Skip to main content

Advertisement

Log in

Fibroblast growth factors and their receptors in the central nervous system

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Fibroblast growth factors (FGFs) and their receptors constitute an elaborate signaling system that participates in many developmental and repair processes of virtually all mammalian tissues. Among the 23 FGF members, ten have been identified in the brain. Four FGF receptors (FGFRs), receptor tyrosine kinases, are known so far. Ligand binding of these receptors greatly depends on the presence of heparan sulfate proteoglycans, which act as low affinity FGFRs. Ligand binding specificity of FGFRs depends on the third extracellular Ig-like domain, which is subject to alternative splicing. Activation of FGFRs triggers several intracellular signaling cascades. These include phosphorylation of src and PLCγ leading finally to activation of PKC, as well as activation of Crk and Shc. SNT/FRS2 serves as an alternative link of FGFRs to the activation of PKC and, in addition, activates the Ras signaling cascade. In the CNS, FGFs are widely expressed; FGF-2 is predominantly synthesized by astrocytes, whereas other FGF family members, e.g., FGF-5, FGF-8, and FGF-9, are primarily synthesized by neurons. During CNS development FGFs play important roles in neurogenesis, axon growth, and differentiation. In addition, FGFs are major determinants of neuronal survival both during development and during adulthood. Adult neurogenesis depends greatly on FGF-2. Finally, FGF-1 and FGF-2 seem to be involved in the regulation of synaptic plasticity and processes attributed to learning and memory.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

References

  • Abe K, Ishiyama J, Saito H (1992) Effects of epidermal growth factor and basic fibroblast growth factor on generation of long-term potentiation in the dentate gyrus of fimbria-fornix-lesioned rats. Brain Res 593:335–338

    Article  CAS  PubMed  Google Scholar 

  • Abraham JA, Mergia A, Whang JL, Tumolo A, Friedman J, Hjerrild KA, Gospodarowicz D, Fiddes JC (1986a) Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor. Science 233:545–548

    CAS  PubMed  Google Scholar 

  • Abraham JA, Whang JL, Tumolo A, Mergia A, Fiddes JC (1986b) Human basic fibroblast growth factor: nucleotide sequence, genomic organization, and expression in mammalian cells. Cold Spring Harb Symp Quant Biol 51(1):657–668

    CAS  PubMed  Google Scholar 

  • Acosta CG, Fabrega AR, Masco DH, Lopez HS (2001) A sensory neuron subpopulation with unique sequential survival dependence on nerve growth factor and basic fibroblast growth factor during development. J Neurosci 21:8873–8885

    CAS  PubMed  Google Scholar 

  • Altman J, Das GD (1965) Autoradiographic and histological evidence for postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–325

    CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Lois C (1995) Neuronal stem cells in the brain of adult vertebrates. Stem Cells 13:263–272

    CAS  PubMed  Google Scholar 

  • Anderson DJ (1993) Cell fate determination in the peripheral nervous system: the sympathoadrenal progenitor. J Neurobiol 24:185–198

    CAS  PubMed  Google Scholar 

  • Anderson KJ, Dam D, Lee S, Cotman CW (1988) Basic fibroblast growth factor prevents death of lesioned cholinergic neurons in vivo. Nature 332:360–361

    Google Scholar 

  • Antoine M, Reimers K, Dickson C, Kiefer P (1997) Fibroblast growth factor 3, a protein with dual subcellular localization, is targeted to the nucleus and nucleolus by the concerted action of two nuclear localization signals and a nucleolar retention signal. J Biol Chem 272:29475–29481

    Article  CAS  PubMed  Google Scholar 

  • Aoyagi A, Nishikawa K, Saito H, Abe K (1994) Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultured rat hippocampal neurons. Brain Res 661:117–126

    Article  CAS  PubMed  Google Scholar 

  • Arnaud E, Touriol C, Boutonnet C, Gensac MC, Vagner S, Prats H, Prats AC (1999) A new 34-kilodalton isoform of human fibroblast growth factor 2 is cap dependently synthesized by using a non-AUG start codon and behaves as a survival factor. Mol Cell Biol 19:505–514

    CAS  PubMed  Google Scholar 

  • Arsenijevic Y, Weiss S, Schneider B, Aebischer P (2001) Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci 21:7194–7202

    CAS  PubMed  Google Scholar 

  • Asai T, Wanaka A, Kato H, Masana Y, Seo M, Tohyama M (1993) Differential expression of two members of FGF receptor gene family, FGFR-1 and FGFR-2 mRNA, in the adult rat central nervous system. Brain Res Mol Brain Res 17:174–178

    Article  CAS  PubMed  Google Scholar 

  • Balaci L, Presta M, Ennas MG, Dell'Era P, Sogos V, Lauro G, Gremo F (1994) Differential expression of fibroblast growth factor receptors by human neurones, astrocytes and microglia. Neuroreport 6:197–200

    CAS  PubMed  Google Scholar 

  • Bean AJ, Elde R, Cao YH, Oellig C, Tamminga C, Goldstein M, Pettersson RF, Hokfelt T (1991) Expression of acidic and basic fibroblast growth factors in the substantia nigra of rat, monkey, and human. Proc Natl Acad Sci U S A 88:10237–10241

    CAS  PubMed  Google Scholar 

  • Belluardo N, Wu G, Mudo G, Hansson AC, Pettersson 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

    Article  CAS  PubMed  Google Scholar 

  • Bethel A, Kirsch JR, Koehler RC, Finklestein SP, Traystman RJ (1997) Intravenous basic fibroblast growth factor decreases brain injury resulting from focal ischemia in cats. Stroke 28:609–615

    CAS  PubMed  Google Scholar 

  • Bieger S, Unsicker K (1996) Functions of fibroblast growth factors (FGFs) in the nervous system. In: Bell C (ed) Chemical factors in neural growth, degeneration and repair. Elsevier Science BV

  • Bizon JL, Lauterborn JC, Isackson PJ, Gall CM (1996) Acidic fibroblast growth factor mRNA is expressed by basal forebrain and striatal cholinergic neurons. J Comp Neurol 366:379–389

    Article  CAS  PubMed  Google Scholar 

  • Blanc EM, Jallageas M, Recasens M, Guiramand J (1999) Potentiation of glutamatergic agonist-induced inositol phosphate formation by basic fibroblast growth factor is related to developmental features in hippocampal cultures: neuronal survival and glial cell proliferation. Eur J Neurosci 11:3377–3386

    Article  CAS  PubMed  Google Scholar 

  • Blanquet PR, Patte C, Fayein N, Courtois Y (1989) Identification and isolation from bovine epithelial lens cells of two basic fibroblast growth factor receptors that possess bFGF-enhanced phosphorylation activities. Biochem Biophys Res Commun 160:1124–1131

    CAS  PubMed  Google Scholar 

  • Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39

    CAS  PubMed  Google Scholar 

  • Bouvier MM, Mytilineou C (1995) Basic fibroblast growth factor increases division and delays differentiation of dopamine precursors in vitro. J Neurosci 15:7141–7149

