Prolonged Mitosis of Neural Progenitors Alters Cell Fate in the Developing Brain

Neuron

Volumn 89, Issue 1, 2016, Pages 83-99

  Pilaz, Louis Jan ^a   McMahon, John J ^a   Miller, Emily E ^a   Lennox, Ashley L ^a   Suzuki, Aussie ^b   Salmon, Edward ^b   Silver, Debra L ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53;

APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN SIZE; CELL CYCLE; CELL DIFFERENTIATION; CELL FATE; CELL VIABILITY; GENE MUTATION; HUMAN; IN VIVO STUDY; MICROCEPHALY; MITOSIS; MITOSIS INHIBITION; MOUSE; NEOCORTEX; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROMETAPHASE; STEM CELL; ANIMAL; BRAIN CORTEX; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NEURAL STEM CELL; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CEREBRAL CORTEX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE, TRANSGENIC; MITOSIS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS;

EID: 84953790901     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.12.007     Document Type: Article

References (54)

1. Arai Y., Pulvers J.N., Haffner C., Schilling B., Nüsslein I., Calegari F., Huttner W.B. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2011, 2:154.
2. Arnold S.J., Sugnaseelan J., Groszer M., Srinivas S., Robertson E.J. Generation and analysis of a mouse line harboring GFP in the Eomes/Tbr2 locus. Genesis 2009, 47:775-781.
3. Asami M., Pilz G.A., Ninkovic J., Godinho L., Schroeder T., Huttner W.B., Gotz M. The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development 2011, 138:5067-5078.
4. Bazzi H., Anderson K.V. Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo. Proc. Natl. Acad. Sci. USA 2014, 111:E1491-E1500.
5. Bonner M.K., Poole D.S., Xu T., Sarkeshik A., Yates J.R., Skop A.R. Mitotic spindle proteomics in Chinese hamster ovary cells. PLoS ONE 2011, 6:e20489.
6. Chen J.-F., Zhang Y., Wilde J., Hansen K.C., Lai F., Niswander L. Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size. Nat. Commun. 2014, 5:3885.
7. Delaunay D., Cortay V., Patti D., Knoblauch K., Dehay C. Mitotic spindle asymmetry: a Wnt/PCP-regulated mechanism generating asymmetrical division in cortical precursors. Cell Rep. 2014, 6:400-414.
8. Franco S.J., Müller U. Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 2013, 77:19-34.
9. Gaglio T., Saredi A., Compton D.A. NuMA is required for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 1995, 131:693-708.
10. Ganem N.J., Pellman D. Linking abnormal mitosis to the acquisition of DNA damage. J. Cell Biol. 2012, 199:871-881.
11. Geschwind D.H., Rakic P. Cortical Evolution: Judge the Brain by Its Cover. Neuron 2013, 80:633-647.
12. Gil-Perotin S., Marin-Husstege M., Li J., Soriano-Navarro M., Zindy F., Roussel M.F., Garcia-Verdugo J.-M., Casaccia-Bonnefil P. Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J. Neurosci. 2006, 26:1107-1116.
13. Gruber R., Zhou Z., Sukchev M., Joerss T., Frappart P.-O., Wang Z.-Q. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 2011, 13:1325-1334. 10.1038/ncb2342.
14. Haydar T.F., Ang E., Rakic P. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl. Acad. Sci. USA 2003, 100:2890-2895. 10.1073/pnas.0437969100.
15. Hu W.F., Chahrour M.H., Walsh C.A. The diverse genetic landscape of neurodevelopmental disorders. Annu. Rev. Genomics Hum. Genet. 2014, 15:195-213.
16. Inomata K., Aoto T., Binh N.T., Okamoto N., Tanimura S., Wakayama T., Iseki S., Hara E., Masunaga T., Shimizu H., Nishimura E.K. Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 2009, 137:1088-1099.
