Molecular and cellular basis of autosomal recessive primary microcephaly

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Barbelanne, Marine ^a   Tsang, William Y ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; CYCLIN DEPENDENT KINASE 6; GEMININ; MULTIPROTEIN COMPLEX; PERICENTRIN; ZINC FINGER PROTEIN; ASPM PROTEIN, HUMAN; CASC5 PROTEIN, HUMAN; CDK5RAP2 PROTEIN, HUMAN; CENPJ PROTEIN, HUMAN; MCPH1 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; SIGNAL PEPTIDE;

ABNORMAL SPINDLE LIKE MICROCEPHALY ASSOCIATED PROTEIN GENE; AUTOSOMAL RECESSIVE INHERITANCE; BASAL CELL NEVUS SYNDROME; BRAIN DEVELOPMENT; BRAIN SIZE; CANCER SUSCEPTIBILITY CANDIDATE 5 GENE; CDK5 REGULATORY SUBUNIT ASSOCIATED PROTEIN 2 GENE; CELL CYCLE CHECKPOINT; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIVISION; CELL PROLIFERATION; CENTROMERE PROTEIN J GENE; CENTROSOMAL PROTEIN 135 GENE; CENTROSOMAL PROTEIN 152 GENE; CENTROSOME; CHROMOSOME CONDENSATION; CYCLIN DEPENDENT KINASE 6 GENE; DWARFISM; GENE FUNCTION; GENE LOCUS; GENE MUTATION; HUMAN; INTELLECTUAL IMPAIRMENT; MICROCEPHALIN GENE; MICROCEPHALY; MITOSIS; MITOSIS SPINDLE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; POLYHOMEOTIC LIKE PROTEIN 1 GENE; PROTEIN PROTEIN INTERACTION; REVIEW; SCL TAL1 INTERRUPTING LOCUS; SECKEL SYNDROME; WD REPEAT CONTAINING PROTEIN 62 GENE; ZINC FINGER PROTEIN 335 GENE; ANIMAL; GENETIC HETEROGENEITY; GENETICS; MUTATION; PATHOPHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CENTROSOME; GENETIC HETEROGENEITY; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROCEPHALY; MICROTUBULE-ASSOCIATED PROTEINS; MULTIPROTEIN COMPLEXES; MUTATION; NERVE TISSUE PROTEINS;

EID: 84919775810     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/547986     Document Type: Review

References (172)

1. J. Cox, A. P. Jackson, J. Bond, and C. G. Woods, "What primary microcephaly can tell us about brain growth," Trends in Molecular Medicine, vol. 12, no. 8, pp. 358-366, 2006
2. S. Mahmood, W. Ahmad, andM. J. Hassan, "Autosomal recessive primary microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum," Orphanet Journal of Rare Diseases, vol. 6, no. 1, article 39, 2011
3. C. G. Woods and A. Parker, "Investigating microcephaly," Archives ofDisease in Childhood, vol. 98,no. 9, pp. 707-713, 2013
4. C. G. Woods, J. Bond, and W. Enard, "Autosomal recessive primary microcephaly (MCPH): a review of clinical,molecular, and evolutionary findings," The American Journal of Human Genetics, vol. 76, no. 5, pp. 717-728, 2005
5. S. Passemard, A. M. Kaindl, and A. Verloes, "Microcephaly," in Handbook of Clinical Neurology, vol. 111, pp. 129-141, 2013
6. S. Passemard, L. Titomanlio,M. Elmaleh et al., "Expanding the clinical and neuroradiologic phenotype of primary microcephaly due to ASPM mutations," Neurology, vol. 73, no. 12, pp. 962-969, 2009
7. G. H. Mochida and C. A. Walsh, "Molecular genetics of human microcephaly," Current Opinion in Neurology, vol. 14, no. 2, pp. 151-156, 2001
8. C. Kerzendorfer, R. Colnaghi, I. Abramowicz, G. Carpenter, and M. O'Driscoll, "Meier-Gorlin syndrome and Wolf-Hirschhorn syndrome: two developmental disorders highlighting the importance of efficient DNA replication for normal development and neurogenesis,"DNA Repair, vol. 12,no. 8, pp. 637-644, 2013
9. G. K. ThorntonandC. G. Woods, "Primarymicrocephaly: do all roads lead to Rome" Trends in Genetics, vol. 25, no. 11, pp. 501-510, 2009
10. A. M. Kaindl, S. Passemard, P. Kumar et al., "Many roads lead to primary autosomal recessive microcephaly," Progress in Neurobiology, vol. 90, no. 3, pp. 363-383, 2010
11. A. Klingseisen and A. P. Jackson, "Mechanisms and pathways of growth failure in primordial dwarfism," Genes and Development, vol. 25, no. 19, pp. 2011-2024, 2011
12. M. O'Driscoll, A. P. Jackson, and P. A. Jeggo, "Microcephalin: a causal link between impaired damage response signalling and microcephaly," Cell Cycle, vol. 5, no. 20, pp. 2339-2344, 2006
13. A. P. Jackson, H. Eastwood, S. M. Bell et al., "Identification of microcephalin, a protein implicated in determining the size of the human brain,"TheAmerican Journal ofHumanGenetics, vol. 71, no. 1, pp. 136-142, 2002
14. J. Bond, E. Roberts, G. H. Mochida et al., "ASPM is a major determinant of cerebral cortical size," Nature Genetics, vol. 32, no. 2, pp. 316-320, 2002
15. J. Bond, E. Roberts, K. Springell et al., "A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size," Nature Genetics, vol. 37, pp. 353-355, 2005
