Advertisement

Molecular Neurobiology

, Volume 55, Issue 7, pp 5409–5424 | Cite as

The Role of WD40-Repeat Protein 62 (MCPH2) in Brain Growth: Diverse Molecular and Cellular Mechanisms Required for Cortical Development

  • Belal Shohayeb
  • Nicholas Rui Lim
  • Uda Ho
  • Zhiheng Xu
  • Mirella Dottori
  • Leonie Quinn
  • Dominic Chi Hiung NgEmail author
Article

Abstract

Genetic disruptions of spindle/centrosome-associated WD40-repeat protein 62 (WDR62) are causative for autosomal recessive primary microcephaly (MCPH) and a broader range of cortical malformations. Since the identification of WDR62 as encoded by the MCPH2 locus in 2010, recent studies that have deleted/depleted WDR62 in various animal models of cortical development have highlighted conserved functions in brain growth. Here, we provide a timely review of our current understanding of WDR62 contributions in the self-renewal, expansion and fate specification of neural stem and progenitor cells that are critical for neocortical development. Recent studies have revealed multiple functions for WDR62 in the regulation of spindle organization, mitotic progression and the duplication and biased inheritance of centrosomes during asymmetric divisions. We also discuss recently elaborated WDR62 interaction partners that include Aurora and c-Jun N-terminal kinases as part of complex signalling mechanisms that may define its neural functions. These studies provide new insights into the molecular and cellular processes that are required for brain formation and implicated in the genesis of primary microcephaly.

Keywords

Neural stem cells Neural signalling Corticogenesis c-Jun N-terminal kinase Microcephaly 

Notes

Acknowledgements

DN acknowledges funding support from the National Health and Medical Research Council (APP1046032), Australian Research Council (FT120100193) and Cancer Council (APP1101931). NL was a recipient of a Melbourne International Research Scholarship from the University of Melbourne and BS is a recipient of a UQ International Scholarship from the University of Queensland.

