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Basic fibroblast growth factor-like immunoreactivity in the rat trigeminal sensory system and peri-oral skin with vibrissae

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Abstract

We have characterized an antiserum against basic fibroblast growth factor (bFGF) by immunoblot, investigated the location of bFGF-like immunoreactivity (bFGF-IR) in the trigeminal sensory system and perioral skin endowed with vibrissae, and demonstrated the site of bFGF mRNA expression in the vibrissae by in situ hybridization histochemistry. Light-microscopic immunohistochemistry has demonstrated that bFGF-IR is present not only in trigeminal ganglion neurons and their central and peripheral processes, but also in cells of the matrix, external root sheath and papillae of vibrissae and the stratum basale of the stratified squamous epithelium of the skin. Electron microscopy has revealed intense bFGF-IR mainly in cytoplasmic regions, other than the lumen of rough endoplasmic reticulum and the Golgi apparatus, in trigeminal ganglion neurons, in fibroblast-like cells in the papillae, and in capsules of vibrissae. In contrast, actively proliferating and/or differentiating cells in the matrix of vibrissae have intensely stained euchromatin and weakly labeled cytoplasm that, unlike that of the aforementioned cells, contain immunoreaction products in discrete spots less than 100 nm in diameter, implying the generation of different molecular forms of bFGF in cells of the matrix and papillae. Moreover, the accumulation of bFGF in the euchromatin appears to take place in cells at non-mitotic stages (possibly interphases), characterized by a conspicuous nucleolus and well-developed nuclear envelope. A digoxigenin-labeled cRNA probe for the demonstration of bFGF mRNA gives conspicuous hybridization signals mainly in the matrix of vibrissae. These findings suggest that bFGF is involved in the growth and differentiation of matrix cells during certain periods of the cell cycle and that it acts as a non-mitogenic mediator in the adult trigeminal sensory system.

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References

  • Anderson JE, Liu L, Kardami E (1991) Distinctive patterns of basic fibroblast growth factor (bFGF) distribution in degenerating and regenerating areas of dystrophic (mdx) striated miscles. Dev Biol 147:96–109

    Google Scholar 

  • Bähr M, Vanselow J, Thanos S (1989) Ability of adult rat ganglion cells to regrow axons in vitro can be influenced by fibroblast growth factor and gangliosides. Neurosci Lett 96:197–201

    Google Scholar 

  • Baldin V, Roman A-M, Bosc-Bierne I, Amalric F, Bouche G (1990) Translocation of bFGF to the nucleus is G1 phase cell cycle specific in bovine aortic endothelial cells. EMBO J 9:1511–1517

    Google Scholar 

  • Bashkin P, Doctrow S, Klagsbrun M, Svahn CM, Folkman J, Vlodavsky I (1989) Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparinase and heparin-like molecules. Biochemistry 28:1737–1743

    Google Scholar 

  • Bohlen P, Baird A, Esch F, Ling N, Gospodarowicz D (1984) Isolation and partial molecular characterization of pituitary fibroblast growth factor. Proc Natl Acad Sci USA 81:5364–5368

    Google Scholar 

  • Bouche G, Gas N, Prats H, Baldin V, Tauber J-P, Teissie J, Amalric F (1987) Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE cells undergoing G0-G1 transition. Proc Natl Acad Sci USA 84:6770–6774

    Google Scholar 

  • Desaki J, Matsuda S, Okumura N, Koyama Y, Sakanaka M (1992) Fine structure of nerve processes containing basic fibroblast growth factor in muscle spindles of the rat masseter muscle. Neurosci Lett 137:237–240

    Google Scholar 

  • DiMario J, Buffinger N, Yamada S, Strohman RC (1989) Fibroblast growth factor in the extracellular matrix of dystrophic (mdx) mouse muscle. Science 244:688–690

