Table of Contents
Journal of Signal Transduction
Volume 2014 (2014), Article ID 962962, 16 pages
http://dx.doi.org/10.1155/2014/962962
Review Article

A Network Map of FGF-1/FGFR Signaling System

1Institute of Bioinformatics, International Tech Park, Bangalore 560066, India
2Centre of Excellence in Bioinformatics, School of Life Sciences, Pondicherry University, Puducherry 605014, India
3Department of Studies in Biotechnology, University of Mysore, Manasagangotri, Mysore 570006, India
4Institute of Molecular Medicine, National Tsing Hua University, Hsinchu 30013, Taiwan
5McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
6Department of Biological Chemistry, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
7Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
8Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA

Received 20 November 2013; Accepted 3 March 2014; Published 16 April 2014

Academic Editor: Shoukat Dedhar

Copyright © 2014 Rajesh Raju et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. J. Harmer, “Insights into the role of heparan sulphate in fibroblast growth factor signalling,” Biochemical Society Transactions, vol. 34, no. 3, pp. 442–445, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. O. A. Ibrahimi, F. Zhang, S. C. L. Hrstka, M. Mohammadi, and R. J. Linhardt, “Kinetic model for FGF, FGFR, and proteoglycan signal transduction complex assembly,” Biochemistry, vol. 43, no. 16, pp. 4724–4730, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. D. M. Ornitz, A. B. Herr, M. Nilsson, J. Westman, C.-M. Svahn, and G. Waksman, “FGF binding and FGF receptor activation by synthetic heparan-derived di- and trisaccharides,” Science, vol. 268, no. 5209, pp. 432–436, 1995. View at Google Scholar · View at Scopus
  4. M. W. Pantoliano, “Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization,” Biochemistry, vol. 33, no. 34, pp. 10229–10248, 1994. View at Google Scholar · View at Scopus
  5. D. M. Ornitz and P. Leder, “Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3,” The Journal of Biological Chemistry, vol. 267, no. 23, pp. 16305–16311, 1992. View at Google Scholar · View at Scopus
  6. D. M. Ornitz, A. Yayon, J. G. Flanagan, C. M. Svahn, E. Levi, and P. Leder, “Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells,” Molecular and Cellular Biology, vol. 12, no. 1, pp. 240–247, 1992. View at Google Scholar · View at Scopus
  7. A. Yayon, M. Klagsbrun, J. D. Esko, P. Leder, and D. M. Ornitz, “Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor,” Cell, vol. 64, no. 4, pp. 841–848, 1991. View at Google Scholar · View at Scopus
  8. O. Saksela, D. Moscatelli, A. Sommer, and D. B. Rifkin, “Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation,” Journal of Cell Biology, vol. 107, no. 2, pp. 743–751, 1988. View at Google Scholar · View at Scopus
  9. D. Gospodarowicz and J. Cheng, “Heparin protects basic and acidic FGF from inactivation,” Journal of Cellular Physiology, vol. 128, no. 3, pp. 475–484, 1986. View at Google Scholar · View at Scopus
  10. N. Itoh and D. M. Ornitz, “Evolution of the Fgf and Fgfr gene families,” Trends in Genetics, vol. 20, no. 11, pp. 563–569, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Beenken and M. Mohammadi, “The FGF family: biology, pathophysiology and therapy,” Nature Reviews Drug Discovery, vol. 8, no. 3, pp. 235–253, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. J. S. Colvin, A. C. white, S. J. Pratt, and D. M. Ornitz, “Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme,” Development, vol. 128, no. 11, pp. 2095–2106, 2001. View at Google Scholar · View at Scopus
