Role of SHP-2 in Fibroblast Growth Factor Receptor-Mediated Suppression of Myogenesis in C2C12 Myoblasts

REFERENCES

• Adachi, M., M. Sekiya, T. Miyachi, K. Matsuno, Y. Hinoda, K. Imai, and A. Yachi. 1992. Molecular cloning of a novel protein-tyrosine phosphatase, SH-PTP3, with sequence similarity to the src-homology region 2. FEBS Lett. 314: 335–339.
   PubMedGoogle Scholar
• Ahmad, S., D. Banville, Z. Zhao, E. H. Fischer, and S.-H. Shen. 1993. A widely expressed human protein tyrosine phosphatase contains src homology 2 domains. Proc. Natl. Acad. Sci. USA 90: 2197–2201.
   PubMedGoogle Scholar
• Bennett, A. M., S. F. Hausdorff, A. M. O'Reilly, R. M. Freeman, and B. G. Neel. 1996. Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol. Cell. Biol. 16: 1189–1202.
   PubMed Web of Science ®Google Scholar
• Bennett, A. M., T. L. Tang, S. Sugimoto, C. T. Walsh, and B. G. Neel. 1994. Protein-tyrosine-phosphatase SHPTP2 couples platelet-derived growth factor receptor β to Ras. Proc. Natl. Acad. Sci. USA 91: 7335–7339.
   PubMed Web of Science ®Google Scholar
• Bennett, A. M., and N. K. Tonks. 1997. Regulation of distinct stages of skeletal muscle differentiation by mitogen-activated protein kinases. Science 278: 1288–1291.
   PubMed Web of Science ®Google Scholar
• Bjorbak, C., R. M. Buchholz, S. M. Davis, S. H. Bates, D. D. Pierroz, H. Gu, B. G. Neel, M. G. Myers, Jr., and J. S. Flier. 2001. Divergent roles of SHP-2 in ERK activation by leptin receptors. J. Biol. Chem. 276: 4747–4755.
   PubMedGoogle Scholar
• Campbell, J. S., M. P. Wenderoth, S. D. Hauschka, and E. G. Krebs. 1995. Differential activation of mitogen-activated protein kinase in response to basic fibroblast growth factor in skeletal muscle. Proc. Natl. Acad. Sci. USA 92: 870–874.
   PubMedGoogle Scholar
• Clegg, C., T. Linkhart, B. Olwin, and S. Hauschka. 1987. Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J. Cell Biol. 105: 949–956.
   PubMed Web of Science ®Google Scholar
• Coolican, S. A., D. S. Samuel, D. Z. Ewton, F. J. McWade, and J. R. Florini. 1997. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J. Biol. Chem. 272: 6653–6662.
   PubMed Web of Science ®Google Scholar
• Delahaye, L., S. Rocchi, and E. Van Obberghen. 2000. Potential involvement of FRS2 in insulin signaling. Endocrinology 141: 621–628.
   PubMedGoogle Scholar
• Dias, P., M. Dilling, and P. Houghton. 1994. The molecular basis of skeletal muscle differentiation. Semin. Diagn. Pathol. 11: 3–14.
   PubMed Web of Science ®Google Scholar
• Fedorov, Y. V., R. S. Rosenthal, and B. B. Olwin. 2001. Oncogenic Ras-induced proliferation requires autocrine fibroblast growth factor 2 signaling in skeletal muscle cells. J. Cell Biol. 152: 1301–1305.
   PubMedGoogle Scholar
• Feng, G. S. 1999. Shp-2 tyrosine phosphatase: signaling one cell or many. Exp. Cell Res. 253: 47–54.
   PubMedGoogle Scholar
• Feng, G.-S., C.-C. Hui, and T. Pawson. 1993. SH2-containing phosphotyrosine phosphatase as a target of protein-tyrosine kinases. Science 259: 1607–1611.
