Basic fibroblast growth factor exhibits dual and rapid regulation of cyclin D1 and p27KIP1 to stimulate proliferation of rat cerebral cortical precursors

Developmental Neuroscience

Volumn 26, Issue 2-4, 2004, Pages 197-207

  Li, Baogang ^a   DiCicco Bloom, Emanuel ^a  

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

Author keywords

Basic fibroblast growth factor; Cortical precursors; Cyclin dependent kinase 2; Cyclin dependent kinase inhibitors; Cyclins; Neurogenesis; p27KIP1; p57KIP2

Indexed keywords

ANTIMITOTIC AGENT; BASIC FIBROBLAST GROWTH FACTOR; BROXURIDINE; CYCLIN D1; CYCLIN D3; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; DNA; MITOGENIC AGENT; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; CDK2 PROTEIN, RAT; CDKN1B PROTEIN, RAT; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE; FIBROBLAST GROWTH FACTOR 2; MESSENGER RNA; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RAT; REACTION TIME; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DOWN REGULATION; DRUG EFFECT; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT; SPRAGUE DAWLEY RAT; STEM CELL;

ANIMALS; BROMODEOXYURIDINE; CDC2-CDC28 KINASES; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN D1; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DNA; DOWN-REGULATION; FIBROBLAST GROWTH FACTOR 2; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STEM CELLS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 17444409620     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000082137     Document Type: Article

References (67)

