Inflammation, stress, and diabetes

Journal of Clinical Investigation

Volumn 115, Issue 5, 2005, Pages 1111-1119

  Wellen, Kathryn E ^a   Hotamisligil, Gökhan S ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; C REACTIVE PROTEIN; COLONY STIMULATING FACTOR 1; FIBRIC ACID DERIVATIVE; HAPTOGLOBIN; I KAPPA B KINASE; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; LIVER X RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROLYLLEUCYLGLYCINAMIDE; RESISTIN; SALICYLIC ACID; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

ATHEROSCLEROSIS; CHRONIC INFLAMMATION; DIABETES MELLITUS; FATTY ACID OXIDATION; GLUCOSE METABOLISM; HUMAN; HYPERLIPIDEMIA; IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; INSULIN RESISTANCE; MACROPHAGE; METABOLISM; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; STRESS;

ADIPOCYTES; ANIMALS; DIABETES MELLITUS; HUMANS; INFLAMMATION; INSULIN RESISTANCE; MACROPHAGES; OBESITY; STRESS;

EID: 18244370762     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200525102     Document Type: Review

References (110)

1. Khovidhunkit, W., et al. 2004. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host [review]. J. Lipid Res. 45:1169-1196.
2. Chandra, R.K. 1996. Nutrition, immunity and infection: from basic knowledge of dietary manipulation of immune responses to practical application of ameliorating suffering and improving survival. Proc. Natl. Acad. Sci. U. S. A. 93:14304-14307.
3. Blackburn, G.L. 2001. Pasteur's Quadrant and malnutrition. Nature. 409:397-401.
4. Cummings, D.E., and Schwartz, M.W. 2003. Genetics and pathophysiology of human obesity. Annu. Rev. Med. 54:453-471.
5. Hotamisligil, G.S. 2004. Inflammation, TNFalpha, and insulin resistance. In Diabetes mellitus: a fundamental and clinical text. D.T.S. LeRoith and J.M. Olefsky, editors. 3rd edition. Lippincott, Williams and Wilkins. New York, New York, USA. 953-962.
6. Hotamisligil, G.S., Shargill, N.S., and Spiegelman, B.M. 1993. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 259:87-91.
7. Sethi, J.K., and Hotamisligil, G.S. 1999. The role of TNF alpha in adipocyte metabolism. Semin. Cell Dev. Biol. 10:19-29.
8. Hotamisligil, G.S., et al. 1995. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J. Clin. Invest. 95:2409-2415.
9. Kern, P.A., et al. 1995. The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J. Clin. Invest. 95:2111-2119.
10. Saghizadeh, M., et al. 1996. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J. Clin. Invest. 97:1111-1116.
11. Uysal, K.T., et al. 1997. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature. 389:610-614.
12. Pickup, J.C. 2004. Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diabetes Care. 27:813-823.
13. Dandona, P., Aljada, A., and Bandyopadhyay, A. 2004. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol. 25:4-7.
14. Miller, C., et al. 1998. Tumor necrosis factor-alpha levels in adipose tissue of lean and obese cats. J. Nutr. 128(Suppl. 12):2751S-2752S.
15. Soukas, A., et al. 2000. Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev. 14:963-980.
16. 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.
17. Xu, H., et al. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112:1821-1830. doi:10.1172/JCI200319451.
18. Fernandes, G., et al. 1978. Immune response in the mutant diabetic C57BL/Ks-dt+ mouse. Discrepancies between in vitro and in vivo immunological assays J. Clin. Invest. 61:243-250.
19. Farooqi, I.S., et al. 2002. Beneficial effects of leptin on obesity, T cell hyporesponsiveness, and neuroendocrine/metabolic dysfunction of human congenital leptin deficiency. J. Clin. Invest. 110:1093-1103. doi:10.1172/JCI200215693.
20. Chandra, R.K. 1980. Cell-mediated immunity in genetically obese C57BL/6J ob/ob) mice. Am. J. Clin. Nutr. 33:13-16.
21. Lotd, G.M., et al. 1998. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 394:897-901.