References

  1. 1.
    Bilguvar K, Ozturk AK, Louvi A, Kwan KY, Choi M, Tatli B, Yalnizoglu D, Tuysuz B et al (2010) Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 467(7312):207–210.  https://doi.org/10.1038/nature09327 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Nicholas AK, Khurshid M, Desir J, Carvalho OP, Cox JJ, Thornton G, Kausar R, Ansar M et al (2010) WDR62 is associated with the spindle pole and is mutated in human microcephaly. Nat Genet 42(11):1010–1014.  https://doi.org/10.1038/ng.682 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Yu TW, Mochida GH, Tischfield DJ, Sgaier SK, Flores-Sarnat L, Sergi CM, Topcu M, McDonald MT et al (2010) Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture. Nat Genet 42(11):1015–1020.  https://doi.org/10.1038/ng.683 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bogoyevitch MA, Yeap YY, Qu Z, Ngoei KR, Yip YY, Zhao TT, Heng JI, Ng DC (2012) WD40-repeat protein 62 is a JNK-phosphorylated spindle pole protein required for spindle maintenance and timely mitotic progression. J Cell Sci 125(Pt 21):5096–5109.  https://doi.org/10.1242/jcs.107326 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Chen JF, Zhang Y, Wilde J, Hansen KC, Lai F, Niswander L (2014) Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size. Nat Commun 5:3885.  https://doi.org/10.1038/ncomms4885 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Jayaraman D, Kodani A, Gonzalez DM, Mancias JD, Mochida GH, Vagnoni C, Johnson J, Krogan N et al (2016) Microcephaly proteins Wdr62 and Aspm define a mother centriole complex regulating centriole biogenesis, apical complex, and cell fate. Neuron 92(4):813–828.  https://doi.org/10.1016/j.neuron.2016.09.056 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Gilmore EC, Walsh CA (2013) Genetic causes of microcephaly and lessons for neuronal development. WIREs Dev Biol 2(4):461–478.  https://doi.org/10.1002/wdev.89 CrossRefGoogle Scholar
  8. 8.
    Morris-Rosendahl DJ, Kaindl AM (2015) What next-generation sequencing (NGS) technology has enabled us to learn about primary autosomal recessive microcephaly (MCPH). Mol Cell Probes 29(5):271–281.  https://doi.org/10.1016/j.mcp.2015.05.015 CrossRefPubMedGoogle Scholar
  9. 9.
    Wasserman T, Katsenelson K, Daniliuc S, Hasin T, Choder M, Aronheim A (2010) A novel c-Jun N-terminal kinase (JNK)-binding protein WDR62 is recruited to stress granules and mediates a nonclassical JNK activation. Mol Biol Cell 21(1):117–130.  https://doi.org/10.1091/mbc.E09-06-0512 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Woods CG, Parker A (2013) Investigating microcephaly. Arch Dis Child 98(9):707–713.  https://doi.org/10.1136/archdischild-2012-302882 CrossRefPubMedGoogle Scholar
  11. 11.
    Woods CG, Bond J, Enard W (2005) Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am J Hum Genet 76(5):717–728.  https://doi.org/10.1086/429930 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Zaqout S, Morris-Rosendahl D, Kaindl AM (2017) Autosomal recessive primary microcephaly (MCPH): an update. Neuropediatrics 48(3):135–142.  https://doi.org/10.1055/s-0037-1601448 CrossRefPubMedGoogle Scholar
  13. 13.
    Roberts E, Jackson AP, Carradice AC, Deeble VJ, Mannan J, Rashid Y, Jafri H, McHale DP et al (1999) The second locus for autosomal recessive primary microcephaly (MCPH2) maps to chromosome 19q13.1-13.2. Eur J Hum Genet 7(7):815–820.  https://doi.org/10.1038/sj.ejhg.5200385 CrossRefPubMedGoogle Scholar
  14. 14.
