The cyclin-dependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors

Cerebral Cortex

Volumn 21, Issue 8, 2011, Pages 1840-1856

  Tury, Anna ^a   Mairet Coello, Georges ^a   Dicicco Bloom, Emanuel ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

gliogenesis; in utero electroporation; neurite outgrowth; neurogenesis; transfection

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1C;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL CYCLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; FEMALE; GENE OVEREXPRESSION; GLIA CELL; IN VIVO STUDY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CELL DIFFERENTIATION; CELL MIGRATION INHIBITION; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASE INHIBITOR P57; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, KNOCKOUT; NEURAL STEM CELLS; NEUROGENESIS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79959189245     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq254     Document Type: Article

References (53)

1. Angevine JB Jr, Sidman RL. 1961. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature. 192:766-768.
2. Besson A, Dowdy SF, Roberts JM. 2008. CDK inhibitors: cell cycle regulators and beyond. Dev Cell. 14:159-169. (Pubitemid 351189186)
3. Besson A, Gurian-West M, Schmidt A, Hall A, Roberts JM. 2004. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18:862-876. (Pubitemid 38529656)
4. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science. 278:477-483. (Pubitemid 27454434)
5. Carey RG, Li B, DiCicco-Bloom E. 2002. Pituitary adenylate cyclase activating polypeptide anti-mitogenic signaling in cerebral cortical progenitors is regulated by p57Kip2-dependent CDK2 activity. J Neurosci. 22:1583-1591. (Pubitemid 35386277)
6. Casaccia-Bonnefil P, Tikoo R, Kiyokawa H, Friedrich V Jr, Chao MV, Koff A. 1997. Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev. 11:2335-2346. (Pubitemid 27408531)
7. Cunningham JJ, Roussel MF. 2001. Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ. 12:387-396. (Pubitemid 32762688)
8. Da Silva JS, Dotti CG. 2002. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci. 3:694-704. (Pubitemid 135706675)
9. Dugas JC, Ibrahim A, Barres BA. 2007. A crucial role for p57(Kip2) in the intracellular timer that controls oligodendrocyte differentiation. J Neurosci. 27:6185-6196. (Pubitemid 46890015)
10. Durand B, Gao FB, Raff M. 1997. Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J. 16:306-317. (Pubitemid 27049388)
11. Dyer MA, Cepko CL. 2000. p57(Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development. 127:3593-3605.
12. Dyer MA, Cepko CL. 2001. The p57Kip2 cyclin kinase inhibitor is expressed by a restricted set of amacrine cells in the rodent retina. J Comp Neurol. 429:601-614. (Pubitemid 32011856)
13. Faigle R, Liu L, Cundiff P, Funa K, Xia Z. 2008. Opposing effects of retinoid signaling on astrogliogenesis in embryonic day 13 and 17 cortical progenitor cells. J Neurochem. 106:1681-1698.
14. Fero ML, Rivkin M, Tasch M, Porter P, Carow CE, Firpo E, Polyak K, Tsai LH, Broudy V, Perlmutter RM, et al. 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell. 85:733-744.
15. Font de Mora J, Uren A, Heidaran M, Santos E. 1997. Biological activity of p27kip1 and its amino-and carboxy-terminal domains in G2/M transition of Xenopus oocytes. Oncogene. 15:2541-2551. (Pubitemid 27507246)
