C-reactive protein induces phosphorylation of insulin receptor substrate-1 on Ser307 and Ser612 in L6 myocytes, thereby impairing the insulin signalling pathway that promotes glucose transport

Diabetologia

Volumn 50, Issue 4, 2007, Pages 840-849

  D'Alessandris, C ^a   Lauro, R ^a   Presta, I ^b   Sesti, G ^b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

CRP; Glucose transport; Insulin resistance; Insulin signalling

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; C REACTIVE PROTEIN; ENDOTOXIN; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P85; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; SERINE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TYROSINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE TRANSLOCATION; GLUCOSE TRANSPORT; GLYCOGEN SYNTHESIS; INSULIN RESISTANCE; MUSCLE CELL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL TRANSPORT; C-REACTIVE PROTEIN; CELL LINE; ENDOTOXINS; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MUSCLE CELLS; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SERINE; SIGNAL TRANSDUCTION;

EID: 33847616879     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-006-0522-y     Document Type: Article

References (50)

1. Pickup JC, Mattock MB, Chusney GD, Burt D (2004) Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diabetes Care 27:813-823
2. Fernandez-Real JM, Ricart J (2003) Insulin resistance and chronic cardiovascular inflammatory syndrome. Endocr Rev 24:278-301
3. Schmidt MI, Duncan BB, Sharrett AR et al (1999) Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis risk in communities study): a cohort study. Lancet 353:1649-1652
4. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286:327-334
5. Festa A, D'Agostino R, Howard G, Mykkanen L, Tracey RP, Haffner SM (2000) Chronic subclinical inflammation as part of the insulin resistance syndrome. The Insulin Resistance Atherosclerosis Study (IRAS). Circulation 101:42-47
6. Ford ES (1999) Body mass index, diabetes, and C-reactive protein among US adults. Diabetes 22:1971-1977
7. Temelkova-Kurktschiev T, Henkel E, Koehler C, Karrei K, Hanefield M (2002) Subclinical inflammation in newly detected type II diabetes and impaired glucose tolerance. Diabetologia 45:151
8. Festa A, D'Agostino R, Tracy RP, Haffner SM (2002) Elevated levels of acute-phase proteins and plasminogen activator inhibitor?1 predict the development of type 2 diabetes. The Insulin Resistance Atherosclerosis Study. Diabetes 51:1131-1137
9. De Fea K, Roth RA (1997) Modulation of insulin receptor substrate-1 tyrosine phosphorylation and function by mitogen-activated protein kinase. J Biol Chem 272:31400-31406
10. De Fea K, Roth RA (1997) Protein kinase C modulation of insulin receptor substrate-1 tyrosine phosphorylation requires serine 612. Biochemistry 36:12939-12947
11. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM (1996) IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271:665-668
12. Aguirre V, Uchida T, Yenush L, Davis R, White MF (2000) The c-Jun NH(2)-termrinal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 275:9047-9054
13. Hirosumi J, Tuncman G, Chang L et al (2002) A central role for JNK in obesity and insulin resistance. Nature 420:333-336
14. Tuncman G, Hirosumi J, Solinas G, Chang L, Karin M, Hotamisligil GS (2006) Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci USA 103:10741-10746
15. Araki E, Lipes MA, Patti ME et al (1994) Alternative pathways of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372:186-190
16. Tamemoto H, Kadowaki T, Tobe K et al (1994) Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature 372:182-186
17. Withers DJ, Gutierrez JS, Towery H et al (1998) Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391:900-903
18. Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ, Dohm GL (1995) Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest 95:2195-2204
19. Rondinone CM, Wang LM, Lonnroth P, Wesslau C, Pierce JH, Smith U (1997) Insulin receptor substrate (IRS) 1 is reduced and IRS-2 is the main docking protein for phosphatidylinositol 3-kinase in adipocytes from subjects with non-insulin-dependent diabetes mellitus. Proc Natl Acad Sci USA 94:4171-4175
20. Bjornholm M, Kawano Y, Lehtihet M, Zierath JR (1997) Insulin receptor substrate-1 phosphorylation and phosphatidylinositol 3-kinase activity in skeletal muscle from NIDDM subjects after in vivo insulin stimulation. Diabetes 46:524-527
21. Sesti G, Federici M, Hribal ML, Lauro D, Sbraccia P, Lauro R (2001) Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J 15:2099-2111
22. Almind K, Bjorbaek C, Vestergaard H, Hansen T, Echwald SM, Pedersen O (1993) Amino acid polymorphism in insulin receptor substrate-1 in non-insulin-dependent diabetes mellitus. Lancet 342:828-832
23. 972 variant in insulin receptor substrate-1 is associated with an atherogenic profile in offspring of type 2 diabetic patients. J Clin Endocrinol Metab 88:3368-3371