    Pervaiz N, Abbasi AA (2016) Molecular evolution of WDR62, a gene that regulates neocorticogenesis. Meta Gene 9:1–9.  https://doi.org/10.1016/j.mgene.2016.02.005 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ramdas Nair A, Singh P, Salvador Garcia D, Rodriguez-Crespo D, Egger B, Cabernard C (2016) The microcephaly-associated protein Wdr62/CG7337 is required to maintain centrosome asymmetry in drosophila neuroblasts. Cell Rep 14(5):1100–1113.  https://doi.org/10.1016/j.celrep.2015.12.097 CrossRefPubMedGoogle Scholar
  16. 16.
    Banerjee S, Chen H, Huang H, Wu J, Yang Z, Deng W, Chen D, Deng J et al (2016) Novel mutations c.28G>T (p.Ala10Ser) and c.189G>T (p.Glu63Asp) in WDR62 associated with early onset acanthosis and hyperkeratosis in a patient with autosomal recessive microcephaly type 2. Oncotarget 7(48):78363–78371.  10.18632/oncotarget.13279 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ahmad I, Baig SM, Abdulkareem AR, Hussain MS, Sur I, Toliat MR, Nurnberg G, Dalibor N et al (2016) Genetic heterogeneity in Pakistani microcephaly families revisited. Clin Genet 92(1):62–68.  https://doi.org/10.1111/cge.12955 CrossRefGoogle Scholar
  18. 18.
    Sajid Hussain M, Marriam Bakhtiar S, Farooq M, Anjum I, Janzen E, Reza Toliat M, Eiberg H, Kjaer KW et al (2013) Genetic heterogeneity in Pakistani microcephaly families. Clin Genet 83(5):446–451.  https://doi.org/10.1111/j.1399-0004.2012.01932.x CrossRefPubMedGoogle Scholar
  19. 19.
    Bastaki F, Mohamed M, Nair P, Saif F, Tawfiq N, Aithala G, El-Halik M, Al-Ali M et al (2016) Novel splice-site mutation in WDR62 revealed by whole-exome sequencing in a Sudanese family with primary microcephaly. Congenit Anom 56(3):135–137.  https://doi.org/10.1111/cga.12144 CrossRefGoogle Scholar
  20. 20.
    Bhat V, Girimaji SC, Mohan G, Arvinda HR, Singhmar P, Duvvari MR, Kumar A (2011) Mutations in WDR62, encoding a centrosomal and nuclear protein, in Indian primary microcephaly families with cortical malformations. Clin Genet 80(6):532–540.  https://doi.org/10.1111/j.1399-0004.2011.01686.x CrossRefPubMedGoogle Scholar
  21. 21.
    Memon MM, Raza SI, Basit S, Kousar R, Ahmad W, Ansar M (2013) A novel WDR62 mutation causes primary microcephaly in a Pakistani family. Mol Biol Rep 40(1):591–595.  https://doi.org/10.1007/s11033-012-2097-7 CrossRefPubMedGoogle Scholar
  22. 22.
    Kousar R, Hassan MJ, Khan B, Basit S, Mahmood S, Mir A, Ahmad W, Ansar M (2011) Mutations in WDR62 gene in Pakistani families with autosomal recessive primary microcephaly. BMC Neurol 11:119.  https://doi.org/10.1186/1471-2377-11-119 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Farag HG, Froehler S, Oexle K, Ravindran E, Schindler D, Staab T, Huebner A, Kraemer N et al (2013) Abnormal centrosome and spindle morphology in a patient with autosomal recessive primary microcephaly type 2 due to compound heterozygous WDR62 gene mutation. Orphanet J Rare Dis 8:178.  https://doi.org/10.1186/1750-1172-8-178 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Poulton CJ, Schot R, Seufert K, Lequin MH, Accogli A, Annunzio GD, Villard L, Philip N et al (2014) Severe presentation of WDR62 mutation: is there a role for modifying genetic factors? Am J Med Genet A 164A(9):2161–2171.  https://doi.org/10.1002/ajmg.a.36611 CrossRefPubMedGoogle Scholar
  25. 25.
    Murdock DR, Clark GD, Bainbridge MN, Newsham I, Wu YQ, Muzny DM, Cheung SW, Gibbs RA et al (2011) Whole-exome sequencing identifies compound heterozygous mutations in WDR62 in siblings with recurrent polymicrogyria. Am J Med Genet A 155A(9):2071–2077.  https://doi.org/10.1002/ajmg.a.34165 CrossRefPubMedGoogle Scholar
  26. 26.
    Najmabadi H, Hu H, Garshasbi M, Zemojtel T, Abedini SS, Chen W, Hosseini M, Behjati F et al (2011) Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature 478(7367):57–63.  https://doi.org/10.1038/nature10423 CrossRefPubMedGoogle Scholar
  27. 27.
