O-linked N-acetylglucosamine modification of insulin receptor substrate-1 occurs in close proximity to multiple SH2 domain binding motifs

Molecular and Cellular Proteomics

Volumn 8, Issue 12, 2009, Pages 2733-2745

  Kleini, Amanda L ^a   Berkaw, Mary N ^a   Buse, Maria G ^a   Ball, Lauren E ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 1; N ACETYLGLUCOSAMINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN MOTIF; RAT; TANDEM MASS SPECTROMETRY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACETYLGLUCOSAMINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POLYMORPHISM, GENETIC; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; RATS; SERINE; SRC HOMOLOGY DOMAINS;

RATTUS;

EID: 72449170135     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900207-MCP200     Document Type: Article

References (43)

1. White, M. F. (2002) IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283, E413-E422
2. Myers, M. G., Jr., Mendez, R., Shi, P., Pierce, J. H., Rhoads, R., and White, M. F. (1998) The COOH-terminal tyrosine phosphorylation sites on IRS-1 bind SHP-2 and negatively regulate insulin signaling. J. Biol. Chem. 273, 26908-26914
3. Paz, K., Liu, Y. F., Shorer, H., Hemi, R., LeRoith, D., Quan, M., Kanety, H., Seger, R., and Zick, Y. (1999) Phosphorylation of insulin receptor substrate-1 (IRS-1) by protein kinase B positively regulates IRS-1 function. J. Biol. Chem. 274, 28816-28822
4. Miller, B. S., Shankavaram, U. T., Homey, M. J., Gore, A. C., Kurtz, D. T., and Rosenzweig, S. A. (1996) Activation of cJun NH2-terminal kinase/stress-activated protein kinase by insulin. Biochemistry 35, 8769-8775
5. Harrington, L. S., Findlay, G. M., Gray, A., Tolkacheva, T., Wigfield, S., Rebholz, H., Barnett, J., Leslie, N. R., Cheng, S., Shepherd, P. R., Gout, I., Downes, C. P., and Lamb, R. F. (2004) The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J. Cell Biol. 166, 213-223
6. Bouzakri, K., Roques, M., Gual, P., Espinosa, S., Guebre-Egziabher, F., Riou, J. P., Laville, M., Le Marchand-Brustel, Y., Tanti, J. F., and Vidal, H. (2003) Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 52, 1319-1325
7. Taniguchi, C. M., Emanuelli, B., and Kahn, C. R. (2006) Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 7, 85-96
8. Luo, M., Langlais, P., Yi, Z., Lefort, N., De Filippis, E. A., Hwang, H., Christ-Roberts, C. Y., and Mandarino, L. J. (2007) Phosphorylation of human insulin receptor substrate-1 at serine 629 plays a positive role in insulin signaling. Endocrinology 148, 4895-4905
9. Krüger, M., Kratchmarova, I., Blagoev, B., Tseng, Y. H., Kahn, C. R., and Mann, M. (2008) Dissection of the insulin signaling pathway via quantitative phosphoproteomics. Proc. Natl. Acad. Sci. U.S.A. 105, 2451-2456
10. Gual, P., Le Marchand-Brustel, Y., and Tanti, J. F. (2005) Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie 87, 99-109
11. Ma, Z., Gibson, S. L., Byme, M. A., Zhang, J., White, M. F., and Shaw, L. M. (2006) Suppression of insulin receptor substrate 1 (IRS-1) promotes mammary tumor metastasis. Mol. Cell. Biol. 26, 9338-9351
12. Chan, B. T., and Lee, A. V. (2008) Insulin receptor substrates (IRSs) and breast tumorigenesis. J. Mammary Gland Biol. Neoplasia 13, 415-422
13. Haltiwanger, R. S., Blomberg, M. A., and Hart, G. W. (1992) Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine:polypeptide beta-N-acetyl- glucosaminyltransferase. J. Biol. Chem. 267, 9005-9013
14. Gao, Y., Wells, L., Comer, F. I., Parker, G. J., and Hart, G. W. (2001) Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276, 9838-9845
15. Whelan, S. A., Lane, M. D., and Hart, G. W. (2008) Regulation of the O-linked beta-N-acetylglucosamine transferase by insulin signaling. J. Biol. Chem. 283, 21411-21417
