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Cellular and Molecular Life Sciences

, Volume 72, Issue 1, pp 11–23 | Cite as

Centriolar satellites: key mediators of centrosome functions

  • Maxim A. X. Tollenaere
  • Niels MailandEmail author
  • Simon Bekker-JensenEmail author
Review

Abstract

Centriolar satellites are small, microscopically visible granules that cluster around centrosomes. These structures, which contain numerous proteins directly involved in centrosome maintenance, ciliogenesis, and neurogenesis, have traditionally been viewed as vehicles for protein trafficking towards the centrosome. However, the recent identification of several new centriolar satellite components suggests that this model offers only an incomplete picture of their cellular functions. While the mechanisms controlling centriolar satellite status and function are not yet understood in detail, emerging evidence points to these structures as important hubs for dynamic, multi-faceted regulation in response to a variety of cues. In this review, we summarize the current knowledge of the roles of centriolar satellites in regulating centrosome functions, ciliogenesis, and neurogenesis. We also highlight newly discovered regulatory mechanisms targeting centriolar satellites and their functional status, and we discuss how defects in centriolar satellite components are intimately linked to a wide spectrum of human diseases.

Keywords

Centriolar satellites Centrosome Ciliogenesis Neurogenesis PCM1 Protein transport 

Notes

Acknowledgments

Work in the laboratory of the authors is funded by the Novo Nordisk Foundation, Danish Medical Research Council, the Danish Cancer Society, and the Lundbeck Foundation.