  13. J. S. Colvin, R. P. Green, J. Schmahl, B. Capel, and D. M. Ornitz, “Male-to-female sex reversal in mice lacking fibroblast growth factor 9,” Cell, vol. 104, no. 6, pp. 875–889, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Tekin, B. Ö. Hişmi, S. Fitoz et al., “Homozygous mutations in fibroblast growth factor 3 are associated with a new form of syndromic deafness characterized by inner ear agenesis, microtia, and microdontia,” American Journal of Human Genetics, vol. 80, no. 2, pp. 338–344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Usui, M. Shibayama, N. Ohbayashi, M. Konishi, S. Takada, and N. Itoh, “Fgf18 is required for embryonic lung alveolar development,” Biochemical and Biophysical Research Communications, vol. 322, no. 3, pp. 887–892, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Ohbayashi, M. Shibayama, Y. Kurotaki et al., “FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis,” Genes and Development, vol. 16, no. 7, pp. 870–879, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Liu, J. Xu, J. S. Colvin, and D. M. Ornitz, “Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18,” Genes and Development, vol. 16, no. 7, pp. 859–869, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Itoh and D. M. Ornitz, “Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease,” Journal of Biochemistry, vol. 149, no. 2, pp. 121–130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Werner, K. G. Peters, M. T. Longaker, F. Fuller-Pace, M. J. Banda, and L. T. Williams, “Large induction of keratinocyte growth factor expression in the dermis during wound healing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 15, pp. 6896–6900, 1992. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Rieck, M. Assouline, M. Savoldelli et al., “Recombinant human basic fibroblast growth factor (Rh-bFGF) in three different wound models in rabbits: corneal wound healing effect and pharmacology,” Experimental Eye Research, vol. 54, no. 6, pp. 987–998, 1992. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Slavin, “Fibroblast growth factors: at the heart of angiogenesis,” Cell Biology International, vol. 19, no. 5, pp. 431–444, 1995. View at Publisher · View at Google Scholar · View at Scopus
  22. W. A. Hossain and D. K. Morest, “Fibroblast growth factors (FGF-1, FGF-2) promote migration and neurite growth of mouse cochlear ganglion cells in vitro: immunohistochemistry and antibody perturbation,” Journal of Neuroscience Research, vol. 62, no. 1, pp. 40–55, 2000. View at Google Scholar
  23. S. Tanaka, T. Kunath, A.-K. Hadjantonakis, A. Nagy, and J. Rossant, “Promotion to trophoblast stem cell proliferation by FGF4,” Science, vol. 282, no. 5396, pp. 2072–2075, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. S. E. Webb, K. K. Lee, M. K. Tang et al., “Fibroblast growth factors 2 and 4 stimulate migration of mouse embryonic limb myogenic cells,” Developmental Dynamics, vol. 209, no. 2, pp. 206–216, 1997. View at Google Scholar
  25. S. Werner, W. Weinberg, X. Liao et al., “Targeted expression of a dominant-negative FGF receptor mutant in the epidermis of transgenic mice reveals a role of FGF in keratinocyte organization and differentiation,” EMBO Journal, vol. 12, no. 7, pp. 2635–2643, 1993. View at Google Scholar · View at Scopus
  26. M. Murphy, J. Drago, and P. F. Bartlett, “Fibroblast growth factor stimulates the proliferation and differentiation of neural precursor cells in vitro,” Journal of Neuroscience Research, vol. 25, no. 4, pp. 463–475, 1990. View at Google Scholar · View at Scopus
  27. N. Turner and R. Grose, “Fibroblast growth factor signalling: from development to cancer,” Nature Reviews Cancer, vol. 10, no. 2, pp. 116–129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Gospodarowicz, “Localisation of a fibroblast growth factor and its effect along and with hydrocortisone on 3T3 cell growth,” Nature, vol. 249, no. 5453, pp. 123–127, 1974. View at Google Scholar · View at Scopus
  29. H. A. Armelin, “Pituitary extracts and steroid hormones in the control of 3T3 cell growth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 70, no. 9, pp. 2702–2706, 1973. View at Google Scholar · View at Scopus