24. Verma S, Wang CH, Li SH et al (2002) A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 106:913-919
25. Verma S, Badiwala MV, Weisel RD et al (2003) C-reactive protein activates the nuclear factor-kB signal transduction pathway in saphenous vein endothelial cells: implications for atherosclerosis and restenosis. J Thorac Cardiovasc Surg 126:1886-1891
26. Hattori Y, Matsumura M, Kasai K (2003) Vascular smooth muscle cell activation by C-reactive protein. Cardiovasc Res 58:186-195
27. 12 myocytes lack an insulin-responsive vescicular compartment despite dexamethasone-induced GLUT4 expression. Am J Physiol Endocrinol Metab 283:E514-E524
28. Lewis TS, Shapiro PS, Ahn NG (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74:49-139
29. Davis RJ (1999) Signal transduction by the c-Jun N terminal kinase. Biochem Soc Symp 64:1-12
30. Esposito DL, Li Y, Cama A (2001) Tyr(612) and Tyr(632) in human insulin receptor substrate-1 are important for full activation of insulin-stimulated phosphatidylinositol 3-kinase activity and translocation of GLUT4 in adipose cells. Endocrinology 142:2833-2840
31. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789
32. Hajduch E, Alessi DR, Hemmings BA, Hundal HS (1998) Constitutive activation of protein kinase B α by membrane targeting promotes glucose and system A amino acid transport, protein synthesis, and inactivation of glycogen synthase kinase 3 in L6 muscle cells. Diabetes 47:1006-1013
33. Klip A, Ramlal T, Douen AG, Bilan PJ, Skoreck L (1998) Inhibition by forskolin of insulin-stimulated glucose transport in L6 muscle cells. Biochem J 255:1023-1029
34. Pedrini MT, Kranebitter M, Niederwanger A et al (2005) Human triglyceride-rich lipoproteins impair glucose metabolism and insulin signaling in L6 muscle cells independently of non-esterified fatty acid levels. Diabetologia 48:756-766
35. Marnell LL, Mold C, Volzer MA, Burlingame RW, Du Clos TW (1995) C-reactive protein binds to FcγRI in transfected COS cells. J Immunol 155:2185-2193
36. Bharadwaj D, Stein P, Volzer M, Mold C, Du Clos TW (1999) The major receptor for C-reactive protein on leukocytes is Fcγ receptor II. J Exp Med 190:585-590
37. Williams TN, Zhang CX, Game BA, He L, Huang Y (2004) C-reactive protein stimulates MMP-1 expression in U937 histocytes through FcγRII and extracellular signal-regulated kinase pathway: an implication of CRP involvement in plaque destabilization. Arterioscler Thromb Vasc Biol 24:61-66
38. Oriente F, Formisano P, Miele C et al (2001) Insulin receptor substrate-2 phosphorylation is necessary for protein kinase C zeta activation by insulin in L6hIR cells. J Biol Chem 276:37109-37119
39. Kaneto H, Nakatani Y, Miyatsuka T et al (2004) Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nat Med 10:1128-1132
40. Bouzakri K, Roques M, Gual P et al (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
41. Carlson CJ, Koterski S, Sciotti RJ, Poccard GB, Rondinone CM (2003) Enhanced basal activation of mitogen-activated protein kinases in adipocytes from type 2 diabetes: potential role of p38 in the downregulation of GLUT4 expression. Diabetes 52:634-641
42. Morino K, Petersen KF, Dufour S et al (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115:3587-3593
43. Bost F, Aouadi M, Caron L et al (2005) The extracellular signal-regulated kinase isoform ERK1 is specifically required for in vitro and in vivo adipogenesis. Diabetes 54:402-411
44. Gual P, Gremeaux T, Gonzalez T, Le Marchand-Brustel Y, Tanti JF (2003) MAP kinases and mTOR mediate insulin-induced phosphorylation of insulin receptor substrate-1 on serine residues 307, 612 and 632. Diabetologia 46:1532-1542
45. van den Berg CW, Taylor KE, Lang D (2004) C-reactive protein-induced in vitro vasorelaxation is an artefact caused by the presence of sodium azide in commercial preparations. Arterioscler Thromb Vasc Biol 24:e168-e171
46. Liu C, Wang S, Deb A et al (2005) Proapoptotic, antimigratory, antiproliferative, and antiangiogenic effects of commercial C-reactive protein on various human endothelial cell types: in vitro implications of contaminating presence of sodium azide in commercial preparation. Circ Res 97:135-143
47. Taylor KE, Giddings JC, van den Berg CW (2005) C-Reactive protein-induced in vitro endothelial cell activation is an artefact caused by azide and lipopolysaccharide. Arterioscler Thromb Vasc Biol 25:1225-1230
48. The Diabetes Prevention Program Research Group (2005) Intensive lifestyle intervention or metformin on inflammation and coagulation in participants with impaired glucose tolerance. Diabetes 54:1566-1572
49. Haffner SM, Greenberg AS, Weston WM, Chen H, Williams K, Freed MI (2002) Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus. Circulation 106:679-684
50. Satoh N, Ogawa Y, Usui T et al (2003) Anti-atherogenic effect of pioglitazone in type 2 diabetic patients irrespective of the responsiveness to its antidiabetic effect. Diabetes Care 26:2493-2499