Mitogenic roles of Gab1 and Grb10 as direct cellular partners in the regulation of map kinase signaling

Journal of Cellular Biochemistry

Volumn 105, Issue 5, 2008, Pages 1172-1182

  Deng, Youping ^a   Zhang, Manchao ^b   Riedel, Heimo ^b  

^a The University of Southern Mississippi   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell permeant peptide; Map kinase; Mitogenesis; Pro rich; SH2; Survival

Indexed keywords

ADAPTOR PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10 BETA; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10 DELTA; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10 ZETA; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PLATELET DERIVED GROWTH FACTOR; PROTEIN GAB1; PROTEIN SH2; RAF PROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; ENZYME REGULATION; FIBROBLAST; GENE DISRUPTION; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL PROLIFERATION; GRB10 ADAPTOR PROTEIN; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NIH 3T3 CELLS; PHOSPHOPROTEINS; PLATELET-DERIVED GROWTH FACTOR; SRC HOMOLOGY DOMAINS;

EID: 57149107981     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21829     Document Type: Article

References (82)

1. Angrist M, Bolk S, Bentley K, Nallasamy S, Halushka MK, Chakravarti A. 1998. Genomic structure of the gene for the SH2 and pleckstrin homology domain-containing protein GRB10 and evaluation of its role in Hirschsprung disease. Oncogene 17:3065-3070.
2. Bai RY, Jahn T, Schrem S, Munzert G, Weidner KM, Wang JY, Duyster J. 1998. The SH2-containing adapter protein GRB10 interacts with BCR-ABL. Oncogene 17:941-948.
3. Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, Shah H, Qu J, Sweezer EM, Place T, Kirby PA, Daly RJ, Kumar S, Yang B. 2008. Nedd4 controls animal growth by regulating IGF-1 signaling. Scl Signal 1:ra5.
4. Cariou B, Bereziat V, Moncoq K, Kasus-Jacobi A, Perdereau D, Le Marcis V, Burnol AF. 2004. Regulation and functional roles of Grb14. Front Biosci 9:1626-1636.
5. Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, Ward A. 2003. Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc Natl Acad Sci USA 100:8292-8297.
6. Cooney GJ, Lyons RJ, Crew AJ, Jensen TE, Molero JC, Mitchell CJ, Biden TJ, Ormandy CJ, James DE, Daly RJ. 2004. Improved glucose homeostasis and enhanced insulin signalling in Grb14-deficient mice. EMBO J 23:582-593.
7. Daly RJ. 1998. The Grb7 family of signalling proteins. Cell Signal 10:613-618.
8. Deng Y, Bhattacharya S, Swamy OR, Tandon R, Wang Y, Janda R, Riedel H. 2003. Growth factor receptor-binding protein 10 (Grb10) as a partner of phosphatidylinositol 3-kinase in metabolic insulin action. J Biol Chem 278:39311-39322.
9. Deng Y, Xu H, Riedel H. 2007. PSM/SH2-B distributes selected mitogenic receptor signals to distinct components in the PI3-kinase and MAP kinase signaling pathways. J Cell Biochem 100:557-573.
10. Denizot F, Lang R. 1986. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89:271-277.
11. Dey BR, Frick K, Lopaczynski W, Nissley SP, Furlanetto RW. 1996. Evidence for the direct interaction of the insulin-like growth factor I receptor with IRS-1, Shc, and Grb10. Mol Endocrinol 10:631-641.
12. Dong LQ, Du H, Porter SG, Kolakowski LF, Jr., Lee AV, Mandarino LJ, Fan J, Yee D, Liu F. 1997a. Cloning, chromosome localization, expression, and characterization of an Src homology 2 and pleckstrin homology domain-containing insulin receptor binding protein hGrb10gamma. J Biol Chem 272:29104-29112.