16. A. K. Nicholas, M. Khurshid, J. Désir et al., "WDR62 is associated with the spindle pole and is mutated in human microcephaly," Nature Genetics, vol. 42, no. 11, pp. 1010-1014, 2010
17. L. Issa, N. Kraemer, C. H. Rickert et al., "CDK5RAP2 expression during murine and human brain development correlates with pathology in primary autosomal recessive microcephaly," Cerebral Cortex, vol. 23, no. 9, pp. 2245-2260, 2013
18. W. B. Huttner and Y. Kosodo, "Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system," Current Opinion in Cell Biology, vol. 17, no. 6, pp. 648-657, 2005
19. E. Peyre and X. Morin, "An oblique view on the role of spindle orientation in vertebrate neurogenesis," Development Growth and Differentiation, vol. 54, no. 3, pp. 287-305, 2012
20. E. Taverna, M. Gotz, and W. B. Huttner, "The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex," Annual Review of Cell and Developmental Biology, vol. 30, 2014
21. J. L. Fish, C. Dehay, H. Kennedy, and W. B. Huttner, "Making bigger brains-the evolution of neural-progenitor-cell division," Journal of Cell Science, vol. 121, no. 17, pp. 2783-2793, 2008
22. X. Zhong, G. P. Pfeifer, and X. Xu, "Microcephalin encodes a centrosomal protein," Cell Cycle, vol. 5, no. 4, pp. 457-458, 2006
23. T. W. Yu, G. H. Mochida, D. J. Tischfield et al., "Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture," Nature Genetics, vol. 42, no. 11, pp. 1015-1020, 2010
24. X. Zhong, L. Liu, A. Zhao, G. P. Pfeifer, and X. Xu, "The abnormal spindle-like, microcephaly-associated (ASPM) gene encodes a centrosomal protein," Cell Cycle, vol. 4, no. 9, pp. 1227-1229, 2005
25. A. Kumar, S. C. Girimaji, M. R. Duvvari, and S. H. Blanton, "Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly," The American Journal of Human Genetics, vol. 84, no. 2, pp. 286-290, 2008
26. M. S. Hussain, S. M. Baig, S. Neumann et al., "A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function,"The American Journal of Human Genetics, vol. 90, no. 5, pp. 871-878, 2012
27. D. L. Guernsey, H. Jiang, J. Hussin et al., "Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4," American Journal of Human Genetics, vol. 87, no. 1, pp. 40-51, 2010
28. J.-H. Sir, A. R. Barr, A. K. Nicholas et al., "A primary microcephaly protein complex forms a ring around parental centrioles," Nature Genetics, vol. 43, no. 11, pp. 1147-1153, 2011
29. M. S. Hussain, S. M. Baig, S. Neumann et al., "CDK6 associates with the centrosome during mitosis and is mutated in a large pakistani familywith primarymicrocephaly," HumanMolecular Genetics, vol. 22, no. 25, pp. 5199-5214, 2013
30. I. B. Alieva and R. E. Uzbekov, "The centrosome is a polyfunctional multiprotein cell complex," Biochemistry, vol. 73, no. 6, pp. 626-643, 2008
31. M. Bornens, "The centrosome in cells and organisms," Science, vol. 335, no. 6067, pp. 422-426, 2012
32. A. Debec, W. Sullivan, and M. Bettencourt-Dias, "Centrioles: active players or passengers during mitosis" Cellular and Molecular Life Sciences, vol. 67, no. 13, pp. 2173-2194, 2010
33. E. A. Nigg and J. W. Raff, "Centrioles, centrosomes, and cilia in health and disease," Cell, vol. 139, no. 4, pp. 663-678, 2009
34. W. Y. Tsang and B. D. Dynlacht, "CP110 and its network of partners coordinately regulate cilia assembly," Cilia, vol. 2, no. 1, article 9, 2013
35. D. Hossain and W. Y. Tsang, "Centrosome dysfunction and senescence: coincidence or causality" Journal of Aging Science, vol. 1, p. 113, 2013
36. E. H. Hinchcliffe and G. Sluder, ""It takes two to tango": understanding how centrosome duplication is regulated throughout the cell cycle," Genes and Development, vol. 15, no. 10, pp. 1167-1181, 2001
37. E. A. Nigg and T. Stearns, "The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries," Nature Cell Biology, vol. 13, no. 10, pp. 1154-1160, 2011
38. R. E. Palazzo, J. M. Vogel, B. J. Schnackenberg,D. R. Hull, and X. Wu, "Centrosomematuration," Current Topics inDevelopmental Biology, vol. 49, pp. 449-470, 1999
39. C. W. Brownlee andG. C. Rogers, "Showme your license, please: deregulation of centriole duplicationmechanisms that promote amplification," Cellular and Molecular Life Sciences, vol. 70, no. 6, pp. 1021-1034, 2013
40. A. P. Jackson, D. P. McHale, D. A. Campbell et al., "Primary autosomal recessive microcephaly (MCPH1) maps to chromosome 8p22-pter,"The American Journal of Human Genetics, vol. 63, no. 2, pp. 541-546, 1998
