Centrosome amplification causes microcephaly

Nature Cell Biology

Volumn 15, Issue 7, 2013, Pages 731-740

  Marthiens, Véronique ^a   Rujano, Maria A ^a   Pennetier, Carole ^a   Tessier, Sarah ^a   Paul Gilloteaux, Perrine ^a   Basto, Renata ^a  

^a INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTROSOME; CENTROSOME AMPLIFICATION; CONTROLLED STUDY; EMBRYO; HOMEOSTASIS; MICROCEPHALY; MITOSIS; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; TISSUE DEGENERATION;

ANEUPLOIDY; ANIMALS; APOPTOSIS; BRAIN; CELLS, CULTURED; CENTROSOME; CHROMOSOMAL INSTABILITY; EMBRYO, MAMMALIAN; MICE; MICE, KNOCKOUT; MICROCEPHALY; MITOSIS; NEURAL STEM CELLS; PROTEIN-SERINE-THREONINE KINASES; SURVIVAL RATE;

EID: 84880332168     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2746     Document Type: Article

References (65)

1. Ring, D., Hubble, R. & Kirschner, M. Mitosis in a cell with multiple centrioles. J. Cell Biol. 94, 549-556 (1982).
2. Quintyne, N. J., Reing, J. E., Hoffelder, D. R., Gollin, S. M. & Saunders, W. S. Spindle multipolarity is prevented by centrosomal clustering. Science 307, 127-129 (2005).
3. Zyss, D. & Gergely, F. Centrosome function in cancer:guilty or innocent? Trends Cell Biol. 19, 334-346 (2009).
4. Holland, A. J. & Cleveland, D. W. Losing balance:the origin and impact of aneuploidy in cancer. EMBO Rep. 13, 501-514 (2012).
5. Pihan, G. A. & Doxsey, S. J. The mitotic machinery as a source of genetic instability in cancer. Semin Cancer Biol. 9, 289-302 (1999).
6. Nigg, E. A. Origins and consequences of centrosome aberrations in human cancers. Int. J. Cancer 119, 2717-2723 (2006).
7. Basto, R. et al. Centrosome ampli-cation can initiate tumorigenesis in -ies. Cell 133, 1032-1042 (2008).
8. Marthiens, V., Piel, M. & Basto, R. Never tear us apart-The importance of centrosome clustering. J. Cell Sci. 125, 3281-3292 (2012).
9. Nigg, E. A. & Raff, J. W. Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678 (2009).
10. Megraw, T. L., Sharkey, J. T. & Nowakowski, R. S. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol. 21, 470-480 (2011).
11. Bettencourt-Dias, M., Hildebrandt, F., Pellman, D., Woods, G. & Godinho, S. A. Centrosomes and cilia in human disease. Trends Genet. 27, 307-315 (2011).
12. Wang, X. et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947-955 (2009).
13. Thornton, G. K. & Woods, C. G. Primary microcephaly:do all roads lead to Rome? Trends Genet. 25, 501-510 (2009).
14. Lizarraga, S. B. et al. Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137, 1907-1917 (2010).
15. Alderton, G. K. et al. Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell Biol. 8, 725-733 (2006).
16. Habedanck, R., Stierhof, Y. D., Wilkinson, C. J. & Nigg, E. A. The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7, 1140-1146 (2005).
17. Kleylein-Sohn, J. et al. Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202 (2007).
18. Bettencourt-Dias, M. et al. SAK/PLK4 is required for centriole duplication and -agella development. Curr. Biol. 15, 2199-2207 (2005).
19. Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99-103 (1999).
20. Cohen, E., Binet, S. & Meininger, V. Ciliogenesis and centriole formation in the mouse embryonic nervous system. An ultrastructural analysis. Biol. Cell 62, 165-169 (1988).
21. Wilsch-Brauninger, M., Peters, J., Paridaen, J. T. & Huttner, W. B. Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. Development 139, 95-105 (2012).
22. Huangfu, D. et al. Hedgehog signalling in the mouse requires intra-agellar transport proteins. Nature 426, 83-87 (2003).
23. Besse, L. et al. Primary cilia control telencephalic patterning and morphogenesis via Gli3 proteolytic processing. Development 138, 2079-2088 (2011).
24. Fode, C., Binkert, C. & Dennis, J. W. Constitutive expression of murine Sak- A suppresses cell growth and induces multinucleation. Mol. Cell Biol. 16, 4665-4672 (1996).
25. Ko, M. A. et al. Plk4 haploinsuf-ciency causes mitotic in-delity and carcinogenesis. Nat. Genet. 37, 883-888 (2005).
26. Holland, A. J. et al. Polo-like kinase 4 controls centriole duplication but does not directly regulate cytokinesis. Mol. Biol. Cell 23, 1838-1845 (2012).
27. Silver, D. L. et al. The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat. Neurosci. 13, 551-558 (2010).
28. Feng, Y. & Walsh, C. A. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279-293 (2004).
29. Pawlisz, A. S. et al. Lis1-Nde1-dependent neuronal fate control determines cerebral cortical size and lamination. Hum. Mol. Genet. 17, 2441-2455 (2008).
30. Yingling, J. et al. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132, 474-486 (2008).