    Google Scholar 

  • Emoto N, Gonzalez A-M, 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

    Google Scholar 

  • Esch F, Baird A, Ling N, Ueno N, Hill F, Denoroy L, Klepper R, Gospodarowicz D, Bohlen P, Guillemin R (1985) Primary structure of bovine pituitary basic fibroblast growth factor (FGF) and comparison with the amino-terminal sequence of bovine acidic FGF. Proc Natl Acad Sci USA 82:6507–6511

    Google Scholar 

  • Ferguson IA, Johnson EM Jr (1991) Fibroblast growth factor receptor-bearing neurons in the CNS: identification by receptor-mediated retrograde transport. J Comp Neurol 313:693–706

    Google Scholar 

  • Ferguson IA, Schweitzer JB, Johnson EM Jr (1990) Basic fibroblast growth factor: receptor-mediated internalization, metabolism, and anterograde axonal transport in retinal ganglion cells. J Neurosci 10:2176–2189

    Google Scholar 

  • Ferrari G, Minozzi M-C, Toffano G, Leon A, Skaper SD (1989) Basic fibroblast growth factor promotes the survival and development of mesencephalic neurons in culture. Dev Biol 133:140–147

    Google Scholar 

  • Florkiewicz RZ, Baird A, Gonzalez A-M (1991) Multiple forms of bFGF: differential nuclear and cell surface localization. Growth Factors 4:265–275

    Google Scholar 

  • 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

    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-formix transection. J Neurosci 12:345–355

    Google Scholar 

  • Gonzalez A-M, Buscaglia M, Ong M, Baird A (1990) Distribution of basic fibroblast growth factor in the 18-day rat fetus: localization in the basement membranes of diverse tissues. J Cell Biol 110:753–765

    Google Scholar 

  • Gospodarowicz D, Cheng J, Lirette M (1983) Bovine brain and pituitary fibroblast growth factors; comparison of their abilities to support the proliferation of human and bovine vascular endothelial cells. J Cell Biol 97:1677–1685

    Google Scholar 

  • Gospodarowicz D, Cheng J, Lui G-M, Baird A, Bohlen P (1984) Isolation of brain fibroblast growth factor by heparin-Sepharose affinity chromatography: identity with pituitary fibroblast growth factor. Proc Natl Acad Sci USA 81:6963–6967

    Google Scholar 

  • Gospodarowicz D, Neufeld G, Schweigerer L (1986) Molecular and biological characterization of fibroblast growth factor, an angiogenic factor which also controls the proliferation and differentiation of mesoderm and neuroectoderm derived cells. Cell Differ 19:1–17

    Google Scholar 

  • Grothe C, Unsicker K (1989) Immunocytochemical loalization of basic fibroblast growth factor in bovine adrenal gland, ovary, and pituitary. J Histochem Cytochem 37:1877–1883

    Google Scholar 

  • Grothe C, Zachmann K, Unsicker K, Westermann R (1990) High molecular weight forms of basic fibroblast growth factor recognized by a new anti-bFGF antibody. FEBS Lett 260:35–38

    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

    Google Scholar 

  • Iwata H, Matsuyama A, Okumura N, Yoshida S, Lee Y, Imaizumi K, Shiosaka S (1991) Localization of basic FGF-like immunoreactivity in the hypothalamo-hypophyseal neuroendocrine axis. Brain Res 550:329–332

    Google Scholar 

  • Janet T, Miche M, Pettmann B, Labourdette G, Sensenbrenner M (1987) Ultrastructural localization of fibroblast growth factor in neurons of rat brain. Neurosci Lett 80:153–157

    Google Scholar 

  • Joseph-Silverstein J, Consigli SA, Lyser KM, Ver Pault C (1989) Basic fibroblast growth factor in the chick embryo: immunolocalization to striated muscle cells and their precursors. J Cell Biol 108:2459–2466

    Google Scholar 

  • Matsuda S, Desaki J, Okumura N, Shiosaka S, Imaoka S, Sakanaka M (1992a) Basic fibroblast growth factor-like immunoreactivity in the trigeminal proprioceptive and motor systems. Brain Res 577:92–100

