The microcephaly protein Asp regulates neuroepithelium morphogenesis by controlling the spatial distribution of myosin II

Nature Cell Biology

Volumn 15, Issue 11, 2013, Pages 1294-1306

  Rujano, Maria A ^a   Sanchez Pulido, Luis ^b   Pennetier, Carole ^a   Le Dez, Gaelle ^a,c   Basto, Renata ^a  

^a INSTITUT CURIE   (France)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABNORMAL SPINDLE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MYOSIN II; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN SIZE; CELL NUCLEUS; CELL POLARITY; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DROSOPHILA; MICROCEPHALY; MITOSIS; MITOSIS SPINDLE; MORPHOGENESIS; NEUROEPITHELIUM; NONHUMAN; OPTIC LOBE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BRAIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIUM; MICROTUBULE-ASSOCIATED PROTEINS; MORPHOGENESIS; MYOSIN TYPE II;

INVERTEBRATA;

EID: 84887217839     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2858     Document Type: Article

References (70)

1. Bond, J. et al. ASPM is a major determinant of cerebral cortical size. Nat. Genet. 32, 316-320 (2002).
2. 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).
3. Thornton, G. K. & Woods, C. G. Primary microcephaly: do all roads lead to Rome? Trends Genet. 25, 501-510 (2009).
4. Kaindl, A. M. et al. Many roads lead to primary autosomal recessive microcephaly. Prog. Neurobiol. 90, 363-383 (2010).
5. Bettencourt-Dias, M., Hildebrandt, F., Pellman, D., Woods, G. & Godinho, S. A. Centrosomes and cilia in human disease. Trends Genet. 27, 307-315 (2011).
6. Darvish, H. et al. A clinical and molecular genetic study of 112 Iranian families with primary microcephaly. J. Med. Genet. 47, 823-828 (2010).
7. Buchman, J. J., Durak, O. & Tsai, L. H. ASPM regulates Wnt signaling pathway activity in the developing brain. Genes Dev. 25, 1909-1914 (2011).
8. Montgomery, S. H. & Mundy, N. I. Brain evolution: microcephaly genes weigh in. Curr. Biol. 20, R244-R246 (2010).
9. Montgomery, S. H. & Mundy, N. I. Evolution of ASPM is associated with both increases and decreases in brain size in primates. Evolution 66, 927-932 (2012).
10. Casal, J., Gonzalez, C., Wandosell, F., Avila, J. & Ripoll, P. Abnormal meiotic spindles cause a cascade of defects during spermatogenesis in asp males of Drosophila. Development 108, 251-260 (1990).
11. Gonzalez, C., Casal, J. & Ripoll, P. Functional monopolar spindles caused by mutation in mgr, a cell division gene of Drosophila melanogaster. J. Cell Sci. 89, 39-47 (1988).
12. Gonzalez, C. et al. Mutations at the asp locus of Drosophila lead to multiple free centrosomes in syncytial embryos, but restrict centrosome duplication in larval neuroblasts. J. Cell Sci. 96, 605-616 (1990).
13. Saunders, R. D., Avides, M. C., Howard, T., Gonzalez, C. & Glover, D. M. The Drosophila gene abnormal spindle encodes a novel microtubule-associated protein that associates with the polar regions of the mitotic spindle. J. Cell Biol. 137, 881-890 (1997). (Pubitemid 27215510)
14. Do Carmo Avides, M. & Glover, D. M. Abnormal spindle protein, Asp, and the integrity of mitotic centrosomal microtubule organizing centers. Science 283, 1733-1735 (1999).
15. Wakefield, J. G., Bonaccorsi, S. & Gatti, M. The Drosophila protein asp is involved in microtubule organization during spindle formation and cytokinesis. J. Cell Biol. 153, 637-648 (2001).
16. Riparbelli, M. G., Callaini, G., Glover, D. M. & Avides Mdo, C. A requirement for the Abnormal Spindle protein to organise microtubules of the central spindle for cytokinesis in Drosophila. J. Cell Sci. 115, 913-922 (2002). (Pubitemid 34257376)
