo S, Bird A, Pinchev D, Ralph A, Richter C, Müller-Reichert T, Kittler R, Hyman AA, Pelletier L (2008) The mammalian SPD-2 ortholog Cep192 regulates centrosome biogenesis. Curr Biol 18:136–141. doi: 10.1016/j.cub.2007.12.055 PubMedCrossRefGoogle Scholar
  144. Zimmerman WC, Sillibourne J, Rosa J, Doxsey SJ (2004) Mitosis-specific anchoring of γ tubulin complexes by pericentrin controls spindle organization and mitotic entry. Mol Biol Cell 15:3642–3657PubMedPubMedCentralCrossRefGoogle Scholar
  145. Zitouni S, Nabais C, Jana SC, Guerrero A, Bettencourt-Dias M (2014) Polo-like kinases: structural variations lead to multiple functions. Nat Rev Mol Cell Biol 15:433–452. doi: 10.1038/nrm3819 PubMedCrossRefGoogle Scholar
  146. Zou C (2005) Centrobin: a novel daughter centriole-associated protein that is required for centriole duplication. J Cell Biol 171:437–445. doi: 10.1083/jcb.200506185 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Lunenfeld-Tanenbaum Research Institute, Mount Sinai HospitalTorontoCanada
  2. 2.Department of Molecular GeneticsUniversity of TorontoTorontoCanada

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