1. KIP1. Mol Cell Biol 17:3850-3857.
2. Altman J, Bayer SA (1995): Atlas of Prenatal Rat Brain Development. Boca Raton, CRC Press.
3. Belachew S, Aguirre AA, Wang H, Vautier F, Yuan X, Anderson S, Kirby M, Gallo V (2002): Cyclin-dependent kinase-2 controls oligodendrocyte progenitor cell cycle progression and is downregulated in adult oligodendrocyte progenitors. J Neurosci 22:8553-8562.
4. Cameron HA, Hazel TG, McKay RD (1998): Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36:287-306.
5. Kip2 dependent CDK2 activity. J Neurosci 22:1583-1591.
6. Cavanagh JF, Mione MC, Pappas IS, Parnavelas JG (1997): Basic fibroblast growth factor prolongs the proliferation of rat cortical progenitor cells in vitro without altering their cell cycle parameters. Cereb Cortex 7:293-302.
7. Caviness VS, Goto T, Tarui T, Takahashi T, Bhide PG, Nowakowski RS (2003): Cell output, cell cycle duration and neuronal specification: A model of integrated mechanisms of the neocortical proliferative process. Cereb Cortex 13: 592-598.
8. Caviness VS, Takahashi T, Nowakowski RS (1995): Numbers, time and neocortical neurogenesis: A general developmental and evolutionary model. Trends Neurosci 18:379-383.
9. Cheng Y, Black IB, DiCicco-Bloom E (2002): Hippocampal granule neuron production and population size are regulated by levels of bFGF. Eur J Neurosci 15:3-12.
10. Cheng Y, Tao Y, Black IB, DiCicco-Bloom E (2001): A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. J Neurobiol 46:220-229.
11. Ciemerych MA, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, Gardner H, Sicinski P (2002): Development of mice expressing a single D-type cyclin. Genes Dev 16:3277-3289.
12. Cunningham JJ, Roussel MF (2001): Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ 12:387-396.
13. 1/S regulatory genes. Mol Cell Biol 15:4215-4224.
14. 1 phase of the cell cycle in the murine neocortical PVE: A quantitative analysis of mRNA in situ hybridization. Cereb Cortex 9:824-832.
15. Kip1 nuclear export. J Biol Chem 278:12443-12451.
16. Dono R, Texido G, Dussel R, Ehmke H, Zeller R (1998): Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J 17:4213-4225.
17. Erlanson M, Portin C, Linderholm B, Lindh J, Roos G, Landberg G (1998): Expression of cyclin E and the cyclin-dependent kinase inhibitor p27 in malignant lymphomas - Prognostic implications. Blood 92:770-777.
18. Ernfors P, Lonnerberg P, Ayer-LeLievre C, Persson H (1990): Developmental and regional expression of basic fibroblast growth factor mRNA in the rat central nervous system. J Neurosci Res 27:10-15.
19. Ferguson KL, Callaghan SM, O'Hare MJ, Park DS, Slack RS (2000): The Rb-CDK4/6 signaling pathway is critical in neural precursor cell cycle regulation. J Biol Chem 275:33593-33600.
20. 1 progression in oligodendrocyte progenitor cells. Mol Cell Neurosci 25:480-492.
21. Gensburger C, Labourdette G, Sensenbrenner M (1987): Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett 217:1-5.
22. Goto T, Takahashi T, Miyama S, Nowakowski RS, Bhide PG, Caviness VS Jr (2002): Developmental regulation of the effects of fibroblast growth factor-2 and 1-octanol on neuronogenesis: Implications for a hypothesis relating to mitogen-antimitogen opposition. J Neurosci Res 69:714-22.
23. Kip2 expression in vivo and in vitro: Implications for Beckwith-Wiedemann syndrome. Proc Natl Acad Sci USA 97:5279-5284.
24. Grim JE, Clurman BE (2003): Cycling without CDK2? Trends Cell Biol 13:396-399.
25. Kip1 in gamma interferon-mediated growth arrest of mammary epithelial cells and related defects in mammary carcinoma cells. Oncogene 14:2111-2122.
26. Hengst L, Reed SI (1998): Inhibitors of the Cip/Kip family. Curr Top Microbiol Immunol 227:25-41.
27. van den Heuvel S, Harlow E (1993): Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262:2050-2054.
28. 1 to S phase in growth-stimulated rat FRTL-5 cells. J Biol Chem 272: 13-16.
29. Hu W, Bellone CJ, Baldassare JJ (1999): RhoA stimulates p27(Kip) degradation through its regulation of cyclin E/CDK2 activity. J Biol Chem 274:3396-3401.
30. Kalyani A, Hobson K, Rao MS (1997): Neuroepithelial stem cells from the embryonic spinal cord: Isolation, characterization, and clonal analysis. Dev Biol 186:202-223.
31. K1p1) of cyclin-dependent kinase 4 activation. Cell 79:487-496.
32. Kenney AM, Rowitch DH (2000): Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055-9067.
33. Korada S, Zheng W, Basilico C, Schwartz ML, Vaccarino FM (2002): Fgf2 is necessary for the growth of glutamate projection neurons in the anterior neocortex. J Neurosci 22:863-875.
34. Lukaszewicz A, Savatier P, Cortay V, Kennedy H, Dehay C (2002): Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J Neurosci 22:6610-6622.
35. McConnell SK (1988): Development and decision-making in the mammalian cerebral cortex. Brain Res 472:1-23.
36. 1 phase in a mouse model that targets inducible gene expression to central nervous system progenitor cells. Proc Natl Acad Sci USA 98:6435-6440.
37. Kip1. Biochem Biophys Res Commun 282:853-860.
38. Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 372:570-573.
39. 1-to-S phase transition. Mol Cell Biol 15:2612-2624.
40. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, Lin SM, Wickramasinghe R, Scott MP, Wechsler-Reya RJ (2003): Transcriptional profiling of the Sonic hedgehog response: A critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci USA 100:7331-7336.
41. Kip1 in anchorage-independent cells. Oncogene 16:2575-2583.
42. Powell PP, Finklestein SP, Dionne CA, Jaye M, Klagsbrun M (1991): Temporal, differential and regional expression of mRNA for basic fibroblast growth factor in the developing and adult rat brain. Brain Res Mol Brain Res 11: 71-77.
43. Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000): Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 20:5012-5023.
44. Ray J, Gage FH (1994): Spinal cord neuroblasts proliferate in response to basic fibroblast growth factor. J Neurosci 14:3548-3564.
45. Sambrook J, Fritsch EF, Maniatis T (1989): Molecular Cloning, ed 2. Cold Spring Harbor, Cold Spring Harbor Laboratory Press, pp 7.39-7.52.
46. Kip1. Genes Dev 11:1464-1478.
47. 1 cyclins. Cell 73: 1059-1065.
48. 1 phase progression: Cycling on cue. Cell 79:551-555.
49. 1-phase progression. Genes Dev 13:1501-1512.
50. Shin DM, Korada S, Raballo R, Shashikant CS, Simeone A, Taylor JR, Vaccarino F (2004): Loss of glutamatergic pyramidal neurons in frontal and temporal cortex resulting from attenuation of FGFR1 signaling is associated with spontaneous hyperactivity in mice. J Neurosci 24:2247-2258.
51. Suh J, Lu N, Nicot A, Tatsuno I, DiCicco-Bloom E (2001a): PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat Neurosci 4:123-124.
52. KIP2 inhibition of CDK2 in developing cortex. Society for Neuroscience Annual Meeting, San Diego, vol 27, abstract 896.16.
53. Singer JD, Gurian-West M, Clurman B, Roberts JM (1999): Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev 13:2375-2387.
54. Takahashi T, Nowakowski RS, Caviness VS (1995): The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:820-833.
55. Takahashi T, Nowakowski RS, Caviness VS Jr (1996): The leaving or Q fraction of the murine cerebral proliferative epithelium: A general model of neocortical neuronogenesis. J Neurosci 16:6183-6196.
56. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS (1999): Sequence of neuron origin and neocortical laminar fate: Relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19:10357-10371.
57. Takuwa N, Takuwa Y (2001): Regulation of cell cycle molecules by the Ras effector system. Mol Cell Endocrinol 177:25-33.
58. 3 expression in the control of astrocyte proliferation induced by endothelin-1. J Neurochem 74:1034-1040.
59. Temple S, Qian X (1995): bFGF, neurotrophins, and the control of cortical neurogenesis. Neuron 15:249-252.
60. Kip1 accompany glial cell differentation of central glial-4 cells. J Biol Chem 272:442-447.
61. Tikoo R, Zanazzi G, Shiffman D, Salzer J, Chao MV (2000): Cell cycle control of Schwann cell proliferation: Role of cyclin-dependent kinase-2. J Neurosci 20:4627-4634.
62. Vaccarino FM, Schwartz ML, Hartigan D, Leckman JF (1995): Effect of basic fibroblast growth factor on the genesis of excitatory and inhibitory neurons in primary cultures of cells from the mammalian telencephalon. Cereb Cortex 1:64-78.
63. Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT (1999): Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2:246-253.
64. Vescovi AL, Reynolds BA, Fraser DD, Weiss S (1993): bFGF regulates the proliferative fate of unipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11:951-966.
65. Vidal A, Koff A (2000): Cell-cycle inhibitors: Three families united by a common cause. Gene 247:1-15.
66. Weise B, Janet T, Grothe C(1993): Localization of bFGF and FGF-receptor in the developing nervous system of the embryonic and newborn rat. J Neurosci Res 34:442-453.
67. 1 arrest mediated by an anti-epidermal growth factor receptor monoclonal antibody. Oncogene 12:1397-1403.