Download PDF
Thromb Haemost 1999; 82(02): 748-754
DOI: 10.1055/s-0037-1615907
Research Article
Schattauer GmbH

Fibroblast Growth Factor Prototype Release and Fibroblast Growth Factor Receptor Signaling

R. Friesel
1   Center for Molecular Medicine, Maine Medical Center Research Institute, South Portland, ME, USA
,
T. Maciag
1   Center for Molecular Medicine, Maine Medical Center Research Institute, South Portland, ME, USA
› Author Affiliations
Further Information

Publication History

Publication Date:
09 December 2017 (online)

Also available at
    Permissions and Reprints

 

 

  • References

  • 1 Szebenyi G, Fallon J. Fibroblast growth factors as multifunctional signaling factors. Int Rev Cytol 1999; 185: 45-106.
    PubMedSearch in Google Scholar
  • 2 Naski MC, Ornitz D. 1998. FGF Signaling in skeletal development. Frontiers in Bioscience 1998; 3: 781-794.
    CrossrefPubMedSearch in Google Scholar
  • 3 Webster MK, Donoghue DJ. 1997. Fgfr activation in skeletal disorders: too much of a good thing. Trends Genet 1997; 13: 178-182.
    CrossrefPubMedSearch in Google Scholar
  • 4 Coulier F, Pontarotti P, Roubin R, Hartung H, Goldfarb M, Birnbaum D. 1997. Of worms and men: An an evolutionary perspective on the fibroblast growth factor (FGF) and FGF receptor families. J.Mol Evol 1997; 44: 43-56.
    PubMedSearch in Google Scholar
  • 5 Friesel RE, Maciag T. 1995. Molecular mechanisms of angiogenesis: fibroblast growth factor signal transduction. FASEB J 1995; 9: 919-925.
    CrossrefPubMedSearch in Google Scholar
  • 6 Johnson DEE, Williams LT. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 1993; 60: 1-40.
    PubMedSearch in Google Scholar
  • 7 Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT. Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 1989; 245: 57-60.
    CrossrefPubMedSearch in Google Scholar
  • 8 Hou JZ, Kan MK, McKeehan K, McBride G, Adams P, McKeehan WL. Fibroblast growth factor receptors from liver vary in three structural domains. Science 1991; 251: 665-668.
    CrossrefPubMedSearch in Google Scholar
  • 9 Chellaiah AT, McEwen DG, Werner S, Xu J, Ornitz DM. 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 1994; 269: 11620-11627.
    PubMedSearch in Google Scholar
  • 10 Cheon HG, Larochelle WJ, Bottaro DP, Burgess WH, Aaronson SA. High affinity binding sites for related FGF ligands reside within different receptor Ig-like domains. Proc Natl Acad Sci USA 1994; 91: 989-993.
    CrossrefPubMedSearch in Google Scholar
  • 11 Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, Chan AML, Aaronson SA. Determination of ligand-binding specificity by alternative splicing - two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci USA 1992; 89: 246-250.
    CrossrefPubMedSearch in Google Scholar
  • 12 Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M. Receptor specificity of the fibroblast growth factor family. J Biol Chem 1996; 271: 15292-15297.
    CrossrefPubMedSearch in Google Scholar
  • 13 Johnson DE, Lee PL, Lu J, Williams LT. Diverse forms of a receptor for acidic and basic fibroblast growth factors. Mol Cell Biol 1990; 10: 4728-4736.
    CrossrefPubMedSearch in Google Scholar
  • 14 Wang F, Kan M, Yan G, Xu J, McKeehan WL. Alternately spliced NH2-terminal immunoglobulin-like loop I in the ectodomain of the fibroblast growth factor (FGF) receptor-1 lowers affinity for both heparin and FGF-1. J Biol Chem 1995; 270: 10231-10235.
    CrossrefPubMedSearch in Google Scholar
  • 15 Yan G, Fukabori Y, McBride GS, Nikolaropolous S, McKeehan WL. Exon switching and activation of stromal and embryonic fibroblast growth factor receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol Cell Biol 1993; 13: 4513-4522.
