IGF-I and FGF-2 coordinately enhance cyclin D1 and cyclin E-cdk2 association and activity to promote G1 progression in oligodendrocyte progenitor cells

Molecular and Cellular Neuroscience

Volumn 25, Issue 3, 2004, Pages 480-492

  Frederick, Terra J ^a   Wood, Teresa L ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 2; CYCLIN E; FIBROBLAST GROWTH FACTOR 2; PROTEIN P27; RETINOBLASTOMA PROTEIN; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; ENZYME ACTIVATION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; CDC2-CDC28 KINASES; CELLS, CULTURED; CYCLIN D1; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; FIBROBLAST GROWTH FACTOR 2; G1 PHASE; INSULIN-LIKE GROWTH FACTOR I; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS;

ANIMALIA;

EID: 1642388592     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.11.015     Document Type: Article

References (61)

1. Bagui T.K., Mohapatra S., Haura E., Pledger W.J. P27Kip1 and p21Cip1 are not required for the formation of active D cyclin-cdk4 complexes. Mol. Cell. Biol. 23:2003;7285-7290.
2. Bansal R. Fibroblast growth factors and their receptors in oligodendrocyte development: implications for demyelination and remyelination. Dev. Neurosci. 24:2002;35-46.
3. Beck K., Powell-Braxton L., Widmer H., Valverde J., Hefti F. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron. 14:1995;717-730.
4. Belachew S., Aguirre A.A., Wang H., Vautier F., Yuan X., Anderson S., Kirby M., Gallo V. Cyclin-dependent kinase-2 controls oligodendrocyte progenitor cell cycle progression and is downregulated in adult oligodendrocyte progenitors. J. Neurosci. 22:2002;8553-8562.
5. Bögler O., Wren D., Barnett S., Land H., Noble M. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 87:1990;6368-6372.
6. Botz J., Zerfass-Thome K., Spitkovsky D., Delius H., Vogt B., Eilers M., Hatzigeorgiou A., Jansen-Durr P. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol. 16:1996;3401-3409.
7. Calver A.R., Hall A.C., Yu W.-P., Walsh F.S., Heath J.K., Betsholtz C., Richardson W.D. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron. 20:1998;869-882.
8. Carson M., Behringer R., Brinster R., McMorris F. Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron. 10:1993;729-740.
9. Casaccia-Bonnefil P., Tikoo R., Kiyokawa H., Friedrich V. Jr., Chao M.V., Koff A. Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev. 11:1997;2335-2346.
10. Casaccia-Bonnefil P., Hardy R.J., Teng K.K., Levine J.M., Koff A., Chao M.V. Loss of p27Kip1 function results in increased proliferative capacity of oligodendrocyte progenitors but unaltered timing of differentiation. Dev., Suppl. 126:1999;4027-4037.
11. Cheng M., Olivier P., Diehl J.A., Fero M., Roussel M.F., Roberts J.M., Sherr C.J. The p21(Cip1) and p27(Kip1) CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18:1999;1571-1583.
12. Coqueret O. New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol. 13:2003;65-70.
13. Delmas C., Manenti S., Boudjelal A., Peyssonnaux C., Eychene A., Darbon J.M. The p42/p44 mitogen-activated protein kinase activation triggers p27Kip1 degradation independently of CDK2/cyclin E in NIH 3T3 cells. J. Biol. Chem. 276:2001;34958-34965.
14. Durand B., Raff M. A cell-intrinsic timer that operates during oligodendrocyte development. BioEssays. 22:2000;64-71.
15. Durand B., Gao F.B., Raff M. Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J. 16:1997;306-317.
16. Fruttiger M., Karlsson L., Hall A.C., Abramsson A., Calver A.R., Bostrom H., Willetts K., Bertold C., Heath J.K., Betsholtz C., Richardson W.D. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development. 126:1999;457-467.
17. Gard A., Pfeiffer S. Glial cell mitogens bFGF and PDGF differentially regulate development of O4+GalC- oligodendrocyte progenitors. Dev. Biol. 159:1993;618-630.