41. T. Venkatesh and P. S. Suresh, "Emerging roles of MCPH1: expedition from primary microcephaly to cancer," European Journal of Cell Biology, vol. 93, no. 3, pp. 98-105, 2014
42. L. J. Jeffers, B. J. Coull, S. J. Stack, andC. G. Morrison, "Distinct BRCT domains in Mcph1/Brit1 mediate ionizing radiationinduced focus formation and centrosomal localization," Oncogene, vol. 27, no. 1, pp. 139-144, 2008
43. S.-Z. Yang, F.-T. Lin, andW.-C. Lin, "MCPH1/BRIT1 cooperates with E2F1 in the activation of checkpoint, DNA repair and apoptosis," EMBO Reports, vol. 9, no. 9, pp. 907-915, 2008
44. G. Peng and S.-Y. Lin, "BRITI/MCPHI is a multifunctional DNA damage responsive protein mediating DNA repairassociated chromatin remodeling," Cell Cycle, vol. 8, no. 19, pp. 3071-3072, 2009
45. G. Peng, E.-K. Yim, H. Dai et al., "BRIT1/MCPH1 links chromatin remodelling to DNA damage response," Nature Cell Biology, vol. 11, no. 7, pp. 865-872, 2009
46. J. L. Wood, Y. Liang, K. Li, and J. Chen, "Microcephalin/MCPH1 associates with the condensin II complex to function in homologous recombination repair," Journal of Biological Chemistry, vol. 283, no. 43, pp. 29586-29592, 2008
47. M. Trimborn, D. Schindler, H. Neitzel, and T. Hirano, "Misregulated chromosome condensation in MCPH1 primary microcephaly is mediated by condensin II," Cell Cycle, vol. 5, no. 3, pp. 322-326, 2006
48. A. Tibelius, J. Marhold, H. Zentgraf et al., "Microcephalin and pericentrin regulate mitotic entry via centrosome-associated Chk1," Journal of Cell Biology, vol. 185, no. 7, pp. 1149-1157, 2009
49. R. Gruber, Z. Zhou, M. Sukchev, T. Joerss, P.-O. Frappart, and Z.-Q. Wang, "MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway," Nature Cell Biology, vol. 13, no. 11, pp. 1325-1334, 2011
50. Y. Liang, H. Gao, S.-Y. Lin et al., "BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice," PLoS Genetics, vol. 6, no. 1, Article ID e1000826, 2010
51. M. Trimborn, M. Ghani, D. J. Walther et al., "Establishment of a mouse model with misregulated chromosome condensation due to defective Mcph1 function," PLoS ONE, vol. 5, no. 2, Article ID e9242, 2010
52. Z. W. Zhou, A. Tapias, C. Bruhn, R. Gruber, M. Sukchev, and Z. Q. Wang, "DNA damage response in microcephaly development of MCPH1 mouse model," DNA Repair, vol. 12, no. 8, pp. 645-655, 2013
53. K. Bilgüvar, A. K. Öztürk, A. Louvi et al., "Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations," Nature, vol. 467, no. 7312, pp. 207-210, 2010
54. C. A. Bacino, L. A. Arriola, J. Wiszniewska, and P. E. Bonnen, "WDR62 missense mutation in a consanguineous family with primary microcephaly,"American Journal ofMedicalGeneticsA, vol. 158, no. 3, pp. 622-625, 2012
55. M. A. Bogoyevitch, Y. Y. C. Yeap, Z. Qu et al., "WD40-repeat protein 62 is a JNK-phosphorylated spindle pole protein required for spindle maintenance and timely mitotic progression," Journal of Cell Science, vol. 125, no. 21, pp. 5096-5109, 2012
56. H. G. Farag, S. Froehler, K. Oexle et al., "Abnormal centrosome and spindle morphology in a patient with autosomal recessive primary microcephaly type 2 due to compound heterozygous WDR62 genemutation," Orphanet Journal of Rare Diseases, vol. 8, no. 1, article 178, 2013
57. R. A. MacCorkle-Chosnek, A. VanHooser, D. W. Goodrich, B. R. Brinkley, and T.-H. Tan, "Cell cycle regulation of c-Jun Nterminal kinase activity at the centrosomes," Biochemical and Biophysical Research Communications, vol. 289, no. 1, pp. 173-180, 2001
58. D. Xu, F. Zhang, Y. Wang, Y. Sun, and Z. Xu, "Microcephalyassociated protein WDR62 regulates neurogenesis through JNK1 in the developing neocortex," Cell Reports, vol. 6, no. 1, pp. 104-116, 2014
59. C. Novorol, J. Burkhardt, K. J. Wood et al., "Microcephaly models in the developing zebrafish retinal neuroepithelium point to an underlying defect in metaphase progression," Open Biology, vol. 3, no. 10, Article ID130065, 2013
60. J.-F. Chen, Y. Zhang, J. Wilde, K. C. Hansen, F. Lai, and L. Niswander, "Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size," Nature Communications, vol. 5, article 3885, 2014
61. V. Joukov, A. De Nicolo, A. Rodriguez, J. C. Walter, and D. M. Livingston, "Centrosomal protein of 192 kDa (Cep192) promotes centrosome-driven spindle assembly by engaging in organelle-specific Aurora A activation," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 49, pp. 21022-21027, 2010