    CrossrefPubMedSearch in Google Scholar
  • 16 Luo Y, Lu W, Mohamedali KA, Jang JH, Jone RB, Gabriel JL, Kan M, McKeehan WL. The glycine box: a determinant of specificity for fibroblast growth factor. Biochemistry 1998; 37: 16506-16515.
    CrossrefPubMedSearch in Google Scholar
  • 17 Orr-Urtreger A., Givol D, Yayon A, Yarden Y, Lonai P. Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development 1991; 113: 1419-1434.
    PubMedSearch in Google Scholar
  • 18 Peters K, Ornitz D, Werner S, Williams L. Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev Biol 1993; 155: 423-430.
    CrossrefPubMedSearch in Google Scholar
  • 19 Wuechner C, Nordqvist AC, Winterpacht A, Zabel B, Schalling M. Developmental expression of splicing variants of fibroblast growth factor receptor 3 (fgfr3) in mouse. Int.J Dev Biol 1996; 40: 1185-1188.
    PubMedSearch in Google Scholar
  • 20 Stark KL, McMahon JA, McMahon AP. FGFR-4, a new member of the fibroblast growth factor receptor family, expressed in the definitive endoderm and skeletal muscle lineages of the mouse. Development 1991; 113: 641-651.
    PubMedSearch in Google Scholar
  • 21 Yamaguchi TP, Harpal K, Henkemeyer M, Rossant J. FGFR-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev 1994; 8: 3032-3044.
    CrossrefPubMedSearch in Google Scholar
  • 22 Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P. Murine FGFR-1 is required for early post-implantation growth and axial organization. Genes Dev 1994; 8: 3045-3057.
    CrossrefPubMedSearch in Google Scholar
  • 23 Arman E, Haffner-Krausz R, Chen Y, Heath J, Lonai P. Targeted disruption of fibroblast grorwth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA 1998; 95: 5082-5087.
    CrossrefPubMedSearch in Google Scholar
  • 24 Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 1996; 84: 911-921.
    CrossrefPubMedSearch in Google Scholar
  • 25 Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM. Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nature Genet 1996; 12: 390-397.
    CrossrefPubMedSearch in Google Scholar
  • 26 Weinstein M, Xu X, Ohyama K, C. Deng C. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 1998; 125: 3615-3623.
    PubMedSearch in Google Scholar
  • 27 Kouhara H., Hadari YR, Spivak-Kroizman T, Schilling J, Bar-Sagi D, Lax I, Schlessinger J. A lipid-anchored grb2-binding protein that links FGF-receptor activation to the ras/mapk signaling pathway. Cell 1997; 89: 693-702.
    CrossrefPubMedSearch in Google Scholar
  • 28 Wang JK, Xu H, Li H-C, Goldfarb M. Broadly expressed SNT-like proteins link FGF receptor stimulation to activators of Ras. Oncogene 1996; 13: 721-729.
    PubMedSearch in Google Scholar
  • 29 Burgess WH, Dionne CA, Kaplow J, Mudd R, Friesel R, Zilberstein A, Schlessinger J, Jaye M. 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 1990; 10: 4770-4777.
    CrossrefPubMedSearch in Google Scholar
  • 30 Tang TL, Freeman Jr RM, O’Reilly AM, Neel BG, Sokol SY. The SH2-containing protein-tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell 1995; 80: 473-483.
    CrossrefPubMedSearch in Google Scholar
  • 31 Hadari YR, Kouhara H, Lax I, Schlessinger J. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol Cell Biol 1998; 18: 3966-3973.
    CrossrefPubMedSearch in Google Scholar
  • 32 Klint P, Kanda S, Claesson-Welsh L. Shc and a novel 89-kDa component couple to the Grb2-Sos complex in fibroblast growth factor-2-stimulated cells. J Biol Chem 1995; 270: 23337-23344.
    CrossrefPubMedSearch in Google Scholar
  • 33 Wang JK, Gao G, Goldfarb M. Fibroblast growth factor receptors have different signaling and mitogenic potentials. Mol Cell Biol 1994; 14: 181-188.