    CAS  PubMed  Google Scholar 

  • Burdine RD, Chen EB, Kwok SF, Stern MJ (1997) Egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc Natl Acad Sci U S A 94:2433–2437

    Article  CAS  PubMed  Google Scholar 

  • Burgess WH, Dionne CA, Kaplow J, Mudd R, Friesel R, Zilberstein A, Schlessinger J, Jaye M (1990) Characterization and cDNA cloning of phospholipase C-gamma, a major substrate for heparin-binding growth factor 1 (acidic fibroblast growth factor)-activated tyrosine kinase. Mol Cell Biol 10:4770–4777

    CAS  PubMed  Google Scholar 

  • Calamandrei G, Alleva E (1995) Neuronal growth factors, neurotrophins and memory deficiency. Behav Brain Res 66:129–132

    Article  CAS  PubMed  Google Scholar 

  • Casper D, Blum M (1995) Epidermal growth factor and basic fibroblast growth factor protect dopaminergic neurons from glutamate toxicity in culture. J Neurochem 65:1016–1026

    CAS  PubMed  Google Scholar 

  • Casper D, Roboz GJ, Blum M (1994) Epidermal growth factor and basic fibroblast growth factor have independent actions on mesencephalic dopamine neurons in culture. J Neurochem 62:2166–2177

    CAS  PubMed  Google Scholar 

  • Chellaiah AT, McEwen DG, Werner S, Xu J, Ornitz DM (1994) Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J Biol Chem 269:11620–11627

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cohen RI, Chandross KJ (2000) Fibroblast growth factor-9 modulates the expression of myelin related proteins and multiple fibroblast growth factor receptors in developing oligodendrocytes. J Neurosci Res 61:273–287

    Article  CAS  PubMed  Google Scholar 

  • Coughlin SR, Barr PJ, Cousens LS, Fretto LJ, Williams LT (1988) Acidic and basic fibroblast growth factors stimulate tyrosine kinase activity in vivo. J Biol Chem 263:988–993

    CAS  PubMed  Google Scholar 

  • Coulier F, Pontarotti P, Roubin R, Hartung H, Goldfarb M, Birnbaum D (1997) Of worms and men: an evolutionary perspective on the fibroblast growth factor (FGF) and FGF receptor families. J Mol Evol 44:43–56

    CAS  PubMed  Google Scholar 

  • Cuevas P, Gimenez-Gallego G (1996) Antiepileptic effects of acidic fibroblast growth factor examined in kainic acid-mediated seizures in the rat. Neurosci Lett 203:66–68

    Article  CAS  PubMed  Google Scholar 

  • Cuevas P, Revilla C, Herreras O, Largo C, Gimenez-Gallego G (1994) Neuroprotective effect of acidic fibroblast growth factor on seizure-associated brain damage. Neurol Res 16:365–369

    CAS  PubMed  Google Scholar 

  • Cuevas P, Carceller F, Munoz-Willery I, Gimenez-Gallego G (1998) Intravenous fibroblast growth factor penetrates the blood-brain barrier and protects hippocampal neurons against ischemia reperfusion injury. Surg Neurol 49:77–83

    Article  CAS  PubMed  Google Scholar 

  • Cummings BJ, Yee GJ, Cotman CW (1992) bFGF promotes the survival of entorhinal layer II neurons after perforant path axotomy. Brain Res 591:271–276

    Article  CAS  PubMed  Google Scholar 

  • Deloulme JC, Gensburger C, Sarhan S, Seiler N, Sensenbrenner M (1991) Effects of basic fibroblast growth factor on the development of GABAergic neurons in culture. Neuroscience 42:561–568

    Article  CAS  PubMed  Google Scholar 

  • Dionne CA, Crumley G, Bellot F, Kaplow JM, Searfoss G, Ruta M, Burgess WH, Jaye M, Schlessinger J (1990) Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J 9:2685–2692

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Eckenstein FP (1994) Fibroblast growth factors in the nervous system. J Neurobiol 25:1467–1480

    CAS  PubMed  Google Scholar 

  • Eckenstein F, Woodward WR, Nishi R (1991) Differential localization and possible functions of aFGF and bFGF in the central and peripheral nervous systems. Ann N Y Acad Sci 638:348–360

    CAS  PubMed  Google Scholar 

  • Eclancher F, Perraud F, Faltin J, Labourdette J, Sensenbrenner M (1990) Reactive astrogliosis after basic fibroblast growth factor (bFGF) injection in the injured rat brain. Glia 3:502–509

    CAS  PubMed  Google Scholar 

  • Elde R, Cao YH, Cintra A, Brelje TC, Pelto-Huikko M, Junttila T, Fuxe K, Pettersson RF, Hokfelt T (1991) Prominent expression of acidic fibroblast growth factor in motor and sensory neurons. Neuron 7:349–364

    CAS  PubMed  Google Scholar 

  • Eriksson AE, Cousens LS, Weaver LH, Matthews BW (1991) Three-dimensional structure of human basic fibroblast growth factor. Proc Natl Acad Sci U S A 88:3441–3445

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Eubanks JH, Perez-Velazquez JL, Kerr RG, Carlen PL, Mills LR, Jones OT (1996) Three distinct neuronal phenotypes exist in embryonic rat hippocampal neurons cultured in basic fibroblast growth factor. Neurosci Lett 204:5–8

    Article  CAS  PubMed  Google Scholar 

  • Faham S, Linhardt RJ, Rees DC (1998) Diversity does make a difference: fibroblast growth factor-heparin interactions. Curr Opin Struct Biol 8:578–586

    Article  CAS  PubMed  Google Scholar 

  • Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267:246–249

    CAS  PubMed  Google Scholar 

  • Fiore F, Planche J, Gibier P, Sebille A, deLapeyriere O, Birnbaum D (1997) Apparent normal phenotype of Fgf6−/− mice. Int J Dev Biol 41:639–642

    CAS  PubMed  Google Scholar 

  • Fiore F, Sebille A, Birnbaum D (2000) Skeletal muscle regeneration is not impaired in Fgf6 −/− mutant mice. Biochem Biophys Res Commun 272:138–143

    Article  CAS  PubMed  Google Scholar 

  • Floss T, Arnold HH, Braun T (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11:2040–2051

    CAS  PubMed  Google Scholar 

  • Frautschy SA, Walicke PA, Baird A (1991) Localization of basic fibroblast growth factor and its mRNA after CNS injury. Brain Res 553:291–299

    CAS  PubMed  Google Scholar 

  • Friesel RE, Maciag T (1995) Molecular mechanisms of angiogenesis: fibroblast growth factor signal transduction. FASEB J 9:919–925

    PubMed  Google Scholar 

  • Friesel R, Maciag T (1999) Fibroblast growth factor prototype release and fibroblast growth factor receptor signaling. Thromb Haemost 82:748–754

    CAS  PubMed  Google Scholar 

  • Friesel R, Burgess WH, Mehlman T, Maciag T (1986) The characterization of the receptor for endothelial cell growth factor by covalent ligand attachment. J Biol Chem 261:7581–7584