22. Berg, A.H., Combs, T.P., and Scherer, P.E. 2002. ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol. Metab. 13:84-89.
23. Ouchi, N., et al. 2003. Obesity, adiponeccin and vascular inflammatory disease. Curr. Opin. Lipidol. 14:561-566.
24. Steppan, C.M., and Lazar, M.A. 2004. The current biology of resistin. J. Intern. Med. 255:439-447.
25. Lehrke, M., et al. 2004. An inflammatory cascade leading to hyperresistinemia in humans. PLoS Med. 1:e45. doi:10.1371/journal.pmed.0010045.
26. Fukuhara, A., et al. 2005. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 307:426-430.
27. Makowski, L., et al. 2001. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat. Med. 7:699-705.
28. Tontonoz, P., et al. 1998. PPARgamma promotes monocyte/macrophage differenciation and uptake of oxidized LDL. Cell. 93:241-252.
29. Bouloumie, A., et al. 2001. Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes. 50:2080-2086.
30. Cousin, B., et al. 1999. A role for preadipocytes as macrophage-like cells. FASEB J. 13:305-312.
31. Charriere, G., et al. 2003. Preadipocyte conversion to macrophage. Evidence of plasticity. J. Biol. Chem. 278:9850-9855.
32. White, M.F. 1997. The insulin signalling system and the IRS proteins. Diabetologia. 40(Suppl. 2):S2-S17.
33. Saltiel, A.R., and Pessin, J.E. 2002. Insulin signaling pathways in time and space. Trends Cell Biol. 12:65-71.
34. Yin, M.J., Yamamoto, Y., and Gaynor, R.B. 1998. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature. 396:77-80.
35. Hotamisligil, G.S., et al. 1996. TRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science. 271:665-668.
36. Aguirre, V., et al. 2000. The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J. Biol. Chem. 275:9047-9054.
37. 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.
38. Paz, K., et al. 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.
39. Ozcan, U., et al. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 306:457-461.
40. Nakatani, Y., et al. 2005. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J. Biol. Chem. 280:847-851.
41. Ozawa, K., et al. 2005. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes. Diabetes. 54:657-663.
42. Lin, Y., et al. 2005. The hyperglycemia-induced inflammatory response in adipocytes: the role of reactive oxygen species. J. Biol. Chem. 280:4617-4626.
43. 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.
44. Zick, Y. 2003. Role of Ser/Thr kinases in the uncoupling of insulin signaling. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3):S56-S60.
45. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135-145.
46. Davis, R.J. 2000. Signal transduction by the JNK group of MAP kinases. Cell. 103:239-252.
47. Hirosumi, J., et al. 2002. A central role for JNK in obesity and insulin resistance. Nature. 420:333-336.
48. Gao, Z., et al. 2004. Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3T3-L1 adipocytes. Mol. Endocrinol. 18:2024-2034.
49. Nakatani, Y., et al. 2004. Modulation of the JNK pathway in liver affects insulin resistance status. J. Biol. Chem. 279:45803-45809.
50. Waeber, G., et al. 2000. The gene MAPK8IP1, encoding islet-brain-1, is a candidate for type 2 diabetes. Nat. Genet. 24:291-295.
51. Jaeschke, A., Czech, M.P., and Davis, R.J. 2004. An essential role of the JIP1 scaffold protein for JNK activation in adipose tissue. Genes Dev. 18:1976-1980.
52. Ricci, R., et al. 2004. Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science. 306:1558-1561.
53. Kaneto, H., et al. 2004. Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nat. Med. 10:1128-1132.
54. Yu, C., et al. 2002. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277:50230-50236.
55. Perseghin, G., Petersen, K., and Shulman, G.I. 2003. Cellular mechanism of insulin resistance: potential links with inflammation. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3):S6-S11.