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1.
    Balczon R, Bao L, Zimmer WE (1994) PCM-1, A 228-kD centrosome autoantigen with a distinct cell cycle distribution. J Cell Biol 124:783–793PubMedCrossRefGoogle Scholar
  2. 2.
    Kubo A, Sasaki H, Yuba-Kubo A et al (1999) Centriolar satellites: molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis. J Cell Biol 147:969–980PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Kubo A, Tsukita S (2003) Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J Cell Sci 116:919–928PubMedCrossRefGoogle Scholar
  4. 4.
    Dammermann A, Merdes A (2002) Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255–266. doi: 10.1083/jcb.200204023 PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Bernhard W, de Harven E (1960) L’ultrastructure du centriole et d’autres éléments de l’appareil achromatique. In: Bargmann W, Peters D, Wolpers C (eds) Verhandlungen Band II/Biologisch-Medizinischer Teil. Springer Berlin Heidelberg, pp 217–227Google Scholar
  6. 6.
    Nigg EA, Raff JW (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139:663–678. doi: 10.1016/j.cell.2009.10.036 PubMedCrossRefGoogle Scholar
  7. 7.
    Doxsey S, Zimmerman W, Mikule K (2005) Centrosome control of the cell cycle. Trends Cell Biol 15:303–311. doi: 10.1016/j.tcb.2005.04.008 PubMedCrossRefGoogle Scholar
  8. 8.
    Ishikawa H, Marshall WF (2011) Ciliogenesis: building the cell’s antenna. Nat Rev Mol Cell Biol 12:222–234. doi: 10.1038/nrm3085 PubMedCrossRefGoogle Scholar
  9. 9.
    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
  10. 10.
    Lopes CAM, Prosser SL, Romio L et al (2011) Centriolar satellites are assembly points for proteins implicated in human ciliopathies, including oral-facial-digital syndrome 1. J Cell Sci 124:600–612. doi: 10.1242/jcs.077156 PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Engelender S, Sharp AH, Colomer V et al (1997) Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum Mol Genet 6:2205–2212PubMedCrossRefGoogle Scholar
  12. 12.
    Wang G, Chen Q, Zhang X et al (2013) PCM1 recruits Plk1 to the pericentriolar matrix to promote primary cilia disassembly before mitotic entry. J Cell Sci 126:1355–1365. doi: 10.1242/jcs.114918 PubMedCrossRefGoogle Scholar
  13. 13.
    Kamiya A, Tan PL, Kubo K-I et al (2008) Recruitment of PCM1 to the centrosome by the cooperative action of DISC1 and BBS4: a candidate for psychiatric illnesses. Arch Gen Psychiatry 65:996–1006. doi: 10.1001/archpsyc.65.9.996 PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Graser S, Stierhof Y-D, Lavoie SB et al (2007) Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol 179:321–330. doi: 10.1083/jcb.200707181 PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Kim K, Rhee K (2011) The pericentriolar satellite protein CEP90 is crucial for integrity of the mitotic spindle pole. J Cell Sci 124:338–347. doi: 10.1242/jcs.078329 PubMedCrossRefGoogle Scholar
  16. 16.
    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 PubMedGoogle Scholar
  17. 17.
    Srsen V, Gnadt N, Dammermann A, Merdes A (2006) Inhibition of centrosome protein assembly leads to p53-dependent exit from the cell cycle. J Cell Biol 174:625–630. doi: 10.1083/jcb.200606051 PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Bärenz F, Inoue D, Yokoyama H et al (2013) The centriolar satellite protein SSX2IP promotes centrosome maturation. J Cell Biol 202:81–95. doi: 10.1083/jcb.201302122 PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Puram SV, Kim AH, Ikeuchi Y et al (2011) A CaMKIIβ signaling pathway at the centrosome regulates dendrite patterning in the brain. Nat Neurosci 14:973–983. doi: 10.1038/nn.2857 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Ge XX, Frank CLC, de Anda FFC, Tsai L-HL (2010) Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 65:13. doi: 10.1016/j.neuron.2010.01.011 CrossRefGoogle Scholar
  21. 21.
    Piel M, Meyer P, Khodjakov A et al (2000) The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J Cell Biol 149:317–330PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Li Q, Hansen D, Killilea A et al (2001) Kendrin/pericentrin-B, a centrosome protein with homology to pericentrin that complexes with PCM-1. J Cell Sci 114:797–809PubMedGoogle Scholar
