SHP-2 activates signaling of the nuclear factor of activated T cells to promote skeletal muscle growth

Journal of Cell Biology

Volumn 175, Issue 1, 2006, Pages 87-97

  Fornaro, Mara ^a,c   Burch, Peter M ^a   Yang, Wentian ^b   Zhang, Lei ^a   Hamilton, Claire E ^a   Kim, Jung H ^a   Neel, Benjamin G ^b   Bennett, Anton M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE KINASE; CYTOKINE; INTERLEUKIN 4; PROTEIN TYROSINE PHOSPHATASE SHP 2; TRANSCRIPTION FACTOR NFAT;

ANIMAL TISSUE; ARTICLE; CATALYSIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; MOUSE; MULTINUCLEAR CELL; MUSCLE CELL; MUSCLE GROWTH; MYOBLAST; MYOTUBE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; T LYMPHOCYTE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CREATINE KINASE, MM FORM; GENE DELETION; GENE EXPRESSION REGULATION; GENES, SRC; INTERLEUKIN-4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MUSCLE FIBERS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; NFATC TRANSCRIPTION FACTORS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; PROTEIN TYROSINE PHOSPHATASES; PROTEIN-TYROSINE-PHOSPHATASE; SIGNAL TRANSDUCTION;

EID: 33749577870     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200602029     Document Type: Article

References (61)