62. K.-W. Fong, Y.-K. Choi, J. B. Rattner, and R. Z. Qi, "CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the tubulin ring complex," Molecular Biology of the Cell, vol. 19, no. 1, pp. 115-125, 2008
63. Y.-K. Choi, P. Liu, S. K. Sze, C. Dai, and R. Z. Qi, "CDK5RAP2 stimulates microtubule nucleation by the tubulin ring complex," Journal of Cell Biology, vol. 191, no. 6, pp. 1089-1095, 2010
64. K. Lee and K. Rhee, "PLK1 phosphorylation of pericentrin initiates centrosome maturation at the onset of mitosis," Journal of Cell Biology, vol. 195, no. 7, pp. 1093-1101, 2011
65. S. Kim and K. Rhee, "Importance of the CEP215-pericentrin interaction for centrosome maturation during mitosis," PLoS ONE, vol. 9, no. 1,Article ID e87016, 2014
66. T. L. Megraw, J. T. Sharkey, and R. S. Nowakowski, "Cdk5rap2 exposes the centrosomal root of microcephaly syndromes," Trends in Cell Biology, vol. 21, no. 8, pp. 470-480, 2011
67. J. A. Barrera, L.-R. Kao, R. E. Hammer, J. Seemann, J. L. Fuchs, and T. L. Megraw, "CDK5RAP2 regulates centriole engagement and cohesion in mice," Developmental Cell, vol. 18, no. 6, pp. 913-926, 2010
68. S. Graser, Y.-D. Stierhof, and E. A. Nigg, "Cep68 and Cep215 (Cdk5rap2) are required for centrosome cohesion," Journal of Cell Science, vol. 120, no. 24, pp. 4321-4331, 2007
69. X. Zhang,D. Liu, S. Lv et al., "CDK5RAP2 is required for spindle checkpoint function," Cell Cycle, vol. 8, no. 8, pp. 1206-1216, 2009
70. J. J. Buchman, H.-C. Tseng, Y. Zhou, C. L. Frank, Z. Xie, and L.-H. Tsai, "Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex," Neuron, vol. 66, no. 3, pp. 386-402, 2010
71. S. B. Lizarraga, S. P. Margossian, M. H. Harris et al., "Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors," Development, vol. 137, no. 11, pp. 1907-1917, 2010
72. A. Genin, J. Desir, N. Lambert et al., "Kinetochore KMN network gene CASC5 mutated in primary microcephaly," Human Molecular Genetics, vol. 21, no. 24, pp. 5306-5317, 2012
73. I. M. Cheeseman, T. Hori, T. Fukagawa, and A. Desai, "KNL1 and the CENP-H/I/K complex coordinately direct kinetochore assembly in vertebrates," Molecular Biology of the Cell, vol. 19, no. 2, pp. 587-594, 2008
74. V. M. Bolanos-Garcia, T. Lischetti, D. Matak-Vinkovic et al., "Structure of a Blinkin-BUBR1 complex reveals an interaction crucial for kinetochore-mitotic checkpoint regulation via an unanticipated binding Site," Structure, vol. 19,no. 11-12, pp. 1691-1700, 2011
75. V. Krenn, A. Wehenkel, X. Li, S. Santaguida, and A. Musacchio, "Structural analysis reveals features of the spindle checkpoint kinase Bub1-kinetochore subunit Knl1 interaction," Journal of Cell Biology, vol. 196, no. 4, pp. 451-467, 2012
76. T. Kiyomitsu, C. Obuse, and M. Yanagida, " Human Blinkin/ AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1," Developmental Cell, vol. 13, no. 5, pp. 663-676, 2007
77. D. Varma and E. D. Salmon, "TheKMNprotein network-Chief conductors of the kinetochore orchestra," Journal of Cell Science, vol. 125, no. 24, pp. 5927-5936, 2012
78. J. Bond, S. Scott, D. J. Hampshire et al., "Protein-truncating mutations in ASPM cause variable reduction in brain size," The American Journal of Human Genetics, vol. 73, no. 5, pp. 1170-1177, 2003
79. A. Kumar, S. H. Blanton, M. Babu, M. Markandaya, and S. C. Girimaji, "Genetic analysis of primary microcephaly in Indian families: novel ASPM mutations," Clinical Genetics, vol. 66, no. 4, pp. 341-348, 2004
80. B. Pichon, S. Vankerckhove,G. Bourrouillou, L. Duprez, andM. J. Abramowicz, "A translocation breakpoint disrupts the ASPM gene in a patient with primary microcephaly," European Journal of Human Genetics, vol. 12, no. 5, pp. 419-421, 2004
81. J. Shen, W. Eyaid, G. H. Mochida et al., "ASPM mutations identified in patients with primary microcephaly and seizures," Journal of Medical Genetics, vol. 42, no. 9, pp. 725-729, 2005
82. A. Gul, M. J. Hassan, S. Mahmood et al., "Genetic studies of autosomal recessive primary microcephaly in 33 Pakistani families: novel sequence variants in ASPMgene," Neurogenetics, vol. 7, no. 2, pp. 105-110, 2006
83. A. Gul, M. Tariq, M. N. Khan, M. J. Hassan, G. Ali, and W. Ahmad, "Novel protein-truncating mutations in the ASPM gene in families with autosomal recessive primary microcephaly," Journal of Neurogenetics, vol. 21, no. 3, pp. 153-163, 2007
84. J. Desir,M. Cassart, P. David, P. van Bogaert, andM. Abramowicz, "Primary microcephaly with ASPM mutation shows simplified cortical gyration with antero-posterior gradient pre-and post-natally," The American Journal of Medical Genetics Part A, vol. 146, no. 11, pp. 1439-1443, 2008
