A cell-autonomous requirement for Cip/Kip cyclin-kinase inhibitors in regulating neuronal cell cycle exit but not differentiation in the developing spinal cord

Developmental Biology

Volumn 301, Issue 1, 2007, Pages 14-26

  Gui, Hongxing ^a   Li, Shike ^a   Matise, Michael P ^a  

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

Author keywords

Cyclin; Differentiation; Neural tube; Neurogenesis; p21Cip1; p27Kip1; p57Kip2; Progenitor; Proliferation; Stem cells

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 1C; MUTANT PROTEIN; PROTEIN P21;

ANIMAL TISSUE; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL POPULATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MITOSIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL CORD; STEM CELL;

VERTEBRATA;

EID: 33845653116     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.10.035     Document Type: Article

References (40)

1. Altman J., and Bayer S.A. The development of the rat spinal cord. Advances in Anatomy, Embryology and Cell Biology vol. 85 (1984), Springer-Verlag, Berlin
2. Assoian R., and Schwartz M. Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11 (2001) 48-53
3. Bartkova J., Lukas J., and Bartek J. Aberrations of the G1- and G1/S-regulating genes in human cancer. Prog. Cell Cycle Res. 3 (1997) 211-220
4. Brinkmeier M.L., Gordon D.F., Dowding J.M., Saunders T.L., Kendall S.K., Sarapura V.D., Wood W.M., Ridgway E.C., and Camper S.A. Cell-specific expression of the mouse glycoprotein hormone alpha-subunit gene requires multiple interacting DNA elements in transgenic mice and cultured cells. Mol. Endocrinol. 12 (1998) 622-633
5. Cunningham J.J., Levine E.M., Zindy F., Goloubeva O., Roussel M.F., and Smeyne R.J. The cyclin-dependent kinase inhibitors p19(Ink4d) and p27(Kip1) are coexpressed in select retinal cells and act cooperatively to control cell cycle exit. Mol. Cell. Neurosci. 19 (2002) 359-374
6. de Nooij J.C., Letendre M.A., and Hariharan I.K. A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87 (1996) 1237-1247
7. Doetsch F., Verdugo J.M., Caille I., Alvarez-Buylla A., Chao M.V., and Casaccia-Bonnefil P. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J. Neurosci. 22 (2002) 2255-2264
8. Dyer M.A., and Cepko C.L. p57(Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development 127 (2000) 3593-3605
9. Dyer M.A., and Cepko C.L. p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J. Neurosci. 21 (2001) 4259-4271
10. Fero M.L., Rivkin M., Tasch M., Porter P., Carow C.E., Firpo E., Polyak K., Tsai L.H., Broudy V., Perlmutter R.M., Kaushansky K., and Roberts J.M. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85 (1996) 733-744
11. Hamburger V., and Hamilton H.C. A series of normal stages in the development of the chick embryo. J. Morphol. 88 (1951) 49-92
12. Hamel P., Gallie B., and Phillips R. The retinoblastoma protein and cell cycle regulation. Trends Genet. 8 (1992) 180
13. Hashimoto Y., Kohri K., Kaneko Y., Morisaki H., Kato T., Ikeda K., and Nakanishi M. Critical role for the 310 helix region of p57(Kip2) in cyclin-dependent kinase 2 inhibition and growth suppression. J. Biol. Chem. 273 (1998) 16544-16550
14. Hong Y., Roy R., and Ambros V. Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125 (1998) 3585-3597
15. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev., Genet. 1 (2000) 20-29
16. John R.M., Ainscough J.F., Barton S.C., and Surani M.A. Distant cis-elements regulate imprinted expression of the mouse p57(Kip2) (Cdkn1c) gene: implications for the human disorder, Beckwith-Wiedemann syndrome. Hum. Mol. Genet. 10 (2001) 1601-1609