1. Abbott, K.L., B.B. Friday, D. Thaloor, T.J. Murphy, and G.K. Pavlath. 1998. Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol. Biol. Cell. 9:2905-2916.
2. Agazie, Y.M., and M.J. Hayman. 2003. Molecular mechanism for a role of SHP2 in epidermal growth factor receptor signaling. Mol. Cell. Biol. 23:7875-7886.
3. Allen, D.L., R.R. Roy, and V.R. Edgerton. 1999. Myonuclear domains in muscle adaptation and disease. Muscle Nerve. 22:1350-1360.
4. Alonso, A., J. Sasin, N. Bottini, I. Friedberg, A. Osterman, A. Godzik, T. Hunter, J. Dixon, and T. Mustelin. 2004. Protein tyrosine phosphatases in the human genome. Cell. 117:699-711.
5. 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.
6. Bruning, J.C., M.D. Michael, J.N. Winnay, T. Hayashi, D. Horsch, D. Accili, L.J. Goodyear, and C.R. Kahn. 1998. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell. 2:559-569.
7. Buckingham, M., L. Bajard, T. Chang, P. Daubas, J. Hadchouel, S. Meilhac, D. Montarras, D. Rocancourt, and F. Relaix. 2003. The formation of skeletal muscle: from somite to limb. J. Anat. 202:59-68.
8. Cary, L.A., R.A. Klinghoffer, C. Sachsenmaier, and J.A. Cooper. 2002. SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 22:2427-2440.
9. Chamberlain, J.S., J.B. Jaynes, and S.D. Hauschka. 1985. Regulation of creatine kinase induction in differentiating mouse myoblasts. Mol. Cell. Biol. 5:484-492.
10. Chin, E.R., E.N. Olson, J.A. Richardson, Q. Yang, C. Humphries, J.M. Shelton, H. Wu, W. Zhu, R. Bassel-Duby, and R.S. Williams. 1998. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12:2499-2509.
11. Cohn, R.D., M.D. Henry, D.E. Michele, R. Barresi, F. Saito, S.A. Moore, J.D. Flanagan, M.W. Skwarchuk, M.E. Robbins, J.R. Mendell, et al. 2002. Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell. 110:639-648.
12. Crabtree, G.R., and E.N. Olson. 2002. NFAT signaling: choreographing the social lives of cells. Cell. 109:S67-S79.
13. Danen, E.H., and A. Sonnenberg. 2003. Integrins in regulation of tissue development and function. J. Pathol. 201:632-641.
14. Darr, K.C., and E. Schultz. 1989. Hindlimb suspension suppresses muscle growth and satellite cell proliferation. J. Appl. Physiol. 67:1827-1834.
15. Engvall, E., and E. Ruoslahti. 1977. Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer. 20:1-5.
16. Farrell, R.L., and V.M. Ingram. 1983. Globin expression in Rous sarcoma virus-transformed quail myoblasts. Prog. Clin. Biol. Res. 134:263-266.
17. Feng, G.S. 1999. Shp-2 tyrosine phosphatase: signaling one cell or many. Exp. Cell Res. 253:47-54.
18. Fortin, J.F., B. Barbeau, G.A. Robichaud, M.E. Pare, A.M. Lemieux, and M.J. Tremblay. 2001. Regulation of nuclear factor of activated T cells by phosphotyrosyl-specific phosphatase activity: a positive effect on HIV-1 long terminal repeat-driven transcription and a possible implication of SHP-1. Blood. 97:2390-2400.
19. Fujioka, Y., T. Matozaki, T. Noguchi, A. Iwamatsu, T. Yamao, N. Takahashi, M. Tsuda, T. Takada, and M. Kasuga. 1996. A novel membrane glycoprotein, SHPS-1, that binds the SH2-domain-containing protein tyrosine phosphatase SHP-2 in response to mitogens and cell adhesion. Mol. Cell. Biol. 16:6887-6899.
20. Hogan, P.G., L. Chen, J. Nardone, and A. Rao. 2003. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17:2205-2232.
21. Horsley, V., B.B. Friday, S. Matteson, K.M. Kegley, J. Gephart, and G.K. Pavlath. 2001. Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J. Cell Biol. 153:329-338.
22. Horsley, V., K.M. Jansen, S.T. Mills, and G.K. Pavlath. 2003. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell. 113:483-494.
23. Jauliac, S., C. Lopez-Rodriguez, L.M. Shaw, L.F. Brown, A. Rao, and A. Toker. 2002. The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat. Cell Biol. 4:540-544.
24. Jaynes, J.B., J.S. Chamberlain, J.N. Buskin, J.E. Johnson, and S.D. Hauschka. 1986. Transcriptional regulation of the muscle creatine kinase gene and regulated expression in transfected mouse myoblasts. Mol. Cell. Biol. 6:2855-2864.
25. Kegley, K.M., J. Gephart, G.L. Warren, and G.K. Pavlath. 2001. Altered primary myogenesis in NFATC3(-/-) mice leads to decreased muscle size in the adult. Dev. Biol. 232:115-126.
26. Kharitonenkov, A., Z. Chen, I. Sures, H. Wang, J. Schilling, and A. Ullrich. 1997. A family of proteins that inhibit signalling through tyrosine kinase receptors. Nature. 386:181-186.
27. Klinghoffer, R.A., and A. Kazlauskas. 1995. Identification of a putative Syp substrate, the PDGFβ receptor. J. Biol. Chem. 270:22208-22217.
28. Kontaridis, M.I., X. Liu, L. Zhang, and A.M. Bennett. 2001. SHP-2 complex formation with the SHP-2 aubstrate-1 during C2C12 myogenesis. J. Cell Sci. 114:2187-2198.
29. Kontaridis, M.I., X. Liu, L. Zhang, and A.M. Bennett. 2002. Role of SHP-2 in fibroblast growth factor receptor-mediated suppression of myogenesis in C2C12 myoblasts. Mol. Cell. Biol. 22:3875-3891.
30. Kontaridis, M.I., S. Eminaga, M. Fornaro, C.I. Zito, R. Sordella, J. Settleman, and A.M. Bennett. 2004. SHP-2 positively regulates myogenesis by coupling to the Rho GTPase signaling pathway. Mol. Cell. Biol. 24:5340-5352.
31. Lu, H., P. Shah, D. Ennis, G. Shinder, J. Sap, H. Le-Tien, and I.G. Fantus. 2002. The differentiation of skeletal muscle cells involves a protein-tyrosine phosphatase-alpha-mediated C-Src signaling pathway. J. Biol. Chem. 277:46687-46695.