18. Ghiani C., Gallo V. Inhibition of cyclin E-cyclin-dependent kinase 2 complex formation and activity is associated with cell cycle arrest and withdrawal in oligodendrocyte progenitor cells. J. Neurosci. 21:2001;1274-1282.
19. Ghiani C.A., Eisen A.M., Yuan X., DePinho R.A., McBain C.J., Gallo V. Neurotransmitter receptor activation triggers p27(Kip1) and p21(CIP1) accumulation and G1 cell cycle arrest in oligodendrocyte progenitors. Dev., Suppl. 126:1999;1077-1090.
20. Goddard D.R., Berry M., Butt A.M. In vivo actions of fibroblast growth factor-2 and insulin-like growth factor-I on oligodendrocyte development and myelination in the central nervous system. J. Neurosci. Res. 57:1999;74-85.
21. Goddard D.R., Berry M., Kirvell S.L., Butt A.M. Fibroblast growth factor-2 inhibits myelin production by oligodendrocytes in vivo. Mol. Cell. Neurosci. 18:2001;557-569.
22. Hallek M., Ando K., Eder M., Slattery K., Ajchenbaum-Cymbalista F., Griffin J.D. Signal transduction of steel factor and granulocyte-macrophage colony-stimulating factor: differential regulation of transcription factor and G1 cyclin gene expression, and of proliferation in the human factor-dependent cell line MO7. Leukemia. 8:1994;740-748.
23. Harbour J.W., Luo R.X., Dei Santi A., Postigo A.A., Dean D.C. Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell. 98:1999;859-869.
24. Hirai A., Nakamura S., Noguchi Y., Yasuda T., Kitagawa M., Tatsuno I., Oeda T., Tahara K., Terano T., Narumiya S., Kohn L.D., Saito Y. Geranylgeranylated rho small GTPase(s) are essential for the degradation of p27Kip1 and facilitate the progression from G1 to S phase in growth-stimulated rat FRTL-5 cells. J. Biol. Chem. 272:1997;13-16.
25. Huang Z., Tang X.M., Cambi F. Down-regulation of the retinoblastoma protein (rb) is associated with rat oligodendrocyte differentiation. Mol. Cell. Neurosci. 19:2002;250-262.
26. Ivanova A., Nakahira E., Kagawa T., Oba A., Wada T., Takebayashi H., Spassky N., Levine J., Zalc B., Ikenaka K. Evidence for a second wave of oligodendrogenesis in the postnatal cerebral cortex of the mouse. J. Neurosci. Res. 73:2003;581-592.
27. Jiang W., Kahn S.M., Zhou P., Zhang Y.J., Cacace A.M., Infante A.S., Doi S., Santella R.M., Weinstein I.B. Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene. 8:1993;3447-3457.
28. Jiang F., Frederick T.J., Wood T.L. IGF-I synergizes with FGF-2 to stimulate oligodendrocyte progenitor entry into the cell cycle. Dev. Biol. 232:2001;414-423.
29. LaBaer J., Garrett M.D., Stevenson L.F., Slingerland J.M., Sandhu C., Chou H.S., Fattaey A., Harlow E. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:1997;847-862.
30. Lee H.T., Kay E.P. Regulatory role of PI 3-kinase on expression of Cdk4 and p27, nuclear localization of Cdk4, and phosphorylation of p27 in corneal endothelial cells. Invest. Ophthalmol. Visual Sci. 44:2003;1521-1528.
31. Levison S., McCarthy K. Astroglia in culture. Banker G., Goslin K. Culturing Nerve Cells. 1991;309-336 MIT Press, Cambridge.
32. Liang J., Zubovitz J., Petrocelli T., Kotchetkov R., Connor M.K., Han K., Lee J.H., Ciarallo S., Catzavelos C., Beniston R., Franssen E., Slingerland J.M. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat. Med. 8:2002;1153-1160.
33. Mantel C., Luo Z., Canfield J., Braun S., Deng C., Broxmeyer H.E. Involvement of p21cip-1 and p27kip-1 in the molecular mechanisms of steel factor-induced proliferative synergy in vitro and of p21cip-1 in the maintenance of stem/progenitor cells in vivo. Blood. 88:1996;3710-3719.
34. McCarthy K., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85:1980;890-902.
35. McKinnon R., Matsui T., Dubois-Dalcq M., Aaronson S. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron. 5:1990;603-614.
36. McKinnon R., Smith C., Behar T., Smith T., Dubois-Dalcq M. Distinct effects of bFGF and PDGF on oligodendrocyte progenitor cells. Glia. 7:1993;245-254.