16. Yang, X., Ongusaha, P. P., Miles, P. D., Havstad, J. C, Zhang, F., So, W. V., Kudlow, J. E., Michell, R. H., Olefsky, J. M., Field, S. J., and Evans, R. M. (2008) Phosphoinositide signalling links O-GIcNAc transferase to insulin resistance. Nature 451, 964-969
17. Vosseller, K., Wells, L., Lane, M. D., and Hart, G. W. (2002) Elevated nucleocytoplasmic glycosylation by O-GIcNAc results in insulin resistance associated with defects in Akt activation in 3T3-L1 adipocytes. Proc. Natl. Acad. Sci. U.S.A. 99, 5313-5318
18. Park, S. Y., Ryu, J., and Lee, W. (2005) O-GIcNAc modification on IRS-1 and Akt2 by PUGNAc inhibits their phosphorylation and induces insulin resistance in rat primary adipocytes. Exp. Mol. Med. 37, 220-229
19. D'Alessandris, C., Andreozzi, F., Federici, M., Cardellini, M., Brunetti, A., Ranalli, M., Del Guerra, S., Lauro, D., Del Prato, S., Marchetti, P., Lauro, R., and Sesti, G. (2004) Increased O-glycosylation of insulin signaling proteins results in their impaired activation and enhanced susceptibility to apoptosis in pancreatic beta-cells. FASEB J. 18, 959-961
20. Federici, M., Menghini, R., Mauriello, A., Hribal, M. L., Ferrelli, F., Laura, D., Sbraccia, P., Spagnoli, L. G., Sesti, G., and Lauro, R. (2002) Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation 106, 466-472
21. Patti, M. E., Virkamäki, A., Landaker, E. J., Kahn, C. R., and Yki-Järvinen, H. (1999) Activation of the hexosamine pathway by glucosamine in vivo induces insulin resistance of early postreceptor insulin signaling events in skeletal muscle. Diabetes 48, 1562-1571
22. Copeland, R. J., Bullen, J. W., and Hart, G. W. (2008) Cross-talk between GIcNAcylation and phosphorylation: roles in insulin resistance and glucose toxicity. Am. J. Physiol. Endocrinol. Metab. 295, E17-E28
23. Buse, M. G. (2006) Hexosamines, insulin resistance, and the complications of diabetes: current status. Am. J. Physiol. Endocrinol. Metab. 290, E1-E8
24. Andreozzi, F., D'Alessandris, C., Federici, M., Laratta, E., Del Guerra, S., Del Prato, S., Marchetti, P., Lauro, R., Perticone, F., Sesti, G., Pandolfi, A., De Filippis, E. A., Pellegrini, G., Menghini, R., Lauro, D., Cardellini, M., Romano, M., and Consoli, A. (2004) Activation of the hexosamine pathway leads to phosphorylation of insulin receptor substrate-1 on Ser307 and Ser612 and impairs the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin insulin biosynthetic pathway in RIN pancreatic beta-cells. Endocrinology 145, 2845-2857
25. Housley, M. P., Rodgers, J. T., Udeshi, N. D., Kelly, T. J., Shabanowitz, J., Hunt, D. F., Puigserver, P., and Hart, G. W. (2008) O-GIcNAc regulates FoxO activation in response to glucose. J. Biol. Chem. 283, 16283-16292
26. Luo, B., Parker, G. J., Cooksey, R. C., Soesanto, Y., Evans, M., Jones, D., and McClain, D. A. (2007) Chronic hexosamine flux stimulates fatty acid oxidation by activating AMP-activated protein kinase in adipocytes. J. Biol. Chem. 282, 7172-7180
27. Dearth, R. K., Cui, X., Kim, H. J., Kuiatse, I., Lawrence, N. A., Zhang. X., Divisova, J., Britton, O. L., Mohsin, S., Allred, D. C., Hadsell, D. L., and Lee, A. V. (2006) Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate 1 (IRS-1) or IRS-2. Mol. Cell. Biol. 26, 9302-9314
28. Mikesh, L. M., Ueberheide, B., CN, A., Coon, J. J., Syka, J. E., Shabanowitz, J., and Hunt, D. F. (2006) The utility of ETD mass spectrometry in proteomic analysis. Biochim. Biophys. Acta 1764, 1811-1822
