Fibroblast growth factor 2 is required for maintaining the neural stem cell pool in the mouse brain subventricular zone

Developmental Neuroscience

Volumn 26, Issue 2-4, 2004, Pages 181-196

  Zheng, Wei ^a   Nowakowski, Richard S ^b   Vaccarino, Flora M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

Cell cycle, progenitor; Fibroblast growth factor; Mouse; Olfactory bulb; Stem cell; Subventricular zone

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; LIPID BINDING PROTEIN; BIOLOGICAL MARKER; CELL CYCLE PROTEIN; FGF2 PROTEIN, MOUSE; FIBROBLAST GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN VENTRICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL DIVISION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; GLIA; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REACTION TIME; WILD TYPE; ANIMAL; BRAIN; BRAIN CORTEX; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; DOWN REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; STEM CELL;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL PROLIFERATION; CEREBRAL CORTEX; DOWN-REGULATION; IMMUNOHISTOCHEMISTRY; LATERAL VENTRICLES; MICE; MICE, KNOCKOUT; NEUROGLIA; NEURONS; OLFACTORY BULB; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTORS, FIBROBLAST GROWTH FACTOR; STEM CELLS;

EID: 17444371643     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000082136     Document Type: Article

References (51)

1. Alvarez-Buylla A, Garcia-Verdugo JM (2002): Neurogenesis in adult subventricular zone. J Neurosci 22:629-634.
2. Belluardo N, Wu G-Y, Mudo G, Hansson AC, Petterson R, Fuxe K (1997): Comparative localization of fibroblast growth factor receptor-1, -2, and -3 mRNAs in the rat brain: In situ hybridization analysis. J Comp Neurol 379:226-246.
3. Capela A, Temple S (2002): LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865-875.
4. Craig CG, Morshead CM, Roach A, van der Kooy D (1994): Evidence for a relatively quiescent stem cell in the adult mammalian forebrain. J Cell Biochem 18:176.
5. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996): In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16:2649-2658.
6. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999): Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
7. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997): Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-5061.
8. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002): EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021-1034.
9. 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.
10. Emoto N, Gonzalez AM, Walicke PA, Wada E, Simmons DM, Shimasaki S, Baird A (1989): Basic fibroblast growth factor (FGF) in the central nervous system: Identification of specific loci of basic FGF expression in the rat brain. Growth Factors 2:21-29.
11. Feng L, Hatten ME, Heintz N (1994): Brain lipid-binding protein (BLBP): A novel signaling system in the developing mammalian CNS. Neuron 12:895-908.
12. Ganat Y, Soni S, Chacon M, Schwartz ML, Vaccarino FM (2002): Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the sub-ependymal zone. Neuroscience 112:977-991.
13. Ghosh A, Greenberg ME (1995): Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103.
14. Gonzalez A-M, Berry M, Maher PA, Logan A, Baird A (1995): A comprehensive analysis of the distribution of FGF-2 and FGF-1 in the rat brain. Brain Res 701:201-226.
15. Hatten ME, Lynch M, Rydel RE, Sanchez J, Joseph-Silverstein J, Moscatelli D, Rifkin DB (1988): In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev Biol 125:280-289.
16. Hayes NL, Nowakowski RS (2000): Exploiting the dynamics of S-phase tracers in developing brain: Interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev Neurosci 22:44-55.
17. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, van der Kooy D (2002): Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16:846-858.
18. Hunter KE, Hatten ME (1995): Radial glial cell transformation to astrocytes is bidirectional: Regulation by a diffusible factor in embryonic forebrain. Proc Natl Acad Sci USA 92:2061-2065.
19. 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.
20. 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.
21. Kuhn HG, Winkler J, Kempermann G, Thal L, Gage FH (1997): Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17:5820-5829.