   PubMed Web of Science ®Google Scholar
• Freeman, R. M., J. Plutzky, and B. G. Neel. 1992. Identification of a human src homology 2-containing protein tyrosine-phosphatase: a putative homolog of Drosophila corkscrew. Proc. Natl. Acad. Sci. USA 89: 11239–11243.
   PubMedGoogle Scholar
• Gredinger, E., A. N. Gerber, Y. Tamir, S. J. Tapscott, and E. Bengal. 1998. Mitogen-activated protein kinase pathway is involved in the differentiation of muscle cells. J. Biol. Chem. 273: 10436–10444.
   PubMed Web of Science ®Google Scholar
• Hadari, Y. R., H. Kouhara, I. Lax, and J. Schlessinger. 1998. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol. Cell. Biol. 18: 3966–3973.
   PubMed Web of Science ®Google Scholar
• Hannon, K., A. J. Kudla, M. J. McAvoy, K. L. Clase, and B. B. Olwin. 1996. Differentially expressed fibroblast growth factors regulate skeletal muscle development through autocrine and paracrine mechanisms. J. Cell Biol. 132: 1151–1159.
   PubMed Web of Science ®Google Scholar
• He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95: 2509–2514.
   PubMed Web of Science ®Google Scholar
• Hof, P., S. Pluskey, S. Dhe-Pagganon, M. J. Eck, and S. E. Shoelson. 1998. Crystal structure of the tyrosine phosphatase SHP-2. Cell 92: 441–450.
   PubMed Web of Science ®Google Scholar
• Itoh, N., T. Mima, and T. Mikawa. 1996. Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122: 291–300.
   PubMedGoogle Scholar
• Jones, N. C., Y. V. Fedorov, R. S. Rosenthal, and B. B. Olwin. 2001. ERK1/2 is required for myoblast proliferation but is dispensable for muscle gene expression and cell fusion. J. Cell. Physiol. 186: 104–115.
   PubMedGoogle Scholar
• Kodama, A., T. Matozaki, A. Fukuhara, M. Kikyo, M. Ichihashi, and Y. Takai. 2000. Involvement of an SHP-2-Rho small G protein pathway in hepatocyte growth factor/scatter factor-induced cell scattering. Mol. Biol. Cell 11: 2565–2575.
   PubMedGoogle Scholar
• Kontaridis, M. I., X. Liu, L. Zhang, and A. M. Bennett. 2001. SHP-2 complex formation with the SHP-2 substrate-1 during C2C12 myogenesis. J. Cell Sci. 114: 2187–2198.
   PubMedGoogle Scholar
• Kouhara, H., Y. R. Hadari, T. Spivak-Kroizman, J. Schilling, D. Bar-Sagi, I. Lax, and J. Schlessinger. 1997. A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89: 693–702.
   PubMed Web of Science ®Google Scholar
• Kudla, A., N. Jones, R. Rosenthal, K. Arthur, K. Clase, and B. Olwin. 1998. The FGF receptor-1 tyrosine kinase domain regulates myogenesis but is not sufficient to stimulate proliferation. J. Cell Biol. 142: 241–250.
   PubMedGoogle Scholar
• Kudla, A. J., M. L. John, D. F. Bowen-Pope, B. Rainish, and B. B. Olwin. 1995. A requirement for fibroblast growth factor in regulation of skeletal muscle growth and differentiation cannot be replaced by activation of platelet-derived growth factor signaling pathways. J. Cell Biol. 15: 3238–3246.
   Google Scholar
• Lassar, A. B., S. X. Skapek, and N. Bennett. 1994. Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6: 788–794.
   PubMed Web of Science ®Google Scholar
• Lathrop, B., K. Thomas, and L. Glaser. 1985. Control of myogenic differentiation by fibroblast growth factor is mediated by position in the G1 phase of the cell cycle. J. Cell Biol. 101: 2194–2198.