    Google Scholar 

  • Matsuda S, Okumura N, Yoshimura H, Koyama Y and Sakanaka M (1992b) Basic fibroblast growth factor-like immunoreactivity in Purkinje cells of the rat cerebellum. Neuroscience 50:99–106

    Google Scholar 

  • McLean IW, Nakane PK (1974) Periodate-lysine-paraformaldehyde fixative: a new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083

    Google Scholar 

  • Moore GP, Du Cros DL, Ioaacs K, Pisansarakit P, Wynn PC (1991) Hair growth induction: roles of growth factors. Ann NY Acad Sci 642:308–325

    Google Scholar 

  • Morrison RS, Sharma A, De Vellis J, Bradshaw RA (1986) Basic fibroblast growth factor supports the survival of cerebral cortical neurons in primary culture. Proc Natl Acad Sci USA 83:7537–7541

    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

    Google Scholar 

  • Okumura N, Takimoto K, Okada M, Nakagawa H (1989) C6 glioma cells produce basic fibroblast growth factor that can stimulate their own proliferation. J Biochem 106:904–909

    Google Scholar 

  • Olwin BB, Hauschka SD (1986) Identification of the fibroblast growth factor receptor of Swiss 3T3 cells and mouse skeletal muscle myoblasts. Biochemistry 25:3492–3495

    Google Scholar 

  • Pettmann B, Janet T, Labourdette G, Sensenbrenner M, Manthorpe M, Varon S (1991) Biologically active basic fibroblast growth factor migrates at 27 KD in “non denaturing” SDS-polyacrylamide gel electrophoresis. Growth Factors 5:209–220

    Google Scholar 

  • 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. Mol Brain Res 11:71–77

    Google Scholar 

  • Rapraeger AC, Krufka A, Olwin BB (1991) Requirement of heparin sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252:1705–1707

    Google Scholar 

  • Rifkin DB, Moscatelli D (1989) Recent developments in the cell biology of basic fibroblast growth factor. J Cell Biol 109:1–6

    Google Scholar 

  • Ruoslahti E (1989) Proteoglycans in cell regulation. J Biol Chem 264:13369–13372

    Google Scholar 

  • Sakanaka M, Shibasaki T, Lederis K (1987) Improved fixation and cobalt-glucose oxidase-diaminobenzidine intensification for immunohistochemical demonstration of corticotropin-releasing factor in rat brain. J Histochem Cytochem 35:207–212

    Google Scholar 

  • Schubert D, Ling N, Baird A (1987) Multiple influences of a heparin-binding growth factor on neuronal development. J Cell Biol 104:635–643

    Google Scholar 

  • Somogyi P, Takagi H (1982) A note on the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry. Neuroscience 7:1779–1783

    Google Scholar 

  • Tessler S, Neufeld G (1990) Basic fibroblast growth factor accumulates in the nuclei of various bFGF-producing cell types. J Cell Physiol 145:310–317

    Google Scholar 

  • Towbin H, Staehelin T, Goudon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheet: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Unsicker K, Reichart-Preibsch H, Schmidt R, Pettmann B, Labourdette G, Sensenbrenner M (1987) Astroglial and fibroblast growth factors have neurotrophic functions for cultured peripheral and central nervous system neurons. Proc Natl Acad Sci USA 84:5459–5463

    Google Scholar 

  • Walicke PA (1988) Basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J Neurosci 8:2618–2627

    Google Scholar 

  • Walicke P, Cowan MW, Ueno N, Baird A, Guillemin R (1986) Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc Natl Acad Sci USA 83:3012–3016

    Google Scholar 

  • Weise B, Unsicker K, Grothe C (1992) Localization of basic fibroblast growth factor in a subpopulation of rat sensory neurons. Cell Tissue Res 267:125–130

    Google Scholar 

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Okada, K., Matsuda, S., Ii, Y. et al. Basic fibroblast growth factor-like immunoreactivity in the rat trigeminal sensory system and peri-oral skin with vibrissae. Cell Tissue Res 272, 417–427 (1993). https://doi.org/10.1007/BF00318548

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  • DOI: https://doi.org/10.1007/BF00318548

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