    CAS  PubMed  Google Scholar 

  • Fuhrmann V, Kinkl N, Leveillard T, Sahel J, Hicks D (1999) Fibroblast growth factor receptor 4 (FGFR4) is expressed in adult rat and human retinal photoreceptors and neurons. J Mol Neurosci 13:187–197

    CAS  PubMed  Google Scholar 

  • Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A 92:11879–11883

    CAS  PubMed  Google Scholar 

  • Goddard DR, Berry M, Kirvell SL, Butt AM (2002) Fibroblast growth factor-2 induces astroglial and microglial reactivity in vivo. J Anat 200:57–67

    Article  PubMed  Google Scholar 

  • Goldschmidt-Clèrmont PJ, Kim JW, Machesky LM, Rhee SG, Pollard TD (1991) Regulation of phospholipase C-gamma 1 by profilin and tyrosine phosphorylation. Science 251:1231–1233

    CAS  PubMed  Google Scholar 

  • Goldman SA, Nedergaard M, Crystal RG, Fraser RA, Goodman R, Harrison-Restelli C, Jiang J, Keyoung HM, Leventhal C, Pincus DW, Shahar A, Wang S (1997) Neural precursors and neuronal production in the adult mammalian forebrain. Ann N Y Acad Sci 835:30–55

    CAS  PubMed  Google Scholar 

  • Gomes FC, Paulin D, Moura Neto V (1999) Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz J Med Biol Res 32:619–631

    CAS  PubMed  Google Scholar 

  • Gomez-Pinilla F, Lee JW, Cotman CW (1992) Basic FGF in adult rat brain: cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J Neurosci 12:345–355

    PubMed  Google Scholar 

  • Gomez-Pinilla F, Lee JW, Cotman CW (1994) Distribution of basic fibroblast growth factor in the developing rat brain. Neuroscience 61:911–923

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez AM, Logan A, Ying W, Lappi DA, Berry M, Baird A (1994) Fibroblast growth factor in the hypothalamic-pituitary axis: differential expression of fibroblast growth factor-2 and a high affinity receptor. Endocrinology 134:2289–2297

    CAS  PubMed  Google Scholar 

  • Gonzalez AM, Berry M, Maher PA, Logan A, Baird A (1995) A comprehensive analysis of the distribution of FGF-2 and FGFR1 in the rat brain. Brain Res 701:201–226

    Article  CAS  PubMed  Google Scholar 

  • Gremo F, Presta M (2000) Role of fibroblast growth factor-2 in human brain: a focus on development. Int J Dev Neurosci 18:271–279

    Article  CAS  PubMed  Google Scholar 

  • Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16:1091–1100

    CAS  PubMed  Google Scholar 

  • Grothe C, Janet T (1995) Expression of FGF-2 and FGF receptor type 1 in the adult rat brainstem: effect of colchicine. J Comp Neurol 353:18–24

    CAS  PubMed  Google Scholar 

  • Grothe C, Wewetzer K (1996) Fibroblast growth factor and its implications for developing and regenerating neurons. Int J Dev Biol 40:403–410

    CAS  PubMed  Google Scholar 

  • Grothe C, Zachmann K, Unsicker K (1991) Basic FGF-like immunoreactivity in the developing and adult rat brainstem. J Comp Neurol 305:328–336

    CAS  PubMed  Google Scholar 

  • Guo ZH, Mattson MP (2000) Neurotrophic factors protect cortical synaptic terminals against amyloid and oxidative stress-induced impairment of glucose transport, glutamate transport and mitochondrial function. Cereb Cortex 10:50–57

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Degenstein L, Fuchs E (1996) Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev 10:165–175

    CAS  PubMed  Google Scholar 

  • Hajihosseini MK, Heath JK (2002) Expression patterns of fibroblast growth factors-18 and -20 in mouse embryos is suggestive of novel roles in calvarial and limb development. Mech Dev 113:79–83

    Article  CAS  PubMed  Google Scholar 

  • Haraguchi R, Suzuki K, Murakami R, Sakai M, Kamikawa M, Kengaku M, Sekine K, Kawano H, Kato S, Ueno N, Yamada G (2000) Molecular analysis of external genitalia formation: the role of fibroblast growth factor (Fgf) genes during genital tubercle formation. Development 127:2471–2479

    CAS  PubMed  Google Scholar 

  • Hartung H, Feldman B, Lovec H, Coulier F, Birnbaum D, Goldfarb M (1997) Murine FGF-12 and FGF-13: expression in embryonic nervous system, connective tissue and heart. Mech Dev 64:31–39

    Article  CAS  PubMed  Google Scholar 

  • Haynes LW (1988) Fibroblast (heparin-binding) growing factors in neuronal development and repair. Mol Neurobiol 2:263–289

    CAS  PubMed  Google Scholar 

  • Hebert JM, Rosenquist T, Gotz J, Martin GR (1994) FGF5 as a regulator of the hair growth cycle: evidence from targeted and spontaneous mutations. Cell 78:1017–1025

    PubMed  Google Scholar 

  • Hisajima H, Saito H, Abe K, Nishiyama N (1992) Effects of acidic fibroblast growth factor on hippocampal long-term potentiation in fasted rats. J Neurosci Res 31:549–553

    CAS  PubMed  Google Scholar 

  • Humpel C, Lippoldt A, Chadi G, Ganten D, Olson L, Fuxe K (1993) Fast and widespread increase of basic fibroblast growth factor messenger RNA and protein in the forebrain after kainate-induced seizures. Neuroscience 57:913–922

    Article  CAS  PubMed  Google Scholar 

  • Ikonomidou C, Turski L (1995) Excitotoxicity and neurodegenerative diseases. Curr Opin Neurol 8:487–497

    CAS  PubMed  Google Scholar 

  • Ikonomidou C, Turski L (1996) Neurodegenerative disorders: clues from glutamate and energy metabolism. Crit Rev Neurobiol 10:239–263

    CAS  PubMed  Google Scholar 

  • Ishihara A, Saito H, Nishiyama N (1992) Basic fibroblast growth factor ameliorates learning deficits in basal forebrain-lesioned mice. Jpn J Pharmacol 59:7-13

    CAS  PubMed  Google Scholar 

  • Ishiyama J, Saito H, Abe K (1991) Epidermal growth factor and basic fibroblast growth factor promote the generation of long-term potentiation in the dentate gyrus of anaesthetized rats. Neurosci Res 12:403–411

    Article  CAS  PubMed  Google Scholar 

  • Itoh N, Yazaki N, Tagashira S, Miyake A, Ozaki K, Minami M, Satoh M, Ohta M, Kawasaki T (1994) Rat FGF receptor-4 mRNA in the brain is expressed preferentially in the medial habenular nucleus. Brain Res Mol Brain Res 21:344–348

    Article  CAS  PubMed  Google Scholar 

  • Johnson DE, Williams LT (1993) Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60:1–41

    CAS  PubMed  Google Scholar 

  • Johnson DE, Lee PL, Lu J, Williams LT (1990) Diverse forms of a receptor for acidic and basic fibroblast growth factors. Mol Cell Biol 10:4728–4736