16. Frederick TJ, Wood TL. 2004. IGF-I and FGF-2 coordinately enhance cyclin D1 and cyclin E-cdk2 association and activity to promote G1 progression in oligodendrocyte progenitor cells. Mol Cell Neurosci. 25:480-492. (Pubitemid 38366413)
17. Ge W, He F, Kim KJ, Blanchi B, Coskun V, Nguyen L, Wu X, Zhao J, Heng JI, Martinowich K, et al. 2006. Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc Natl Acad Sci USA. 103:1319-1324. (Pubitemid 43191163)
18. Hand R, Bortone D, Mattar P, Nguyen L, Heng JI, Guerrier S, Boutt E, Peters E, Barnes AP, Parras C, et al. 2005. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron. 48:45-62. (Pubitemid 41384165)
19. Heinen A, Kremer D, Hartung HP, Kury P. 2008. p57 kip2's role beyond Schwann cell cycle control. Cell Cycle. 7:2781-2786.
20. Itoh Y, Masuyama N, Nakayama K, Nakayama KI, Gotoh Y. 2007. The cyclin-dependent kinase inhibitors p57 and p27 regulate neuronal migration in the developing mouse neocortex. J Biol Chem. 282:390-396. (Pubitemid 47076663)
21. Joseph B, Wallen-Mackenzie A, Benoit G, Murata T, Joodmardi E, Okret S, Perlmann T. 2003. p57(Kip2) cooperates with Nurr1 in developing dopamine cells. Proc Natl Acad Sci USA. 100:15619-15624. (Pubitemid 38021039)
22. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M. 2006. Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol. 8:17-26. (Pubitemid 43064793)
23. Koguchi K, Nakatsuji Y, Nakayama K, Sakoda S. 2002. Modulation of astrocyte proliferation by cyclin-dependent kinase inhibitor p27(Kip1). Glia. 37:93-104. (Pubitemid 34161540)
24. Li B, DiCicco-Bloom E. 2004. Basic fibroblast growth factor exhibits dual and rapid regulation of cyclin D1 and p27 to stimulate proliferation of rat cerebral cortical precursors. Dev Neurosci. 26:197-207. (Pubitemid 40867975)
25. Lu N, DiCicco-Bloom E. 1997. Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc Natl Acad Sci USA. 94:3357-3362. (Pubitemid 27157316)
26. Mairet-Coello G, Tury A, DiCicco-Bloom E. 2009. Insulin-like growth factor-1 promotes G(1)/S cell cycle progression through bidirectional regulation of cyclins and cyclin-dependent kinase inhibitors via the phosphatidylinositol 3-kinase/Akt pathway in developing rat cerebral cortex. J Neurosci. 29:775-788.
27. Mayer BJ. 2001. SH3 domains: complexity in moderation. J Cell Sci. 114:1253-1263. (Pubitemid 32409462)
28. McConnell SK, Kaznowski CE. 1991. Cell cycle dependence of laminar determination in developing neocortex. Science. 254:282-285. (Pubitemid 21917342)
29. Megason SG, McMahon AP. 2002. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development. 129:2087-2098. (Pubitemid 34874223)
30. Miller FD, Gauthier AS. 2007. Timing is everything: making neurons versus glia in the developing cortex. Neuron. 54:357-369. (Pubitemid 46659814)
31. Mochizuki T, Bilitou A, Waters CT, Hussain K, Zollo M, Ohnuma S. 2009. Xenopus NM23-X4 regulates retinal gliogenesis through interaction with p27Xic1. Neural Dev. 4:1.
32. Nakayama K. 1998. Cip/Kip cyclin-dependent kinase inhibitors: brakes of the cell cycle engine during development. Bioessays. 20:1020-1029. (Pubitemid 29032180)
33. Nakayama K, Ishida N, Shirane M, Inomata A, Inoue T, Shishido N, Horii I, Loh DY. 1996. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell. 85:707-720.
34. Nguyen L, Besson A, Heng JI, Schuurmans C, Teboul L, Parras C, Philpott A, Roberts JM, Guillemot F. 2006. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20:1511-1524. (Pubitemid 43830657)
35. Ohnuma S, Philpott A, Harris WA. 2001. Cell cycle and cell fate in the nervous system. Curr Opin Neurobiol. 11:66-73. (Pubitemid 32155951)
