Insulin-like growth factor-I (IGF-I)-dependent activation of pp42/44 mitogen-activated protein kinase occurs independently of IGF-I receptor kinase activation and IRS-1 tyrosine phosphorylation

European Journal of Biochemistry

Volumn 266, Issue 3, 1999, Pages 1147-1157

  Yau, Lorraine ^a,b   Lukes, Helena ^a,b   McDiarmid, Heather ^a   Werner, Julieta ^a   Zahradka, Peter ^a,b  

^a ST BONIFACE GENERAL HOSPITAL RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Insulin; Insulin receptor substrate 1 (IRS 1); Insulin like growth factor I (IGF I); Mitogen activated protein (MAP) kinase; Tyrosine kinase

Indexed keywords

GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL METABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; GLUCOSE METABOLISM; HEPATOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RNA SYNTHESIS;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELL DIVISION; ENZYME ACTIVATION; GLUCOSE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LIVER NEOPLASMS, EXPERIMENTAL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPROTEINS; PHOSPHORYLATION; RATS; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TYROSINE;

EID: 0033572809     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00968.x     Document Type: Article

References (60)

1. 1. Whíte, M.F. & Kahn, C.R. (1994) The insulin signaling system. J. Biol. Chem. 269, 1-4.
2. 2. De Meyts, P., Wallach, B., Christoffersen, C.T., Urso, B., Gronskov, K., Latus, L.J., Yakushiji, F., Hondo, M.M. & Shymko, R.M. (1994) The insulin-like growth factor-I receptor. Structure, ligand-binding mechanism and signal transduction. Horm. Res. 42, 152-169.
3. 3. Seely, B.L., Reichart, D.R., Stauhs, P.A., Jhun, B.H., Hsu, D., Maegawa, H., Milarski, K.L., Saltiel, A.R. & Olefsky, J.M. (1995) Localization of the insulin-like growth factor I receptor binding sites for the SH2 domain proteins p85, Syp, and GTPase activating protein. J. Biol. Chem. 270, 19151-19157.
4. 4. Karin, M. (1996) The regulation of AP-1 activity by mitogen-activated protein kinases. Philos. Trans. R. Soc. Lond. Ser. B. Biol. Sci. 351, 127-134.
5. 5. Czech, M.P. (1977) Molecular basis of insulin action. Annu. Rev. Biochem. 46, 359-384.
6. 6. Cohick, W.S. & Cletnmons, D.R. (1993) The insulin-like growth factors. Annu. Rev. Physiol. 55, 131-153.
7. 7. Baserga, R., Porcu, P., Rubini, M. & Sell, C. (1994) Cell cycle control by the IGF-1 receptor and its ligands. In Current Directions in Insulin-Like Growth Factor Research (LeRoith, D. & Raizada, M.K., eds), pp. 105-112. Plenum Press, New York.
8. 8. Coolican, S.A., Samuel, D.S., Ewton, D.Z., McWade, F.J. & Florini, J.R. (1997) The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J. Biol. Chem. 272, 6653-6662.
9. 9. Scrimgeour, A.C., Blakesley, V.A., Stannard, B.S. & LeRoith, D. (1997) Mitogen-activated protein kinase and phosphatidylinositol 3-kinase pathways are not sufficient for insulin-like growth factor I-induced mitogenesis and tumorigenesis. Endocrinology 138, 2552-2558.
10. 10. Knebel, B., Kellner, S., Kotzka, J., Siemeister, G., Dreyer, M., Streicher, R., Schiller, M., Rudiger, H.W., Seemanova, E., Krone, W. & Muller-Wieland, D. (1997) Defects of insulin and IGF-1 action at receptor and postreceptor level in a patient with type A syndrome of insulin resistance. Biochem. Biophys. Rex. Commun. 234, 626-630.
11. 11. Takata, Y, Imamura, T., Haruta, T., Sasaoka, T., Morioka, H., Ishihara, H., Sawa, T., Usui, I., Ishiki, M. & Kobayashi, M, (1996) The dominant negative effect of a kinase-defective insulin receptor on insulin-like growth factor-I-stimulated signaling in Rat-1 fibroblasts. Metabolism 45, 1474-1482.