  23. 23.
    Young A, Dictenberg JB, Purohit A et al (2000) Cytoplasmic dynein-mediated assembly of pericentrin and gamma tubulin onto centrosomes. Mol Biol Cell 11:2047–2056PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Kim JC, Badano JL, Sibold S et al (2004) The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat Genet 36:462–470. doi: 10.1038/ng1352 PubMedCrossRefGoogle Scholar
  25. 25.
    Kodani A, Tonthat V, Wu B, Sütterlin C (2010) Par6 alpha interacts with the dynactin subunit p150 Glued and is a critical regulator of centrosomal protein recruitment. Mol Biol Cell 21:3376–3385. doi: 10.1091/mbc.E10-05-0430 PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Kim J, Krishnaswami SR, Gleeson JG (2008) CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum Mol Genet 17:3796–3805. doi: 10.1093/hmg/ddn277 PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Hames RSR, Crookes RER, Straatman KRK et al (2005) Dynamic recruitment of Nek2 kinase to the centrosome involves microtubules, PCM-1, and localized proteasomal degradation. Mol Biol Cell 16:1711–1724. doi: 10.1091/mbc.E04-08-0688 PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Oshimori N, Li X, Ohsugi M, Yamamoto T (2009) Cep72 regulates the localization of key centrosomal proteins and proper bipolar spindle formation. EMBO J 28:2066–2076. doi: 10.1038/emboj.2009.161 PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Stowe TR, Wilkinson CJ, Iqbal A, Stearns T (2012) The centriolar satellite proteins Cep72 and Cep290 interact and are required for recruitment of BBS proteins to the cilium. Mol Biol Cell 23:3322–3335. doi: 10.1091/mbc.E12-02-0134 PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    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 USA 101:1584–1588. doi: 10.1073/pnas.0308205100 PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Avidor-Reiss T, Gopalakrishnan J (2013) Building a centriole. Curr Opin Cell Biol 25:72–77. doi: 10.1016/j.ceb.2012.10.016 PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Doxsey S (2001) Re-evaluating centrosome function. Nat Rev Mol Cell Biol 2:688–698. doi: 10.1038/35089575 PubMedCrossRefGoogle Scholar
  33. 33.
    Blagden SP, Glover DM (2003) Polar expeditions–provisioning the centrosome for mitosis. Nat Cell Biol 5:505–511. doi: 10.1038/ncb0603-505 PubMedCrossRefGoogle Scholar
  34. 34.
    Staples CJ, Myers KN, Beveridge RDD et al (2012) The centriolar satellite protein Cep131 is important for genome stability. J Cell Sci 125:4770–4779. doi: 10.1242/jcs.104059 PubMedCrossRefGoogle Scholar
  35. 35.
    Staples CJ, Myers KN, Beveridge RDD et al (2014) Ccdc13; a novel human centriolar satellite protein required for ciliogenesis and genome stability. J Cell Sci. doi: 10.1242/jcs.147785 PubMedGoogle Scholar
  36. 36.
    Nachury MV, Loktev AV, Zhang Q et al (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201–1213. doi: 10.1016/j.cell.2007.03.053 PubMedCrossRefGoogle Scholar
  37. 37.
    Chamling X, Seo S, Searby CC et al (2014) The centriolar satellite protein AZI1 interacts with BBS4 and regulates ciliary trafficking of the BBSome. PLoS Genet 10:e1004083. doi: 10.1371/journal.pgen.1004083 PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Kim K, Lee K, Rhee K (2012) CEP90 is required for the assembly and centrosomal accumulation of centriolar satellites, which is essential for primary cilia formation. PLoS One 7:e48196. doi: 10.1371/journal.pone.0048196 PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    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
  40. 40.
    Kimura M, Yoshioka T, Saio M et al (2013) Mitotic catastrophe and cell death induced by depletion of centrosomal proteins. Cell Death Dis 4:e603. doi: 10.1038/cddis.2013.108 PubMedCentralPubMedCrossRefGoogle Scholar
  41. 41.
    Vladar EK, Stearns T (2007) Molecular characterization of centriole assembly in ciliated epithelial cells. J Cell Biol 178:31–42. doi: 10.1083/jcb.200703064 PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Ye X, Zeng H, Ning G et al (2014) C2cd3 is critical for centriolar distal appendage assembly and ciliary vesicle docking in mammals. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1318737111 Google Scholar