85. F. Muhammad, S. M. Baig, L. Hansen et al., "Compound heterozygous aspmmutations in pakistaniMCPHfamilies,"The American Journal of MedicalGenetics Part A, vol. 149, no. 5, pp. 926-930, 2009
86. A. K. Nicholas, E. A. Swanson, J. J. Cox et al., "The molecular landscape of ASPM mutations in primary microcephaly," Journal of Medical Genetics, vol. 46, no. 4, pp. 249-253, 2009
87. A. Saadi, G. Borck, N. Boddaert et al., "Compound heterozygous ASPM mutations associated with microcephaly and simplified cortical gyration in a consanguineous Algerian family," European Journal ofMedical Genetics, vol. 52, no. 4, pp. 180-184, 2009
88. H. Darvish, S. Esmaeeli-Nieh, G. B. Monajemi et al., "A clinical andmolecular genetic study of 112 Iranian familieswith primary microcephaly," Journal of Medical Genetics, vol. 47, no. 12, pp. 823-828, 2010
89. R. Kousar, H. Nawaz, M. Khurshid et al., "Mutation analysis of theASPMgene in 18 Pakistani families with autosomal recessive primary microcephaly," Journal of Child Neurology, vol. 25, no. 6, pp. 715-720, 2010
90. C. R. Jamieson, J.-P. Fryns, J. Jacobs, G. Matthijs, and M. J. Abramowicz, "Primary autosomal recessive microcephaly: MCPH5 maps to 1q25-q32," The American Journal of Human Genetics, vol. 67, no. 6, pp. 1575-1577, 2000
91. W. Y. Tsang, A. Spektor, D. J. Luciano et al., "CP110 cooperates with two calcium-binding proteins to regulate cytokinesis and genome stability,"Molecular Biology of the Cell, vol. 17, no. 8, pp. 3423-3434, 2006
92. J. Higgins, C. Midgley, A. M. Bergh et al., "Human ASPM participates in spindle organisation, spindle orientation and cytokinesis," BMC Cell Biology, vol. 11, article 85, 2010
93. J. L. Fish, Y. Kosodo, W. Enard, S. Paabo, and W. B. Huttner, "Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells," Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 27, pp. 10438-10443, 2006
94. C. Gonzalez, R. D. C. Saunders, J. Casal et al., "Mutations at the asp locus of Drosophila lead to multiple free centrosomes in syncytial embryos, but restrict centrosome duplication in larval neuroblasts," Journal of Cell Science, vol. 96, no. 4, pp. 605-616, 1990
95. M. G. Riparbelli, G. Callaini, D. M. Glover, and M. do Carmo Avides, "A requirement for the abnormal spindle protein to organise microtubules of the central spindle for cytokinesis in Drosophila," Journal of Cell Science, vol. 115, no. 5, pp. 913-922, 2002
96. J. N. Pulvers, J. Bryk, J. L. Fish et al., "Mutations in mouse Aspm (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 38, pp. 16595-16600, 2010
97. J. Casal, C. Gonzalez, F. Wandosell, J. Avila, and P. Ripoll, "Abnormal meiotic spindles cause a cascade of defects during spermatogenesis in asp males of Drosophila," Development, vol. 108, no. 2, pp. 251-260, 1990
98. A. Fujimori, K. Itoh, S. Goto et al., "Disruption of Aspm causes microcephaly with abnormal neuronal differentiation," Brain and Development, vol. 36, no. 8, pp. 661-669, 2014
99. X.-L. Xu, W. Ma, Y.-B. Zhu et al., "The microtubule-associated protein ASPM regulates spindle assembly and meiotic progression in mouse oocytes," PLoS ONE, vol. 7, no. 11, Article ID e49303, 2012
100. N. Kouprina, A. Pavlicek,N. K. Collins et al., "The microcephaly ASPM gene is expressed in proliferating tissues and encodes for a mitotic spindle protein," Human Molecular Genetics, vol. 14, no. 15, pp. 2155-2165, 2005
101. C. Hagemann, J. Anacker, S. Gerngras et al., "Expression analysis of the autosomal recessive primary microcephaly genesMCPH1 (microcephalin) andMCPH5 (ASPM, abnormal spindle-like, microcephaly associated) in human malignant gliomas," Oncology Reports, vol. 20, no. 2, pp. 301-308, 2008
102. S.-Y. Lin, H.-W. Pan, S.-H. Liu et al., "ASPM is a novel marker for vascular invasion, early recurrence, and poor prognosis of hepatocellular carcinoma," Clinical Cancer Research, vol. 14, no. 15, pp. 4814-4820, 2008
103. R. Alsiary, A. Brüning-Richardson, J. Bond, E. E. Morrison, N. Wilkinson, and S. M. Bell, "Deregulation of microcephalin and ASPM expression are correlated with epithelial ovarian cancer progression," PLoS ONE, vol. 9, no. 5,Article ID e97059, 2014
104. P. Gönczy, "Towards a molecular architecture of centriole assembly," Nature Reviews Molecular Cell Biology, vol. 13, no. 7, pp. 425-435, 2012