17. Insolera R., Bazzi H., Shao W., Anderson K.V., Shi S.-H. Cortical neurogenesis in the absence of centrioles. Nat. Neurosci. 2014, 17:1528-1535.
18. Ishigaki Y., Nakamura Y., Tatsuno T., Hashimoto M., Iwabuchi K., Tomosugi N. RNA-binding protein RBM8A (Y14) and MAGOH localize to centrosome in human A549 cells. Histochem. Cell Biol. 2014, 141:101-109.
19. Konno D., Shioi G., Shitamukai A., Mori A., Kiyonari H., Miyata T., Matsuzaki F. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 2008, 10:93-101.
20. Kowalczyk T., Pontious A., Englund C., Daza R.A.M., Bedogni F., Hodge R., Attardo A., Bell C., Huttner W.B., Hevner R.F. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 2009, 19:2439-2450.
21. LaMonica B.E., Lui J.H., Hansen D.V., Kriegstein A.R. Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex. Nat. Commun. 2013, 4:1665.
22. Lancaster M.A., Renner M., Martin C.-A., Wenzel D., Bicknell L.S., Hurles M.E., Homfray T., Penninger J.M., Jackson A.P., Knoblich J.A. Cerebral organoids model human brain development and microcephaly. Nature 2013, 501:373-379.
23. Lange C., Huttner W.B., Calegari F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 2009, 5:320-331.
24. Lizarraga S.B., Margossian S.P., Harris M.H., Campagna D.R., Han A.-P., Blevins S., Mudbhary R., Barker J.E., Walsh C.A., Fleming M.D. Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 2010, 137:1907-1917.
25. Malatesta P., Hartfuss E., Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000, 127:5253-5263.
26. Mao H., Pilaz L.-J., McMahon J.J., Golzio C., Wu D., Shi L., Katsanis N., Silver D.L. Rbm8a haploinsufficiency disrupts embryonic cortical development resulting in microcephaly. J. Neurosci. 2015, 35:7003-7018.
27. Marthiens V., Rujano M.A., Pennetier C., Tessier S., Paul-Gilloteaux P., Basto R. Centrosome amplification causes microcephaly. Nat. Cell Biol. 2013, 15:731-740.
28. McIntyre R.E., Lakshminarasimhan Chavali P., Ismail O., Carragher D.M., Sanchez-Andrade G., Forment J.V., Fu B., Del Castillo Velasco-Herrera M., Edwards A., van der Weyden L., et al. Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome. PLoS Genet. 2012, 8:e1003022. Sanger Mouse Genetics Project.
29. McMahon J.J., Shi L., Silver D.L. Generation of a Magoh conditional allele in mice. Genesis 2014, 52:752-758.
30. Micklem D.R., Dasgupta R., Elliott H., Gergely F., Davidson C., Brand A., González-Reyes A., St Johnston D. The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila. Curr. Biol. 1997, 7:468-478.
31. Mora-Bermúdez F., Matsuzaki F., Huttner W.B. Specific polar subpopulations of astral microtubules control spindle orientation and symmetric neural stem cell division. eLife 2014, 3:e02875.
32. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409:714-720.
33. Novorol C., Burkhardt J., Wood K.J., Iqbal A., Roque C., Coutts N., Almeida A.D., He J., Wilkinson C.J., Harris W.A. Microcephaly models in the developing zebrafish retinal neuroepithelium point to an underlying defect in metaphase progression. Open Biol. 2013, 3:130065.
34. Ostergaard P., Simpson M.A., Mendola A., Vasudevan P., Connell F.C., van Impel A., Moore A.T., Loeys B.L., Ghalamkarpour A., Onoufriadis A., et al. Mutations in KIF11 cause autosomal-dominant microcephaly variably associated with congenital lymphedema and chorioretinopathy. Am. J. Hum. Genet. 2012, 90:356-362.
35. Ostrem B.E.L., Lui J.H., Gertz C.C., Kriegstein A.R. Control of outer radial glial stem cell mitosis in the human brain. Cell Rep. 2014, 8:656-664.