  30. C. M. Carreira, M. Landriscina, S. Bellum, I. Prudovsky, and T. Maciag, “The comparative release of FGF1 by hypoxia and temperature stress,” Growth Factors, vol. 18, no. 4, pp. 277–285, 2001. View at Google Scholar · View at Scopus
  31. A. Jackson, S. Friedman, X. Zhan, K. A. Engleka, R. Forough, and T. Maciag, “Heat shock induces the release of fibroblast growth factor 1 from NIH 3T3 cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 22, pp. 10691–10695, 1992. View at Publisher · View at Google Scholar · View at Scopus
  32. J. T. Shin, S. R. Opalenik, J. N. Wehby et al., “Serum-starvation induces the extracellular appearance of FGF-1,” Biochimica et Biophysica Acta, Molecular Cell Research, vol. 1312, no. 1, pp. 27–38, 1996. View at Publisher · View at Google Scholar · View at Scopus
  33. N. M. Ananyeva, A. V. Tjurmin, J. A. Berliner et al., “Oxidized LDL mediates the release of fibroblast growth factor-1,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 3, pp. 445–453, 1997. View at Publisher · View at Google Scholar
  34. S. K. Mohan, S. G. Rani, S. M. Kumar, and C. Yu, “S100A13-C2A binary complex structure-a key component in the acidic fibroblast growth factor for the non-classical pathway,” Biochemical and Biophysical Research Communications, vol. 380, no. 3, pp. 514–519, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Landriscina, C. Bagalá, A. Mandinova et al., “Copper induces the assembly of a multiprotein aggregate implicated in the release of fibroblast growth factor 1 in response to stress,” The Journal of Biological Chemistry, vol. 276, no. 27, pp. 25549–25557, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. C. M. Carreira, T. M. LaVallee, F. Tarantini et al., “S100A13 is involved in the regulation of fibroblast growth factor-1 and p40 synaptotagmin-1 release in vitro,” The Journal of Biological Chemistry, vol. 273, no. 35, pp. 22224–22231, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Tarantini, T. Lavallee, A. Jackson et al., “The extravesicular domain of synaptotagmin-1 is released with the latent fibroblast growth factor-1 homodimer in response to heat shock,” The Journal of Biological Chemistry, vol. 273, no. 35, pp. 22209–22216, 1998. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Uriel, E. M. Brey, and H. P. Greisler, “Sustained low levels of fibroblast growth factor-1 promote persistent microvascular network formation,” American Journal of Surgery, vol. 192, no. 5, pp. 604–609, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Iwakura, M. Fujita, M. Ikemoto et al., “Myocardial ischemia enhances the expression of acidic fibroblast growth factor in human pericardial fluid,” Heart and Vessels, vol. 15, no. 3, pp. 112–116, 2000. View at Google Scholar · View at Scopus
  40. P. Cuevas, D. Reimers, F. Carceller et al., “Fibroblast growth factor-1 prevents myocardial apoptosis triggered by ischemia reperfusion injury,” European Journal of Medical Research, vol. 2, no. 11, pp. 465–468, 1997. View at Google Scholar · View at Scopus
  41. J.-C. Wu, W.-C. Huang, Y.-A. Tsai, Y.-C. Chen, and H. Cheng, “Nerve repair using acidic fibroblast growth factor in human cervical spinal cord injury: a preliminary Phase I clinical study,” Journal of Neurosurgery: Spine, vol. 8, no. 3, pp. 208–214, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. X. Xia, J. P. Babcock, S. I. Blaber et al., “Pharmacokinetic properties of 2nd-generation fibroblast growth factor-1 mutants for therapeutic application,” PLoS ONE, vol. 7, no. 11, Article ID e48210, 2012. View at Publisher · View at Google Scholar