105. S. Leidel and P. Gönczy, "Centrosome duplication and nematodes: recent insights from an old relationship," Developmental Cell, vol. 9, no. 3, pp. 317-325, 2005
106. J. Kleylein-Sohn, J. Westendorf, M. le Clech, R. Habedanck, Y.-D. Stierhof, and E. A. Nigg, "Plk4-induced centriole biogenesis in human cells," Developmental Cell, vol. 13, no. 2, pp. 190-202, 2007
107. K. F. Sonnen, A. M. Gabryjonczyk, E. Anselm, E. A. Nigg, and Y. D. Stierhof, "Human cep192 and cep152 cooperate in plk4 recruitment and centriole duplication," Journal of Cell Science, vol. 126, no. 14, pp. 3223-3233, 2013
108. T.-S. Kim, J.-E. Park, A. Shukla et al., "Hierarchical recruitment of Plk4 and regulation of centriole biogenesis by two centrosomal scaffolds, Cep192 and Cep152," Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 50, pp. E4849-E4857, 2013
109. E. M. Hatch, A. Kulukian, A. J. Holland, D. W. Cleveland, and T. Stearns, "Cep152 interacts with Plk4 and is required for centriole duplication," Journal of Cell Biology, vol. 191, no. 4, pp. 721-729, 2010
110. O. Cizmecioglu, M. Arnold, R. Bahtz et al., "Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome," Journal of Cell Biology, vol. 191, no. 4, pp. 731-739, 2010
111. N. S. Dzhindzhev, Q. D. Yu, K. Weiskopf et al., "Asterless is a scaffold for the onset of centriole assembly," Nature, vol. 467, no. 7316, pp. 714-718, 2010
112. M. van Breugel, M. Hirono, A. Andreeva et al., "Structures of SAS-6 suggest its organization in centrioles," Science, vol. 331, no. 6021, pp. 1196-1199, 2011
113. D. Kitagawa, I. Vakonakis, N. Olieric et al., "Structural basis of the 9-fold symmetry of centrioles," Cell, vol. 144, no. 3, pp. 364-375, 2011
114. R. Qiao, G. Cabral, M. M. Lettman, A. Dammermann, and G. Dong, "SAS-6 coiled-coil structure and interaction with SAS-5 suggest a regulatory mechanism in C. elegans centriole assembly," The EMBO Journal, vol. 31, no. 22, pp. 4334-4347, 2012
115. M. Lettman, Y. Wong, V. Viscardi et al., "Direct binding of SAS-6 to ZYG-1 recruits SAS-6 to the mother centriole for cartwheel assembly," Developmental Cell, vol. 25, no. 3, pp. 284-298, 2013
116. M. Delattre, C. Canard, and P. Gönczy, "Sequential protein recruitment in C. elegans centriole formation," Current Biology, vol. 16, no. 18, pp. 1844-1849, 2006
117. L. Pelletier, E. O'Toole, A. Schwager, A. A. Hyman, and T. Müller-Reichert, "Centriole assembly in Caenorhabditis elegans," Nature, vol. 444, no. 7119, pp. 619-623, 2006
118. C. J. C. Tang, S. Y. Lin, W. B. Hsu et al., "The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation," The EMBO Journal, vol. 30, no. 23, pp. 4790-4804, 2011
119. L.-Y. Hung, H.-L. Chen, C.-W. Chang, B.-R. Li, and T. K. Tang, "Identification of a novel microtubule-destabilizing motif in CPAP that binds to tubulin heterodimers and inhibits microtubule assembly,"Molecular Biology of the Cell, vol. 15, no. 6, pp. 2697-2706, 2004
120. W.-B. Hsu, L.-Y. Hung, C.-J. C. Tang, C.-L. Su, Y. Chang, and T. K. Tang, "Functional characterization of the microtubulebinding and-destabilizing domains of CPAP and d-SAS-4," Experimental Cell Research, vol. 314, no. 14, pp. 2591-2602, 2008
121. D. Comartin, G. D. Gupta, E. Fussner et al., "CEP120 and SPICE1 cooperate with CPAP in centriole elongation," Current Biology, vol. 23, no. 14, pp. 1360-1366, 2013
122. Y.-N. Lin, C.-T. Wu, Y.-C. Lin et al., "CEP120 interacts with CPAP and positively regulates centriole elongation," Journal of Cell Biology, vol. 202, no. 2, pp. 211-219, 2013
123. Y. C. Lin, C. W. Chang,W. B. Hsu et al., "Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly," The EMBO Journal, vol. 32, no. 8, pp. 1141-1154, 2013
124. C.-J. C. Tang, R.-H. Fu, K.-S. Wu, W.-B. Hsu, and T. K. Tang, "CPAP is a cell-cycle regulated protein that controls centriole length," Nature Cell Biology, vol. 11, no. 7, pp. 825-831, 2009
125. T. I. Schmidt, J. Kleylein-Sohn, J. Westendorf et al., "Control of centriole length by CPAP and CP110," Current Biology, vol. 19, no. 12, pp. 1005-1011, 2009
126. G. Kohlmaier, J. Loncarek, X. Meng et al., "Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP," Current Biology, vol. 19, no. 12, pp. 1012-1018, 2009
127. J.-H. Cho, C.-J. Chang, C.-Y. Chen, and T. K. Tang, "Depletion of CPAP by RNAi disrupts centrosome integrity and induces multipolar spindles," Biochemical and Biophysical Research Communications, vol. 339, no. 3, pp. 742-747, 2006
