Inflammation and insulin resistance

Journal of Clinical Investigation

Volumn 116, Issue 7, 2006, Pages 1793-1801

  Shoelson, Steven E ^a,b   Lee, Jongsoon ^a   Goldfine, Allison B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOSLIN DIABETES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ACETYLSALICYLIC ACID; CHOLINE MAGNESIUM TRISALICYLATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; I KAPPA B KINASE INHIBITOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PIOGLITAZONE; ROSIGLITAZONE; SALICYLIC ACID DERIVATIVE; SALSALATE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TROGLITAZONE;

ANTIINFLAMMATORY ACTIVITY; BLEEDING; CLINICAL TRIAL; DISEASE ASSOCIATION; DRUG EFFECT; DRUG USE; GASTROINTESTINAL IRRITATION; GENETIC TRANSCRIPTION; GLUCOSE METABOLISM; HUMAN; HYPERGLYCEMIA; IMMUNOPATHOLOGY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MACROPHAGE; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; RISK ASSESSMENT;

ADIPOCYTES; ANTI-INFLAMMATORY AGENTS; CLINICAL TRIALS; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; LIVER; OBESITY; SIGNAL TRANSDUCTION;

EID: 33745861300     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI29069     Document Type: Review

References (95)

1. Ebstein, W. 1876. Zur therapie des Diabetes mellitus, insbesondere über die Anwendung des salicylsauren Natron bei demselben. Berliner Klinische Wochenschrift. 13:337-340.
2. Williamson, R.T. 1901. On the treatment of glycosuria and diabetes mellitus with sodium salicylate. Br. Med. J. 1:760-762.
3. Shoelson, S. 2002. Invited comment on W. Ebstein: on the therapy of diabetes mellitus, in particular on the application of sodium salicylate. J. Mol. Med. 80:618-619.
4. Reid, J., Macdougall, A.I., and Andrews, M.M. 1957. On the efficacy of salicylate in treating diabetes mellitus. Br. Med. J. 2:1071-1074.
5. Hecht, A., and Goldner, M.G. 1959. Reappraisal of the hypoglycemic action of acetylsalicylate. Metabolism. 8:418-428.
6. Gilgore, S.G. 1960. The influence of salicylate on hyperglycemia. Diabetes. 9:392-393.
7. Baron, S.H. 1982. Salicylates as hypoglycemic agents. Diabetes Care. 5:64-71.
8. Yuan, M., et al. 2001. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkβ. Science. 293:1673-1677.
9. Hundal, R.S., et al. 2002. Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J. Clin. Invest. 109:1321-1326. doi:10.1172/JCI200214955.
10. Shoelson, S.E., Lee, J., and Yuan, M. 2003. Inflammation and the IKKβ/IkkB/NF-κB axis in obesityand diet-induced insulin resistance. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3):S49-S52.
11. Fearnley, G.R., Vincent, C.T., and Chakrabarti, R. 1959. Reduction of blood fibrinolytic activity in diabetes mellitus by insulin. Lancet. 2:1067.
12. Ogston, D., and McAndrew, G.M. 1964. Fibrinolysis in obesity. Lancet. 14:1205-1207.
13. Grace, C.S., and Goldrick, R.B. 1968. Fibrinolysis and body build. Interrelationships between blood fibrinolysis, body composition and parameters of lipid and carbohydrate metabolism. J. Atheroscler. Res. 8:705-719.
14. Tataranni, P.A., and Ortega, E. 2005. A burning question: does an adipokine-induced activation of the immune system mediate the effect of overnutrition on type 2 diabetes? Diabetes. 54:917-927.
15. Schmidt, M.I., 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.
16. Duncan, B.B., et al. 2003. Low-grade systemic inflammation and the development of type 2 diabetes: the Atherosclerosis Risk in Communities study. Diabetes. 52:1799-1805.
17. Pradhan, A.D., Manson, J.E., Rifai, N., Buring, J.E., and Ridker, P.M. 2001. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 286:327-334.
18. Barzilay, J.I., et al. 2001. The relation of markers of inflammation to the development of glucose disorders in the elderly: the Cardiovascular Health Study. Diabetes. 50:2384-2389.