17. Rebollo, E., Llamazares, S., Reina, J. & Gonzalez, C. Contribution of noncentrosomal microtubules to spindle assembly in Drosophila spermatocytes. PLoS Biol. 2, 0054-0064 (2004).
18. Morales-Mulia, S. & Scholey, J. M. Spindle pole organization in Drosophila S2 cells by dynein, abnormal spindle protein (Asp), and KLP10A. Mol. Biol. Cell 16, 3176-3186 (2005). (Pubitemid 40962590)
19. Fish, J. L., Kosodo, Y., Enard, W., Paabo, S. & Huttner, W. B. Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl Acad. Sci. USA 103, 10438-10443 (2006). (Pubitemid 44051185)
20. Kwon, M. et al. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 22, 2189-2203 (2008).
21. 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).
22. Hofbauer, A. & Campos-Ortega, J. A. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Roux's Arch. Dev. Biol. 198, 264-274 (1990). (Pubitemid 20064278)
23. 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).
24. Richter, C., Oktaba, K., Steinmann, J., Muller, J. & Knoblich, J. A. The tumour suppressor L(3)mbt inhibits neuroepithelial proliferation and acts on insulator elements. Nat. Cell Biol. 13, 1029-1039 (2011).
25. Yasugi, T., Umetsu, D., Murakami, S., Sato, M. & Tabata, T. Drosophila optic lobe neuroblasts triggered by a wave of proneural gene expression that is negatively regulated by JAK/STAT. Development 135, 1471-1480 (2008). (Pubitemid 351753637)
26. Ripoll, P., Pimpinelli, S., Valdivia, M. M. & Avila, J. A cell division mutant of Drosophila with a functionally abnormal spindle. Cell 41, 907-912 (1985). (Pubitemid 15243396)
27. Meinertzhagen, I. & Hanson, T. in The Development of Drosophila melanogaster (eds Bate, M. & Martinez-Arias, A.) 1363-1491 (Cold Spring Harbor, 1993).
28. Holland, A. J. & Cleveland, D. W. Losing balance: the origin and impact of aneuploidy in cancer. EMBO Rep. 13, 501-514 (2012).
29. Brumby, A. M. & Richardson, H. E. scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 22, 5769-5779 (2003). (Pubitemid 37408816)
30. Morin, X. & Bellaiche, Y. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev. Cell 21, 102-119 (2011).
31. Sauer, F. C. Mitosis in the neural tube. J. Comput. Neurol. 62, 377-405 (1935).
32. Del Bene, F., Wehman, A. M., Link, B. A. & Baier, H. Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134, 1055-1065 (2008).
33. Norden, C., Young, S., Link, B. A. & Harris, W. A. Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138, 1195-1208 (2009).
34. Meyer, E. J., Ikmi, A. & Gibson, M. C. Interkinetic nuclear migration is a broadly conserved feature of cell division in pseudostratified epithelia. Curr. Biol. 21, 485-491 (2011).
35. Tsai, J. W., Lian, W. N., Kemal, S., Kriegstein, A. R. & Vallee, R. B. Kinesin 3 and cytoplasmic dynein mediate interkinetic nuclear migration in neural stem cells. Nat. Neurosci. 13, 1463-1471 (2010).
36. Cappello, S., Monzo, P. & Vallee, R. B. NudC is required for interkinetic nuclear migration and neuronal migration during neocortical development. Dev. Biol. 357, 326-335 (2011).
37. Kosodo, Y. et al. Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain. EMBO J. 30, 1690-1704 (2011).
38. Lee, H. O. & Norden, C. Mechanisms controlling arrangements and movements of nuclei in pseudostratified epithelia. Trends Cell Biol. 23, 141-150 (2012).
39. Baye, L. M. & Link, B. A. Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J. Neurosci. 27, 10143-10152 (2007). (Pubitemid 47450458)
40. Schenk, J., Wilsch-Brauninger, M., Calegari, F. & Huttner, W. B. Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc. Natl Acad. Sci. USA 106, 16487-16492 (2009).