12. 12. Massague, J. & Czech, M.P. (1982) The subunit structures of two distinct receptors for insulin-like growth factors I and II and their relationship to the insulin receptor. J. Biol. Chem. 257, 5038-5045.
13. 13. Bucher, M.L. & Swaffield, M.N. (1975) Regulation of hepatic-regeneration in rats by synergistic action of insulin and glucagon. Proc. Natl Acad. Sci. USA 72, 1157-1160.
14. 14. Gressner, A.M., Lahme, B. & Brenzel, A. (1995) Molecular dissection of the mitogenic effect of hepatocytes on cultured hepatic stellate cells. Hepatology 22, 1507-1518.
15. 15. Freemark, M, D'Ercole, A.J. & Handwerger, S. (1985) Somatomedin-C stimulates glycogen synthesis in fetal rat hepatocytes. Endocrinology 116, 2578-2582.
16. 16. Heato, J.H., Schilling, E.E., Gelehrter, T.D., Rechter, MM, Spencer, C.J. & Nissley, S.P. (1980) Induction of tyrosine aminotransferase and amino acid transport in rat hepatoma cells by insulin and the insulin-like growth factor, multiplication-stimulating activity. Mediation by insulin and multiplication-stimulating activity receptors. Biochim. Biophys. Acta 632, 192-203.
17. 17. Verspohl, E.J., Roth, R.A., Vigneri, R. & Goldfine, I.D. (1984) Dual regulation of glycogen metabolism by insulin and insulin-like growth factors in human hepatoma cells (HEP-G2). Analysis with an anti-receptor monoclonal antibody. J. Clin. Invest. 74, 1436-1443.
18. 18. Di Cola, G., Cool, M.H. & Accili, D. (1997) Hypoglycemic effect of insulin-like growth factor-I in mice lacking insulin receptors. J. Clin. Invest. 99, 2538-2544.
19. 19. Lauris, V., Crettaz, M. & Kahn, C.R. (1986) Coordinate roles of insulin and glucose on the growth of hepatoma cells in culture. Endocrinology 118, 2519-2524.
20. 20. Taub, R., Roy, A., Dieter, R. & Koontz, J. (1987) Insulin as a growth factor in rat hepatoma cells. Stimulation of proto-oncogene expression. J. Biol. Chem. 262, 10893-10897.
21. 21. Mohn, K.L., Laz, T.M., Hsu, J.C., Melby, A.E., Bravo, R. & Taub, R. (1991) The immediate-early growth response in regenerating liver and insulin-stimulated H-35 cells: comparison with serum-stimulated 3T3 cells and identification of 41 novel immediate-early genes. Mol. Cell. Biol. 11, 381-390.
22. 22. Zahradka, P., Werner, J. & Yau, L. (1998) Expression and regulation of the insulin-like growth factor-I (IGF-I) receptor by growing and quiescent H4IIE hepatoma. Biochim. Biophys. Acta 1375, 131-139.
23. 23. Yau, L., Elliot, T., Lalonde, C. & Zahradka, P. (1998) Repression of phosphoenolpyruvate carboxykinase gene activity by insulin is blocked by 3-aminobenzamide but not by PD128763, a selective inhibitor of poly (ADP-ribose) polymerase. Ear. J. Biochem. 253, 91-100.
24. 24. Saward, L. & Zahradka, P. (1996) Insulin is required for angiotensin II-mediated hypertrophy of smooth muscle cells. Mol. Cell. Endocrinol. 122, 93-100.
25. 25. Kato, H., Faria, T.N., Stannard, B., Roberts, C.T.J. & LeRoith, D. (1993) Role of tyrosine kinase activity in signal transduction by the insulin-like growth factor-I (IGF-I) receptor. Characterization of kinase-deficient IGF-I receptors and the action of an IGF-I-mimetic antibody (alpha IR-3). J. Biol. Chem. 268, 2655-2661.
26. 26. Saward, L. & Zahradka, P. (1997) Angiotensin II activates phosphatidylinositol 3-kinase in vascular smooth muscle cells. Circ: Res. 81, 249-257.
27. 27. Yau, L. & Zahradka, P. (1997) Immunodetection of activated mitogen-activaled protein kinase in vascular tissues. Mol. Cell. Biochem. 172, 59-66.
28. 28. Koshio, O., Akanuma, Y. & Kasuga, M. (1988) Hydrogen peroxide stimulates tyrosine phosphorylation of the insulin receptor and its tyrosine kinase actívity in intact cells. Biochem. J. 250, 95-101.
29. 29. Zahradka, P. & Yau, L. (1994) ADP-ribosylation and gene expression. Mol. Cell. Biochem. 138, 91-98.