  43. 43.
    Hames RS, Fry AM (2002) Alternative splice variants of the human centrosome kinase Nek2 exhibit distinct patterns of expression in mitosis. Biochem J 361:77–85PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Lacey KR, Jackson PK, Stearns T (1999) Cyclin-dependent kinase control of centrosome duplication. Proc Natl Acad Sci USA 96:2817–2822PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Krämer A, Mailand N, Lukas C et al (2004) Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 6:884–891. doi: 10.1038/ncb1165 PubMedCrossRefGoogle Scholar
  46. 46.
    Brown NJ, Marjanović M, Lüders J et al (2013) Cep63 and cep152 cooperate to ensure centriole duplication. PLoS One 8:e69986. doi: 10.1371/journal.pone.0069986 PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    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 PubMedCrossRefGoogle Scholar
  48. 48.
    Mikule K, Delaval B, Kaldis P et al (2007) Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest. Nat Cell Biol 9:160–170PubMedCrossRefGoogle Scholar
  49. 49.
    Goetz SC, Anderson KV (2010) The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11:331–344. doi: 10.1038/nrg2774 PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Babu D, Roy S (2013) Left-right asymmetry: cilia stir up new surprises in the node. Open Biol 3:130052. doi: 10.1098/rsob.130052 PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Ansley SJ, Badano JL, Blacque OE et al (2003) Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425:628–633. doi: 10.1038/nature02030 PubMedCrossRefGoogle Scholar
  52. 52.
    Tsang WY, Bossard C, Khanna H et al (2008) CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev Cell 15:187–197. doi: 10.1016/j.devcel.2008.07.004 PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Goetz SC, Liem KF, Anderson KV (2012) The spinocerebellar ataxia-associated gene Tau tubulin kinase 2 controls the initiation of ciliogenesis. Cell 151:847–858. doi: 10.1016/j.cell.2012.10.010 PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Pedersen LB, Rosenbaum JL (2008) Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85:23–61. doi: 10.1016/S0070-2153(08)00802-8 PubMedCrossRefGoogle Scholar
  55. 55.
    Jin H, White SR, Shida T et al (2010) The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141:1208–1219. doi: 10.1016/j.cell.2010.05.015 PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Tadenev ALD, Kulaga HM, May-Simera HL et al (2011) Loss of Bardet-Biedl syndrome protein-8 (BBS8) perturbs olfactory function, protein localization, and axon targeting. Proc Natl Acad Sci USA 108:10320–10325. doi: 10.1073/pnas.1016531108 PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Tan PL, Barr T, Inglis PN et al (2007) Loss of Bardet Biedl syndrome proteins causes defects in peripheral sensory innervation and function. Proc Natl Acad Sci USA 104:17524–17529. doi: 10.1073/pnas.0706618104 PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Kulaga HM, Leitch CC, Eichers ER et al (2004) Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 36:994–998. doi: 10.1038/ng1418 PubMedCrossRefGoogle Scholar
  59. 59.
    Eichers ER, Abd-El-Barr MM, Paylor R et al (2006) Phenotypic characterization of Bbs4 null mice reveals age-dependent penetrance and variable expressivity. Hum Genet 120:211–226. doi: 10.1007/s00439-006-0197-y PubMedCrossRefGoogle Scholar
  60. 60.
    Coppieters F, Lefever S, Leroy BP, De Baere E (2010) CEP290, a gene with many faces: mutation overview and presentation of CEP290base. Hum Mutat 31:1097–1108. doi: 10.1002/humu.21337 PubMedCrossRefGoogle Scholar
  61. 61.
    Fattahi Z, Rostami P, Najmabadi A et al (2014) Mutation profile of BBS genes in Iranian patients with Bardet-Biedl syndrome: genetic characterization and report of nine novel mutations in five BBS genes. J Hum Genet. doi: 10.1038/jhg.2014.28 PubMedGoogle Scholar
  62. 62.
    Zhang Q, Yu D, Seo S et al (2012) Intrinsic protein–protein interaction-mediated and chaperonin-assisted sequential assembly of stable Bardet-Biedl syndrome protein complex, the BBSome. J Biol Chem 287:20625–20635. doi: 10.1074/jbc.M112.341487 PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Zhang Y, Seo S, Bhattarai S et al (2014) BBS mutations modify phenotypic expression of CEP290-related ciliopathies. Hum Mol Genet 23:40–51. doi: 10.1093/hmg/ddt394 PubMedCrossRefGoogle Scholar