    Rupp V, Rauf S, Naveed I, Windpassinger C, Mir A (2014) A novel single base pair duplication in WDR62 causes primary microcephaly. BMC Med Genet 15:107.  https://doi.org/10.1186/s12881-014-0107-4 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Naseer MI, Rasool M, Sogaty S, Chaudhary RA, Mansour HM, Chaudhary AG, Abuzenadah AM, Al-Qahtani MH (2017) A novel WDR62 mutation causes primary microcephaly in a large consanguineous Saudi family. Ann Saudi Med 37(2):148–153.  https://doi.org/10.5144/0256-4947.2017.148 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Xu D, Zhang F, Wang Y, Sun Y, Xu Z (2014) Microcephaly-associated protein WDR62 regulates neurogenesis through JNK1 in the developing neocortex. Cell Rep 6(1):104–116.  https://doi.org/10.1016/j.celrep.2013.12.016 CrossRefPubMedGoogle Scholar
  30. 30.
    Cohen-Katsenelson K, Wasserman T, Darlyuk-Saadon I, Rabner A, Glaser F, Aronheim A (2013) Identification and analysis of a novel dimerization domain shared by various members of c-Jun N-terminal kinase (JNK) scaffold proteins. J Biol Chem 288(10):7294–7304.  https://doi.org/10.1074/jbc.M112.422055 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Cohen-Katsenelson K, Wasserman T, Khateb S, Whitmarsh AJ, Aronheim A (2011) Docking interactions of the JNK scaffold protein WDR62. Biochem J 439(3):381–390.  https://doi.org/10.1042/BJ20110284 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Novorol C, Burkhardt J, Wood KJ, Iqbal A, Roque C, Coutts N, Almeida AD, He J et al (2013) Microcephaly models in the developing zebrafish retinal neuroepithelium point to an underlying defect in metaphase progression. Open Biol 3(10):130065.  https://doi.org/10.1098/rsob.130065 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sgourdou P, Mishra-Gorur K, Saotome I, Henagariu O, Tuysuz B, Campos C, Ishigame K, Giannikou K et al (2017) Disruptions in asymmetric centrosome inheritance and WDR62-Aurora kinase B interactions in primary microcephaly. Sci Rep 7:43708.  https://doi.org/10.1038/srep43708 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lim NR, Shohayeb B, Zaytseva O, Mitchell N, Millard SS, Ng DC, Quinn LM (2017) Glial-specific functions of microcephaly protein WDR62, and interaction with the mitotic kinase AURKA, are essential for Drosophila brain growth. Stem Cell Rep S2213-6711(17):30222–30229.  https://doi.org/10.1016/j.stemcr.2017.05.015 CrossRefGoogle Scholar
  35. 35.
    Florio M, Huttner WB (2014) Neural progenitors, neurogenesis and the evolution of the neocortex. Development 141(11):2182–2194.  https://doi.org/10.1242/dev.090571 CrossRefPubMedGoogle Scholar
  36. 36.
    Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C, Nicholas CR, Shuga J, Liu SJ et al (2015) Molecular identity of human outer radial glia during cortical development. Cell 163(1):55–67.  https://doi.org/10.1016/j.cell.2015.09.004 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Cunningham CL, Martinez-Cerdeno V, Noctor SC (2013) Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J Neurosci 33(10):4216–4233.  https://doi.org/10.1523/JNEUROSCI.3441-12.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Fietz SA, Huttner WB (2011) Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol 21(1):23–35.  https://doi.org/10.1016/j.conb.2010.10.002 CrossRefPubMedGoogle Scholar
  39. 39.
    Lesage B, Gutierrez I, Marti E, Gonzalez C (2010) Neural stem cells: the need for a proper orientation. Curr Opin Genet Dev 20(4):438–442.  https://doi.org/10.1016/j.gde.2010.04.013 CrossRefPubMedGoogle Scholar
  40. 40.