    CAS  PubMed  Google Scholar 

  • Johnson DE, Lu J, Chen H, Werner S, Williams LT (1991) The human fibroblast growth factor receptor genes: a common structural arrangement underlies the mechanisms for generating receptor forms that differ in their third immunoglobulin domain. Mol Cell Biol 11:4627–4634

    Google Scholar 

  • Joy A, Moffett J, Neary K, Mordechai E, Stachowiak EK, Coons S, Rankin-Shapiro J, Florkiewicz RZ, Stachowiak MK (1997) Nuclear accumulation of FGF-2 is associated with proliferation of human astrocytes and glioma cells. Oncogene 14:171–183

    CAS  PubMed  Google Scholar 

  • Kalcheim C (1996) The role of neurotrophins in development of neural-crest cells that become sensory ganglia. Philos Trans R Soc Lond B Biol Sci 351:375–381

    CAS  PubMed  Google Scholar 

  • Kalil K, Szebenyi G, Dent EW (2000) Common mechanisms underlying growth cone guidance and axon branching. J Neurobiol 44:145–158

    Article  CAS  PubMed  Google Scholar 

  • Kelley MJ, Pech M, Seuanez HN, Rubin JS, O'Brien SJ, Aaronson SA (1992) Emergence of the keratinocyte growth factor multigene family during the great ape radiation. Proc Natl Acad Sci U S A 89:9287–9291

    CAS  PubMed  Google Scholar 

  • Kiefer P, Acland P, Pappin D, Peters G, Dickson C (1994) Competition between nuclear localization and secretory signals determines the subcellular fate of a single CUG-initiated form of FGF3. EMBO J 13:4126–4136

    CAS  PubMed  Google Scholar 

  • Kiessling M, Gass P (1994) Stimulus-transcription coupling in focal cerebral ischemia. Brain Pathol 4:77–83

    CAS  PubMed  Google Scholar 

  • Kirino T (2000) Delayed neuronal death. Neuropathology 20:95–97

    Article  Google Scholar 

  • Konishi M, Mikami T, Yamasaki M, Miyake A, Itoh N (2000) Fibroblast growth factor-16 is a growth factor for embryonic brown adipocytes. J Biol Chem 275:12119–12122

    Article  CAS  PubMed  Google Scholar 

  • Kornbluth S, Paulson KE, Hanafusa H (1988) Novel tyrosine kinase identified by phosphotyrosine antibody screening of cDNA libraries. Mol Cell Biol 8:5541–5544

    CAS  PubMed  Google Scholar 

  • Kouhara H, Hadari YR, Spivak-Kroizman T, Schilling J, Bar-Sagi D, Lax I, Schlessinger J (1997) A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89:693–702

    CAS  PubMed  Google Scholar 

  • Krieglstein K, Reuss B, Maysinger D, Unsicker K (1998) Short communication: transforming growth factor-beta mediates the neurotrophic effect of fibroblast growth factor-2 on midbrain dopaminergic neurons. Eur J Neurosci 10:2746–2750

    Article  CAS  PubMed  Google Scholar 

  • Langren E, Blume-Jensen P, Courtneidge SA, Claesson-Welsh L (1995) Fibroblast growth factor receptor-1 regulation of Src family kinases. Oncogene 10:2027–2035

    PubMed  Google Scholar 

  • Langren E, Klint P, Landgren E, Claesson-Welsh L (1998) Fibroblast growth factor receptor-1 mediates chemotaxis independently of direct SH2-domain protein binding. Oncogene 17:283–291

    Article  PubMed  Google Scholar 

  • Larsson H, Klint P, Landgren E, Claesson-Welsh L (1999) Fibroblast growth factor receptor-1-mediated endothelial cell proliferation is dependent on the Src homology (SH) 2/SH3 domain-containing adaptor protein Crk. J Biol Chem 274:25726–25734

    Article  CAS  PubMed  Google Scholar 

  • Le R, Esquenazi S (2002) Astrocytes mediate cerebral cortical neuronal axon and dendrite growth, in part, by release of fibroblast growth factor. Neurol Res 24:81–92

    PubMed  Google Scholar 

  • Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT (1989) Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245:57–60

    CAS  PubMed  Google Scholar 

  • Lenhard T, Schober A, Suter-Crazzolara C, Unsicker K (2002) Fibroblast growth factor-2 requires glial-cell-line-derived neurotrophic factor for exerting its neuroprotective actions on glutamate-lesioned hippocampal neurons. Mol Cell Neurosci 20:181–197

    Article  CAS  PubMed  Google Scholar 

  • Leung DSY, Unsicker K, Reuss B (2001) Gap junctions modulate survival-promoting effects of fibroblast growth factor-2 on cultured midbrain dopaminergic neurons. Mol Cell Neurosci 18:44–55

    Article  PubMed  Google Scholar 

  • Li LY, Safran M, Aviezer D, Bohlen P, Seddon AP, Yayon A (1994) Diminished heparin binding of a basic fibroblast growth factor mutant is associated with reduced receptor binding, mitogenesis, plasminogen activator induction, and in vitro antiogenesis. Biochemistry 33:10999–11007

    CAS  PubMed  Google Scholar 

  • Li L, Donly C, Li Q, Willis LG, Keddie BA, Erlandson MA, Theilmann DA (2002) Identification and genomic analysis of a second species of nucleopolyhedrovirus isolated from Mamestra configurata. Virology 297:226–244

    Article  CAS  PubMed  Google Scholar 

  • Lim YP, Low BC, Lim J, Wong ES, Guy GR (1999) Association of atypical protein kinase C isotypes with the docker protein FRS2 in fibroblast growth factor signaling. J Biol Chem 274:19025–19034

    Article  CAS  PubMed  Google Scholar 

  • Lindholm D, Harikka J, da Penha BM, Castren E, Tzimagiorgis G, Hughes RA, Thoenen H (1994) Fibroblast growth factor-5 promotes differentiation of cultured rat septal cholinergic and raphe serotonergic neurons: comparison with the effects of neurotrophins. Eur J Neurosci 6:244–252

    CAS  PubMed  Google Scholar 

  • Liu Z, Holmes GL (1997a) Basic fibroblast growth factor is highly neuroprotective against seizure-induced long-term behavioural deficits. Neuroscience 76:1129–1138

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Holmes GL (1997b) Basic fibroblast growth factor-induced seizures in rats. Neurosci Lett 233:85–88

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Zhu XZ (1999) Increased expression and nuclear accumulation of basic fibroblast growth factor in primary cultured astrocytes following ischemic-like insults. Brain Res Mol Brain Res 71:171–177

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, D'Amore PA, Mikati M, Gatt A, Holmes GL (1993) Neuroprotective effect of chronic infusion of basic fibroblast growth factor on seizure-associated hippocampal damage. Brain Res 626:335–338

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Cai J, Liu Y, Xue H, Chrest FJ, Wersto RP, Rao M (2002) Microarray analysis of selected genes in neural stem and progenitor cells. J Neurochem 83:1481–1497