19. Vozarova, B., et al. 2002. High white blood cell count is associated with a worsening of insulin sensitivity and predicts the development of type 2 diabetes. Diabetes. 51:455-461.
20. Festa, A., D'Agostino, R., Jr., Tracy, R.P., and Haffner, S.M. 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.
21. Freeman, D.J., et al. 2002. C-reactive protein is an independent predictor of risk for the development of diabetes in the West of Scotland Coronary Prevention Study. Diabetes. 51:1596-1600.
22. Ford, E.S. 2002. Leukocyte count, erythrocyte sedimentation rate, and diabetes incidence in a national sample of US adults. Am. J. Epidemiol. 155:57-64.
23. Prince, R.L., Larkins, R.G., and Alford, F.P. 1981. The effect of acetylsalicylic acid on plasma glucose and the response of glucose regulatory hormones to intravenous glucose and arginine in insulin treated diabetics and normal subjects. Metabolism. 30:293-298.
24. Nakanishi, N., Yoshida, H., Matsuo, Y., Suzuki, K., and Tatara, K. 2002. White blood-cell count and the risk of impaired fasting glucose or type II diabetes in middle-aged Japanese men. Diabetologia. 45:42-48.
25. Spranger, J., et al. 2003. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes. 52:812-817.
26. Haffner, S., et al. 2005. Intensive lifestyle intervention or metformin on inflammation and coagulation in participants with impaired glucose tolerance. Diabetes. 54:1566-1572.
27. Hotamisligil, G.S., Shargill, N.S., and Spiegelman, B.M. 1993. Adipose expression of tumor necrosis factor-a: direct role in obesity-linked insulin resistance. Science. 259:87-91.
28. Feinstein, R., Kanety, H., Papa, M.Z., Lunenfeld, B., and Karasik, A. 1993. Tumor necrosis factor-a suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J. Biol. Chem. 268:26055-26058.
29. Hotamisligil, G.S., and Spiegelman, B.M. 1994. Tumor necrosis factor alpha: a key component of the obesity-diabetes link. Diabetes. 43:1271-1278.
30. Pickup, J.C., and Crook, M.A. 1998. Is type II diabetes mellitus a disease of the innate immune system? Diabetologia. 41:1241-1248.
31. Kolb, H., and Mandrup-Poulsen, T. 2005. An immune origin of type 2 diabetes? Diabetologia. 48:1038-1050.
32. Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., and Friedman, J.M. 1994. Positional cloning of the mouse obese gene and its human homologue. Nature. 372:425-432.
33. Fried, S.K., Bunkin, D.A., and Greenberg, A.S. 1998. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J. Clin. Endocrinol. Metab. 83:847-850.
34. Steppan, C.M., et al. 2001. The hormone resistin links obesity to diabetes. Nature. 409:307-312.
35. Shimomura, I., et al. 1996. Enhanced expression of PAI-1 in visceral fat: possible contributor to vascular disease in obesity. Nat. Med. 2:800-803.
36. Fukuhara, A., et al. 2005. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 307:426-430.
37. Scherer, P.E., Williams, S., Fogliano, M., Baldini, G., and Lodish, H.F. 1995. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270:26746-26749.
38. Kopp, E., and Ghosh, S. 1994. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science. 265:956-959.
39. Pierce, J.W., Read, M.A., Ding, H., Luscinskas, F.W., and Collins, T. 1996. Salicylates inhibit I kappa B-alpha phosphorylation, endothelial-leukocyte adhesion molecule expression, and neutrophil transmigration. J. Immunol. 156:3961-3969.
40. Yin, M.J., Yamamoto, Y., and Gaynor, R.B. 1998. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I.B kinase-β. Nature. 396:77-80.
41. Aguirre, V., Uchida, T., Yenush, L., Davis, R., and White, M.F. 2000. The c-Jun N-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J. Biol. Chem. 275:9047-9054.
42. Hirosumi, J., et al. 2002. A central role for JNK in obesity and insulin resistance. Nature. 420:333-336.