30. 30. Wilden, P.A., Siddle, K., Haring, E., Backer, J.M., White, M.F. & Kahn, C.R. (1992) The role of insulin receptor kinase domain autophosphorylation in receptor-meduued activities. Analysis with insulin and anti-receptor antibodies. J. Biol. Chem. 267, 13719-13727.
31. 31. Frattali, A.L., Treadway, IL. & Pessin, J.E. (1992) Transmembrane signaling by the human insulin receptor kinase. Relationship between intramolecular beta subunit trans-and cis-aulophosphorylation and substrate kinase activation. J. Biol. Chem. 267, 19521-19528.
32. 32. LeRoith, D., Wemer, H., Beitner-Johnson, D. & Roberts, C.T.J. (1995) Molecular and cellular aspects of the insulin-like growth factor 1 receptor. Endocr. Rev. 16, 143-163.
33. 33. Giorgelli, S., Pelicci, P.C., Van Pelicci, G. & Obberghen, E. (1994) Involvement of Src-homology/collagen (SHC) proteins in signaling through the insulin receptor and the insulin-like-growth-factor-I-receptor. Eur. J. Biochcm. 223, 195-202.
34. 34. He, W., Craparo, A., Zhu, Y., O'Neill, T.J., Wang, L.M., Pierce, J.H. & Gustafson, T.A. (1996) Interaction of insulin receptor substrate-2 (IRS-2) with the insulin and insulin-like growth factor I receptors. Evidence for two distinct phosphotyrosine-dependent interaction domains within IRS-2. J. Biol. Chem. 271, 11641-11645.
35. 35. Bonfini, L., Migliaccio, E., Pelicci, G., Lanfrancone, L. & Pelicci, P.G. (1996) Not all She's roads lead to Ras. Trends Biochem. Sci. 21, 257-261.
36. 36. Ouwens, D.M., van der Zon, G.C., Pronk, G.J., Bos, J.L., Moller, W., Cheatham, B., Kahn, C.R. & Maassen, J.A. (1994) A mutant insulin receptor induces formation of a Shc-growth factor receptor bound protein 2 (Grb2) complex and p2Iras-GTP without detectable interaction of insulin receptor substrate I (IRS1) with Grb2. Evidence for IRS 1-independent p2Iras-GTP formation. J. Biol. Chem. 269, 33116-33122.
37. 37. Kim, SJ. & Kahn, C.R. (1997) Insulin regulation of mitogen-activated protein kinase kinase (MEK), milogen-activated protein kinase and casein kinase in the cell nucleus: a possible role in the regulation of gene expression. Biochem. J. 323, 621 -627.
38. 38. Payne, D.M., Rossomando, A.J., Martino, P., Erickson, A.K., Her, J.H., Shabanowitz, J., Hunt, D.F., Weber, M.J. & Sturgill, T.W. (1991) Identification of the regulatory phosphorylation sites in pp42/mitogen-activaled protein kinase (MAP kinase). EMBO J. 10, 885-892.
39. 39. Xu, Y.J., Yau, L., Yu, L.P., Elimban, V, Zahradka, P. & Dhalla, N.S. (1996) Stimulation of protein synthesis by phosphatidic acid in rat cardiomyocytes. Biochcm. Pharmacol. 52, 1735-1740.
40. 40. Dudley, D.T., Pang, L., Decker, S.J., Bridges, A.J. & Saltiel, A.R. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl Acad. Sci. USA 92, 7686-7689.
41. 41. Koontz, J.W. (1984) The role of the insulin receptor in mediating the insulin-stimulated growth response in Reuber H-35 cells. Mol. Cell. Biochem. 58, 139-146.
42. 42. Prager, D. & Melmed, S. (1993) Insulin and insulin-like growth factor I receptors: are there functional distinctions? Endocrinology 132, 1419-1420.
43. 43. Kadowaki, T., Tobe, K., Honda-Yamamoto, R., Tamemolo, H., Kahuragi, Y., Momomura, K., Ueki, K., Takahashi, Y, Yamauchi, T., Akanuma, Y. & Yazaki, Y. (1996) Signal transduetion mechanism of insulin and insulin-like growth factor-I. Endocr. J. 43 (Suppl.) S33-S41.
44. 44. Sasaoka, T., Ishiki, M., Sawa, T., Ishihara, H., Takata, Y, Imamura, T., Usui, I., Olefsky, J.M. & Kobayashi, M. (I996) Comparison of the insulin and insulin-like growth factor I milogenic intracellular signaling pathways. Endocrinology 137, 4427-4434.
45. 45. McClain, D.A., Maegawa, H., Thies, R.S. &Olefsky, J.M. (1990) Dissection of the growth versus metabolic effects of insulin and insulin-like growth factor-I in transfecied cells expressing kinase-defective human insulin receptors. J. Biol. Chem. 265, 1678-1682.