    Article  CAS  PubMed  Google Scholar 

  • Mansour SL, Goddard JM, Capecchi MR (1993) Mice, homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development 117:13–28

    CAS  PubMed  Google Scholar 

  • Mark RJ, Fuson KS, Keane-Lazar K, May PC (1999) Fibroblast growth factor-8 protects cultured rat hippocampal neurons from oxidative insult. Brain Res 830:88–93

    Article  CAS  PubMed  Google Scholar 

  • Martinez G, Di Giacomo C, Sorrenti V, Camazza ML, Ragusa N, Barcellona ML, Vanella A (2001) Fibroblast growth factor-2 and transforming growth factor beta 1 immunostaining in rat brain after cerebral postischemic reperfusion. J Neurosci Res 63:136–142

    Article  CAS  PubMed  Google Scholar 

  • Martone ME, Hu BR, Ellisman MH (2000) Alterations of hippocampal postsynaptic densities following transient ischemia. Hippocampus 10:610–616

    Article  CAS  PubMed  Google Scholar 

  • Masumara M, Murayama N, Inoue T, Ohno T (1996) Selective induction of fibroblast growth factor receptor-1 mRNA after transient focal ischemia in the cerebral cortex of rats. Neurosci Lett 213:119–122

    Article  PubMed  Google Scholar 

  • Mattson MP, Murrain M, Guthrie PB, Kater SB (1989) Fibroblast growth factor and glutamate: opposing roles in the generation and degeneration of hippocampal neuroarchitecture. J Neurosci 9:3728–3740

    CAS  PubMed  Google Scholar 

  • Mattson MP, Kumar KN, Wang H, Cheng B, Michaelis EK (1993) Basic FGF regulates the expression of a functional 71 kDa NMDA receptor protein that mediates calcium influx and neurotoxicity in hippocampal neurons. J Neurosci 13:4575–4588

    CAS  PubMed  Google Scholar 

  • McWhirter JR, Goulding M, Weiner JA, Chun J, Murre C (1997) A novel fibroblast growth factor gene expressed in the developing nervous system is a downstream target of the chimeric homeodomain oncoprotein E2A-Pbx1. Development 124:3221–3232

    CAS  PubMed  Google Scholar 

  • Meyers EN, Lewandoski M, Martin GR (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18:136–141

    CAS  PubMed  Google Scholar 

  • Mignatti P, Morimoto T, Rifkin DB (1992) Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J Cell Physiol 151:81–93

    CAS  PubMed  Google Scholar 

  • Miller DL, Ortega S, Bashayan O, Basch R, Basilico C (2000) Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotypic defects observed in FGF2 null mice. Mol Cell Biol 20:2260–2268

    Google Scholar 

  • Miyagawa T, Saito H, Nishiyama N (1993) Branching enhancement by basic fibroblast growth factor in cut neurite of hippocampal neurons. Neurosci Lett 153:29–31

    Article  CAS  PubMed  Google Scholar 

  • Miyakawa K, Hatsuzawa K, Kurokawa T, Asada M, Kuroiwa T, Imamura T (1999) A hydrophobic region locating at the center of fibroblast growth factor-9 is crucial for its secretion. J Biol Chem 274:29352–29357

    Article  CAS  PubMed  Google Scholar 

  • Miyake A, Hattori Y, Ohta M, Itoh N (1996) Rat oligodendrocytes and astrocytes preferentially express fibroblast growth factor receptor-2 and -3 mRNAs. J Neurosci Res 45:534–541

    Article  CAS  PubMed  Google Scholar 

  • Miyake A, Konishi M, Martin FH, Hernday NA, Ozaki K, Yamamoto S, Mikami T, Arakawa T, Itoh N (1998) Structure and expression of a novel member, FGF-16, on the fibroblast growth factor family. Biochem Biophys Res Commun 243:148–152

    CAS  PubMed  Google Scholar 

  • Miyamoto M, Naruo K, Seko C, Matsumoto S, Kondo T, Kurokawa T (1993) Molecular cloning of a novel cytokine cDNA encoding the ninth member of the fibroblast growth factor family, which has a unique secretion property. Mol Cell Biol 13:4251–4259

    Google Scholar 

  • Mocchetti I, Wrathall JR (1995) Neurotrophic factors in central nervous system trauma. J Neurotrauma 12:853–870

    CAS  PubMed  Google Scholar 

  • Moenner M, Chevallier B, Badet J, Barritault D (1986) Evidence and characterization of the receptor to eye-derived growth factor I, the retinal form of basic fibroblast growth factor, on bovine epithelial lens cells. Proc Natl Acad Sci U S A 83:5024–5028

    CAS  PubMed  Google Scholar 

  • Mohammadi M, Honegger AM, Rotin D, Fischer R, Bellot F, Li W, Dionne CA, Jaye M, Rubinstein M, Schlessinger J (1991) A tyrosine-phosphorylated carboxy-terminal peptide of the fibroblast growth factor receptor (Flg) is a binding site for the SH2 domain of phospholipase C-gamma 1. Mol Cell Biol 11:5068–5078

    CAS  PubMed  Google Scholar 

  • Mohammadi M, Dionne CA, Li W, Li N, Spivak T, Honegger AM, Jaye M, Schlessinger J (1992) Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature 358:681–684

    CAS  PubMed  Google Scholar 

  • Mohammadi M, Schlessinger J, Hubbard SR (1996) Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86:577–587

    CAS  PubMed  Google Scholar 

  • Molteni R, Fumagalli F, Magnaghi V, Roceri M, Gennarelli M, Racagni G, Melcangi RC, Riva MA (2001) Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity. Brain Res Brain Res Rev 37:249–258

    Article  CAS  PubMed  Google Scholar 

  • Moscatelli D (1987) High and low affinity binding sites for basic fibroblast growth factor on cultured cells: absence of a role for low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells. J Cell Physiol 131:123–130

    CAS  PubMed  Google Scholar 

  • Moy FJ, Seddon AP, Bohlen P, Powers R (1996) High-resolution solution structure of basic fibroblast growth factor determined by multidimensional heteronuclear magnetic resonance spectroscopy. Biochemistry 35:13552–13561

    Article  PubMed  Google Scholar 

  • Mufson EJ, Kroin JS, Sendera TJ, Sobreviela T (1999) Distribution and retrograde transport of trophic factors in the central nervous system: functional implications for the treatment of neurodegenerative diseases. Prog Neurobiol 57:451–484

    Article  CAS  PubMed  Google Scholar 

  • Muslin AJ, Peters KG, Williams LT (1994) Direct activation of phospholipase C-gamma by fibroblast growth factor receptor is not required for mesoderm induction in Xenopus animal caps. Mol Cell Biol 14:3006–3012

    CAS  PubMed  Google Scholar 

  • Nakagami Y, Saito H, Matsuki N (1997) Basic fibroblast growth factor and brain-derived neurotrophic factor promote survival and neuronal circuit formation in organotypic hippocampal culture. Jpn J Pharmacol 75:319–326