  43. J. Belch, W. R. Hiatt, I. Baumgartner et al., “Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia,” The Lancet, vol. 377, no. 9781, pp. 1929–1937, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. A. J. Comerota, R. C. Throm, K. A. Miller et al., “Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: preliminary results of a phase I trial,” Journal of Vascular Surgery, vol. 35, no. 5, pp. 930–936, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Birrer, “Whole genome oligonucleotide-based array comparative genomic hybridization analysis identified fibroblast growth factor 1 as a prognostic marker for advanced-stage serous ovarian adenocarcinomas,” Journal of Clinical Oncology, vol. 25, no. 21, p. 3184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Kwabi-Addo, M. Ozen, and M. Ittmann, “The role of fibroblast growth factors and their receptors in prostate cancer,” Endocrine-Related Cancer, vol. 11, no. 4, pp. 709–724, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. V. P. Eswarakumar, I. Lax, and J. Schlessinger, “Cellular signaling by fibroblast growth factor receptors,” Cytokine and Growth Factor Reviews, vol. 16, no. 2, pp. 139–149, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. D. M. Ornitz and N. Itoh, “Fibroblast growth factors,” Genome Biology, vol. 2, no. 3, article 3005, 2001. View at Google Scholar · View at Scopus
  49. M. Bhattacharjee, R. Raju, A. Radhakrishnan et al., “A bioinformatics resource for TWEAK-Fn14 signaling pathway,” Journal of Signal Transduction, vol. 2012, Article ID 376470, 10 pages, 2012. View at Publisher · View at Google Scholar
  50. D. Telikicherla, A. Ambekar, S. Palapetta et al., “A comprehensive curated resource for follicle stimulating hormone signaling,” BMC Research Notes, vol. 4, article 408, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Kandasamy, S. Sujatha Mohan, R. Raju et al., “NetPath: A public resource of curated signal transduction pathways,” Genome Biology, vol. 11, no. 1, article r3, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Raju, V. Nanjappa, L. Balakrishnan et al., “NetSlim: high-confidence curated signaling maps,” The Journal of Biological Databases and Curation, vol. 2011, p. bar032, 2011. View at Google Scholar · View at Scopus
  53. M. Manuvakhova, J. V. Thottassery, S. Hays et al., “Expression of the SNT-1/FRS2 phosphotyrosine binding domain inhibits activation of MAP kinase and PI3-kinase pathways and antiestrogen resistant growth induced by FGF-1 in human breast carcinoma cells,” Oncogene, vol. 25, no. 44, pp. 6003–6014, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. S. H. Ong, Y. R. Hadari, N. Gotoh, G. R. Guy, J. Schlessinger, and I. Lax, “Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 11, pp. 6074–6079, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. R. Hadari, H. Kouhara, I. Lax, and J. Schlessinger, “Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation,” Molecular and Cellular Biology, vol. 18, no. 7, pp. 3966–3973, 1998. View at Google Scholar · View at Scopus
  56. H. Kouhara, Y. R. Hadari, T. Spivak-Kroizman et al., “A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway,” Cell, vol. 89, no. 5, pp. 693–702, 1997. View at Google Scholar · View at Scopus
  57. M. Kanai, M. Göke, S. Tsunekawa, and D. K. Podolsky, “Signal transduction pathway of human fibroblast growth factor receptor 3. Identification of a novel 66-kDa phosphoprotein,” The Journal of Biological Chemistry, vol. 272, no. 10, pp. 6621–6628, 1997. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. R. Hadari, H. Kouhara, I. Lax, and J. Schlessinger, “Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation,” Molecular and Cellular Biology, vol. 18, no. 7, pp. 3966–3973, 1998. View at Google Scholar · View at Scopus
  59. W.-F. Lin, C.-J. Chen, Y.-J. Chang, S.-L. Chen, I.-M. Chiu, and L. Chen, “SH2B1β enhances fibroblast growth factor 1 (FGF1)-induced neurite outgrowth through MEK-ERK1/2-STAT3-Egr1 pathway,” Cellular Signalling, vol. 21, no. 7, pp. 1060–1072, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Mohammadi, I. Dikic, A. Sorokin, W. H. Burgess, M. Jaye, and J. Schlessinger, “Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction,” Molecular and Cellular Biology, vol. 16, no. 3, pp. 977–989, 1996. View at Google Scholar · View at Scopus