31. Gotz, M. & Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788 (2005).
32. Lui, J. H., Hansen, D. V. & Kriegstein, A. R. Development and evolution of the human neocortex. Cell 146, 18-36 (2011).
33. Englund, C. et al. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247-251 (2005).
34. Molyneaux, B. J., Arlotta, P., Menezes, J. R. & Macklis, J. D. Neuronal subtype speci-cation in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437 (2007).
35. Fish, J. L., Dehay, C., Kennedy, H. & Huttner, W. B. Making bigger brains-The evolution of neural-progenitor-cell division. J. Cell Sci. 121, 2783-2793 (2008).
36. Pulvers, J. N. et al. Mutations in mouse Aspm (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline. Proc. Natl Acad. Sci. USA 107, 16595-16600 (2010).
37. Silkworth, W. T., Nardi, I. K., Scholl, L. M. & Cimini, D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS One 4, e6564 (2009).
38. Ganem, N. J., Godinho, S. A. & Pellman, D. A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282 (2009).
39. Egger, B., Boone, J. Q., Stevens, N. R., Brand, A. H. & Doe, C. Q. Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe. Neural Dev. 2, 1 (2007).
40. Yang, Z., Loncarek, J., Khodjakov, A. & Rieder, C. L. Extra centrosomes and/or chromosomes prolong mitosis in human cells. Nat. Cell Biol. 10, 748-751 (2008).
41. Gergely, F. & Basto, R. Multiple centrosomes:together they stand, divided they fall. Genes Dev. 22, 2291-2296 (2008).
42. Leidel, S., Delattre, M., Cerutti, L., Baumer, K. & Gonczy, P. SAS-6 de-nes a protein family required for centrosome duplication in C. elegans and in human cells. Nat. Cell Biol. 7, 115-125 (2005).
43. Kitagawa, D. et al. Structural basis of the 9-fold symmetry of centrioles. Cell 144, 364-375 (2011).
44. Peel, N., Stevens, N. R., Basto, R. & Raff, J. W. Overexpressing centriole-replication proteins in vivo induces centriole overduplication and de novo formation. Curr. Biol. 17, 834-843 (2007).
45. Holland, A. J. et al. The autoregulated instability of Polo-like kinase 4 limits centrosome duplication to once per cell cycle. Genes Dev. 26, 2684-2689 (2012).
46. Thompson, S. L. & Compton, D. A. Examining the link between chromosomal instability and aneuploidy in human cells. J. Cell Biol. 180, 665-672 (2008).
47. Thompson, S. L. & Compton, D. A. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J. Cell Biol. 188, 369-381 (2010).
48. Jonkers, J. et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418-425 (2001).
49. Faggioli, F., Wang, T., Vijg, J. & Montagna, C. Chromosome-speci-c accumulation of aneuploidy in the aging mouse brain. Hum. Mol. Genet. 21, 5246-5253 (2012).
50. Doxsey, S. Duplicating dangerously:linking centrosome duplication and aneuploidy. Mol. Cell 10, 439-440 (2002).
51. Woods, C. G., Bond, J. & Enard, W. Autosomal recessive primary microcephaly (MCPH):A review of clinical, molecular, and evolutionary -ndings. Am. J. Hum. Genet. 76, 717-728 (2005).
52. Bond, J. et al. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat. Genet. 37, 353-355 (2005).
53. Gruber, R. et al. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 13, 1325-1334 (2011).
54. Morin, X., Jaouen, F. & Durbec, P. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440-1448 (2007).
55. Barrera, J. A. et al. CDK5RAP2 regulates centriole engagement and cohesion in mice. Dev. Cell 18, 913-926 (2010).
56. Hussain, M. S. et al. A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am. J. Hum. Genet. 90, 871-878 (2012).
57. McIntyre, R. E. et al. Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome. PLoS Genet. 8, e1003022 (2012).
58. Arquint, C., Sonnen, K. F., Stierhof, Y. D. & Nigg, E. A. Cell-cycle-regulated expression of STIL controls centriole number in human cells. J. Cell Sci. 125, 1342-1352 (2012).
59. Tang, C. J. et al. The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J. 30, 4790-4804 (2011).
60. Hanks, S. et al. Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat. Gene. 36, 1159-1161 (2004).
61. Snape, K. et al. Mutations in CEP57 cause mosaic variegated aneuploidy syndrome. Nat. Gene. 43, 527-529 (2011).
62. Oromendia, A. B., Dodgson, S. E. & Amon, A. Aneuploidy causes proteotoxic stress in yeast. Genes Dev. 26, 2696-2708 (2012).
63. Friedmann-Morvinski, D. et al. Dedifferentiation of neurons and astrocytes By oncogenes can induce gliomas in mice. Science 338, 1080-1084 (2012).
64. el Marjou, F. et al. Tissue-speci-c and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186-193 (2004).
65. Haydar, T.F., Ang, E. Jr & Rakic, P. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl Acad. Sci. USA 100, 2890-2895 (2003).