128. J. Gopalakrishnan, V. Mennella, S. Blachon et al., "Sas-4 provides a scaffold for cytoplasmic complexes and tethers them in a centrosome," Nature Communications, vol. 2, article 359, 2011
129. L.-Y. Hung, C.-J. C. Tang, and T. K. Tang, "Protein 4. 1 R-135 interacts with a novel centrosomal protein (CPAP) which is associated with the tubulin complex," Molecular and Cellular Biology, vol. 20, no. 20, pp. 7813-7825, 2000
130. J. Gopalakrishnan, Y.-C. Chim, A. Ha et al., "Tubulin nucleotide status controls Sas-4-dependent pericentriolarmaterial recruitment," Nature Cell Biology, vol. 14, no. 8, pp. 865-873, 2012
131. L. Shi, Q. Lin, and B. Su, "Human-specific hypomethylation of CENPJ, a key brain size regulator," Molecular Biology and Evolution, vol. 31, no. 3, pp. 594-604, 2014
132. R. E. McIntyre, P. L. Chavali, O. Ismail et al., "Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome," PLoS Genetics, vol. 8, no. 11, Article ID e1003022, 2012
133. S. Ladha, "Step to CEP152: uncovering a new mutation implicated in Seckel syndrome," Clinical Genetics, vol. 79, no. 5, pp. 428-430, 2011
134. J. Vulprecht, A. David, A. Tibelius et al., "STIL is required for centriole duplication in human cells," Journal of Cell Science, vol. 125, no. 5, pp. 1353-1362, 2012
135. C. Arquint, K. F. Sonnen, Y.-D. Stierhof, and E. A. Nigg, "Cellcycle-regulated expression of STIL controls centriole number in human cells," Journal of Cell Science, vol. 125, no. 5, pp. 1342-1352, 2012
136. R. Habedanck, Y.-D. Stierhof, C. J. Wilkinson, and E. A. Nigg, "The Polo kinase Plk4 functions in centriole duplication," Nature Cell Biology, vol. 7, no. 11, pp. 1140-1146, 2005
137. S. Leidel, M. Delattre, L. Cerutti, K. Baumer, and P. Gönczy, "SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells," Nature Cell Biology, vol. 7, no. 2, pp. 115-125, 2005
138. D. Kitagawa, G. Kohlmaier, D. Keller et al., "Spindle positioning in human cells relies on proper centriole formation and on the microcephaly proteins CPAP and STIL," Journal of Cell Science, vol. 124, no. 22, pp. 3884-3893, 2011
139. K. L. Pfaff, C. T. Straub, K. Chiang, D. M. Bear, Y. Zhou, and L. I. Zon, "The zebra fish cassiopeia mutant reveals that SIL is required for mitotic spindle organization," Molecular and Cellular Biology, vol. 27, no. 16, pp. 5887-5897, 2007
140. S. Izraeli, L. A. Lowe, V. L. Bertness et al., "The SIL gene is required formouse embryonic axial development and left-right specification," Nature, vol. 399, no. 6737, pp. 691-694, 1999
141. K. Kim, S. Lee, J. Chang, and K. Rhee, "A novel function of CEP135 as a platform protein of C-NAP1 for its centriolar localization," Experimental Cell Research, vol. 314, no. 20, pp. 3692-3700, 2008
142. A. Kumar, V. Rajendran, R. Sethumadhavan, and R. Purohit, "CEP proteins: the knights of centrosome dynasty," Protoplasma, vol. 250, no. 5, pp. 965-983, 2013
143. B. Inanç, M. Pütz, P. Lalor et al., "Abnormal centrosomal structure and duplication in Cep135-deficient vertebrate cells," Molecular Biology of the Cell, vol. 24,no. 17, pp. 2645-2654, 2013
144. Z. Carvalho-Santos, P. Machado, I. Alvarez-Martins et al., "BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair," Developmental Cell, vol. 23, no. 2, pp. 412-424, 2012
145. H. Roque, A. Wainman, J. Richens, K. Kozyrska,A. Franz, and J. W. Raff, "Drosophila Cep135/Bld10 maintains proper centriole structure but is dispensable for cartwheel formation," Journal of Cell Science, vol. 125, no. 23, pp. 5881-5886, 2012
146. K. Matsuura, P. A. Lefebvre, R. Kamiya, and M. Hirono, "Bld10p, a novel protein essential for basal body assembly in Chlamydomonas: localization to the cartwheel, the first ninefold symmetrical structure appearing during assembly," Journal of Cell Biology, vol. 165, no. 5, pp. 663-671, 2004
147. M. Hiraki, Y. Nakazawa, R. Kamiya, and M. Hirono, "Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole," Current Biology, vol. 17, no. 20, pp. 1778-1783, 2007
148. M. Jerka-Dziadosz, D. Gogendeau, C. Klotz, J. Cohen, J. Beisson, and F. Koll, "Basal body duplication in paramecium: the key role of Bld10 in assembly and stability of the Cartwheel," Cytoskeleton, vol. 67, no. 3, pp. 161-171, 2010
149. B. A. Bayless, T. H. Giddings Jr., M. Winey, and C. G. Pearson, "Bld10/Cep135 stabilizes basal bodies to resist cilia-generated forces," Molecular Biology of the Cell, vol. 23, no. 24, pp. 4820-4832, 2012
150. V. Mottier-Pavie and T. L. Megraw, "Drosophila Bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly," Molecular Biology of the Cell, vol. 20, no. 10, pp. 2605-2614, 2009