46. 46. Myers, M.G.J., Grammer, T.C., Wang, L.M., Sun, X.J., Pierce, J.H., Blenis, J. & White, M.F. (1994) Insulin receptor substrate-I mediates phosphatidylinositol 3′-kinase and p70S6k signaling during insulin, insulin-like growth factor-1, and interleukin-4 stimulation. J. Biol. Chem. 269, 28783-28789.
47. 47. Myers, M.G.J., Sun, X.J. & White, M.F. (1994) The IRS-1 signaling system. Trends Biochem. Sci. 19, 289-293.
48. 48. Krook, A., Moller, D.E., Dib, K. & O'Rahilly, S. (1996) Two naturally occurring mutant insulin receptors phosphorylate insulin receptor substrate-I (IRS-1) but fail to mediate the biological effects of insulin. Evidence that IRS-1 phosphorylalion is not sufficient for normal insulin action. J. Biol. Chem. 271, 7134-7140.
49. 49. Waters, S.B., Yamauchi, K. & Pessin, J.E. (1993) Functional expression of insulin receptor substrate-1 is required for insulin-stimulated mitogenic signaling. J. Biol. Chem. 268, 22231-22234.
50. 50. Waters, S.B. & Pessin, J.E. (1996) Insulin receptor substrate 1 and 2 (IRS1 and IRS2): what a tangled web we weave. Trends Cell Biol. 6, 1-4.
51. 51. Skolnik, E.Y., Batzer, A., Li, N., Lee, C.H., Lowenstein, E., Mohammadi, M., Margolis, B. & Schlessinger, J. (1993) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science 260, 1953-55.
52. 52. Yonezawa, K., Ando, A., Kaburagi, Y., Yamamoto-Honda, R., Kitamura, T., Kara, K., Nakafuku, M., Okabayashi, Y, Kadowaki, T. & Kaziro, Y. (1994) Signal transduction pathways from insulin receptors to Ras. Analysis by mutant insulin receptors. J. Biol. Chem. 269, 4634-4640.
53. 53. Tsakiridis, T., Bergman, A., Somwar, R., Taha, C, Aktories, K., Cruz, T.F., Klip, A. & Downey, G.P. (1998) Actin filaments facilitate insulin activation of the src and collagen homologous/mitogen-activated protein kinase pathway leading to DNA synthesis and c-fos expression. J. Biol. Chem. 273, 28322-28331.
54. 54. Sutherland, C., Waltner-Law, M., Gnudi, L., Kahn, B.B. & Granner, D.K. (1998) Activation of the ras mitogen-activated protein kinase-ribosomal protein kinase pathway is not required for the repression of phosphoenolpyruvate carboxykinase gene transcription by insulin. J. Biol. Chem. 273, 3198-3204.
55. 55. Lazar, D.F., Wiese, R.J., Brady, M.J., Mastick, C.C., Waters, S.B., Yamauchi, K., Pessin, J.E., Cuatrecasas, P. & Saltiel, A.R. (1995) Mitogen-activatecl protein kinase kinase inhibition does not block the stimulation of glucose utilization by insulin. J. Biol. Chem. 270, 20801-20807.
56. 56. Combettes-Souverain, M. & Issad, T. (1998) Molecular basis of insulin action. Diabetes Metab. 24, 477-489.
57. 57. van Biesen, T., Hawes, B.E., Luttrell, D.K., Krueger, K.M., Touhara, K., Porfiri, E., Sakaue, M., Luttrell, L.M. & Lefkowitz, R.J. (1995) Receptor-tyrosine-kinase-and G beta gamma-mediated MAP kinase activation by a common signalling pathway. Nature (London) 376, 781-784.
58. 58. Luttrell, L.M., Biesen, T., Hawes, B.E., Koch, W.J., Touhara, K. & Lefkowitz, R.J. (1995) G beta gamma subunits mediate mitogen-activated protein kinase activation by the tyrosine kinase insulin-like growth factor 1 receptor. J. Biol. Chem. 270, 16495-16498.
59. 59. Rizzo, M.A. & Romero, G. (1998) The role of G proteins in insulin signalling. J Basic Clin. Physiol. Pharmacol. 9, 167-195.
60. 60. Uehara, T., Tokumitsu, Y. & Nomura, Y. (1999) Pertussis toxin-sensitive and insensitive intracellular signalling pathways in undifferentiated 3T3-L1 cells stimulated by insulin converge with phosphatidylinositol 3-kinase upstream of the Ras milogen-activated protein kinase cascade. Eur. J. Biochem. 259, 801-808.