  61. A. Willems-Widyastuti, B. M. Vanaudenaerde, R. Vos et al., “Azithromycin attenuates fibroblast growth factors induced vascular endothelial growth factor Via p38MAPK signaling in human airway smooth muscle cells,” Cell Biochemistry and Biophysics, vol. 67, no. 2, pp. 331–339, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Nishida, J.-I. Ito, Y. Nagayasu, and S. Yokoyama, “FGF-1-induced reactions for biogenesis of apoE-HDL are mediated by Src in rat astrocytes,” Journal of Biochemistry, vol. 146, no. 6, pp. 881–886, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. C. W. Chen, C. S. Liu, I. M. Chiu et al., “The signals of FGFs on the neurogenesis of embryonic stem cells,” Journal of Biomedical Science, vol. 17, p. 33, 2010. View at Publisher · View at Google Scholar
  64. G. Lungu, L. Covaleda, O. Mendes, H. Martini-Stoica, and G. Stoica, “FGF-1-induced matrix metalloproteinase-9 expression in breast cancer cells is mediated by increased activities of NF-kappa;B and activating protein-1,” Molecular Carcinogenesis, vol. 47, no. 6, pp. 424–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. F. S. Newell, H. Su, H. Tornqvist, J. P. Whitehead, J. B. Prins, and L. J. Hutley, “Characterization of the transcriptional and functional effects of fibroblast growth factor-1 on human preadipocyte differentiation,” The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, vol. 20, no. 14, pp. 2615–2617, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. D. R. Newman, C.-M. Li, R. Simmons, J. Khosla, and P. L. Sannes, “Heparin affects signaling pathways stimulated by fibroblast growth factor-1 and -2 in type II cells,” American Journal of Physiology, Lung Cellular and Molecular Physiology, vol. 287, no. 1, pp. L191–L200, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Buehlera, A. Martirea, C. Strohma et al., “Angiogenesis-independent cardioprotection in FGF-1 transgenic mice,” Cardiovascular Research, vol. 55, no. 4, pp. 768–777, 2002. View at Publisher · View at Google Scholar
  68. C. A. Castaneda, H. Cortes-Funes, H. L. Gomez, and E. M. Ciruelos, “The phosphatidyl inositol 3-kinase/AKT signaling pathway in breast cancer,” Cancer Metastasis Reviews, vol. 29, no. 4, pp. 751–759, 2010. View at Google Scholar · View at Scopus
  69. J.-I. Ito, Y. Nagayasu, K. Okumura-Noji et al., “Mechanism for FGF-1 to regulate biogenesis of apoE-HDL in astrocytes,” Journal of Lipid Research, vol. 48, no. 9, pp. 2020–2027, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Forough, B. Weylie, C. Patel, S. Ambrus, U. S. Singh, and J. Zhu, “Role of AKT/PKB signaling in fibroblast growth factor-1 (FGF-1)-induced angiogenesis in the chicken chorioallantoic membrane (CAM),” Journal of Cellular Biochemistry, vol. 94, no. 1, pp. 109–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Wang, T. Ito, N. Udaka, K. Okudela, T. Yazawa, and H. Kitamura, “PI3K-AKT pathway mediates growth and survival signals during development of fetal mouse lung,” Tissue and Cell, vol. 37, no. 1, pp. 25–35, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. W.-F. Lin, C.-J. Chen, Y.-J. Chang, S.-L. Chen, I.-M. Chiu, and L. Chen, “SH2B1β enhances fibroblast growth factor 1 (FGF1)-induced neurite outgrowth through MEK-ERK1/2-STAT3-Egr1 pathway,” Cellular Signalling, vol. 21, no. 7, pp. 1060–1072, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. M. A. Hossain, J. C. Russell, R. Gomes, and J. Laterra, “Neuroprotection by scatter factor/hepatocyte growth factor and FGF-1 in cerebellar granule neurons is phosphatidylinositol 3-kinase/Akt-dependent and MAPK/CREB-independent,” Journal of Neurochemistry, vol. 81, no. 2, pp. 365–378, 2002. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Li, S. Oparil, W. Feng, and Y.