   PubMed Web of Science ®Google Scholar
• Lechleider, R. J., R. M. Freeman, Jr., and B. G. Neel. 1993. Tyrosyl phosphorylation and growth factor receptor association of the human corkscrew homologue, SH-PTP2. J. Biol. Chem. 268: 13434–13438.
   PubMedGoogle Scholar
• Lechleider, R. J., S. Sugimoto, A. M. Bennett, A. Kashishian, J. A. Cooper, S. E. Shoelson, C. T. Walsh, and B. G. Neel. 1993. Activation of the SH2-containing phosphotyrosine phosphatase SH-PTP2 by its binding site, phosphotyrosine 1009, on the human platelet-derived growth factor receptor β. J. Biol. Chem. 268: 21478–21481.
   PubMedGoogle Scholar
• Li, W., R. Nishimura, A. Kashishian, A. G. Batzer, W. J. H. Kim, J. A. Cooper, and J. Schlessinger. 1994. A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14: 509–517.
   PubMed Web of Science ®Google Scholar
• Maher, P. 1999. p38 mitogen-activated protein kinase activation is required for fibroblast growth factor-2-stimulated proliferation but not differentiation. J. Biol. Chem. 274: 17491–17498.
   PubMed Web of Science ®Google Scholar
• Meakin, S. O., J. I. MacDonald, E. A. Gryz, C. J. Kubu, and J. M. Verdi. 1999. The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation. J. Biol. Chem. 274: 9861–9870.
   PubMed Web of Science ®Google Scholar
• Meriane, M., P. Roux, M. Primig, P. Fort, and C. Gauthier-Rouviere. 2000. Critical activities of Rac1 and Cdc42Hs in skeletal myogenesis: antagonistic effects of JNK and p38 pathways. Mol. Biol. Cell 11: 2513–2528.
   PubMedGoogle Scholar
• Milasincic, D. J., M. R. Calera, S. R. Farmer, and P. F. Pilch. 1996. Stimulation of C2C12 myoblast growth by basic fibroblast growth factor and insulin-like growth factor 1 can occur via mitogen-activated protein kinase-dependent and -independent pathways. Mol. Cell. Biol. 16: 5964–5973.
   PubMed Web of Science ®Google Scholar
• Morgenstern, J. P., and H. Land. 1990. A series of mammalian expression vectors and characterisation of their expression of a reporter gene in stably and transiently transfected cells. Nucleic Acids Res. 18: 1068.
   PubMed Web of Science ®Google Scholar
• Naya, F. S., and E. Olson. 1999. MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr. Opin. Cell Biol. 11: 683–688.
   PubMed Web of Science ®Google Scholar
• Neel, B. G. 1997. Role of phosphatases in lymphocyte activation. Curr. Opin. Immunol. 9: 405–420.
   PubMed Web of Science ®Google Scholar
• Neel, B. G. 1993. Structure and function of SH2-domain-containing tyrosine phosphatases. Semin. Cell Biol. 4: 419–432.
   PubMedGoogle Scholar
• Neel, B. G., and N. K. Tonks. 1997. Protein tyrosine phosphatases in signal transduction. Curr. Opin. Cell Biol. 9: 193–204.
   PubMed Web of Science ®Google Scholar
• Noguchi, T., T. Matozaki, K. Horita, Y. Fujioka, and M. Kasuga. 1994. Role of SH-PTP2, a protein-tyrosine phosphatase with src homology 2 domains, in insulin-stimulated ras activation. Mol. Cell. Biol. 14: 6674–6682.
   PubMed Web of Science ®Google Scholar
• Olson, E., and W. Klein. 1994. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8: 1–8.
   PubMed Web of Science ®Google Scholar
• Olwin, B. B., and S. D. Hauschka. 1988. Cell surface fibroblast growth factor and epidermal growth factor receptors are permanently lost during skeletal muscle terminal differentiation in culture. J. Cell Biol. 107: 761–769.
   PubMed Web of Science ®Google Scholar
• Ong, S. H., G. R. Guy, Y. R. Hadari, S. Laks, N. Gotoh, J. Schlessinger, and I. Lax. 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.