37. McMorris F., McKinnon R. Regulation of oligodendrocyte development and CNS myelination by growth factors: prospects for therapy of demyelinating disease. Brain Pathol. 6:1996;313-329.
38. Mittnacht S. Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8:1998;21-27.
39. Morgan D.O. Principles of CDK regulation. Nature. 374:1995;131-134.
40. Nakayama K.I., Hatakeyama S., Nakayama K. Regulation of the cell cycle at the G1-S transition by proteolysis of cyclin E and p27Kip1. Biochem. Biophys. Res. Commun. 282:2001;853-860.
41. Ohtani K., DeGregori J., Nevins J.R. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. U. S. A. 92:1995;12146-12150.
42. Olashaw N., Pledger W.J. Paradigms of growth control: relation to Cdk activation. Sci. STKE 2002. 134:2002;RE7. Review. PMID 12034920.
43. Pardee A.B. G1 events and regulation of cell proliferation. Science. 246:1989;603-608.
44. Rechler M.M., Nissley S.P. The nature and regulation of the receptors for insulin-like growth factors. Annu. Rev. Physiol. 47:1985;425-442.
45. Rivard N., Boucher M.J., Asselin C., L'Allemain G. MAP kinase cascade is required for p27 downregulation and S phase entry in fibroblasts and epithelial cells. Am. J. Physiol. 277:1999;C652-C664.
46. Sheaff R.J., Groudine M., Gordon M., Roberts J.M., Clurman B.E. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 11:1997;1464-1478.
47. Sherr C.J. Mammalian G1 cyclins. Cell. 73:1993;1059-1065.
48. Sherr C.J., Roberts J.M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1995;1149-1163.
49. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1999;1501-1512.
50. Spassky N., Heydon K., Mangatal A., Jankovski A., Olivier C., Queraud-Lesaux F., Goujet-Zalc C., Thomas J.L., Zalc B. Sonic hedgehog-dependent emergence of oligodendrocytes in the telencephalon: evidence for a source of oligodendrocytes in the olfactory bulb that is independent of PDGFRalpha signaling. Development. 128:2001;4993-5004.
51. Tang X.-M., Strocchi P., Cambi F. Changes in the activity of cdk2 and cdk5 accompany differentiation of rat primary oligodendrocytes. J. Cell. Biochem. 68:1998;128-137.
52. Tang X.M., Beesley J.S., Grinspan J.B., Seth P., Kamholz J., Cambi F. Cell cycle arrest induced by ectopic expression of p27 is not sufficient to promote oligodendrocyte differentiation. J. Cell. Biochem. 76:1999;270-279.
53. Tang D.G., Tokumoto Y.M., Apperly J.A., Lloyd A.C., Raff M.C. Lack of replicative senescence in cultured rat oligodendrocyte precursor cells. Science. 291:2001;868-871.
54. Tikoo R., Osterhout D.J., Casaccia-Bonnefil P., Seth P., Koff A., Chao M.V. Ectopic expression of p27Kip1 in oligodendrocyte progenitor cells results in cell-cycle growth arrest. J. Neurobiol. 36:1998;431-440.
55. Vidal A., Koff A. Cell-cycle inhibitors: three families united by a common cause. Gene. 247:2000;1-15.
56. Winston J., Dong F., Pledger W.J. Differential modulation of G1 cyclins and the Cdk inhibitor p27kip1 by platelet-derived growth factor and plasma factors in density-arrested fibroblasts. J. Biol. Chem. 271:1996;11253-11260.
57. Ye P., Carson J., D'Ercole A.J. In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein (IGFBP-1) transgenic mice. J. Neurosci. 15:1995;7344-7356.
58. Ye P., Li L., Richards G., DiAugustine R.P., D'Ercole A.J. Myelination is altered in insulin-like growth factor-I null mutant mice. J. Neurosci. 22:2002;6041-6051.
59. Young G., Levison S. An improved method for propagating oligodendrocyte progenitors in vitro. J. Neurosci. Methods. 77:1997;163-168.
60. Zezula J., Casaccia-Bonnefil P., Ezhevsky S.A., Osterhout D.J., Levine J.M., Dowdy S.F., Chao M.V., Koff A. p21cip1 is required for the differentiation of oligodendrocytes independently of cell cycle withdrawal. EMBO Rep. 2:2001;27-34.
61. Zhang H.S., Gavin M., Dahiya A., Postigo A.A., Ma D., Luo R.X., Harbour J.W., Dean D.C. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell. 101:2000;79-89.