13. Dong LQ, Farris S, Christal J, Liu F. 1997b. Site-directed mutagenesis and yeast two-hybrid studies of the insulin and insulin-like growth factor-1 receptors: The Src homology-2 domain-containing protein hGrb10 binds to the autophosphorylated tyrosine residues in the kinase domain of the insulin receptor. Mol Endocrinol 11:1757-1765.
14. Dong LQ, Porter S, Hu D, Liu F. 1998. Inhibition of hGrb10 binding to the insulin receptor by functional domain-mediated oligomerization. J Biol Chem 273:17720-17725.
15. Dufresne AM, Smith RJ. 2005. The adapter protein GRB10 is an endogenous negative regulator of insulin-like growth factor signaling. Endocrinology 146:4399-4409.
16. Durick K, Wu RY, Gill GN, Taylor SS. 1996. Mitogenic signaling by Ret/ptc2 requires association with enigma via a LIM domain. J Biol Chem 271:12691-12694.
17. Frantz JD, Giorgetti-Peraldi S, Ottinger EA, Shoelson SE. 1997. Human GRB-IRbeta/ G RB10.Splice variants of an insulin and growth factor receptor-binding protein with PH and SH2 domains. J Biol Chem 272:2659-2667.
18. Giorgetti-Peraldi S, Murdaca J, Mas JC, Van Obberghen E. 2001. The adapter protein, Grb10, is a positive regulator of vascular endothelial growth factor signaling. Oncogene 20:3959-3968.
19. Giovannone B, Lee E, Laviola L, Giorgino F, Cleveland KA, Smith RJ. 2003. Two novel proteins that are linked to insulin-like growth factor (IGF-I) receptors by the Grb10 adapter and modulate IGF-I signaling. J Biol Chem 278:31564-31573.
20. Gu H, Neel BG. 2003. The "Gab" in signal transduction. Trends Cell Biol 13:122-130.
21. Guan H, Smirnov DA, Ricciardi RP. 2003. Identification of genes associated with adenovirus 12 tumorigenesis by microarray. Virology 309:114-124.
22. Hansen H, Svensson U, Zhu J, Laviola L, Giorgino F, Wolf G, Smith RJ, Riedel H. 1996. Interaction between the Grb10 SH2 domain and the insulin receptor carboxyl terminus. J Biol Chem 271:8882-8886.
23. He W, Rose DW, Olefsky JM, Gustafson TA. 1998. Grb10 interacts differentially with the insulin receptor, insulin-like growth factor I receptor, and epidermal growth factor receptor via the Grb10 Src homology 2 (SH2) domain and a second novel domain located between the pleckstrin homology and SH2 domains. J Biol Chem 273:6860-6867.
24. Hitchins MP, Monk D, Bell GM, Ali Z, Preece MA, Stanier P, Moore GE. 2001. Maternal repression of the human GRB10 gene in the developing central nervous system; evaluation of the role for GRB10 in Silver-Russell syndrome. Eur J Hum Genet 9:82-90.
25. Holgado-Madruga M, Wong AJ. 2004. Role of the Grb2-associated binder 1/SHP-2 interaction in cell growth and transformation. Cancer Res 64:2007-2015.
26. Holt LJ, Daly RJ. 2005. Adapter protein connections: The MRL and Grb7 protein families. Growth Factors 23:193-201.
27. Holt LJ, Siddle K. 2005. Grb10 and Grb14: Enigmatic regulators of insulin action - And more? Biochem J 388:393-406.
28. Jahn T, Seipel P, Urschel S, Peschel C, Duyster J. 2002. Role for the adaptor protein Grb10 in the activation of Akt. Mol Cell Biol 22:979-991.
29. Jerome CA, Scherer SW, Tsui LC, Gietz RD, Triggs-Raine B. 1997. Assignment of growth factor receptor-bound protein 10 (GRB10) to human chromosome 7p11.2-p12. Genomics 40:215-216.