-F. Chen, “Hypoxia-responsive growth factors upregulate periostin and osteopontin expression via distinct signaling pathways in rat pulmonary arterial smooth muscle cells,” Journal of Applied Physiology, vol. 97, no. 4, pp. 1550–1558, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Raucci, E. Laplantine, A. Mansukhani, and C. Basilico, “Activation of the ERK1/2 and p38 mitogen-activated protein kinase pathways mediates fibroblast growth factor-induced growth arrest of chondrocytes,” The Journal of Biological Chemistry, vol. 279, no. 3, pp. 1747–1756, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Jiao, J. S. Greendorfer, P. Zhang, K. R. Zinn, C. A. Diglio, and J. A. Thompson, “Alternatively spliced FGFR-1 isoform signaling differentially modulates endothelial cell responses to peroxynitrite,” Archives of Biochemistry and Biophysics, vol. 410, no. 2, pp. 187–200, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. P. B. Mehta, C. N. Robson, D. E. Neal, and H. Y. Leung, “Keratinocyte growth factor activates p38 MAPK to induce stress fibre formation in human prostate DU145 cells,” Oncogene, vol. 20, no. 38, pp. 5359–5365, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. J. Chang, K. W. Chen, C. J. Chen et al., “SH2B1β interacts with STAT3 and enhances fibroblast growth factor 1-induced gene expression during neuronal differentiation,” Molecular and Cellular Biology, vol. 34, no. 6, pp. 1003–1019, 2014. View at Google Scholar
  79. A. A. Dudka, S. M. M. Sweet, and J. K. Heath, “Signal transducers and activators of transcription-3 binding to the fibroblast growth factor receptor is activated by receptor amplification,” Cancer Research, vol. 70, no. 8, pp. 3391–3401, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. W.-F. Lin, C.-J. Chen, Y.-J. Chang, S.-L. Chen, I.-M. Chiu, and L. Chen, “SH2B1β enhances fibroblast growth factor 1 (FGF1)-induced neurite outgrowth through MEK-ERK1/2-STAT3-Egr1 pathway,” Cellular Signalling, vol. 21, no. 7, pp. 1060–1072, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Lungu, L. Covaleda, O. Mendes, H. Martini-Stoica, and G. Stoica, “FGF-1-induced matrix metalloproteinase-9 expression in breast cancer cells is mediated by increased activities of NF-kappa;B and activating protein-1,” Molecular Carcinogenesis, vol. 47, no. 6, pp. 424–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. X. Zhu, J. Sasse, D. McAllister et al., “Evidence that fibroblast growth factors 1 and 4 participate in regulation of cardiogenesis,” Developmental Dynamics, vol. 207, no. 4, pp. 429–438, 1996. View at Google Scholar
  83. X. Qu, K. Hertzler, Y. Pan, K. Grobe, M. L. Robinson, and X. Zhang, “Genetic epistasis between heparan sulfate and FGF-Ras signaling controls lens development,” Developmental Biology, vol. 355, no. 1, pp. 12–20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. A. E. Serls, S. Doherty, P. Parvatiyar, J. M. Wells, and G. H. Deutsch, “Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung,” Development, vol. 132, no. 1, pp. 35–47, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. D. Lebeche, S. Malpel, and W. V. Cardoso, “Fibroblast growth factor interactions in the developing lung,” Mechanisms of Development, vol. 86, no. 1-2, pp. 125–136, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Jung, M. Zheng, M. Goldfarb, and K. S. Zaret, “Initiation of mammalian liver development from endoderm by fibroblast growth factors,” Science, vol. 284, no. 5422, pp. 1998–2003, 1999. View at Publisher · View at Google Scholar · View at Scopus
  87. X. Luo, L. J. Hutley, J. A. Webster et al., “Identification of BMP and activin membrane-bound inhibitor (BAMBI) as a potent negative regulator of adipogenesis and modulator of autocrine/paracrine adipogenic factors,” Diabetes, vol. 61, no. 1, pp. 124–136, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. L. Hutley, W. Shurety, F. Newell et al., “Fibroblast growth factor 1: a key regulator of human adipogenesis,” Diabetes, vol. 53, no. 12, pp. 3097–3106, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Tran, V. Kolupaeva, and C. Basilico, “FGF inhibits the activity of the cyclin B1/CDK1 kinase to induce a transient G2 arrest in RCS