56. Schmitz-Peiffer, C. 2002. Protein kinase C and lipid-induced insulin resistance in skeletal muscle. Ann. N. Y. Acad. Sci. 967:146-157.
57. Gao, Z., et al. 2002. Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J. Biol. Chem. 277:48115-48121.
58. Shoelson, S.E., Lee, J., and Yuan, M. 2003. Inflammation and the IKK beta/1 kappa B/NF-kappa B axis in obesity- and diet-induced insulin resistance. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3):S49-S52.
59. Yuan, M., et al. 2001. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science. 293:1673-1677.
60. Kim, J.K., et al. 2001. Prevention of fat-induced insulin resistance by salicylate. J. Clin. Invest. 108:437-446. doi:10.1172/JCI200111559.
61. 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.
62. Cai, D., et al. 2005. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat. Med. 11:183-190.
63. Arkan, M.C., et al. 2005. IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 11:191-198.
64. Rohl, M., et al. 2004. Conditional disruption of IkappaB kinase 2 fails to prevent obesity-induced insulin resistance. J. Clin. Invest. 113:474-481. doi:10.1172/JCI200418712.
65. Rui, L., et al. 2002. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J. Biol. Chem. 277:42394-42398.
66. Mooney, R.A., et al. 2001. Suppressors of cytokine signaling-1 and -6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance. J. Biol. Chem. 276:25889-25893.
67. Emanuelli, B., et al. 2001. SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-alpha in the adipose tissue of obese mice. J. Biol. Chem. 276:47944-47949.
68. Ueki, K., Kondo, T., and Kahn, C.R. 2004. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol. Cell Biol. 24:5434-5446.
69. Mori, H., et al. 2004. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med. 10:739-743.
70. Howard, J.K., et al. 2004. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat. Med. 10:734-738.
71. Shimabukuro, M., et al. 1997. Role of nitric oxide in obesity-induced beta cell disease. J. Clin. Invest. 100:290-295.
72. Perreault, M., and Marette, A. 2001. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat. Med. 7:1138-1143.
73. Seo, J.B., et al. 2004. Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-activated receptor gamma expression. Mol. Cell. Biol. 24:3430-3444.
74. Moller, D.E., and Berger, J.P. 2003. Role of PPARs in the regulation of obesity-related insulin sensitivity and inflammation. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3):S17-S21.
75. Joseph, S.B., et al. 2003. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat. Med. 9:213-219.
76. Jiang, C., Ting, A.T., and Seed, B. 1998. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature. 391:82-86.
77. Chawla, A., et al. 2001. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 7:48-52.
78. Chawla, A., et al. 2001. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol. Cell. 7:161-171.
79. Daynes, R.A., and Jones, D.C. 2002. Emerging roles of PPARs in inflammation and immunity. Nat. Rev. Immunol. 2:748-759.
80. Castrillo, A., et al. 2003. Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol. Cell. 12:805-816.
81. Bjorkbacka, H., et al. 2004. Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat. Med. 10:416-421.
82. Joseph, S.B., et al. 2004. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell. 119:299-309.
83. Lee, C.H., et al. 2003. Transcriptional repression of atherogenic inflammation: modulation by PPARdelta. Science. 302:453-457.
84. Maeda, K., et al. 2005. Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metabolism. 1:107-119.
85. Spiegelman, B.M. 1998. PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes. 47:507-514.
86. Makowski, L., and Hotamisligil, G.S. 2004. Fatty acid binding proteins - the evolutionary crossroads of inflammatory and metabolic responses. J. Nutr. 134:2464S-2468S.