43. Cai, D., et al. 2005. Local and systemic insulin resistance resulting from hepatic activation of IKKβ and NF-.B. Nat. Med. 11:183-190.
44. Akira, S., Uematsu, S., and Takeuchi, O. 2006. Pathogen recognition and innate immunity. Cell. 124:783-801.
45. Lee, J.Y., Sohn, K.H., Rhee, S.H., and Hwang, D. 2001. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276:16683-16689.
46. Ramasamy, R., Yan, S.F., and Schmidt, A.M. 2005. The RAGE axis and endothelial dysfunction: maladaptive roles in the diabetic vasculature and beyond. Trends Cardiovasc. Med. 15:237-243.
47. Bierhaus, A., et al. 2005. Understanding RAGE, the receptor for advanced glycation end products. J. Mol. Med. 83:876-886.
48. Keaney, J.F., Jr., et al. 2003. Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler. Thromb. Vasc. Biol. 23:434-439.
49. Furukawa, S., et al. 2004. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114:1752-1761. doi:10.1172/JCI200421625.
50. Lin, Y., et al. 2005. The hyperglycemia-induced inflammatory response in adipocytes: the role of reactive oxygen species. J. Biol. Chem. 280:4617-4626.
51. Ozcan, U., et al. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 306:457-461.
52. Straczkowski, M., et al. 2004. Relationship between insulin sensitivity and sphingomyelin signaling pathway in human skeletal muscle. Diabetes. 53:1215-1221.
53. Summers, S.A. 2006. Ceramides in insulin resistance and lipotoxicity. Prog. Lipid Res. 45:42-72.
54. Griffin, M.E., et al. 1999. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes. 48:1270-1274.
55. 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 IkappaB-alpha. Diabetes. 51:2005-2011.
56. Kim, J.K., et al. 2001. Prevention of fat-induced insulin resistance by salicylate. J. Clin. Invest. 108:437-446.
57. Aguirre, V., et al. 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.
58. Werner, E.D., Lee, J., Hansen, L., Yuan, M., and Shoelson, S.E. 2004. Insulin resistance due to phosphorylation of insulin receptor substrate-1 at serine 302. J. Biol. Chem. 279:35298-35305.
59. Zick, Y. 2005. Ser/Thr phosphorylation of IRS proteins: a molecular basis for insulin resistance. Sci. STKE. 268:e4.
60. Tedder, T.F., Steeber, D.A., Chen, A., and Engel, P. 1995. The selectins: vascular adhesion molecules. FASEB J. 9:866-873.
61. Adams, D.H., and Shaw, S. 1994. Leucocyte-endothelial interactions and regulation of leucocyte migration. Lancet. 343:831-836.
62. Warner, S.J., and Libby, P. 1989. Human vascular smooth muscle cells. Target for and source of tumor necrosis factor. J. Immunol. 142:100-109.
63. Barath, P., et al. 1990. Detection and localization of tumor necrosis factor in human atheroma. Am. J. Cardiol. 65:297-302.
64. Seino, Y., et al. 1994. Interleukin 6 gene transcripts are expressed in human atherosclerotic lesions. Cytokine. 6:87-91.
65. Rus, H.G., Vlaicu, R., and Niculescu, F. 1996. Interleukin-6 and interleukin-8 protein and gene expression in human arterial atherosclerotic wall. Atherosclerosis. 127:263-271.
66. Schonbeck, U., and Libby, P. 2001. CD40 signaling and plaque instability. Circ. Res. 89:1092-1103.
67. Mach, F., Schonbeck, U., Bonnefoy, J.Y., Pober, J.S., and Libby, P. 1997. Activation of monocyte/macrophage functions related to acute atheroma complication by ligation of CD40: induction of collagenase, stromelysin, and tissue factor. Circulation. 96:396-399.
68. Libby, P. 2001. Current concepts of the pathogenesis of the acute coronary syndromes. Circulation. 104:365-372.
69. Johnson, P.R., and Hirsch, J. 1972. Cellularity of adipose depots in six strains of genetically obese mice. J. Lipid Res. 13:2-11.
70. Krotkiewski, M., Bjorntorp, P., Sjostrom, L., and Smith, U. 1983. Impact of obesity on metabolism in men and women. Importance of regional adipose tissue distribution. J. Clin. Invest. 72:1150-1162.