    CAS  PubMed  Google Scholar 

  • Nakamura S, Todo T, Motoi Y, Haga S, Aizawa T, Ueki A, Ikeda K (1999) Glial expression of fibroblast growth factor-9 in rat central nervous system. Glia 28:53–65

    Article  CAS  PubMed  Google Scholar 

  • Nakata N, Kato H, Kogure K (1993) Protective effects of basic fibroblast growth factor against hippocampal neuronal damage following cerebral ischemia in the gerbil. Brain Res 605:354–356

    Article  CAS  PubMed  Google Scholar 

  • Nakatake Y, Hoshikawa M, Asaki T, Kassai Y, Itoh N (2001) Identification of a novel fibroblast growth factor, FGF-22, preferentially expressed in the inner root sheath of the hair follicle. Biochim Biophys Acta 1517:460–463

    Article  CAS  PubMed  Google Scholar 

  • Namaka MP, Sawchuk M, MacDonald SC, Jordan LM, Hochman S (2001) Neurogenesis in postnatal mouse dorsal root ganglia. Exp Neurol 172:60–69

    Article  CAS  PubMed  Google Scholar 

  • Neufeld G, Gospodarowicz D (1985) The identification and partial characterization of the fibroblast growth factor receptor of baby hamster kidney cells. J Biol Chem 260:13860–13868

    CAS  PubMed  Google Scholar 

  • Neufeld G, Gospodarowicz D (1986) Basic and acidic fibroblast growth factors interact with the same cell surface receptors. J Biol Chem 261:5631–5637

    CAS  PubMed  Google Scholar 

  • Nishimura T, Nakatake Y, Konishi M, Itoh N (2000) Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochim Biophys Acta 1492:203–206

    Article  CAS  PubMed  Google Scholar 

  • Ohbayashi N, Shibayama M, Kurotaki Y, Imanishi M, Fujimori T, Itoh N, Takada S (2002) FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev 16:870–879

    Article  CAS  PubMed  Google Scholar 

  • Ogata N, Matsushima M, Takada Y, Tobe T, Takahashi K, Yi X, Yamamoto C, Yamada H, Uyuma M (1996) Expression of basic fibroblast growth factor mRNA in developing choroidal neovascularization. Curr Eye Res 15:1008–1018

    CAS  PubMed  Google Scholar 

  • Ohmachi S, Watanabe Y, Mikami T, Kusu N, Ibi T, Akaike A, Itoh N (2000) FGF-20, a novel neurotrophic factor, preferentially expressed in the substantia nigra pars compacta of rat brain. Biochem Biophys Res Commun 277:355–360

    Article  CAS  PubMed  Google Scholar 

  • Olney JW, Collins RC, Sloviter RS (1986) Excitotoxic mechanisms of epileptic brain damage. Adv Neurol 44:857–877

    CAS  PubMed  Google Scholar 

  • Ong SH, Lim YP, Low BC, Guy GR (1997) SHP2 associates directly with tyrosine phosphorylated p90 (SNT) protein in FGF-stimulated cells. Biochem Biophys Res Commun 238:261–266

    Article  CAS  PubMed  Google Scholar 

  • Ong SH, Guy GR, Hadari YR, Laks S, Gotoh N, Schlessinger J, Lax I (2000) FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol Cell Biol 20:979–989

    Article  CAS  PubMed  Google Scholar 

  • Ornitz DM (2000) FGFs, heparan sulfate and FGFRs: complex interactions essential for development. Bioessays 22:108–112

    CAS  PubMed  Google Scholar 

  • Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2:3005.1–3005.12

    Article  Google Scholar 

  • Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292–15297

    CAS  PubMed  Google Scholar 

  • Otto D, Unsicker K (1990) Basic FGF reverses chemical and morphological deficits in the nigrostriatal system of MPTP-treated mice. J Neurosci 10:1912–1921

    CAS  PubMed  Google Scholar 

  • Otto D, Unsicker K (1993a) FGF-2-mediated protection of cultured mesencephalic dopaminergic neurons against MPTP and MPP+: specificity and impact of culture conditions, non-dopaminergic neurons, and astroglial cells. J Neurosci Res 34:382–393

    CAS  PubMed  Google Scholar 

  • Otto D, Unsicker K (1993b) FGF-2 modulates dopamine and dopamine-related striatal transmitter systems in the intact and MPTP-lesioned mouse. Eur J Neurosci 5:927–932

    CAS  PubMed  Google Scholar 

  • Otto D, Frotscher M, Unsicker K (1989) Basic fibroblast growth factor and nerve growth factor administered in gel foam rescue medial septal neurons after fimbria fornix transection. J Neurosci Res 22:83–91

    CAS  PubMed  Google Scholar 

  • Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH (1999) Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487–8497

    CAS  PubMed  Google Scholar 

  • Patel MN, McNamara JO (1995) Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience 69:763–770

    Article  CAS  PubMed  Google Scholar 

  • Pellegrini L, Burke DF, von Delft F, Mulloy B, Blundell TL (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407:1029–1034

    Article  CAS  PubMed  Google Scholar 

  • Perkins LA, Cain LD (1995) Basic fibroblast growth factor (bFGF) increases the survival of embryonic and postnatal basal forebrain cholinergic neurons in primary culture. Int J Dev Neurosci 13:51–61

    Article  CAS  PubMed  Google Scholar 

  • Perraud F, Labourdette G, Eclancher F, Sensenbrenner M (1990) Primary cultures of astrocytes from different brain areas of newborn rats and effects of basic fibroblast growth factor. Dev Neurosci 12:11–21

    CAS  PubMed  Google Scholar 

  • Perrone-Capano C, Di Porzio U (2000) Genetic and epigenetic control of midbrain dopaminergic neuron development. Int J Dev Biol 44:679–687

    CAS  PubMed  Google Scholar 

  • Peters KG, Marie J, Wilson E, Ives HE, Escobedo J, Del Rosario M, Mirda D, Williams LT (1992) Point mutation of an FGF receptor abolishes phosphatidylinositol turnover and Ca2+ flux but not mitogenesis. Nature 358:678–681

    CAS  PubMed  Google Scholar 

  • Plotnikov AN, Hubbard SR, Schlessinger J, Mohammadi M (2000) Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell 101:413–424

    CAS  PubMed  Google Scholar 

  • Powers CJ, McLeskey SW, Wellstein A (2000) Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 7:165–197

    CAS  PubMed  Google Scholar 

  • Qiao J, Uzzo R, Obara-Ishihara T, Degenstein L, Fuchs E, Herzlinger D (1999) FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. Development 126:547–554

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Raffioni S, Thomas D, Foehr ED, Thompson LM, Bradshaw RA (1999) Comparison of the intracellular signaling responses by three chimeric fibroblast growth factor receptors in PC12 cells. Proc Natl Acad Sci U S A 96:7178–7183

    Article  CAS  PubMed  Google Scholar 

  • Ramirez JJ, Finklestein SP, Keller J, Abrams W, George MN, Parakh T (1999) Basic fibroblast growth factor enhances axonal sprouting after cortical injury in rats. Neuroreport 10:1201–1204