    Manzini MC, Walsh CA (2011) What disorders of cortical development tell us about the cortex: one plus one does not always make two. Curr Opin Genet Dev 21(3):333–339.  https://doi.org/10.1016/j.gde.2011.01.006 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Alshawaf A, Antonic A, Skafidas E, Ng DCH, Dottori M (2017) WDR62 regulates early neural and glial progenitor specification from human pluripotent stem cells. Stem Cells Int 2017:7848932.  https://doi.org/10.1155/2017/7848932 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Koyano S, Ito M, Takamatsu N, Shiba T, Yamamoto K, Yoshioka K (1999) A novel Jun N-terminal kinase (JNK)-binding protein that enhances the activation of JNK by MEK kinase 1 and TGF-beta-activated kinase 1. FEBS Lett 457(3):385–388CrossRefPubMedGoogle Scholar
  43. 43.
    Stirnimann CU, Petsalaki E, Russell RB, Muller CW (2010) WD40 proteins propel cellular networks. Trends Biochem Sci 35(10):565–574.  https://doi.org/10.1016/j.tibs.2010.04.003 CrossRefPubMedGoogle Scholar
  44. 44.
    Macia MS, Halbritter J, Delous M, Bredrup C, Gutter A, Filhol E, Mellgren AE, Leh S et al (2017) Mutations in MAPKBP1 cause juvenile or late-onset cilia-independent nephronophthisis. Am J Human Genet 100(2):323–333.  https://doi.org/10.1016/j.ajhg.2016.12.011 CrossRefGoogle Scholar
  45. 45.
    Hadad M, Aviram S, Darlyuk-Saadon I, Cohen-Katsenelson K, Whitmarsh AJ, Aronheim A (2015) The association of the JNK scaffold protein, WDR62, with the mixed lineage kinase 3, MLK3. MAP Kinase 4(1):5307CrossRefGoogle Scholar
  46. 46.
    Zhang F, Yu J, Yang T, Xu D, Chi Z, Xia Y, Xu Z (2016) A novel c-Jun N-terminal kinase (JNK) signaling complex involved in neuronal migration during brain development. J Biol Chem 291(22):11466–11475.  https://doi.org/10.1074/jbc.M116.716811 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kodani A, Yu TW, Johnson JR, Jayaraman D, Johnson TL, Al-Gazali L, Sztriha L, Partlow JN (2015) Centriolar satellites assemble centrosomal microcephaly proteins to recruit CDK2 and promote centriole duplication. eLife 4, e07519.  https://doi.org/10.7554/eLife.07519
  48. 48.
    Lim NR, Yeap YY, Ang CS, Williamson NA, Bogoyevitch MA, Quinn LM, Ng DC (2016) Aurora A phosphorylation of WD40-repeat protein 62 in mitotic spindle regulation. Cell Cycle 15(3):413–424.  https://doi.org/10.1080/15384101.2015.1127472 CrossRefPubMedGoogle Scholar
  49. 49.
    Lim NR, Yeap YY, Zhao TT, Yip YY, Wong SC, Xu D, Ang CS, Williamson NA et al (2015) Opposing roles for JNK and Aurora A in regulating the association of WDR62 with spindle microtubules. J Cell Sci 128(3):527–540.  https://doi.org/10.1242/jcs.157537 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Bogoyevitch MA, Ngoei KR, Zhao TT, Yeap YY, Ng DC (2010) c-Jun N-terminal kinase (JNK) signaling: recent advances and challenges. Biochim Biophys Acta 1804(3):463–475.  https://doi.org/10.1016/j.bbapap.2009.11.002 CrossRefPubMedGoogle Scholar
  51. 51.
    Guarguaglini G, Duncan PI, Stierhof YD, Holmstrom T, Duensing S, Nigg EA (2005) The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol Biol Cell 16(3):1095–1107.  https://doi.org/10.1091/mbc.E04-10-0939 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Rome P, Montembault E, Franck N, Pascal A, Glover DM, Giet R (2010) Aurora A contributes to p150(glued) phosphorylation and function during mitosis. J Cell Biol 189(4):651–659.  https://doi.org/10.1083/jcb.201001144 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA (2011) Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci Signal 4(179):rs5.  https://doi.org/10.1126/scisignal.2001497 CrossRefPubMedGoogle Scholar
  54. 54.
    Barr AR, Gergely F (2007) Aurora-A: the maker and breaker of spindle poles. J Cell Sci 120(Pt 17):2987–2996.  https://doi.org/10.1242/jcs.013136 CrossRefPubMedGoogle Scholar
  55. 55.
