Modulation of human insulin receptor substrate-1 tyrosine phosphorylation by protein kinase Cδ

Biochemical Journal

Volumn 378, Issue 1, 2004, Pages 105-116

  Greene, Michael W ^a   Morrice, Nick ^b   Garofalo, Robert S ^c   Roth, Richard A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c PFIZER INC   (United States)

Author keywords

Insulin resistance; IRS 1 (insulin receptor substrate 1); nPKC (novel protein kinase C); Tyrosine phosphorylation

Indexed keywords

ENZYMES; ESTERIFICATION; ESTERS; FATTY ACIDS; INSULIN;

MUTATION; PHOSPHORYLATION;

BIOCHEMISTRY;

ALANINE; INSULIN RECEPTOR SUBSTRATE 1; PROTEIN KINASE C DELTA; SERINE; TYROSINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; INSULIN RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; HUMANS; ISOENZYMES; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-DELTA; PROTEIN-TYROSINE KINASES; TYROSINE;

ANIMALIA;

EID: 1542284652     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031493     Document Type: Article

References (50)

1. Saltiel, A. R. (2001) New perspectives into the molecular pathogenesis and treatment of type 2 diabetes. Cell (Cambridge, Mass.) 104, 517-529
2. Zick, Y. (2001) Insulin resistance: a phosphorylation-based uncoupling of insulin signaling. Trends Cell Biol. 11, 437-441
3. White, M. F. (2002) IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283, E413-E422
4. Shepherd, P. R., Withers, D. J. and Siddle, K. (1998) Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem. J. 333, 471-490
5. Lawlor, M. A. and Alessi, D. R. (2001) PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114, 2903-2910
6. Birnbaum, M. J. (2001) Turning down insulin signaling. J. Clin. Invest. 108, 655-659
7. Mellor, H. and Parker, P. J. (1998) The extended protein kinase C superfamily. Biochem. J. 332, 281-292
8. Farese, R. V. (2002) Function and dysfunction of aPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states. Am. J. Physiol. Endocrinol. Metab. 283, E1-E11
9. Kotani, K., Ogawa, W., Matsumoto, M., Kitamura, T., Sakaue, H., Hino, Y., Miyake, K., Sano, W., Akimoto, K., Ohno, S. et al. (1998) Requirement of atypical protein kinase Cλ for insulin stimulation of glucose uptake but not for Akt activation in 3T3-L1 adipocytes. Mol. Cell. Biol. 18, 6971-6982
10. Chin, J. E., Dickens, M., Tavare, J. M. and Roth, R. A. (1993) Overexpression of protein kinase C isoenzymes α, β1, γ, and ε in cells overexpressing the insulin receptor. Effects on receptor phosphorylation and signaling. J. Biol. Chem. 268, 6338-6347
11. Kellerer, M., Mushack, J., Seffer, E., Mischak, H., Ullrich, A. and Haring, H. U. (1998) Protein kinase C isoforms α, δ and θ require insulin receptor substrate-1 to inhibit the tyrosine kinase activity of the insulin receptor in human kidney embryonic cells (HEK 293 cells). Diabetologia 41, 833-838
12. Formisano, P., Oriente, F., Miele, C., Caruso, M., Auricchio, R., Vigliotta, G., Condorelli, G. and Beguinot, F. (1998) In NIH-3T3 fibroblasts, insulin receptor interaction with specific protein kinase C isoforms controls receptor intracellular routing. J. Biol. Chem. 273, 13197-13202
13. Liu, Y. F., Paz, K., Herschkovitz, A., Alt, A., Tennenbaum, T., Sampson, S. R., Ohba, M., Kuroki, T., LeRoith, D. and Zick, Y. (2001) Insulin stimulates PKCζ-mediated phosphorylation of insulin receptor substrate-1 (IRS-1). A self-attenuated mechanism to negatively regulate the function of IRS proteins. J. Biol. Chem. 276, 14459-14465