    CrossrefPubMedSearch in Google Scholar
  • 34 Kanai M, Goke M, Tsunekawa S, Podolsky DK. Signal transduction pathway of human fibroblast growth factor receptor 3. J Biol Chem 1997; 272: 6621-6628.
    CrossrefPubMedSearch in Google Scholar
  • 35 LaVallee TM, Prudovsky IA, McMahon GA, Hu X, Maciag T. Activation of the MAP kinase pathway by FGF-1 correlates with cell proliferation induction while activation of the Src pathway correlates with migration. J Cell Biol 1998; 141: 1647-1658.
    CrossrefPubMedSearch in Google Scholar
  • 36 Mohammadi M., Dikic I, Sorokin A, Burgess WH, Jaye M, Schlessinger J. Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol Cell Biol 1996; 16: 977-989.
    CrossrefPubMedSearch in Google Scholar
  • 37 Mohammadi M, Honegger AM, Rotin D, Fischer R, Bellot F, Li W, Dionne CA, Jaye M, Rubinstein M, Schlessinger J. 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 1991; 11: 5068-5078.
    CrossrefPubMedSearch in Google Scholar
  • 38 Mohammadi M, Dionne CA, Li W, Li N, Spivak T, Honegger AM, M. Jaye M, Schlessinger J. Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature 1992; 358: 681-684.
    CrossrefPubMedSearch in Google Scholar
  • 39 Peters KG, Marie J, Wilson E, Ives HE, Escobedo J, Delrosario M, Mirda D, Williams LT. Point mutation of an FGF receptor abolishes phosphatidylinositol turnover and Ca2+ flux but not mitogenesis. Nature 1992; 358: 678-681.
    CrossrefPubMedSearch in Google Scholar
  • 40 Muslin AJ, Peters KG, Williams LT. Direct activation of phospholipase C-gamma by fibroblast growth factor receptor is not required for mesoderm induction in Xenopus animal caps. Mol Cell Biol 1994; 14: 3006-3012.
    CrossrefPubMedSearch in Google Scholar
  • 41 Spivak-Kroizman T, Mohammadi M, Hu P, Jaye M, Schlessinger J, Lax I. Point mutation in the fibroblast growth factor receptor eliminates phosphatidylinositol hydrolysis without affecting neuronal differentiation of PC12 cells. J Biol Chem 1994; 269: 14419-14423.
    PubMedSearch in Google Scholar
  • 42 Friesel R, Burgess WH, Maciag T. Heparin-binding growth factor 1 stimulates tyrosine phosphorylation in NIH 3T3 cells. Mol Cell Biol 1989; 9: 1857-1865.
    CrossrefPubMedSearch in Google Scholar
  • 43 Goh KC, Lim YP, Ong SH, Siak CB, Cao X, Tan YH, Guy GR. Identification of p90, a prominent tyrosine-phosphorylated protein in fibroblast growth factor-stimulated cells, as 80K-H. J Biol Chem 1996; 271: 5832-5838.
    CrossrefPubMedSearch in Google Scholar
  • 44 Xu H, Lee KW, Goldfarb M. Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J Biol Chem 1998; 273: 17987-17990.
    CrossrefPubMedSearch in Google Scholar
  • 45 Kremer NE, Darcangelo G, Thomas SM, Demarco M, Brugge JS, Halegoua S. Signal transduction by nerve growth factor and fibroblast growth factor in PC12 cells requires a sequence of src and ras actions. J Cell Biol 1991; 115: 809-819.
    CrossrefPubMedSearch in Google Scholar
  • 46 Zhan X, Hu X, Friesel R, Maciag T. Long term growth factor exposure and differential tyrosine phosphorylation are required for DNA synthesis in BALB/c 3T3 cells. J Biol Chem 1993; 268: 9611-9620.
    PubMedSearch in Google Scholar
  • 47 Weinstein DC, Marden J, Carnevali F, Hemmati-Brivanlou A. FGF-mediated mesoderm induction involves the Src-family kinase Laloo. Nature 1998; 394: 904-908.
    CrossrefPubMedSearch in Google Scholar
  • 48 Huang C, Liu J, Haudenschild CC, Zhan X. The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J Biol Chem 1998; 273: 25770-25776.
    CrossrefPubMedSearch in Google Scholar
  • 49 Mason I.J.. The ins and outs of fibroblast growth factors. Cell 1994; 78: 547-552.