29. Chalkley, R. J., Baker, P. R., Huang, L, Hansen, K. C, Allen, N. P., Rexach, M., and Burlingame, A. L (2005) Comprehensive analysis of a multidimensional liquid chromatography mass spectrometry dataset acquired on a quadrupole selecting, quadrupole collision cell, time-of-flight mass spectrometer: II. new developments in Protein Prospector allow for reliable and comprehensive automatic analysis of large datasets. Mol. Cell. Proteomics 4, 1194-1204
30. McGettrick, A. J., Feener, E. P., and Kahn, C. R. (2005) Human insulin receptor substrate-1 (IRS-1) polymorphism G972R causes IRS-1 to associate with the insulin receptor and inhibit receptor autophosphorylation. J. Biol. Chem. 280, 6441-6446
31. Ball, L. E., Berkaw, M. N., and Buse, M. G. (2006) Identification of the major site of O-linked beta-N-acetylglucosamine modification in the C terminus of insulin receptor substrate-1. Mol. Cell. Proteomics 5, 313-323
32. Comer, F. I., Vosseller, K., Wells, L, Accavitti, M. A., and Hart, G. W. (2001) Characterization of a mouse monoclonal antibody specific for O-linked N-acetylglucosamine. Anal. Biochem. 293, 169-177
33. Skolnik, E. Y., Lee, C. H., Batzer, A., Vicentini, L. M., Zhou, M., Daly, R., Myers, M. J., Jr., Backer, J. M., Ullrich, A., White, M. F. J. Schlessing et al. (1993) The SH2/SH3 domain-containing protein GRB2 interacts with tyrosine-phosphorylated IRS1 and Shc: implications for insulin control of ras signalling. EMBO J. 12, 1929-1936
34. Luo, M., Reyna, S., Wang, L., Yi, Z., Carroll, C, Dong, L. Q., Langlais, P., Weintraub, S. T., and Mandarino, L. J. (2005) Identification of IRS-1 serine/threonine phosphorylation sites using mass spectrometry analysis; regulatory role of serine 1223. Endocrinology 146, 4410-4416
35. Sun, X. J., Crimmins, D. L., Myers, M. G., Jr., Miralpeix, M., and White, M. F. (1993) Pleiotropic insulin signals are engaged by multiSite phosphorylation of IRS-1. Mol. Cell. Biol. 13, 7418-7428
36. Yi, Z., Langlais, P., De Filippis, E. A., Luo, M., Flynn, C. R., Schroeder, S., Weintraub, S. T., Mapes, R., and Mandarino, L. J. (2007) Global assessment of regulation of phosphorylation of insulin receptor substrate-1 by insulin in vivo in human muscle. Diabetes 56, 1508-1516
37. Lu, X. M., Lu, M. Y., Fischman, A. J., and Tompkins, R. G. (2005) A new approach for sequencing human IRS1 phosphotyrosine-containing peptides using CapLC-Q-TOF(micro). J. Mass Spectrom. 40, 599-607
38. Schmelzle, K., Kane, S., Gridley, S., Lienhard, G. E., and White, F. M. (2006) Temporal dynamics of tyrosine phosphorylation in insulin signaling. Diabetes 55, 2171-2179
39. Hanke, S., and Mann, M. (2009) The phosphotyrosine interactome of the insulin receptor family and its substrates IRS-1 and IRS-2. Mol. Cell. Proteomics 8, 519-534
40. Mammarella, S., Creati, B., Esposito, D. L., Arcuri, P., Delia Loggia, F., Capani, F., Mariani-Costantini, R., Caramia, F. G., Battista, P., and Cama, A. (1998) Novel allele of the insulin receptor substrate-1 bearing two non-conservative amino acid substitutions in a patient with noninsulin-dependent diabetes mellitus. Mutations in brief no. 130. Online. Hum. Mutat. 11, 411
41. Hribal, M. L., Federici, M., Porzio, O., Lauro, D., Borboni, P., Accili, D., Lauro, R., and Sesti, G. (2000) The Gly->Arg972 amino acid polymorphism in insulin receptor substrate-1 affects glucose metabolism in skeletal muscle cells. .J. Clin. Endocrinol. Metab. 85, 2004-2013
42. Myers, M. G., Jr., Zhang, Y., Aldaz, G. A., Grammer, T., Glasheen, E. M., Yenush, L, Wang, L M., Sun, X. J., Blenis, J., Pierce, J. H., and White, M. F. (1996) YMXM motifs and signaling by an insulin receptor substrate 1 molecule without tyrosine phosphorylation sites. Mol. Cell. Biol. 16, 4147-4155
43. Seet, B. T., Dikic, I., Zhou, M. M., and Pawson, T. (2006) Reading protein modifications with interaction domains. Nat. Rev. Mol. Cell Biol. 7, 473-483