    Lee CY, Andersen RO, Cabernard C, Manning L, Tran KD, Lanskey MJ, Bashirullah A, Doe CQ (2006) Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes Dev 20(24):3464–3474.  https://doi.org/10.1101/gad.1489406 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Wang H, Somers GW, Bashirullah A, Heberlein U, Yu F, Chia W (2006) Aurora-A acts as a tumor suppressor and regulates self-renewal of Drosophila neuroblasts. Genes Dev 20(24):3453–3463.  https://doi.org/10.1101/gad.1487506 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Molofsky AV, Krencik R, Ullian EM, Tsai HH, Deneen B, Richardson WD, Barres BA, Rowitch DH (2012) Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26(9):891–907.  https://doi.org/10.1101/gad.188326.112 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Sfakianos AP, Whitmarsh AJ, Ashe MP (2016) Ribonucleoprotein bodies are phased in. Biochem Soc Trans 44(5):1411–1416.  https://doi.org/10.1042/BST20160117 CrossRefPubMedGoogle Scholar
  59. 59.
    Antoniou X, Borsello T (2012) The JNK signalling transduction pathway in the brain. Front Biosci 4:2110–2120CrossRefGoogle Scholar
  60. 60.
    Sabapathy K (2012) Role of the JNK pathway in human diseases. Prog Mol Biol Transl Sci 106:145–169.  https://doi.org/10.1016/B978-0-12-396456-4.00013-4 CrossRefPubMedGoogle Scholar
  61. 61.
    Sabapathy K, Jochum W, Hochedlinger K, Chang L, Karin M, Wagner EF (1999) Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 89(1–2):115–124CrossRefPubMedGoogle Scholar
  62. 62.
    Westerlund N, Zdrojewska J, Padzik A, Komulainen E, Bjorkblom B, Rannikko E, Tararuk T, Garcia-Frigola C et al (2011) Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate. Nat Neurosci 14(3):305–313.  https://doi.org/10.1038/nn.2755 CrossRefPubMedGoogle Scholar
  63. 63.
    Barr AR, Kilmartin JV, Gergely F (2010) CDK5RAP2 functions in centrosome to spindle pole attachment and DNA damage response. J Cell Biol 189(1):23–39.  https://doi.org/10.1083/jcb.200912163 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Knoblich JA (2008) Mechanisms of asymmetric stem cell division. Cell 132(4):583–597.  https://doi.org/10.1016/j.cell.2008.02.007 CrossRefPubMedGoogle Scholar
  65. 65.
    Siller KH, Doe CQ (2008) Lis1/dynactin regulates metaphase spindle orientation in Drosophila neuroblasts. Dev Biol 319(1):1–9.  https://doi.org/10.1016/j.ydbio.2008.03.018 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Januschke J, Nathke I (2014) Stem cell decisions: a twist of fate or a niche market? Semin Cell Dev Biol 34:116–123.  https://doi.org/10.1016/j.semcdb.2014.02.014 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Insolera R, Bazzi H, Shao W, Anderson KV, Shi SH (2014) Cortical neurogenesis in the absence of centrioles. Nat Neurosci 17(11):1528–1535.  https://doi.org/10.1038/nn.3831 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Marjanovic M, Sanchez-Huertas C, Terre B, Gomez R, Scheel JF, Pacheco S, Knobel PA, Martinez-Marchal A et al (2015) CEP63 deficiency promotes p53-dependent microcephaly and reveals a role for the centrosome in meiotic recombination. Nat Commun 6:7676.  https://doi.org/10.1038/ncomms8676 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Kim S, Lehtinen MK, Sessa A, Zappaterra MW, Cho SH, Gonzalez D, Boggan B, Austin CA et al (2010) The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66(1):69–84.  https://doi.org/10.1016/j.neuron.2010.03.019 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Higginbotham H, Guo J, Yokota Y, Umberger NL, Su CY, Li J, Verma N, Hirt J et al (2013) Arl13b-regulated cilia activities are essential for polarized radial glial scaffold formation. Nat Neurosci 16(8):1000–1007.  https://doi.org/10.1038/nn.3451 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Tong CK, Han YG, Shah JK, Obernier K, Guinto CD, Alvarez-Buylla A (2014) Primary cilia are required in a unique subpopulation of neural progenitors. Proc Natl Acad Sci U S A 111(34):12438–12443.  https://doi.org/10.1073/pnas.1321425111 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Paridaen JT, Wilsch-Brauninger M, Huttner WB (2013) Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155(2):333–344.  https://doi.org/10.1016/j.cell.2013.08.060 CrossRefPubMedGoogle Scholar