30. Kallin A, Demoulin JB, Nishida K, Hirano T, Ronnstrand L, Heldin CH. 2004. Gab1 contributes to cytoskeletal reorganization and chemotaxis in response to platelet-derived growth factor. J Biol Chem 279:17897-17904.
31. Kebache S, Ash J, Annis MG, Hagan J, Huber M, Hassard J, Stewart CL, Whiteway M, Nantel A. 2007. Grb10 and active Raf-1 kinase promote Bad-dependent cell survival. J Biol Chem 282:21873-21883.
32. Langlais P, Dong LQ, Hu D, Liu F. 2000. Identification of Grb10 as a direct substrate for members of the Src tyrosine kinase family. Oncogene 19:2895-2903.
33. Langlais P, Dong LQ, Ramos FJ, Hu D, Li Y, Quon MJ, Liu F. 2004. Negative regulation of insulin-stimulated mitogen-activated protein kinase signaling by Grb10. Mol Endocrinol 18:350-358.
34. Langlais P, Wang C, Dong LQ, Carroll CA, Weintraub ST, Liu F. 2005. Phosphorylation of Grb10 by mitogen-activated protein kinase: Identification of Ser150 and Ser476 of human Grb10zeta as major phosphorylation sites. Biochemistry 44:8890-8897.
35. Laviola L, Giorgino F, Chow JC, Baquero JA, Hansen H, Ooi J, Zhu J, Riedel H, Smith RJ. 1997. The adapter protein Grb10 associates preferentially with the insulin receptor as compared with the IGF-I receptor in mouse fibroblasts. J Clin Invest 99:830-837.
36. Lehr S, Kotzka J, Avci H, Sickmann A, Meyer HE, Herkner A, Muller-Wieland D. 2004. Identification of major ERK-related phosphorylation sites in Gab1. Biochemistry 43:12133-12140.
37. Lim MA, Riedel H, Liu F. 2004. Grb10: More than a simple adaptor protein. Front Biosci 9:387-403.
38. Liu Y, Rohrschneider LR. 2002. The gift of Gab. FEBS Lett 515:1-7.
39. Liu F, Roth RA. 1995. Grb-IR: A SH2-domain-containing protein that binds to the insulin receptor and inhibits its function. Proc Natl Acad Sci USA 92:10287-10291.
40. Mano H, Ohya K, Miyazato A, Yamashita Y, Ogawa W, Inazawa J, Ikeda U, Shimada K, Hatake K, Kasuga M, Ozawa K, Kajigaya S. 1998. Grb10/GrbIR as an in vivo substrate of Tec tyrosine kinase. Genes Cells 3:431-441.
41. Manser J, Roonprapunt C, Margolis B. 1997. C. elegans cell migration gene mig-10 shares similarities with a family of SH2 domain proteins and acts cell nonautonomously in excretory canal development. Dev Biol 184:150-164.
42. McClain DA, Maegawa H, Levy J, Huecksteadt T, Dull TJ, Lee J, Ullrich A, Olefsky JM. 1988. Properties of a human insulin receptor with a COOH-terminal truncation. I. Insulin binding, autophosphorylation, and endocytosis. J Biol Chem 263:8904-8911.
43. Meng S, Chen Z, Munoz-Antonia T, Wu J. 2005. Participation of both Gab1 and Gab2 in the activation of the ERK/MAPK pathway by epidermal growth factor. Biochem J 391:143-151.
44. Monami G, Emiliozzi V, Morrione A. 2008. Grb10/Nedd4-mediated multi-ubiquitination of the insulin-like growth factor receptor regulates receptor internalization. J Cell Physiol 216:426-437.
45. Mood K, Saucier C, Bong YS, Lee HS, Park M, Daar IO. 2006. Gab1 is required for cell cycle transition, cell proliferation, and transformation induced by an oncogenic met receptor. Mol Biol Cell 17:3717-3728.
46. Mori K, Giovannone B, Smith RJ. 2005. Distinct Grb10 domain requirements for effects on glucose uptake and insulin signaling. Mol Cell Endocrinol 230:39-50.
47. Morrione A. 2003. Grb10 adapter protein as regulator of insulin-like growth factor receptor signaling. J Cell Physiol 197:307-311.