32. Milarski, K.L., and A.R. Saltiel. 1994. Expression of catalytically inactive Syp phosphatase in 3T3 cells blocks stimulation of mitogen-activated protein kinase by insulin. J. Biol. Chem. 269:21239-21243.
33. Mitchell, P.O., and G.K. Pavlath. 2001. A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy. Am. J. Physiol. Cell Physiol. 281:C1706-C1715.
34. Montagner, A., A. Yart, M. Dance, B. Perret, J.P. Salles, and P. Raynal. 2005. A novel role for Gab1 and SHP2 in epidermal growth factor-induced Ras activation. J. Biol. Chem. 280:5350-5360.
35. Mozdziak, P.E., E. Schultz, and R.G. Cassens. 1997. Myonuclear accretion is a major determinant of avian skeletal muscle growth. Am. J. Physiol. 272:C565-C571.
36. Nakayama, A.Y., M.B. Harms, and L. Luo. 2000. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20:5329-5338.
37. Naya, F.J., B. Mercer, J. Shelton, J.A. Richardson, R.S. Williams, and E.N. Olson. 2000. Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275:4545-4548.
38. Neel, B.G., H. Gu, and L. Pao. 2003. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem. Sci. 28:284-293.
39. 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.
40. Oh, E.S., H. Gu, T.M. Saxton, J.F. Timms, S. Hausdorff, E.U. Frevert, B.B. Kahn, T. Pawson, B.G. Neel, and S.M. Thomas. 1999. Regulation of early events in integrin signaling by protein tyrosine phosphatase SHP-2. Mol. Cell. Biol. 19:3205-3215.
41. Oh, M., I.I. Rybkin, V. Copeland, M.P. Czubryt, J.M. Shelton, E. van Rooij, J.A. Richardson, J.A. Hill, L.J. De Windt, R. Bassel-Duby, et al. 2005. Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers. Mol. Cell. Biol. 25:6629-6638.
42. Ontell, M., D. Hughes, and D. Bourke. 1988. Morphometric analysis of the developing mouse soleus muscle. Am. J. Anat. 181:279-288.
43. Rando, T.A., and H.M. Blau. 1994. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125:1275-1287.
44. Ren, Y., S. Meng, L. Mei, Z.J. Zhao, R. Jove, and J. Wu. 2004. Roles of Gab1 and SHP2 in paxillin tyrosine dephosphorylation and Src activation in response to epidermal growth factor. J. Biol. Chem. 279:8497-8505.
45. Sanna, B., O.F. Bueno, Y.S. Dai, B.J. Wilkins, and J.D. Molkentin. 2005. Direct and indirect interactions between calcineurin-NFAT and MEK1-extracellular signal-regulated kinase 1/2 signaling pathways regulate cardiac gene expression and cellular growth. Mol. Cell. Biol. 25:865-878.
46. 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.
47. Schultz, E., and K.M. McCormick. 1994. Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol. 123:213-257.
48. Schulze, M., F. Belema-Bedada, A. Technau, and T. Braun. 2005. Mesenchymal stem cells are recruited to striated muscle by NFAT/IL-4-mediated cell fusion. Genes Dev. 19:1787-1798.
49. 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.
50. Timmerman, L.A., N.A. Clipstone, S.N. Ho, J.P. Northrop, and G.R. Crabtree. 1996. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature. 383:837-840.
51. Tsuda, M., T. Matozaki, K. Fukunaga, Y. Fujioka, A. Imamoto, T. Noguchi, T. Takada, T. Yamao, H. Takeda, F. Ochi, et al. 1998. Integrin-mediated tyrosine phosphorylation of SHPS-1 and its association with SHP-2. Roles of Fak and Src family kinases. J. Biol. Chem. 273:13223-13229.
52. Uhlen, P., P.M. Burch, C.I. Zito, M. Estrada, B.E. Ehrlich, and A.M. Bennett. 2006. Gain-of-function/Noonan syndrome SHP-2/Ptpn11 mutants enhance calcium oscillations and impair NFAT signaling. Proc. Natl. Acad. Sci. USA. 103:2160-2165.
53. van Beek, E.M., F. Cochrane, A.N. Barclay, and T.K. van den Berg. 2005. Signal regulatory proteins in the immune system. J. Immunol. 175:7781-7787.
54. van den Berg, T.K., E.M. van Beek, H.J. Buhring, M. Colonna, M. Hamaguchi, C.J. Howard, M. Kasuga, Y. Liu, T. Matozaki, B.G. Neel, et al. 2005. A nomenclature for signal regulatory protein family members. J. Immunol. 175:7788-7789.
55. Wilkins, B.J., Y.S. Dai, O.F. Bueno, S.A. Parsons, J. Xu, D.M. Plank, F. Jones, T.R. Kimball, and J.D. Molkentin. 2004. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 94:110-118.
56. Wu, C.J., D.M. O'Rourke, G.S. Feng, G.R. Johnson, Q. Wang, and M.I. Greene. 2001. The tyrosine phosphatase SHP-2 is required for mediating phosphatidylinositol 3-kinase/Akt activation by growth factors. Oncogene. 20:6018-6025.
57. Yang, W., L.D. Klaman, B. Chen, T. Araki, H. Harada, S.M. Thomas, E.L. George, and B.G. Neel. 2006. An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev. Cell. 10:317-327.
58. Yu, D.H., C.K. Qu, O. Henegariu, X. Lu, and G.S. Feng. 1998. Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J. Biol. Chem. 273:21125-21131.
59. Zhang, S.Q., W.G. Tsiaras, T. Araki, G. Wen, L. Minichiello, R. Klein, and B.G. Neel. 2002. Receptor-specific regulation of phosphatidylinositol 3′-kinase activation by the protein tyrosine phosphatase Shp2. Mol. Cell. Biol. 22:4062-4072.
60. Zhang, S.Q., W. Yang, M.I. Kontaridis, T.G. Bivona, G. Wen, T. Araki, J. Luo, J.A. Thompson, B.L. Schraven, M.R. Philips, and B.G. Neel. 2004. Shp2 regulates SRC family kinase activity and ras/erk activation by controlling csk recruitment. Mol. Cell. 13:341-355.
61. Zito, C.I., M.I. Kontaridis, M. Fornaro, G.S. Feng, and A.M. Bennett. 2004. SHP-2 regulates the phosphatidylinositide 3′-kinase/Akt pathway and suppresses caspase 3-mediated apoptosis. J. Cell. Physiol. 199:227-236.