87. Lee, C.H., Olson, P., and Evans, R.M. 2003. Mini-review: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology. 144:2201-2207.
88. Laffitte, B.A., et al. 2003. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. U. S. A. 100:5419-5424.
89. Wellen, K.E., et al. 2004. Interaction of tumor necrosis factor-alpha- and thiazolidinedione-regulated pathways in obesity. Endocrinology. 145:2214-2220.
90. Peraldi, P., Xu, M., and Spiegelman, B.M. 1997. Thiazolidinediones block tumor necrosis factor-alpha-induced inhibition of insulin signaling. J. Clin. Invest. 100:1863-1869.
91. Ruan, H., Pownall, H.J., and Lodish, H.F. 2003. Troglitazone antagonizes tumor necrosis factor-alpha-induced reprogramming of adipocyte gene expression by inhibiting the transcriptional regulatory functions of NF-kappaB. J. Biol. Chem. 278:28181-28192.
92. Miles, P.D., et al. 1997. TNF-alpha-induced insulin resistance in vivo and its prevention by troglitazone. Diabetes. 46:1678-1683.
93. Lehmann, J.M., et al. 1995. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J. Biol. Chem. 270:12953-12956.
94. Staels, B., et al. 1998. Activation of human aortic smooth-muscle cells is inhibited by PPARalpha but not by PPARgamma activators. Nature. 393:790-793.
95. Knobler, H., et al. 2003. Tumor necrosis factor-alpha-induced insulin resistance may mediate the hepatitis C virus-diabetes association. Am. J. Gastroenterol. 98:2751-2756.
96. Bahtiyar, G., et al. 2004. Association of diabetes and hepatitis C infection: epidemiologic evidence and pathophysiologic insights. Curr. Diab. Rep. 4:194-198.
97. Iribarren, C., Tolstykh, I.V., and Eisner, M.D. 2004. Are patients with asthma at increased risk of coronary heart disease? Int. J. Epidemiol. 33:743-748.
98. Rana, J.S., et al. 2004. Chronic obstructive pulmonary disease, asthma, and risk of type 2 diabetes in women. Diabetes Care. 27:2478-2484.
99. Sattar, N., et al. 2003. Explaining how "high-grade" systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation. 108:2957-2963.
100. Hung, J.H., et al. 2004, Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-kappaB and pp38 mitogen-activated protein kinase. J. Biol. Chem. 279:46384-46392.
101. Brownlee, M. 2001. Biochemistry and molecular cell biology of diabetic complications. Nature. 414:813-820.
102. Hatada, E.N., Krappmann, D., and Scheidereit, C. 2000. NF-kappaB and the innate immune response. Curr. Opin. Immunol. 12:52-58.
103. Bluher, M., et al. 2002. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev. Cell. 3:25-38.
104. Xu, H., et al. 2002. Exclusive action of transmembrane TNF alpha in adipose tissue leads to reduced adipose mass and local but not systemic insulin resistance. Endocrinology. 143:1502-1511.
105. Lowell, B.B., and Shulman, G.I. 2005. Mitochondrial dysfunction and type 2 diabetes. Science. 307:384-387.
106. Vozarova, B., et al. 2003. The interleukin-6 (-174) G/C promoter polymorphism is associated with type-2 diabetes mellitus in Native Americans and Caucasians. Hum. Genet. 112:409-413.
107. Dalziel, B., et al. 2002. Association of the TNF-alpha -308 G/A promoter polymorphism with insulin resistance in obesity. Obes. Res. 10:401-407.
108. Costa, A., et al. 2003. Lower rate of tumor necrosis factor-alpha -863A allele and higher concentration of tumor necrosis factor-alpha receptor 2 in first-degree relatives of subjects with type 2 diabetes. Metabolism. 52:1068-1071.
109. Furuta, M., et al. 2002. Relationship of the tumor necrosis factor-alpha-308 A/G promoter polymorphism with insulin sensitivity and abdominal fat distribution in Japanese patients with type 2 diabetes mellitus. Diabetes Res. Clin. Pract. 56:141-145.
110. Florez, J.C., Hirschhorn, J., and Altshuler, D. 2003. The inherited basis of diabetes mellitus: implications for the genetic analysis of complex traits. Annu. Rev. Genomics Hum. Genet. 4:257-291.