   PubMed Web of Science ®Google Scholar
• O'Reilly, A., S. Pluskey, S. E. Shoelson, and B. G. Neel. 2000. Activated mutants of SHP-2 preferentially induce elongation of Xenopus animal caps. Mol. Cell. Biol. 20: 299–311.
   PubMed Web of Science ®Google Scholar
• Patel, S. G., P. E. Funk, and J. X. DiMario. 1999. Regulation of avian fibroblast growth factor receptor 1 (FGFR-1) gene expression during skeletal muscle differentiation. Gene 237: 265–276.
   PubMedGoogle Scholar
• Rabin, S. J., V. Cleghon, and D. R. Kaplan. 1993. SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells. Mol. Cell. Biol. 13: 2203–2213.
   PubMedGoogle Scholar
• Raffioni, S., D. Thomas, E. D. Foehr, L. M. Thompson, and R. A. Bradshaw. 1999. Comparison of the intracellular signaling responses by three chimeric fibroblast growth factor receptors in PC12 cells. Proc. Natl. Acad. Sci. USA 96: 7178–7183.
   PubMedGoogle Scholar
• Ramocki, M., S. Johnson, M. White, C. Ashendel, S. Konieczny, and E. Taparowsky. 1997. Signaling through mitogen-activated protein kinase and Rac/Rho does not duplicate the effects of activated Ras on skeletal myogenesis. Mol. Cell. Biol. 17: 3547–3555.
   PubMed Web of Science ®Google Scholar
• Ramocki, M. B., M. A. White, S. F. Konieczny, and E. J. Taparowsky. 1998. A role for RalGDS and a novel Ras effector in the Ras-mediated inhibition of skeletal myogenesis. J. Biol. Chem. 273: 17696–17701.
   PubMedGoogle Scholar
• Rapraeger, A. C., A. Krufka, and B. B. Olwin. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth factor and myoblast differentiation. Science 252: 1705–1708.
   PubMed Web of Science ®Google Scholar
• Saxton, T. M., M. Henkemeyer, S. Gasca, R. Shen, D. J. Rossi, F. Shalaby, G. S. Feng, and T. Pawson. 1997. Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J. 16: 2352–2364.
   PubMed Web of Science ®Google Scholar
• Schoenwaelder, S. M., L. A. Petch, D. Williamson, R. Shen, G. Feng, and K. Burridge. 2000. The protein tyrosine phosphatase shp-2 regulates RhoA activity. Curr. Biol. 10: 1523–1526.
   PubMed Web of Science ®Google Scholar
• Shi, Z. Q., D. H. Yu, M. Park, M. Marshall, and G. S. Feng. 2000. Molecular mechanism for the Shp-2 tyrosine phosphatase function in promoting growth factor stimulation of Erk activity. Mol. Cell. Biol. 20: 1526–1536.
   PubMedGoogle Scholar
• Skapek, S., J. Rhee, D. Spicer, and A. Lassar. 1995. Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267: 1022–1024.
   PubMed Web of Science ®Google Scholar
• Spizz, G., D. Roman, A. Strauss, and E. Olson. 1986. Serum and fibroblast growth factor inhibit myogenic differentiation through a mechanism dependent on protein synthesis and independent of cell proliferation. J. Biol. Chem. 261: 9483–9488.
   PubMed Web of Science ®Google Scholar
• Takano, H., I. Komuro, T. Oka, I. Shiojima, Y. Hiroi, T. Mizuno, and Y. Yazaki. 1998. The Rho family G proteins play a critical role in muscle differentiation. Mol. Cell. Biol. 18: 1580–1589.
   PubMedGoogle Scholar
• Tang, T. L., R. M. Freeman, Jr., A. M. O'Reilly, B. G. Neel, and S. Y. Sokol. 1995. The SH2-containing protein tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell 80: 473–483.