    CAS  PubMed  Google Scholar 

  • Ray J, Gage FH (1994) Spinal cord neuroblasts proliferate in response to basic fibroblast growth factor. J Neurosci 14:3548–3564

    CAS  PubMed  Google Scholar 

  • Reifers F, Bohli H, Walsh EC, Crossley PH, Stainier DY, Brand M (1998) Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125:2381–2395

    CAS  PubMed  Google Scholar 

  • Reilly JF, Maher PA, Kumari VG (1998) Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2. Glia 22:202–210

    Article  CAS  PubMed  Google Scholar 

  • Reuss B, Unsicker K (2000) Survival and differentiation of dopaminergic mesencephalic neurons are promoted by dopamine-mediated induction of FGF-2 in striatal astroglial cells. Mol Cell Neurosci 16:781–792

    Article  CAS  PubMed  Google Scholar 

  • Reuss B, Dermietzel R, Unsicker K (1998) Fibroblast growth factor 2 (FGF-2) differentially regulates connexin (cx) 43 expression and function in astroglial cells from distinct brain regions. Glia 22:19–30

    Article  CAS  PubMed  Google Scholar 

  • Reuss B, Hertel M, Werner S, Unsicker K (2000a) Fibroblast growth factors-5 and -9 distinctly regulate expression and function of the gap junction protein connexin43 in cultured astroglial cells from different brain regions. Glia 30:231–241

    Article  CAS  PubMed  Google Scholar 

  • Reuss B, Leung DS, Ohlemeyer C, Kettenmann H, Unsicker K (2000b) Regionally distinct regulation of astroglial neurotransmitter receptors by fibroblast growth factor-2. Mol Cell Neurosci 16:42–58

    Article  CAS  PubMed  Google Scholar 

  • Revest JM, DeMoerlooze L, Dickson C (2000) Fibroblast growth factor 9 secretion is mediated by a non-cleaved amino-terminal signal sequence. J Biol Chem 275:8083–8090

    Article  CAS  PubMed  Google Scholar 

  • Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565–4574

    CAS  PubMed  Google Scholar 

  • Riva MA, Gale K, Mocchetti I (1992) Basic fibroblast growth factor mRNA increases in specific brain regions following convulsive seizures. Brain Res Mol Brain Res 15:311–318

    Article  CAS  PubMed  Google Scholar 

  • Riva MA, Donati E, Tascedda F, Zolli M, Racagni G (1994) Short- and long-term induction of basic fibroblast growth factor gene expression in rat central nervous system following kainate injection. Neuroscience 59:55–65

    Article  CAS  PubMed  Google Scholar 

  • Rothman SM, Olney JW (1986) Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol 19:105–111

    CAS  PubMed  Google Scholar 

  • Ruta M, Burgess W, Givol D, Epstein J, Neiger N, Kaplow J, Crumley G, Dionne C, Jaye M, Schlessinger J (1989) Receptor for acidic fibroblast growth factor is related to the tyrosine kinase encoded by the fms-like gene (FLG). Proc Natl Acad Sci U S A 86:8722–8726

    CAS  PubMed  Google Scholar 

  • Sadohara T, Sugahara K, Urashima Y, Terasaki H, Lyama K (2001) Keratinocyte growth factor prevents ischemia-induced delayed neuronal death in the hippocampal CA1 field of the gerbil brain. Neuroreport 12:71–76

    CAS  PubMed  Google Scholar 

  • Sah DW, Ray J, Gage FH (1997) Regulation of voltage- and ligand-gated currents in rat hippocampal progenitor cells in vitro. J Neurobiol 32:95–110

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Oomura Y, Suzuki K, Hanai K, Yagi H (1992) Acidic fibroblast growth factor prevents death of hippocampal CA1 pyramidal cells following ischemia. Neurochem Int 21:397–402

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Oomura Y, Figurov A, Yagi H (1994) Acidic fibroblast growth factor facilitates generation of long-term potentiation in rat hippocampal slices. Brain Res Bull 33:505–511

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Tooyama I, Li AJ, Oomura Y, Kimura H (1999) Effects of an acidic fibroblast growth factor fragment analog on learning and memory and on medial septum cholinergic neurons in senescence-accelerated mice. Neuroscience 92:1287–1294

    Article  CAS  PubMed  Google Scholar 

  • Shanmugalingam S, Houart C, Picker A, Reifers F, Macdonald R, Barth A, Griffin K, Brand M, Wilson SW (2000) Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 127:2549–2561

    CAS  PubMed  Google Scholar 

  • Spivak-Kroizman T, Lemmon MA, Dikic I, Ladbury JE, Pinchasi D, Huang J, Jaye M, Crumley G, Schlessinger J, Lax I (1994a) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 79:1015–1024

    CAS  PubMed  Google Scholar 

  • Spivak-Kroizman T, Mohammadi M, Hu P, Jaye M, Schlessinger J, Lax I (1994b) Point mutation in the fibroblast growth factor receptor eliminates phosphatidylinositol hydrolysis without affecting neuronal differentiation of PC12 cells. J Biol Chem 269:14419–14423

    CAS  PubMed  Google Scholar 

  • Stachowiak MK, Moffett J, Maher P, Tucholski J, Stachowiak EK (1997) Growth factor regulation of cell growth and proliferation in the nervous system. A new intracrine nuclear mechanism. Mol Neurobiol 15:257–283

    CAS  PubMed  Google Scholar 

  • Stauber DJ, DiGabriele AD, Hendrickson WA (2000) Structural interactions of fibroblast growth factor receptor with its ligands. Proc Natl Acad Sci U S A 97:49–54

    Article  CAS  PubMed  Google Scholar 

  • Stock A, Kuzis K, Woodward WR, Nishi R, Eckenstein FP (1992) Localization of acidic fibroblast growth factor in specific subcortical neuronal populations. J Neurosci 12:4688–4700

    CAS  PubMed  Google Scholar 

  • Streppel M, Azzolin N, Dohm S, Guntinas-Lichius O, Haas C, Grothe C, Wevers A, Neiss WF, Angelov DN (2002) Focal application of neutralizing antibodies to soluble neurotrophic factors reduces collateral axonal branching after peripheral nerve lesion. Eur J Neurosci 15:1327–1342

    CAS  PubMed  Google Scholar 

  • Sun X, Meyers EN, Lewandoski M, Martin GR (1999) Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev 13:1834–1846

    CAS  PubMed  Google Scholar 

  • Sun X, Mariani FV, Martin GR (2002) Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418:501–508

    Article  CAS  PubMed  Google Scholar 

  • Sutherland D, Samakovlis C, Krasnow MA (1996) Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87:1091–1101

    CAS  PubMed  Google Scholar 

  • Suzuki K, Yamanishi K, Mori O, Kamikawa M, Andersen B, Kato S, Toyoda T, Yamada G (2000) Defective terminal differentiation and hypoplasia of the epidermis in mice lacking the Fgf10 gene. FEBS Lett 481:53–56