41. Levayer, R. & Lecuit, T. Biomechanical regulation of contractility: spatial control and dynamics. Trends Cell Biol. 22, 61-81 (2012).
42. Franke, J. D., Boury, A. L., Gerald, N. J. & Kiehart, D. P. Native nonmuscle myosin II stability and light chain binding in Drosophila melanogaster. Cell Motil. Cytoskeleton 63, 604-622 (2006). (Pubitemid 44454022)
43. Royou, A., Sullivan, W. & Karess, R. Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J. Cell Biol. 158, 127-137 (2002).
44. Jordan, P. & Karess, R. Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J. Cell Biol. 139, 1805-1819 (1997). (Pubitemid 28079244)
45. Winter, C. G. et al. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91 (2001). (Pubitemid 32323918)
46. Farhadifar, R., Roper, J. C., Aigouy, B., Eaton, S. & Julicher, F. The infiuence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 17, 2095-2104 (2007). (Pubitemid 50014864)
47. Rauzi, M. & Lenne, P. F. Cortical forces in cell shape changes and tissue morphogenesis. Curr. Top Dev. Biol. 95, 93-144 (2011).
48. Baum, B. & Georgiou, M. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J. Cell Biol. 192, 907-917 (2011).
49. Marthiens, V. et al. Centrosome amplification causes microcephaly. Nat. Cell Biol. 15, 731-740 (2013).
50. Del Bene, F. Interkinetic nuclear migration: cell cycle on the move. EMBO J. 30, 1676-1677 (2011).
51. Tepass, U. The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu. Rev. Cell Dev. Biol. 28, 655-685 (2012).
52. Basto, R. et al. Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042 (2008). (Pubitemid 351787756)
53. Dobbelaere, J. et al. A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol. 6, 1975-1990 (2008).
54. Gervais, L., Claret, S., Januschke, J., Roth, S. & Guichet, A. PIP5K-dependent production of PIP2 sustains microtubule organization to establish polarized transport in the Drosophila oocyte. Development 135, 3829-3838 (2008).
55. Martin, A. C., Kaschube, M. & Wieschaus, E. F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495-499 (2009).
56. Huang, J., Zhou, W., Dong, W., Watson, A. M. & Hong, Y. From the cover: directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc. Natl Acad. Sci. USA 106, 8284-8289 (2009).
57. Basler, K. & Struhl, G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214 (1994). (Pubitemid 24108836)
58. Golic, K. G. & Lindquist, S. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509 (1989). (Pubitemid 19284463)
59. Xu, T. & Rubin, G. M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237 (1993). (Pubitemid 23154489)
60. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254 (2001). (Pubitemid 32304463)
61. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (1993). (Pubitemid 23214028)
62. Basto, R. et al. Flies without centrioles. Cell 125, 1375-1386 (2006). (Pubitemid 43929089)
63. Martinez-Campos, M., Basto, R., Baker, J., Kernan, M. & Raff, J. W. The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J. Cell Biol. 165, 673-683 (2004). (Pubitemid 38765769)
64. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676-682 (2012).
65. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997). (Pubitemid 27359211)
66. Wu, C. H. et al. The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res. 34, D187-D191 (2006).
67. Notredame, C., Higgins, D. G. & Heringa, J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217 (2000).
68. Sonnhammer, E. L. & Hollich, V. Scoredist: a simple and robust protein sequence distance estimator. BMC Bioinformat. 6, 108 (2005).
69. Eddy, S. R. Hidden Markov models. Curr. Opin. Struct. Biol. 6, 361-365 (1996). (Pubitemid 26197437)
70. Soding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248 (2005). (Pubitemid 44529917)