48. Morrione A, Valentinis B, Li S, Ooi JY, Margolis B, Baserga R. 1996. Grb10: A new substrate of the insulin-like growth factor I receptor. Cancer Res 56:3165-3167.
49. Morrione A, Valentinis B, Resnicoff M, Xu S, Baserga R. 1997. The role of mGrb10alpha in insulin-like growth factor I-mediated growth. J Biol Chem 272:26382-26387.
50. Morrione A, Plant P, Valentinis B, Staub O, Kumar S, Rotin D, Baserga R. 1999. mGrb10 interacts with Nedd4. J Biol Chem 274:24094-24099.
51. Moutoussamy S, Renaudie F, Lago F, Kelly PA, Finidori J. 1998. Grb10 identified as a potential regulator of growth hormone (GH) signaling by cloning of GH receptor target proteins. J Biol Chem 273:15906-15912.
52. Murdaca J, Treins C, Monthouel-Kartmann MN, Pontier-Bres R, Kumar S, Van Obberghen E, Giorgetti-Peraldi S. 2004. Grb10 prevents Nedd4-mediated vascular endothelial growth factor receptor-2 degradation. J Biol Chem 279:26754-26761.
53. Nantel A, Mohammad-Ali K, Sherk J, Posner BI, Thomas DY. 1998. Interaction of the Grb10 adapter protein with the Raf1 and MEK1 kinases. J Biol Chem 273:10475-10484.
54. Nantel A, Huber M, Thomas DY. 1999. Localization of endogenous Grb10 to the mitochondria and its interaction with the mitochondrial-associated Raf-1 pool. J Biol Chem 274:35719-35724.
55. Nishida K, Hirano T. 2003. The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci 94:1029-1033.
56. Okino K, Konishi H, Doi D, Yoneyama K, Ota Y, Jin E, Kawanami O, Takeshita T. 2005. Up-regulation of growth factor receptor-bound protein 10 in cervical squamous cell carcinoma. Oncol Rep 13:1069-1074.
57. O'Neill TJ, Rose DW, Pillay TS, Hotta K, Olefsky JM, Gustafson TA. 1996. Interaction of a GRB-IR splice variant (a human GRB10 homolog) with the insulin and insulin-like growth factor I receptors. Evidence for a role in mitogenic signaling. J Biol Chem 271:22506-22513.
58. Ooi J, Yajnik V, Immanuel D, Gordon M, Moskow JJ, Buchberg AM, Margolis B. 1995. The cloning of Grb10 reveals a new family of SH2 domain proteins. Oncogene 10:1621-1630.
59. O-Sullivan I, Chopra A, Carr J, Kim TS, Cohen EP. 2008. Immunity to growth factor receptor-bound protein 10, a signal transduction molecule, inhibits the growth of breast cancer in mice. Cancer Res 68:2463-2470.
60. Pandey A, Duan H, Di Fiore PP, Dixit VM. 1995. The Ret receptor protein tyrosine kinase associates with the SH2-containing adapter protein Grb10. J Biol Chem 270:21461-21463.
61. Pillai S, Moran ST. 2002. Tec kinase pathways in lymphocyte development and transformation. Biochim Biophys Acta 1602:162-167.
62. Ramos FJ, Langlais PR, Hu D, Dong LQ, Liu F. 2006. Grb10 mediates insulin-stimulated degradation of the insulin receptor: A mechanism of negative regulation. Am J Physiol Endocrinol Metab 290:E1262-E1266.
63. Riedel H. 2004. Grb10 exceeding the boundaries of a common signaling adapter. Front Biosci 9:603-618.
64. Schaeper U, Gehring NH, Fuchs KP, Sachs M, Kempkes B, Birchmeier W. 2000. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J Cell Biol 149:1419-1432.
65. Shen TL, Guan JL. 2004. Grb7 in intracellular signaling and its role in cell regulation. Front Biosci 9:192-200.
66. Shiura H, Miyoshi N, Konishi A, Wakisaka-Saito N, Suzuki R, Muguruma K, Kohda T, Wakana S, Yokoyama M, Ishino F, Kaneko-Ishino T. 2005. Meg1/Grb10 overexpression causes postnatal growth retardation and insulin resistance via negative modulation of the IGF1R and IR cascades. Biochem Biophys Res Commun 329:909-916.