    CrossrefPubMedSearch in Google Scholar
  • 50 Westermann R., Unsicker K. Basic fibroblast growth factor (bFGF) and rat C6 glioma cells: regulation of expression, absence of release, and response to exogenous bFGF. Glia 1990; 3: 510-521.
    CrossrefPubMedSearch in Google Scholar
  • 51 Acland P, Dixon M, Peters G, Dickson C. Subcellular fate of the int-2 oncoprotein is determined by choice of initiation codon. Nature 1990; 343: 662-665.
    CrossrefPubMedSearch in Google Scholar
  • 52 Prudovsky I, Savion N, Zhan X, Friesel R, Xu J, Hou J, Mckeehan WL, Maciag T. Intact and functional fibroblast growth factor (FGF) receptor-1 traffics near the nucleus in response to FGF-1. J Biol. Chem 1994; 269: 31720-31724.
    PubMedSearch in Google Scholar
  • 53 Prudovsky I., N. Savion N, T.M. LaVallee TM, and T, Maciag T. 1996. The nuclear trafficking of extracellular FGF-1 correlates with the perinuclear association of the FGFR-1α isoforms but not the FGFR-1β isoforms. J.Biol.Chem 1996; 271: 14198-14205.
    PubMedSearch in Google Scholar
  • 54 Stachowiak MK, Maher PA, Joy A, Mordechai E, Stachowiak EK. Nuclear accumulation of fibroblast growth factor receptors is regulated by multiple signals in adrenal medullary cells. Mol Biol Cell 1996; 7: 1299-1317.
    CrossrefPubMedSearch in Google Scholar
  • 55 Stachowiak EK, Maher PA, Tucholski J, Mordechai E, Joy A, Moffett J, Coons S, Stachowiak MK. Nuclear accumulation of fibroblast growth factor receptors in human glial cells-association with cell proliferation. Oncogene 1997; 14: 2201-2211.
    CrossrefPubMedSearch in Google Scholar
  • 56 Johnston C.L., H.C. Cox HC, J.J. Gomm JJ, R.C. Coombes RC. 1995. Fibroblast growth factor receptors (fgfrs) localize in different cellular compartments. J.Biol.Chem 1995; 270: 30643-30650.
    PubMedSearch in Google Scholar
  • 57 Neilson KM, Friesel RE. Constitutive activation of fibroblast growth factor receptor-2 by a point mutation associated with Crouzon syndrome. J Biol Chem 1995; 270: 26037-26040.
    CrossrefPubMedSearch in Google Scholar
  • 58 Neilson KM, Friesel R. Ligand-independent activation of fibroblast growth factor receptors by point mutations in the extracellular, transmembrane, and kinase domains. J Biol Chem 1996; 271: 25049-25057.
    CrossrefPubMedSearch in Google Scholar
  • 59 Naski MC, Wang Q, Xu J, Ornitz DM. Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nature Genet 1996; 13: 233-237.
    CrossrefPubMedSearch in Google Scholar
  • 60 Su WCS, Kitagawa M, Xue N, Xie B, Garofalo S, Cho J, Deng C, Horton WA, Fu X-Y. Activation of STAT 1 by mutant fibroblast growth-factor receptor in thanatophoric dysplasia type II dwarfism. Nature 1997; 386: 288-292.
    CrossrefPubMedSearch in Google Scholar
  • 61 Jackson A, Friedman S, Zhan X, Engleka KA, Forough R, Maciag T. Heat shock induces the release of fibroblast growth factor-1 from NIH-3T3 cells. Proc Natl Acad Sci USA 1992; 89: 10691-10695.
    CrossrefPubMedSearch in Google Scholar
  • 62 Jackson A, Tarantini F, Gamble S, Friedman S, Maciag T. The release of fibroblast growth factor-1 from NIH 3T3 cells in response to temperature involves the function of cysteine residues. J Biol Chem 1995; 270: 33-36.
    CrossrefPubMedSearch in Google Scholar
  • 63 Mignatti P, Morimoto T, Rifkin DB. 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 1992; 151: 81-93.
    CrossrefPubMedSearch in Google Scholar
  • 64 Tarantini F, Gamble S, Jackson A, Maciag T. The cysteine residue responsible for the release of fibroblast growth factor-1 resides in a domain independent of the domain for phosphatidylserine binding. J Biol Chem 1995; 270: 29039-29042.