   PubMed Web of Science ®Google Scholar
• Tauchi, T., G.-S. Feng, M. S. Marshall, R. Shen, C. Mantel, T. Pawson, and H. E. Broxmeyer. 1994. The ubiquitously expressed Syp phosphatase interacts with c-kit and Grb2 in hematopoietic cells. J. Biol. Chem. 269: 25206–25211.
   PubMed Web of Science ®Google Scholar
• Tauchi, T., G.-S. Feng, R. Shen, M. Hoatlin, G. C. Bagby, D. Kabat, and H. E. Broxmeyer. 1995. Involvement of SH2-containing phosphotyrosine phosphatase Syp in erythropoietin receptor signal transduction pathways. J. Biol. Chem. 270: 5631–5635.
   PubMed Web of Science ®Google Scholar
• Tonks, N. K., and B. G. Neel. 1996. From form to function: signaling by protein tyrosine phosphatases. Cell 87: 365–368.
   PubMed Web of Science ®Google Scholar
• Vaidya, T. B., S. J. Rhodes, E. J. Taparowsky, and S. F. Konieczny. 1989. Fibroblast growth factor and transforming growth factor β repress transcription of the myogenic regulatory gene MyoD1. Mol. Cell. Biol. 9: 3576–3579.
   PubMedGoogle Scholar
• Vincent, C. K., A. Gualberto, C. V. Patel, and K. Walsh. 1993. Different regulatory sequences control creatine kinase-M gene expression in directly injected skeletal and cardiac muscle. Mol. Cell. Biol. 13: 1264–1272.
   PubMed Web of Science ®Google Scholar
• Vogel, W., R. Lammers, J. Huang, and A. Ullrich. 1993. Activation of a phosphotyrosine phosphatase by tyrosine phosphorylation. Science 259: 1611–1614.
   PubMed Web of Science ®Google Scholar
• Vogel, W., and A. Ullrich. 1996. Multiple in vivo phosphorylated tyrosine phosphatase SHP-2 engages binding to Grb2 via tyrosine 584. Cell Growth Differ. 7: 1589–1597.
   PubMedGoogle Scholar
• Weintraub, H. 1993. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75: 1241–1244.
   PubMed Web of Science ®Google Scholar
• Welham, M. J., U. Dechert, K. B. Leslie, F. Jirik, and J. W. Schrader. 1994. Interleukin (IL)-3 and granulocyte/macrophage colony-stimulating factor, but not IL-4, induce tyrosine phosphorylation, activation, and association of SHPTP2 with Grb2 and phosphatidylinositol 3′-kinase. J. Biol. Chem. 269: 23764–23768.
   PubMedGoogle Scholar
• Weyman, C. M., and A. Wolfman. 1998. Mitogen-activated protein kinase kinase (MEK) activity is required for inhibition of skeletal muscle differentiation by insulin-like growth factor 1 or fibroblast growth factor 2. Endocrinology 139: 1794–1800.
   PubMedGoogle Scholar
• Wu, Z., P. J. Woodring, K. S. Bhakta, K. Tamura, F. Wen, J. R. Feramisco, M. Karin, J. Y. Wang, and P. L. Puri. 2000. p38 and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol. Cell. Biol. 20: 3951–3964.
   PubMed Web of Science ®Google Scholar
• Xu, H., K. W. Lee, and M. Goldfarb. 1998. Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J. Biol. Chem. 273: 17987–17990.
   PubMedGoogle Scholar
• Yang, S. H., A. J. Whitmarsh, R. J. Davis, and A. D. Sharrocks. 1998. Differential targeting of MAP kinases to the ETS-domain transcription factor Elk-1. EMBO J. 17: 1740–1749.
   PubMed Web of Science ®Google Scholar
• Yoshida, S., A. Fujisawa-Sehara, T. Taki, and Y. Nabeshima. 1996. Lysophosphatidic acid and bFGF control different modes in proliferating myoblasts. J. Cell Biol. 132: 181–193.
   PubMedGoogle Scholar