    Article  CAS  PubMed  Google Scholar 

  • Szebenyi G, Callaway JL, Dent EW, Kalil K (1998) Interstitial branches develop from active regions of the axon demarcated by the primary growth cone during pausing behaviors. J Neurosci 18:7930–7940

    CAS  PubMed  Google Scholar 

  • Szebenyi G, Dent EW, Callaway JL, Seys C, Lueth H, Kalil K (2001) Fibroblast growth factor-2 promotes axon branching of cortical neurons by influencing morphology and behavior of the primary growth cone. J Neurosci 21:3932–3941

    CAS  PubMed  Google Scholar 

  • Takami K, Matsuo A, Terai K, Walker DG, McGeer EG, McGeer PL (1998) Fibroblast growth factor receptor-1 expression in the cortex and hippocampus in Alzheimer's disease. Brain Res 802:89–97

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson E, Fu L, John L, Hultgren B, Huang X, Renz M, Stephan JP, Tsai SP, Powell-Braxton L, French D, Stewart TA (2002) Transgenic mice expressing human fibroblast growth factor-19 display increased metabolic rate and decreased adiposity. Endocrinology 143:1741–1747

    CAS  PubMed  Google Scholar 

  • Tooyama I, Walker D, Yamada T, Hanai K, Kimura H, McGeer EG, McGeer PL (1992) High molecular weight basic fibroblast growth factor-like protein is localized to a subpopulation of mesencephalic dopaminergic neurons in the rat brain. Brain Res 593:274–280

    Article  CAS  PubMed  Google Scholar 

  • Vaccarino FM, Schwartz ML, Raballo R, Rhee J, Lyn-Cook R (1999) Fibroblast growth factor signaling regulates growth and morphogenesis at multiple steps during brain development. Curr Top Dev Biol 46:179–200

    CAS  PubMed  Google Scholar 

  • Vaccarino FM, Ganat Y, Zhang Y, Zheng W (2001) Stem cells in neurodevelopment and plasticity. Neuropsychopharmacology 25:805–815

    Article  CAS  PubMed  Google Scholar 

  • Vainikka S, Partanen J, Bellosta P, Coulier F, Birnbaum D, Basilico C, Jaye M, Alitalo K (1992) Fibroblast growth factor receptor-4 shows novel features in genomic structure, ligand binding and signal transduction. EMBO J 11:4273–4280

    CAS  PubMed  Google Scholar 

  • Venkataraman G, Raman R, Sasisekharan V, Sasisekharan R (1999) Fibroblast growth factors 1 and 2 are distinct in oligomerization in the presence of heparin-like glycosaminoglycans. Proc Natl Acad Sci U S A 96:1892–1897

    Article  CAS  PubMed  Google Scholar 

  • Vescovi AL, Reynolds BA, Fraser DD, Weiss S (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11:951–966

    CAS  PubMed  Google Scholar 

  • Vicario-Abejon C, Johe KK, Hazel TG, Collazo D, McKay RD (1995) Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15:105–114

    CAS  PubMed  Google Scholar 

  • von Bohlen und Halbach O, Dermietzel R (2002) Neurotransmitters and neuromodulators. Wiley-VCH, Weinheim

  • Wagner JP, Black IB, DiCicco-Bloom E (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 19:6006–6016

    CAS  PubMed  Google Scholar 

  • Wanaka A, Milbrandt J, Johnson EM (1991) Expression of FGF receptor gene in rat development. Development 111:455–468

    CAS  PubMed  Google Scholar 

  • Wang JK, Xu H, Li HC, Goldfarb M (1996) Broadly expressed SNT-like proteins link FGF receptor stimulation to activators of Ras. Oncogene 13:721–729

    CAS  PubMed  Google Scholar 

  • Wang Q, Bardgett ME, Wong M, Wozniak DF, Lou J, McNeil BD, Chen C, Nardi A, Reid DC, Yamada K, Ornitz DM (2002) Ataxia and paroxysmal dyskinesia in mice lacking axonally transported FGF14. Neuron 35:25–38

    CAS  PubMed  Google Scholar 

  • Wei OY, Huang YL, Da CD, Cheng JS (2000) Alteration of basic fibroblast growth factor expression in rat during cerebral ischemia. Acta Pharmacol Sin 21:296–300

    CAS  PubMed  Google Scholar 

  • Wilcox BJ, Unnerstall JR (1991) Expression of acidic fibroblast growth factor mRNA in the developing and adult rat brain. Neuron 6:397–409

    CAS  PubMed  Google Scholar 

  • Wu H, Reynolds AB, Kanner SB, Vines RR, Parsons JT (1991) Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol Cell Biol 11:5113–5124

    CAS  PubMed  Google Scholar 

  • Xu H, Lee KW, Goldfarb M (1998) Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J Biol Chem 273:17987–17990

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Liu Z, Ornitz DM (2000) Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127:1833–1843

    CAS  PubMed  Google Scholar 

  • Yamashita T, Yoshioka M, Itoh N (2000) Identification of a novel fibroblast growth factor, FGF-23, preferentially expressed in the ventrolateral thalamic nucleus of the brain. Biochem Biophys Res Commun 277:494–498

    Article  CAS  PubMed  Google Scholar 

  • Yan KS, Kuti M, Yan S, Mujtaba S, Farooq A, Goldfarb MP, Zhou MM (2002) FRS2 PTB domain conformation regulates interactions with divergent neurotrophic receptors. J Biol Chem 277:17088–17094

    Article  CAS  PubMed  Google Scholar 

  • Yazaki N, Hosoi Y, Kawabata K, Miyake A, Minami M, Satoh M, Ohta M, Kawasaki T, Itoh N (1994) Differential expression patterns of mRNAs for members of the fibroblast growth factor receptor family, FGFR-1-FGFR-4, in rat brain. J Neurosci Res 37:445–452

    CAS  PubMed  Google Scholar 

  • Yenush L, White MF (1997) The IRS-signalling system during insulin and cytokine action. Bioessays 19:491–500

    CAS  PubMed  Google Scholar 

  • Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci U S A 98:5874–5879

    Article  CAS  PubMed  Google Scholar 

  • Zhan X, Plourde C, Hu X, Friesel R, Maciag T (1994) Association of fibroblast growth factor receptor-1 with c-Src correlates with association between c-Src and cortactin. J Biol Chem 269:20221–20224

    CAS  PubMed  Google Scholar 

  • Zhang Y, Tatsuno T, Carney JM, Mattson MP (1993) Basic FGF, NGF, and IGFs protect hippocampal and cortical neurons against iron-induced degeneration. J Cereb Blood Flow Metab 13:378–388

    PubMed  Google Scholar 

  • 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 control of vascular tone. Nat Med 4:201–207

    CAS  PubMed  Google Scholar 

  • Zhu X, Komiya H, Chirino A, Faham S, Fox GM, Arakawa T, Hsu BT, Rees DC (1991) Three-dimensional structures of acidic and basic fibroblast growth factors. Science 251:90–93

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bernhard Reuss.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reuss, B., von Bohlen und Halbach, O. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 313, 139–157 (2003). https://doi.org/10.1007/s00441-003-0756-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-003-0756-7

Keywords

Navigation