151. E. Kalay, G. Yigit, Y. Aslan et al., "CEP152 is a genome maintenance protein disrupted in Seckel syndrome," Nature Genetics, vol. 43, no. 1, pp. 23-26, 2011
152. T. Avidor-Reiss and J. Gopalakrishnan, "Building a centriole," Current Opinion in Cell Biology, vol. 25, no. 1, pp. 72-77, 2013
153. N. J. Brown, M. Marjanovic, J. Lüders, T. H. Stracker, and V. Costanzo, "Cep63 and cep152 cooperate to ensure centriole duplication," PLoS ONE, vol. 8, no. 7,Article ID e69986, 2013
154. G. Lukinavicius, D. Lavogina, M. Orpinell et al., "Selective chemical crosslinking reveals a Cep57-Cep63-Cep152 centrosomal complex," Current Biology, vol. 23, no. 3, pp. 265-270, 2013
155. S. Garapaty, C.-F. Xu, P. Trojer, M. A. Mahajan, T. A. Neubert, and H. H. Samuels, "Identification and characterization of a novel nuclear protein complex involved in nuclear hormone receptor-mediated gene regulation," The Journal of Biological Chemistry, vol. 284, no. 12, pp. 7542-7552, 2009
156. Y. J. Yang, A. E. Baltus, R. S. Mathew et al., "Microcephaly gene links trithorax and REST/NRSF to control neural stemcell proliferation and differentiation," Cell, vol. 151, no. 5, pp. 1097-1112, 2012
157. S. Awad, M. S. Al-Dosari, N. Al-Yacoub et al., "Mutation in PHC1 implicates chromatin remodeling in primary microcephaly pathogenesis," Human Molecular Genetics, vol. 22, no. 11, pp. 2200-2213, 2013
158. K.-E. K. Tachibana, M. A. Gonzalez, G. Guarguaglini, E. A. Nigg, and R. A. Laskey, "Depletion of licensing inhibitor geminin causes centrosome overduplication and mitotic defects," EMBO Reports, vol. 6, no. 11, pp. 1052-1057, 2005
159. F. Lu, R. Lan, H. Zhang, Q. Jiang, and C. Zhang, "Geminin is partially localized to the centrosome and plays a role in proper centrosome duplication," Biology of the Cell, vol. 101, no. 5, pp. 273-285, 2009
160. C. Bertoli, J. M. Skotheim, and R. A. M. de Bruin, "Control of cell cycle transcription during G1 and S phases," Nature Reviews Molecular Cell Biology, vol. 14, no. 8, pp. 518-528, 2013
161. D. Mahony, D. A. Parry, and E. Lees, "Active cdk6 complexes are predominantly nuclear and represent only a minority of the cdk6 in T cells," Oncogene, vol. 16, no. 5, pp. 603-611, 1998
162. D. M. Kohrt, J. I. Crary, V. Gocheva, P. W. Hinds, and M. J. Grossel, "Distinct subcellular distribution of cyclin dependent kinase 6," Cell Cycle, vol. 8, no. 17, pp. 2837-2843, 2009
163. T. K. Kwon, M. A. Buchholz, E. W. Gabrielson, andA. A. Nordin, "Anovel cytoplasmic substrate for cdk4 and cdk6 innormal and malignant epithelial derived cells," Oncogene, vol. 11, no. 10, pp. 2077-2083, 1995
164. M. Malumbres, R. Sotillo, D. Santamaría et al., "Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6," Cell, vol. 118, no. 4, pp. 493-504, 2004
165. D. Mi, C. Carr, P. A. Georgala et al., "Pax6 Exerts regional control of cortical progenitor proliferation via direct repression of Cdk6 and Hypophosphorylation of pRb," Neuron, vol. 78, no. 2, pp. 269-284, 2013
166. P. Beukelaers, R. Vandenbosch, N. Caron et al., "Cdk6-dependent regulation of G1 length controls adult neurogenesis," Stem Cells, vol. 29, no. 4, pp. 713-724, 2011
167. A. Rauch, C. T. Thiel, D. Schindler et al., "Mutations in the pericentrin (PCNT) gene cause primordial dwarfism," Science, vol. 319, no. 5864, pp. 816-819, 2008
168. V. Marthiens, M. A. Rujano, C. Pennetier, S. Tessier, P. Paul-Gilloteaux, and R. Basto, "Centrosome amplification causes microcephaly," Nature Cell Biology, vol. 15, no. 7, pp. 731-740, 2013
169. E. Roberts, A. P. Jackson, A. C. Carradice et al., "The second locus for autosomal recessive primary microcephaly (MCPH2) maps to chromosome 19q13. 1-13. 2," European Journal of Human Genetics, vol. 7, no. 7, pp. 815-820, 1999
170. L. Moynihan, A. P. Jackson, E. Roberts et al., "A third novel locus for primary autosomal recessive microcephaly maps to chromosome 9q34," The American Journal of Human Genetics, vol. 66, no. 2, pp. 724-727, 2000
171. C. R. Jamieson, C. Govaerts, and M. J. Abramowicz, "Primary autosomal recessive microcephaly: homozygosity mapping of MCPH4 to chromosome 15," The American Journal of Human Genetics, vol. 65, no. 5, pp. 1465-1469, 1999
172. L. Pattison, Y. J. Crow, V. J. Deeble et al., "A fifth locus for primary autosomal recessive microcephaly maps to chromosome 1q31," American Journal of Human Genetics, vol. 67, no. 6, pp. 1578-1580, 2000.