    CrossrefPubMedSearch in Google Scholar
  • 65 Shi J, Friedman S, Maciag T. The carboxy-terminal half of FGF-1 is involved in the regulation of FGF-1 secretion in response to heat shock. J Biol Chem 1997; 272: 1142-1147
    CrossrefPubMedSearch in Google Scholar
  • 66 Perin MS, Johnston PA, Ozcelik T, Jahn R, Francke U, Sudhof T. Structural and functional conservation of synaptotagmin in Drosophila and humans. J Biol Chem 1991; 266: 615-622.
    PubMedSearch in Google Scholar
  • 67 Zhang JZ, Davletov BA, Sudhof TC, Anderson RGW. 1994. Synaptotagmin I is a high affinity receptor for clathrin AP-2: Implications for membrane recycling. Cell 1994; 78: 751-760.
    CrossrefPubMedSearch in Google Scholar
  • 68 Tarantini F, LaVallee T, Jackson A, Gamble S, Mouta Carreira C, Garfinkel S, Burgess WH, Maciag T. The extravesicular domain of synaptotagmin-1 is released with the latent fibroblast growth factor-1 homodimer in response to heat shock. J Biol Chem 1998; 273: 22209-22216.
    CrossrefPubMedSearch in Google Scholar
  • 69 Perin MS, Fried VA, Mignery GA, Jahn R, Sudhof TC. Phospholipid-binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 1990; 345: 260-263.
    CrossrefPubMedSearch in Google Scholar
  • 70 Mach H, Middaugh CR. Interaction of partially structured states of acidic fibroblast growth factor with phospholipid membranes. Biochemistry 1995; 34: 9913-9920.
    CrossrefPubMedSearch in Google Scholar
  • 71 Chapman ER, Davis AF. Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. J Biol Chem 1998; 273: 13995-14001.
    CrossrefPubMedSearch in Google Scholar
  • 72 LaVallee T, Tarantini F, Gamble S, Mouta Carreira C, Jackson A, Maciag T. Synaptotagmin-1 is required for Fibroblast Growth Factor-1 release. J Biol Chem 1998; 273: 22217-22223.
    CrossrefPubMedSearch in Google Scholar
  • 73 Kassam G, Le BH, Choi K, Kang H, Fitzpatrick S, Louie P, Waisman D. The p11 subunit of the annexin II tetramer plays a key role in the stimulation of t-PA-dependent plasminogen activation. Biochemistry 1998; 37: 16958-16966.
    CrossrefPubMedSearch in Google Scholar
  • 74 Oyama Y, Shishibori T, Yamashita K, Naya T, Nakagiri S, Maeta H, Kobayashi R. Two distinct anti-allergic drugs, amlexanox and cromolyn, bind to the same kinds of calcium-binding proteins, except calmodulin, in bovine lung extract. Biochem Biophys Res Commun 1997; 240: 341-347.
    CrossrefPubMedSearch in Google Scholar
  • 75 Mouta Carreira C, LaVallee T, Tarrantini F, Jackson A, Tait Lathrop J, Hampton B, Burgess WH, Maciag T. S100A13 is involved in the regulation of fibroblast growth factor-1 and p40 synaptotagmin-1 release in vitro. J Biol Chem 1998; 273: 22224-22231.
    CrossrefPubMedSearch in Google Scholar
  • 76 Schafer BW, Heizman CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. TIBS 1996; 21 PII, S0968-0004 134-140.
    PubMedSearch in Google Scholar
  • 77 Rammes A., Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C. Myeloid-related protein (mrp) 8 and MRP14, calcium-binding proteins of the s100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem 1997; 272: 9496-9502.
    CrossrefPubMedSearch in Google Scholar
  • 78 Hajjar KA, Guevara CA, Lev E, Dowling K, Chacko J. Interaction of the fibrinolyctic receptor, annexin II, with the endothelial cell surface. Essential role of endonexin repeat 2. J Biol Chem 1996; 271: 21652-21659.
    CrossrefPubMedSearch in Google Scholar
  • 79 Zhao J, Zhou Q, Wiedmer T, Sims PJ. Level of expression of phospholipid scramblase regulates induced movement of phosphatidylserine to the cell surface. J Biol Chem 1998; 273: 6603-6606.
    CrossrefPubMedSearch in Google Scholar