22. Kuzis K, Reed S, Cherry NJ, Woodward WR, Eckenstein FP (1995): Developmental time course of acidic and basic fibroblast growth factors expression in distinct cellular populations of the rat central nervous system. J Comp Neurol 358:142-153.
23. Lewandoski M, Sun X, Martin GR (2000): Fgf8 signaling from the AER is essential for normal limb development. Nat Genet 26:460-463.
24. Lois C, Alvarez-Buylla A (1993): Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90:2074-2077.
25. Luskin MB (1993): Restricted proliferation and migration of postnatally generated neurons derived from the forebrain ventricular zone. Neuron 11:173-189.
26. McKinnon RD, Matsui T, Dubois-Dalq M, Aaronson SA (1990): FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5:603-614.
27. Martens DJ, Tropepe V, van der Kooy D (2000): Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J Neurosci 20:1085-1095.
28. Matsuzaki K, Toshitake Y, Matuo Y, Sasaki H, Nishikawa K (1989): Monoclonal antibodies against heparin-binding factor II/basic fibroblast growth factor that block its biological activity: Invalidity of the antibodies for tumor angiogenesis. Proc Natl Acad Sci USA 86: 9911-9915.
29. Morshead CM, Craig CG, van der Kooy D (1998): In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125:2251-2268.
30. Morshead CM, van der Kooy D (1992): Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12:249-256.
31. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D (1994): Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
32. Murphy M, Drago J, Bartlett PF (1990): Fibroblast growth factor stimulates the proliferation and differentiation of neural precursor cells in vitro. J Neurosci Res 25:463-475.
33. Nowakowski RS, Lewin SB, Miller MW (1989): Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311-318.
34. Ohkubo Y, Uchida AO, Shin D, Partanen J, Vaccarino FM (2004): Fibroblast growth factor receptor 1 is required for the proliferation of hippocampal progenitor cells and for hippocampal growth in mouse. J Neurosci 24:6057-6069.
35. Ortega S, Ittmann M, Tsang SH, Ehrich M, Basilico C (1998): Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci USA 95:5672-5677.
36. 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.
37. Ray J, Peterson DA, Schinstine M, Gage FH (1993): Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc Natl Acad Sci USA 90:3602-3606.
38. Rousselot P, Heintz N, Nottebohm F (1997): Expression of brain lipid binding protein in the brain of the adult canary and its implications for adult neurogenesis. J Comp Neurol 385: 415-426.
39. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001): Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
40. Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y (1997): Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci 17:9212-9219.
41. Song H, Stevens CF, Gage FH (2002): Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44.
42. Takahashi T, Nowakowski RS, Caviness VS (1993): Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13: 820-833.
43. Takahashi T, Nowakowski RS, Caviness VS Jr (1995): The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046-6057.
44. Takahashi T, Nowakowski RS, Caviness VS (1996): The leaving or Q fraction of the murine cerebral proliferative epithelium: A general model of neocortical neuronogenesis. J Neurosci 16:6183-6196.
45. Vaccarino FM, Ganat Y, Zhang Y, Zheng W (2001): Stem cells in neurodevelopment and plasticity. Neuropsychopharmacology 25:806-815.
46. Vaccarino FM, Ghetti B, Nurnberger JI (1985): Residual benzodiazepine (BZ) binding in the cortex of pcd mutant cerebella and qualitative BZ binding in the deep cerebellar nuclei of control and mutant mice: An autoradiographic study. Brain Res 343:70-78.
47. 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.
48. Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung Y-TE (1999): Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2:246-253.
49. Vicario-Abejon C, Johe KK, Hazel TG, Collazo D, McKay RDG (1995): Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15:105-114.
50. Williams TE, Meshul CK, Cherry NJ, Tiffany NM, Eckenstein FP, Woodward WR (1996): Characterization and distribution of basic fibroblast growth factor-containing cells in the rat hippocampus. J Comp Neurol 370:147-158.
51. Zhou M, Sutliff RL, Paul RJ, Lorenz JN, Hoying JB, Haudenschild CC, Yin M, Coffin JD, Kong L, Kranias EG, Luo W, Boivin GP, Duffy JJ, Pawlowski SA, Doetschman T (1998): Fibroblast growth factor 2 controls vascular tone. Nat Med 4:201-207.