36. Pilaz L.-J., Silver D.L. Live imaging of mitosis in the developing mouse embryonic cortex. J. Vis. Exp. 2014, 4. e51298-e51298.
37. Pilaz L.-J., Silver D.L. Post-transcriptional regulation in corticogenesis: how RNA-binding proteins help build the brain. Wiley Interdiscip. Rev. RNA 2015, 6:501-515.
38. Pilaz L.-J., Patti D., Marcy G., Ollier E., Pfister S., Douglas R.J., Betizeau M., Gautier E., Cortay V., Doerflinger N., et al. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl. Acad. Sci. USA 2009, 106:21924-21929.
39. Quinn J.C., Molinek M., Martynoga B.S., Zaki P.A., Faedo A., Bulfone A., Hevner R.F., West J.D., Price D.J. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev. Biol. 2007, 302:50-65.
40. Sauer G., Körner R., Hanisch A., Ries A., Nigg E.A., Silljé H.H. Proteome analysis of the human mitotic spindle. Mol. Cell. Proteomics 2005, 4:35-43.
41. Shen Q., Zhong W., Jan Y., Temple S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 2002, 129:4843-4853.
42. Sherman M.H., Bassing C.H., Teitell M.A. Regulation of cell differentiation by the DNA damage response. Trends Cell Biol. 2011, 21:312-319.
43. Silver D.L., Watkins-Chow D.E., Schreck K.C., Pierfelice T.J., Larson D.M., Burnetti A.J., Liaw H.-J., Myung K., Walsh C.A., Gaiano N., Pavan W.J. The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat. Neurosci. 2010, 13:551-558.
44. Silver D.L., Leeds K.E., Hwang H.-W., Miller E.E., Pavan W.J. The EJC component Magoh regulates proliferation and expansion of neural crest-derived melanocytes. Dev. Biol. 2013, 375:172-181.
45. Skoufias D.A., DeBonis S., Saoudi Y., Lebeau L., Crevel I., Cross R., Wade R.H., Hackney D., Kozielski F. S-trityl-L-cysteine is a reversible, tight binding inhibitor of the human kinesin Eg5 that specifically blocks mitotic progression. J. Biol. Chem. 2006, 281:17559-17569.
46. Takahashi T., Nowakowski R.S., Caviness V.S. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 1995, 15:6046-6057.
47. Tretyakova I., Zolotukhin A.S., Tan W., Bear J., Propst F., Ruthel G., Felber B.K. Nuclear export factor family protein participates in cytoplasmic mRNA trafficking. J. Biol. Chem. 2005, 280:31981-31990.
48. Tsai J.-W., Bremner K.H., Vallee R.B. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat. Neurosci. 2007, 10:970-979.
49. Tyler W.A., Medalla M., Guillamon-Vivancos T., Luebke J.I., Haydar T.F. Neural precursor lineages specify distinct neocortical pyramidal neuron types. J. Neurosci. 2015, 35:6142-6152.
50. Uetake Y., Sluder G. Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Curr. Biol. 2010, 20:1666-1671.
51. Wang X., Qiu R., Tsark W., Lu Q. Rapid promoter analysis in developing mouse brain and genetic labeling of young neurons by doublecortin-DsRed-express. J. Neurosci. Res. 2007, 85:3567-3573.
52. Wang J., Sun Q., Morita Y., Jiang H., Gross A., Lechel A., Hildner K., Guachalla L.M., Gompf A., Hartmann D., et al. A differentiation checkpoint limits hematopoietic stem cell self-renewal in response to DNA damage. Cell 2012, 148:1001-1014.
53. Xie Y., Jüschke C., Esk C., Hirotsune S., Knoblich J.A. The phosphatase PP4c controls spindle orientation to maintain proliferative symmetric divisions in the developing neocortex. Neuron 2013, 79:254-265.
54. Yingling J., Youn Y.H., Darling D., Toyo-Oka K., Pramparo T., Hirotsune S., Wynshaw-Boris A. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 2008, 132:474-486.