chondrocytes,” Cell Cycle, vol. 9, no. 21, pp. 4379–4386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. V. Kolupaeva, E. Laplantine, and C. Basilico, “PP2A-mediated dephosphorylation of p107 plays a critical role in chondrocyte cell cycle arrest by FGF,” PLoS ONE, vol. 3, no. 10, Article ID e3447, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. R. Priore, L. Dailey, and C. Basilico, “Downregulation of Akt activity contributes to the growth arrest induced by FGF in chondrocytes,” Journal of Cellular Physiology, vol. 207, no. 3, pp. 800–808, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. L. Dailey, E. Laplantine, R. Priore, and C. Basilico, “A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation,” Journal of Cell Biology, vol. 161, no. 6, pp. 1053–1066, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. P. Zhang, J. S. Greendorfer, J. Jiao, S. C. Kelpke, and J. A. Thompson, “Alternatively spliced FGFR-1 isoforms differentially modulate endothelial cell activation of c-YES,” Archives of Biochemistry and Biophysics, vol. 450, no. 1, pp. 50–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  94. B. Fernandez, A. Buehler, S. Wolfram et al., “Transgenic myocardial overexpression of fibroblast growth factor-1 increases coronary artery density and branching,” Circulation Research, vol. 87, no. 3, pp. 207–213, 2000. View at Google Scholar · View at Scopus
  95. B. Schumacher, P. Peecher, B. U. Von Specht, and T. Stegmann, “Induction of neoangiogenesis in ischemic myocardium by human growth factors: first clinical results of a new treatment of coronary heart disease,” Circulation, vol. 97, no. 7, pp. 645–650, 1998. View at Google Scholar · View at Scopus
  96. J.-I. Ito, Y. Nagayasu, R. Lu, A. Kheirollah, M. Hayashi, and S. Yokoyama, “Astrocytes produce and secrete FGF-1, which promotes the production of apoE-HDL in a manner of autocrine action,” Journal of Lipid Research, vol. 46, no. 4, pp. 679–686, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. L. Sun, L. Xu, H. Chang et al., “Transfection with aFGF cDNA improves wound healing,” Journal of Investigative Dermatology, vol. 108, no. 3, pp. 313–318, 1997. View at Google Scholar · View at Scopus
  98. U. Pirvola, Y. Cao, C. Oellig, Z. Suoqiang, R. F. Pettersson, and J. Ylikoski, “The site of action of neuronal acidic fibroblast growth factor is the organ of corti of the rat cochlea,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 20, pp. 9269–9273, 1995. View at Publisher · View at Google Scholar · View at Scopus
  99. M. Palmen, M. J. A. P. Daemen, L. J. De Windt et al., “Fibroblast growth factor-1 improves cardiac functional recovery and enhances cell survival after ischemia and reperfusion: a fibroblast growth factor receptor, protein kinase C, and tyrosine kinase-dependent mechanism,” Journal of the American College of Cardiology, vol. 44, no. 5, pp. 1113–1123, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. A. Buehler, A. Martire, C. Strohm et al., “Angiogenesis-independent cardioprotection in FGF-1 transgenic mice,” Cardiovascular Research, vol. 55, no. 4, pp. 768–777, 2002. View at Publisher · View at Google Scholar · View at Scopus
  101. P. Htun, W. D. Ito, I. E. Hoefer, J. Schaper, and W. Schaper, “Intramyocardial infusion of FGF-1 mimics ischemic preconditioning in pig myocardium,” Journal of Molecular and Cellular Cardiology, vol. 30, no. 4, pp. 867–877, 1998. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Hashimoto, Y. Sagara, D. Langford et al., “Fibroblast growth factor 1 regulates signaling via the glycogen synthase kinase-3β pathway. Implications for neuroprotection,” The Journal of Biological Chemistry, vol. 277, no. 36, pp. 32985–32991, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. J. Taeger, C. Moser, C. Hellerbrand et al., “Targeting FGFR/PDGFR/VEGFR impairs tumor growth, angiogenesis, and metastasis by effects on tumor cells, endothelial cells, and pericytes in pancreatic cancer,” Molecular Cancer Therapeutics, vol. 10, no. 11, pp. 2157–2167, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. E. M. Haugsten, M. Zakrzewska, A. Brech et al., “Clathrin- and dynamin-independent endocytosis of fgfr3—implications for signalling,” PLoS ONE, vol. 6, no. 7, Article ID e21708, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. C. Bonneton, J. B. Sibarita, and J. P. Thiery, “Relationship between cell migration and cell cycle during the initiation of epithelial to fibroblastoid transition,” Cell Motility and the Cytoskeleton, vol. 43, no. 4, pp. 288–295, 1999. View at Google Scholar
  106. Z. Liu, Y. E. Hartman, J. M. Warram et al., “Fibroblast growth factor receptor mediates fibroblast-dependent growth in EMMPRIN-depleted head and neck cancer tumor cells,” Molecular Cancer Research, vol. 9, no. 8, pp. 1008–1017, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. N. R. Estes II, J. V. Thottassery, L. Westbrook, and F. G. Kern, “MEK ablation in MCF-7 cells blocks DNA synthesis induced by serum, but not by estradiol or growth factors,” International Journal of Oncology, vol. 29, no. 6, pp. 1573–1580, 2006. View at Google Scholar · View at Scopus
  108. O. Klingenberg, A. Wiçdłocha, A. Rapak, R. Muñoz, P. Ø. Falnes, and S. Olsnes, “Inability of the acidic fibroblast growth factor mutant K132E to stimulate DNA synthesis after translocation into cells,” The Journal of Biological Chemistry, vol. 273, no. 18, pp. 11164–11172, 1998. View at Publisher · View at Google Scholar · View at Scopus
  109. J.-M. Rodier, A. M. Valles, M. Denoyelle, J. P. Thiery, and B. Boyer, “pp60(c-src) Is a positive regulator of growth factor-induced cell scattering in a rat bladder carcinoma cell line,” Journal of Cell Biology, vol. 131, no. 3, pp. 761–773, 1995. View at Publisher · View at Google Scholar · View at Scopus
  110. A. M. Valles, B. Boyer, J. Badet, G. C. Tucker, D. Barritault, and J. P. Thiery, “Acidic fibroblast growth factor is a modulator of epithelial plasticity in a rat bladder carcinoma cell line,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 3, pp. 1124–1128, 1990. View at Google Scholar · View at Scopus
  111. J. Jouanneau, J. Plouet, G. Moens, and J. P. Thiery, “FGF-2 and FGF-1 expressed in rat bladder carcinoma cells have similar angiogenic potential but different tumorigenic properties in vivo,” Oncogene, vol. 14, no. 6, pp. 671–676, 1997. View at Google Scholar · View at Scopus
  112. J. Jouanneau, J. Gavrilovic, D. Caruelle et al., “Secreted or nonsecreted forms of acidic fibroblast growth factor produced by transfected epithelial cells influence cell morphology, motility, and invasive potential,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 7, pp. 2893–2897, 1991. View at Google Scholar · View at Scopus
  113. P. Shannon, A. Markiel, O. Ozier et al., “Cytoscape: a software environment for integrated models of biomolecular interaction networks,” Genome Research, vol. 13, no. 11, pp. 2498–2504, 2003. View at Publisher · View at Google Scholar · View at Scopus
  114. O. Babur, U. Dogrusoz, E. Demir, and C. Sander, “ChiBE: interactive visualization and manipulation of BioPAX pathway models,” Bioinformatics, vol. 26, no. 3, pp. 429–431, 2010. View at Google Scholar · View at Scopus
  115. A. Dilek, M. E. Belviranli, and U. Dogrusoz, “VISIBIOweb: visualization and layout services for BioPAX pathway models,” Nucleic Acids Research, vol. 38, no. 2, Article ID gkq352, pp. W150–W154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. M. P. van Iersel, T. Kelder, A. R. Pico et al., “Presenting and exploring biological pathways with PathVisio,” BMC Bioinformatics, vol. 9, article 399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. T. S. K. Prasad, R. Goel, K. Kandasamy et al., “Human protein reference database—2009 update,” Nucleic Acids Research, vol. 37, no. 1, pp. D767–D772, 2009. View at Publisher · View at Google Scholar · View at Scopus