36. Ohnuma S, Philpott A, Wang K, Holt CE, Harris WA. 1999. p27Xic1, a Cdk inhibitor, promotes the determination of glial cells in Xenopus retina. Cell. 99:499-510. (Pubitemid 129746828)
37. Perez-Martinez L, Jaworski DM. 2005. Tissue inhibitor of metal-loproteinase-2 promotes neuronal differentiation by acting as an anti-mitogenic signal. J Neurosci. 25:4917-4929. (Pubitemid 40712835)
38. Potikha T, Kassem S, Haber EP, Ariel I, Glaser B. 2005. p57Kip2 (cdkn1c): sequence, splice variants and unique temporal and spatial expression pattern in the rat pancreas. Lab Invest. 85:364-375. (Pubitemid 40333153)
39. Rakic P. 1974. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science. 183:425-427.
40. Sanada K, Tsai LH. 2005. G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors. Cell. 122:119-131. (Pubitemid 40977945)
41. Sherr CJ, Roberts JM. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501-1512. (Pubitemid 29297917)
42. Song JH, Wang CX, Song DK, Wang P, Shuaib A, Hao C. 2005. Interferon gamma induces neurite outgrowth by up-regulation of p35 neuron-specific cyclin-dependent kinase 5 activator via activation of ERK1/2 pathway. J Biol Chem. 280:12896-12901.
43. Song MR, Ghosh A. 2004. FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci. 7:229-235. (Pubitemid 38280446)
44. Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME. 2001. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell. 104:365-376. (Pubitemid 32206457)
45. Tanaka H, Yamashita T, Asada M, Mizutani S, Yoshikawa H, Tohyama M. 2002. Cytoplasmic p21(Cip1/WAF1) regulates neurite remodeling by inhibiting Rho-kinase activity. J Cell Biol. 158:321-329.
46. Tikoo R, Casaccia-Bonnefil P, Chao MV, Koff A. 1997. Changes in cyclin-dependent kinase 2 and p27kip1 accompany glial cell differentiation of central glia-4 cells. J Biol Chem. 272:442-447. (Pubitemid 27021178)
47. Tojima T, Ito E. 2004. Signal transduction cascades underlying de novo protein synthesis required for neuronal morphogenesis in differentiating neurons. Prog Neurobiol. 72:183-193. (Pubitemid 38591295)
48. van Lookeren Campagne M, Gill R. 1998. Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax. J Comp Neurol. 397:181-198. (Pubitemid 28303354)
49. Watanabe H, Pan ZQ, Schreiber-Agus N, DePinho RA, Hurwitz J, Xiong Y. 1998. Suppression of cell transformation by the cyclin-dependent kinase inhibitor p57KIP2 requires binding to proliferating cell nuclear antigen. Proc Natl Acad Sci USA. 95:1392-1397.
50. Ye W, Mairet-Coello G, DiCicco-Bloom E. 2007. DNAse I pre-treatment markedly enhances detection of nuclear cyclin-dependent kinase inhibitor p57Kip2 and BrdU double immunostaining in embryonic rat brain. Histochem Cell Biol. 127:195-203. (Pubitemid 46147273)
51. Yokoo T, Toyoshima H, Miura M, Wang Y, Iida KT, Suzuki H, Sone H, Shimano H, Gotoda T, Nishimori S, et al. 2003. p57Kip2 regulates actin dynamics by binding and translocating LIM-kinase 1 to the nucleus. J Biol Chem. 278:52919-52923. (Pubitemid 38035893)
52. Zezula J, Casaccia-Bonnefil P, Ezhevsky SA, Osterhout DJ, Levine JM, Dowdy SF, Chao MV, Koff A. 2001. p21cip1 is required for the differentiation of oligodendrocytes independently of cell cycle withdrawal. EMBO Rep. 2:27-34. (Pubitemid 32229718)
53. Zhang P, Liegeois NJ, Wong C, Finegold M, Hou H, Thompson JC, Silverman A, Harper JW, DePinho RA, Elledge SJ. 1997. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature. 387: 151-158. (Pubitemid 27209424)