14. Ravichandran, L. V., Esposito, D. L., Chen, J. and Quon, M. J. (2001) Protein kinase C-ζ phosphorylates insulin receptor substrate-1 and impairs its ability to activate phosphatidylinositol 3-kinase in response to insulin. J. Biol. Chem. 276, 3543-3549
15. Beck, A., Moeschel, K., Deeg, M., Haring, H. U., Voelter, W., Schleicher, E. D. and Lehmann, R. (2003) Identification of an in vitro insulin receptor substrate-1 phosphorylation site by negative-ion μLC/ES-API-CID-MS hybrid scan technique. J. Am. Soc. Mass Spectrom. 14, 401-405
16. De Fea, K. and Roth, R. A. (1997) Modulation of Insulin receptor substrate-1 tyrosine phosphorylation and function by mitogen-activated protein kinase. J. Biol. Chem. 272, 31400-31406
17. Boden, G. (2002) Interaction between free fatty acids and glucose metabolism. Curr. Opin. Clin. Nutr. Metab. Care 5, 545-549
18. Shulman, G. I. (1999) Cellular mechanisms of insulin resistance in humans. Am. J. Cardiol. 84, 3J-10J
19. Shah, P., Basu, A. and Rizza, R. (2003) Fat-induced liver insulin resistance. Curr. Diabetes Rep. 3, 214-218
20. Itani, S. I., Ruderman, N. B., Schmieder, F. and Boden, G. (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IκB-α. Diabetes 51, 2005-2011
21. Lam, T. K., Yoshii, H., Haber, C. A., Bogdanovic, E., Lam, L., Fantus, I. G. and Giacca, A. (2002) Free fatty acid-induced hepatic insulin resistance: a potential role for protein kinase C-δ. Am. J. Physiol. Endocrinol. Metab. 283, E682-E691
22. Yu, C., Chen, Y., Cline, G. W., Zhang, D., Zong, H., Wang, Y., Bergeron, R., Kim, J. K., Cushman, S. W., Cooney, G. J. et al. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277, 50230-50236
23. Boden, G., Cheung, P., Stein, T. P., Kresge, K. and Mozzoli, M. (2002) FFA cause hepatic insulin resistance by inhibiting insulin suppression of glycogenolysis. Am. J. Physiol. Endocrinol. Metab. 283, E12-E19
24. Vainshtein, I., Kovacina, K. S. and Roth, R. A. (2001) The insulin receptor substrate (IRS)-1 pleckstrin homology domain functions in downstream signaling. J. Biol. Chem. 276, 8073-6078
25. Stempka, L., Girod, A., Muller, H. J., Rincke, G., Marks, F., Gschwendt, M. and Bossemeyer, D. (1997) Phosphorylation of protein kinase Cδ (PKCδ) at threonine 505 is not a prerequisite for enzymatic activity. Expression of rat PKCδ and an alanine 505 mutant in bacteria in a functional form. J. Biol. Chem. 272, 6805-6811
26. Garofalo, R. S. and Rosen, O. M. (1989) Insulin and insulin-like growth factor 1 (IGF-1) receptors during central nervous system development: expression of two immunologically distinct IGF-1 receptor β subunits. Mol. Cell. Biol. 9, 2806-2817
27. Campbell, D. G. and Morrice, N. A. (2002) Identification of protein phosphorylation sites by a combination of mass spectrometry and solid phase Edman sequencing. J. Biomol. Tech. 13, 119-130
28. Ellis, L., Clauser, E., Morgan, D. O., Edery, M., Roth, R. A. and Rutter, W. J. (1986) Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell (Cambridge, Mass.) 45, 721-732
29. Greene, M. W., Sakaue, H., Wang, L., Alessi, D. R. and Roth, R. A. (2003) Modulation of insulin-stimulated degradation of human insulin receptor substrate-1 by serine 312 phosphorylation. J. Biol. Chem. 278, 8199-8211
30. Reks, S. E., Smith, P. H., Messina, J. L. and Weinstock, R. S. (1998) Translocation of PKC δ by insulin in a rat hepatoma cell line. Endocrine 8, 161-167
31. Soh, J. W., Lee, E. H., Prywes, R. and Weinstein, I. B. (1999) Novel roles of specific isoforms of protein kinase C in activation of the c-fos serum response element. Mol. Cell. Biol. 19, 1313-1324