67. Smith FM, Holt LJ, Garfield AS, Charalambous M, Koumanov F, Perry M, Bazzani R, Sheardown SA, Hegarty BD, Lyons RJ, Cooney GJ, Daly RJ, Ward A. 2007. Mice with a disruption of the imprinted Grb10 gene exhibit altered body composition, glucose homeostasis, and insulin signaling during postnatal life. Mol Cell Biol 27:5871-5886.
68. Stein E, Cerretti DP, Daniel TO. 1996. Ligand activation of ELK receptor tyrosine kinase promotes its association with Grb10 and Grb2 in vascular endothelial cells. J Biol Chem 271:23588-23593.
69. Stein EG, Ghirlando R, Hubbard SR. 2003. Structural basis for dimerization of the Grb10 Src homology 2 domain. Implications for ligand specificity. J Biol Chem 278:13257-13264.
70. Tezuka N, Brown AM, Yanagawa S. 2007. GRB10 binds to LRP6, the Wnt co-receptor and inhibits canonical Wnt signaling pathway. Biochem Biophys Res Commun 356:648-654.
71. Urschel S, Bassermann F, Bai RY, Munch S, Peschel C, Duyster J. 2005. Phosphorylation of grb10 regulates its interaction with 14-3-3. J Biol Chem 280:16987-16993.
72. Vecchione A, Marchese A, Henry P, Rotin D, Morrione A. 2003. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol Cell Biol 23:3363-3372.
73. Vidal M, Goudreau N, Cornille F, Cussac D, Gincel E, Garbay C. 1999. Molecular and cellular analysis of Grb2 SH3 domain mutants: Interaction with Sos and dynamin. J Mol Biol 290:717-730.
74. Wang J, Dai H, Yousaf N, Moussaif M, Deng Y, Boufelliga A, Swamy OR, Leone ME, Riedel H. 1999. Grb10, a positive, stimulatory signaling adapter in platelet-derived growth factor BB-, insulin-like growth factor I-, and insulin-mediated mitogenesis. Mol Cell Biol 19:6217-6228.
75. Wang L, Balas B, Christ-Roberts CY, Kim RY, Ramos FJ, Kikani CK, Li C, Deng C, Reyna S, Musi N, Dong LQ, DeFronzo RA, Liu F. 2007. Peripheral disruption of the Grb10 gene enhances insulin signaling and sensitivity in vivo. Mol Cell Biol 27:6497-6505.
76. Webb BL, Jimenez E, Martin GS. 2000. v-Src generates a p53-independent apoptotic signal. Mol Cell Biol 20:9271-9280.
77. Wick KR, Werner ED, Langlais P, Ramos FJ, Dong LQ, Shoelson SE, Liu F. 2003. Grb10 inhibits insulin-stimulated insulin receptor substrate (IRS)-phosphatidylinositol 3-kinase/Akt signaling pathway by disrupting the association of IRS-1/IRS-2 with the insulin receptor. J Biol Chem 278:8460-8467.
78. Winnay JN, Bruning JC, Burks DJ, Kahn CR. 2000. Gab-1-mediated IGF-1 signaling in IRS-1-deficient 3T3 fibroblasts. J Biol Chem 275:10545-10550.
79. Wojcik J, Girault JA, Labesse G, Chomilier J, Mornon JP, Callebaut I. 1999. Sequence analysis identifies a ras-associating (RA)-like domain in the N-termini of band 4.1/JEF domains and in the Grb7/10/14 adapter family. Biochem Biophys Res Commun 259:113-120.
80. Yamamoto Y, Ishino F, Kaneko-Ishino T, Shiura H, Uchio-Yamada K, Matsuda J, Suzuki O, Sato K. 2008. Type 2 diabetes mellitus in a non-obese mouse model induced by Meg 1/Grb 10 overexpression. Exp Anim 57:385-395.
81. Yamasaki S, Nishida K, Yoshida Y, Itoh M, Hibi M, Hirano T. 2003. Gab1 is required for EGF receptor signaling and the transformation by activated Erb B2. Oncogene 22:1546-1556.
82. Yousaf N, Deng Y, Kang Y, Riedel H. 2001. Four PSM/SH2-B alternative splice variants and their differential roles in mitogenesis. J Biol Chem 276:40940-40948.