17. Kiyokawa H., Kineman R.D., Manova-Todorova K.O., Soares V.C., Hoffman E.S., Ono M., Khanam D., Hayday A.C., Frohman L.A., and Koff A. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85 (1996) 721-732
18. Lane M.E., Sauer K., Wallace K., Jan Y.N., Lehner C.F., and Vaessin H. Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87 (1996) 1225-1235
19. Lei Q., Zelman A.K., Kuang E., Li S., and Matise M.P. Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord. Development 131 (2004) 3593-3604
20. Li G., Domenico J., Lucas J.J., and Gelfand E.W. Identification of multiple cell cycle regulatory functions of p57Kip2 in human T lymphocytes. J. Immunol. 173 (2004) 2383-2391
21. Lo L., Dormand E., Greenwood A., and Anderson D.J. Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 129 (2002) 1553-1567
22. Macleod K. pRb and E2f-1 in mouse development and tumorigenesis. Curr. Opin. Genet. Dev. 9 (1999) 31-39
23. Matise M.P., and Joyner A.L. Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J. Neurosci. 17 (1997) 7805-7816
24. Matise M.P., Epstein D.J., Park H.L., Platt K.A., and Joyner A.L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125 (1998) 2759-2770
25. Megason S.G., and McMahon A.P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129 (2002) 2087-2098
26. Nagahama H., Hatakeyama S., Nakayama K., Nagata M., and Tomita K. Spatial and temporal expression patterns of the cyclin-dependent kinase (CDK) inhibitors p27Kip1 and p57Kip2 during mouse development. Anat. Embryol. (Berl) 203 (2001) 77-87
27. Nakayama K., Ishida N., Shirane M., Inomata A., Inoue T., Shishido N., Horii I., and Loh D.Y. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85 (1996) 707-720
28. Novitch B.G., Chen A.I., and Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31 (2001) 773-789
29. Sapir T., Geiman E.J., Wang Z., Velasquez T., Mitsui S., Yoshihara Y., Frank E., Alvarez F.J., and Goulding M. Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J. Neurosci. 24 (2004) 1255-1264
30. Sherr C.J. D-type cyclins. Trends Biochem. Sci. 20 (1995) 187-190
31. Sherr C.J., and Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13 (1999) 1501-1512
32. Tarui T., Takahashi T., Nowakowski R.S., Hayes N.L., Bhide P.G., and Caviness V.S. Overexpression of p27 Kip 1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb. Cortex 15 (2005) 1343-1355
33. Westbury J., Watkins M., Ferguson-Smith A.C., and Smith J. Dynamic temporal and spatial regulation of the cdk inhibitor p57(kip2) during embryo morphogenesis. Mech. Dev. 109 (2001) 83-89
34. Yan Y., Frisen J., Lee M.H., Massague J., and Barbacid M. Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev. 11 (1997) 973-983
35. Zhang P. The cell cycle and development: redundant roles of cell cycle regulators. Curr. Opin. Cell Biol. 11 (1999) 655-662
36. Zhang P., Liegeois N.J., Wong C., Finegold M., Hou H., Thompson J.C., Silverman A., Harper J.W., DePinho R.A., and Elledge S.J. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387 (1997) 151-158
37. Zhang P., Wong C., DePinho R.A., Harper J.W., and Elledge S.J. Cooperation between the Cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development. Genes Dev. 12 (1998) 3162-3167
38. Zindy F., Quelle D.E., Roussel M.F., and Sherr C.J. Expression of the p16INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene 15 (1997) 203-211
39. Zindy F., Soares H., Herzog K.H., Morgan J., Sherr C.J., and Roussel M.F. Expression of INK4 inhibitors of cyclin D-dependent kinases during mouse brain development. Cell Growth Differ. 8 (1997) 1139-1150
40. Zindy F., Cunningham J.J., Sherr C.J., Jogal S., Smeyne R.J., and Roussel M.F. Postnatal neuronal proliferation in mice lacking Ink4d and Kip1 inhibitors of cyclin-dependent kinases. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13462-13467