32. 307. J. Biol. Chem. 275, 9047-9054
33. De Fea, K. and Roth, R. A. (1997) Protein kinase C modulation of insulin receptor substrate-1 tyrosine phosphorylation requires serine 612. Biochemistry 36, 12939-12947
34. Eldar-Finkelman, H. and Krebs, E. G. (1997) Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action. Proc. Natl. Acad. Sci. U.S.A. 94, 9660-9664
35. Ozes, O. N., Akca, H., Mayo, L. D., Gustin, J. A., Maehama, T., Dixon, J. E. and Donner, D. B. (2001) A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through Insulin receptor substrate-1. Proc. Natl. Acad. Sci. U.S.A. 98, 4640-4645
36. Qiao, L. Y., Zhande, R., Jetton, T. L., Zhou, G. and Sun, X. J. (2002) In vivo phosphorylation of insulin receptor substrate 1 at serine 789 by a novel serine kinase in insulin-resistant rodents. J. Biol. Chem. 277, 26530-26539
37. Tanasijevic, M. J., Myers, Jr, M. G., Thoma, R. S., Crimmins, D. L., White, M. F. and Sacks, D. B. (1993) Phosphorylation of the insulin receptor substrate IRS-1 by casein kinase II. J. Biol. Chem. 268, 18157-18166
38. Jakobsen, S. N., Hardie, D. G., Morrice, N. and Tornqvist, H. E. (2001) 5′-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J. Biol. Chem. 276, 46912-46916
39. Liu, F. and Roth, R. A. (1994) Identification of serines-1035/1037 in the kinase domain of the insulin receptor as protein kinase C α mediated phosphorylation sites. FEBS Lett. 352, 389-392
40. Obenauer, J. C., Cantley, L. C. and Yaffe, M. B. (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641
41. Steen, H., Fernandez, M., Ghaffari, S., Pandey, A. and Mann, M. (2003) Phosphotyrosine mapping in Bcr/Abl oncoprotein using phosphotyrosine-specific immonium ion scanning. Mol. Cell Proteomics 2, 138-145
42. Greene, M. W. and Garofalo, R. S. (2002) Positive and negative regulatory role of insulin receptor substrate 1 and 2 (IRS-1 and IRS-2) serine/threonine phosphorylation. Biochemistry 41, 7082-7091
43. Aguirre, V., Werner, E. D., Giraud, J., Lee, Y. H., Shoelson, S. E. and White, M. F. (2002) Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem. 277, 1531-1537
44. Johnston, A. M., Pirola, L. and Van Obberghen, E. (2003) Molecular mechanisms of insulin receptor substrate protein-mediated modulation of insulin signalling. FEBS Lett. 546, 32-36
45. Clark, S. F., Molero, J. C. and James, D. E. (2000) Release of insulin receptor substrate proteins from an intracellular complex coincides with the development of insulin resistance. J. Biol. Chem. 275, 3819-3826
46. Paz, K., Hemi, R., LeRoith, D., Karasik, A., Elhanany, E., Kanety, H. and Zick, Y. (1997) A molecular basis for insulin resistance. Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxtamembrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation. J. Biol. Chem. 272, 29911-29918
47. Pederson, T. M., Kramer, D. L. and Rondinone, C. M. (2001) Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes 50, 24-31
48. Kruszynska, Y. T., Worrall, D. S., Ofrecio, J., Frias, J. P., Macaraeg, G. and Olefsky, J. M. (2002) Fatty acid-induced insulin resistance: decreased muscle PI3K activation but unchanged Akt phosphorylation. J. Clin. Endocrinol. Metab. 87, 226-234
49. Itani, S. I., Pories, W. J., MacDonald, K. G. and Dohm, G. L. (2001) Increased protein kinase C θ in skeletal muscle of diabetic patients. Metabolism 50, 553-557
50. Qu, X., Seale, J. P. and Donnelly, R. (1999) Tissue and isoform-selective activation of protein kinase C in insulin-resistant obese Zucker rats - effects of feeding. J. Endocrinol. 162, 207-214