71. Coon, P.J., Rogus, E.M., Drinkwater, D., Muller, D.C., and Goldberg, A.P. 1992. Role of body fat distribution in the decline in insulin sensitivity and glucose tolerance with age. J. Clin. Endocrinol. Metab. 75:1125-1132.
72. Gastaldelli, A., et al. 2002. Metabolic effects of visceral fat accumulation in type 2 diabetes. J. Clin. Endocrinol. Metab. 87:5098-5103.
73. Arkan, M.C., et al. 2005. IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 11:191-198.
74. Sartipy, P., and Loskutoff, D.J. 2003. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 100:7265-7270.
75. Weisberg, S.P., et al. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112:1796-1808. doi:10.1172/JCI200319246.
76. Weisberg, S.P., et al. 2006. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Invest. 116:115-124. doi:10.1172/JCI24335.
77. Kolonin, M.G., Saha, P.K., Chan, L., Pasqualini, R., and Arap, W. 2004. Reversal of obesity by targeted ablation of adipose tissue. Nat. Med. 10:625-632.
78. Crandall, D.L., Hausman, G.J., and Kral, J.G. 1997. A review of the microcirculation of adipose tissue: anatomic, metabolic, and angiogenic perspectives. Microcirculation. 4:211-232.
79. Blake, G.J., and Ridker, P.M. 2002. Inflammatory bio-markers and cardiovascular risk prediction. J. Intern. Med. 252:283-294.
80. Racanelli, V., and Rehermann, B. 2006. The liver as an immunological organ. Hepatology. 43(Suppl. 1): S54-S62.
81. Guebre-Xabier, M., et al. 2000. Altered hepatic lymphocyte subpopulations in obesity-related murine fatty livers: potential mechanism for sensitization to liver damage. Hepatology. 31:633-640.
82. Li, Z., Soloski, M.J., and Diehl, A.M. 2005. Dietary factors alter hepatic innate immune system in mice with nonalcoholic fatty liver disease. Hepatology. 42:880-885.
83. Elinav, E., et al. 2006. Adoptive transfer of regulatory NKT lymphocytes ameliorates non-alcoholic steatohepatitis and glucose intolerance in ob/ob mice and is associated with intrahepatic CD8 trapping. J. Pathol. 209:121-128.
84. Rohl, M., et al. 2004. Conditional disruption of IêB kinase 2 fails to prevent obesity-induced insulin resistance. J. Clin. Invest. 113:474-481. doi:10.1172/JCI200418712.
85. Cai, D., et al. 2004. IKKâ/NF-êB activation causes severe muscle wasting in mice. Cell. 119:285-298.
86. Dominguez, H., et al. 2005. Metabolic and vascular effects of tumor necrosis factor-alpha blockade with etanercept in obese patients with type 2 diabetes. J. Vasc. Res. 42:517-525.
87. Gonzalez-Gay, M.A., et al. 2006. Anti-tumor necrosis factor-alpha blockade improves insulin resistance in patients with rheumatoid arthritis. Clin. Exp. Rheumatol. 24:83-86.
88. Yki-Jarvinen, H. 2004. Thiazolidinediones. N. Engl. J. Med. 351:1106-1118.
89. Pascual, G., et al. 2005. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature. 437:759-763.
90. Ialenti, A., et al. 2005. Mechanism of the antiinflammatory effect of thiazolidinediones: relationship with the glucocorticoid pathway. Mol. Pharmacol. 67:1620-1628.
91. Xiang, A.H., et al. 2006. Effect of pioglitazone on pancreatic beta-cell function and diabetes risk in Hispanic women with prior gestational diabetes. Diabetes. 55:517-522.
92. Meisner, F., et al. 2006. Effect of rosiglitazone treatment on plaque inflammation and collagen content in nondiabetic patients: data from a randomized placebo-controlled trial. Arterioscler. Thromb. Vasc. Biol. 26:845-850.
93. Dormandy, J.A., et al. 2005. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet. 366:1279-1289.
94. Glass, C.K., and Ogawa, S. 2006. Combinatorial roles of nuclear receptors in inflammation and immunity. Nat. Rev. Immunol. 6:44-55.
95. Castrillo, A., and Tontonoz, P. 2004. Nuclear receptors in macrophage biology: at the crossroads of lipid metabolism and inflammation. Annu. Rev. Cell Dev. Biol. 20:455-480.