  64. 64.
    Wilkinson CJ, Carl M, Harris WA (2009) Cep70 and Cep131 contribute to ciliogenesis in zebrafish embryos. BMC Cell Biol 10:17. doi: 10.1186/1471-2121-10-17 PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Ma L, Jarman AP (2011) Dilatory is a drosophila protein related to AZI1 (CEP131) that is located at the ciliary base and required for cilium formation. J Cell Sci 124:2622–2630. doi: 10.1242/jcs.084798 PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Hall EA, Keighren M, Ford MJ et al (2013) Acute versus chronic loss of mammalian azi1/cep131 results in distinct ciliary phenotypes. PLoS Genet 9:e1003928. doi: 10.1371/journal.pgen.1003928 PubMedCentralPubMedCrossRefGoogle Scholar
  67. 67.
    Akimov V, Rigbolt KTG, Nielsen MM, Blagoev B (2011) Characterization of ubiquitination dependent dynamics in growth factor receptor signaling by quantitative proteomics. Mol BioSyst 7:3223–3233. doi: 10.1039/c1mb05185g PubMedCrossRefGoogle Scholar
  68. 68.
    Villumsen BH, Danielsen JR, Povlsen L et al (2013) A new cellular stress response that triggers centriolar satellite reorganization and ciliogenesis. EMBO J. doi: 10.1038/emboj.2013.223 PubMedCentralPubMedGoogle Scholar
  69. 69.
    Chavali PL, Gergely F (2013) Cilia born out of shock and stress. EMBO J 32:3011–3013. doi: 10.1038/emboj.2013.241 PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Tang Z, Lin MG, Stowe TR et al (2013) Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature. doi: 10.1038/nature12606 Google Scholar
  71. 71.
    Romio L, Fry AM, Winyard PJD et al (2004) OFD1 is a centrosomal/basal body protein expressed during mesenchymal-epithelial transition in human nephrogenesis. J Am Soc Nephrol 15:2556–2568. doi: 10.1097/01.ASN.0000140220.46477.5C PubMedCrossRefGoogle Scholar
  72. 72.
    Singla V, Romaguera-Ros M, Garcia-Verdugo JM, Reiter JF (2010) Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev Cell 18:410–424. doi: 10.1016/j.devcel.2009.12.022 PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Ferrante MI, Zullo A, Barra A et al (2006) Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Nat Genet 38:112–117. doi: 10.1038/ng1684 PubMedCrossRefGoogle Scholar
  74. 74.
    Coene KLM, Roepman R, Doherty D et al (2009) OFD1 is mutated in X-linked Joubert syndrome and interacts with LCA5-encoded lebercilin. Am J Hum Genet 85:465–481. doi: 10.1016/j.ajhg.2009.09.002 PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Pampliega O, Orhon I, Patel B et al (2013) Functional interaction between autophagy and ciliogenesis. Nature 502:194–200. doi: 10.1038/nature12639 PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    McEwen DP, Koenekoop RK, Khanna H et al (2007) Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons. Proc Natl Acad Sci USA 104:15917–15922. doi: 10.1073/pnas.0704140104 PubMedCentralPubMedCrossRefGoogle Scholar
  77. 77.
    Craige B, Tsao C-C, Diener DR et al (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190:927–940. doi: 10.1083/jcb.201006105 PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Kobayashi T, Kim S, Lin Y-C et al (2014) The CP110-interacting proteins Talpid3 and Cep290 play overlapping and distinct roles in cilia assembly. J Cell Biol. doi: 10.1083/jcb.201304153 PubMedCentralPubMedGoogle Scholar
  79. 79.
    Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117. doi: 10.1038/35052055 PubMedCrossRefGoogle Scholar
  80. 80.
    Nachury MV, Seeley ES, Jin H (2010) Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 26:59–87. doi: 10.1146/annurev.cellbio.042308.113337 PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Chang BB, Khanna HH, Hawes NN et al (2006) In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 15:1847–1857. doi: 10.1093/hmg/ddl107 PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    Chen Z, Indjeian VB, McManus M et al (2002) CP110, a cell cycle-dependent CDK substrate, regulates centrosome duplication in human cells. Dev Cell 3:339–350PubMedCrossRefGoogle Scholar
  83. 83.