  73. 73.
    Pelletier L, Yamashita YM (2012) Centrosome asymmetry and inheritance during animal development. Curr Opin Cell Biol 24(4):541–546.  https://doi.org/10.1016/j.ceb.2012.05.005 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Conduit PT, Raff JW (2010) Cnn dynamics drive centrosome size asymmetry to ensure daughter centriole retention in Drosophila neuroblasts. Curr Biol 20(24):2187–2192.  https://doi.org/10.1016/j.cub.2010.11.055 CrossRefPubMedGoogle Scholar
  75. 75.
    Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461(7266):947–955.  https://doi.org/10.1038/nature08435 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Zhang Y, Tian Y, Yu JJ, He J, Luo J, Zhang S, Tang CE, Tao YM (2013) Overexpression of WDR62 is associated with centrosome amplification in human ovarian cancer. J Ovar Res 6(1):55.  https://doi.org/10.1186/1757-2215-6-55 CrossRefGoogle Scholar
  77. 77.
    Liang Y, Gao H, Lin SY, Peng G, Huang X, Zhang P, Goss JA, Brunicardi FC et al (2010) BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice. PLoS Genet 6(1):e1000826.  https://doi.org/10.1371/journal.pgen.1000826 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Pulvers JN, Bryk J, Fish JL, Wilsch-Brauninger M, Arai Y, Schreier D, Naumann R, Helppi J et al (2010) Mutations in mouse Aspm (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline. Proc Natl Acad Sci U S A 107(38):16595–16600.  https://doi.org/10.1073/pnas.1010494107 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Zaqout S, Bessa P, Kramer N, Stoltenburg-Didinger G, Kaindl AM (2017) CDK5RAP2 is required to maintain the germ cell pool during embryonic development. Stem Cell Rep 8(2):198–204.  https://doi.org/10.1016/j.stemcr.2017.01.002 CrossRefGoogle Scholar
  80. 80.
    Shinmura K, Kato H, Kawanishi Y, Igarashi H, Inoue Y, Yoshimura K, Nakamura S, Fujita H et al (2017) WDR62 overexpression is associated with a poor prognosis in patients with lung adenocarcinoma. Mol Carcinog 56(8):1984–1991.  https://doi.org/10.1002/mc.22647 CrossRefPubMedGoogle Scholar
  81. 81.
    Zeng S, Tao Y, Huang J, Zhang S, Shen L, Yang H, Pei H, Zhong M et al (2013) WD40 repeat-containing 62 overexpression as a novel indicator of poor prognosis for human gastric cancer. Eur J Cancer 49(17):3752–3762.  https://doi.org/10.1016/j.ejca.2013.07.015 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Belal Shohayeb
    • 1
  • Nicholas Rui Lim
    • 2
    • 3
  • Uda Ho
    • 1
  • Zhiheng Xu
    • 4
  • Mirella Dottori
    • 5
  • Leonie Quinn
    • 6
  • Dominic Chi Hiung Ng
    • 1
    Email author
  1. 1.School of Biomedical Sciences, Faculty of MedicineUniversity of QueenslandSt LuciaAustralia
  2. 2.Department of Biochemistry and Molecular BiologyUniversity of MelbourneParkvilleAustralia
  3. 3.Duke-NUS Medical SchoolSingaporeSingapore
  4. 4.State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina
  5. 5.Centre for Neural EngineeringThe University of MelbourneCarltonAustralia
  6. 6.Department of Cancer Biology and Therapeutics, John Curtin School of Medical ResearchAustralian National UniversityCanberraAustralia

Personalised recommendations