    Spektor A, Tsang WY, Khoo D, Dynlacht BD (2007) Cep97 and CP110 suppress a cilia assembly program. Cell 130:678–690. doi: 10.1016/j.cell.2007.06.027 PubMedCrossRefGoogle Scholar
  84. 84.
    Tsang WY, Dynlacht BD (2013) CP110 and its network of partners coordinately regulate cilia assembly. Cilia 2:9. doi: 10.1186/2046-2530-2-9 PubMedCentralPubMedGoogle Scholar
  85. 85.
    Pugacheva EN, Jablonski SA, Hartman TR et al (2007) HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129:1351–1363. doi: 10.1016/j.cell.2007.04.035 PubMedCentralPubMedCrossRefGoogle Scholar
  86. 86.
    Lee JY, Stearns T (2013) FOP is a centriolar satellite protein involved in ciliogenesis. PLoS One 8:e58589. doi: 10.1371/journal.pone.0058589 PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Sedjaï F, Acquaviva C, Chevrier V et al (2010) Control of ciliogenesis by FOR20, a novel centrosome and pericentriolar satellite protein. J Cell Sci 123:2391–2401. doi: 10.1242/jcs.065045 PubMedCrossRefGoogle Scholar
  88. 88.
    Klinger M, Wang W, Kuhns S et al (2013) The novel centriolar satellite protein SSX2IP targets Cep290 to the ciliary transition zone. Mol Biol Cell. doi: 10.1091/mbc.E13-09-0526 PubMedGoogle Scholar
  89. 89.
    Keryer G, Pineda JR, Liot G et al (2011) Ciliogenesis is regulated by a huntingtin-HAP1-PCM1 pathway and is altered in Huntington disease. J Clin Invest 121:4372–4382. doi: 10.1172/JCI57552 PubMedCentralPubMedCrossRefGoogle Scholar
  90. 90.
    Porteous DJ, Thomson P, Brandon NJ, Millar JK (2006) The genetics and biology of DISC1–an emerging role in psychosis and cognition. Biol Psychiatry 60:123–131. doi: 10.1016/j.biopsych.2006.04.008 PubMedCrossRefGoogle Scholar
  91. 91.
    Park N, Juo SH, Cheng R et al (2004) Linkage analysis of psychosis in bipolar pedigrees suggests novel putative loci for bipolar disorder and shared susceptibility with schizophrenia. Mol Psychiatry 9:1091–1099. doi: 10.1038/sj.mp.4001541 PubMedCrossRefGoogle Scholar
  92. 92.
    Puram SV, Riccio A, Koirala S et al (2011) A TRPC5-regulated calcium signaling pathway controls dendrite patterning in the mammalian brain. Genes Dev 25:2659–2673. doi: 10.1101/gad.174060.111 PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    Lazic SE, Goodman AOG, Grote HE et al (2007) Olfactory abnormalities in Huntington’s disease: decreased plasticity in the primary olfactory cortex of R6/1 transgenic mice and reduced olfactory discrimination in patients. Brain Res 1151:219–226. doi: 10.1016/j.brainres.2007.03.018 PubMedCrossRefGoogle Scholar
  94. 94.
    Liu J-P, Zeitlin SO (2011) The long and the short of aberrant ciliogenesis in Huntington disease. J Clin Invest 121:4237–4241. doi: 10.1172/JCI60243 PubMedCentralPubMedCrossRefGoogle Scholar
  95. 95.
    Spalluto C, Wilson DI, Hearn T (2013) Evidence for centriolar satellite localization of CDK1 and cyclin B2. Cell Cycle 12:1802–1803PubMedCentralPubMedCrossRefGoogle Scholar
  96. 96.
    Olsen JV, Vermeulen M, Santamaria A et al (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3:ra3. doi: 10.1126/scisignal.2000475 PubMedCrossRefGoogle Scholar
  97. 97.
    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 PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Löffler H, Fechter A, Liu FY et al (2012) DNA damage-induced centrosome amplification occurs via excessive formation of centriolar satellites. Oncogene. doi: 10.1038/onc.2012.310 PubMedGoogle Scholar
  99. 99.
    Pihan GA, Wallace J, Zhou Y, Doxsey SJ (2003) Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas. Cancer Res 63:1398–1404PubMedGoogle Scholar
  100. 100.
    Dodson H, Bourke E, Jeffers LJ et al (2004) Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J 23:3864–3873. doi: 10.1038/sj.emboj.7600393 PubMedCentralPubMedCrossRefGoogle Scholar
  101. 101.
    Franceschini A, Szklarczyk D, Frankild S et al (2013) STRING v9.1: protein–protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808–D815. doi: 10.1093/nar/gks1094 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel 2014

Authors and Affiliations

  1. 1.Faculty of Health Sciences, Ubiquitin Signaling Group, The Novo Nordisk Foundation Center for Protein ResearchUniversity of CopenhagenCopenhagen NDenmark

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