Inflammation and metabolic disorders

Nature

Volumn 444, Issue 7121, 2006, Pages 860-867

  Hotamisligil, Gökhan S ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID;

CARDIOVASCULAR DISEASE; DIABETES; HOMEOSTASIS; IMMUNE RESPONSE; METABOLISM; OBESITY; PUBLIC HEALTH;

ADIPOSE TISSUE; ENDOPLASMIC RETICULUM; EVOLUTION; HORMONE ACTION; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INSULIN RESISTANCE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

ADIPOSE TISSUE; ANIMALS; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; METABOLIC SYNDROME X; OBESITY;

EID: 33845866857     PISSN: 00280836     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/nature05485     Document Type: Review

References (100)

1. The World Health Report 2002 Reducing Risks, Promoting Healthy Life (World Health Organization, Geneva, 2002).
2. Rocchini, A. P. Childhood obesity and a diabetes epidemic. N. Engl. J. Med. 346, 854-855 (2002).
3. Semenkovich, C. F. Insulin resistance and atherosclerosis. J. Clin. Invest. 116, 1813-1822 (2006).
4. Wellen, K. E. & Hotamisligil, G. S. Inflammation, stress, and diabetes. J. Clin. Invest. 115, 1111-1119 (2005).
5. Larsen, G. L. & Henson, P. M. Mediators of inflammation. Annu. Rev. Immunol. 1, 335-359 (1983).
6. Beutler, B. Innate immunity: an overview. Mol. Immunol. 40, 845-859 (2004).
7. Levin, B. R., Lipsitch, M. & Bonhoeffer, S. Population biology, evolution, and infectious disease: convergence and synthesis. Science 283, 806-809 (1999).
8. Sondergaard, L. Homology between the mammalian liver and the Drosophila fat body. Trends Genet. 9, 193 (1993).
9. Leclerc, V. & Reichhart, J. M. The immune response of Drosophila melanogaster. Immunol. Rev. 198, 59-71 (2004).
10. Tong, Q. et al. Function of GATA transcription factors in preadipocyte-adipocyte transition. Science 290, 134-138 (2000).
11. Rusten, T. E. et al. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 7, 179-192 (2004).
12. Song, M. J., Kim, K. H., Yoon, J. M. & Kim, J. B. Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Biochem. Biophys. Res. Commun. 346, 739-745 (2006).
13. Shi, H. et al. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025 (2006).
14. Shoelson, S. E., Lee, J. & Goldfine, A. B. Inflammation and insulin resistance. J. Clin. Invest. 116, 1793-1801 (2006).
15. Dionne, M., Pham, L. N., Shirasu-Hiza, M. & Schneider, D. S. Akt and foxo dysregulation contribute to infection-induced wasting in Drosophila. Curr. Biol. 16, 1977-1985 (2006).
16. Charlton, M. R., Pockros, P. J. & Harrison, S. A. Impact of obesity on treatment of chronic hepatitis C. Hepatology 43, 1177-1186 (2006).
17. Dandona, P., Aljada, A. & Bandyopadhyay, A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol. 25, 4-7 (2004).
18. Hotamisligil, G. S., Shargill, N. S. & Spiegelman, B. M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259, 87-91 (1993).
19. Uysal, K. .T, Wiesbrock, S. M., Marino, M. W. & Hotamisligil, G. S. Protection from obesityinduced insulin resistance in mice lacking TNF-α function. Nature 389, 610-614 (1997).
20. Ventre, J. et al. Targeted disruption of the tumor necrosis factor-alpha gene - metabolic consequences in obese and nonobese mice. Diabetes 46, 1526-1531 (1997).
21. Hotamisligil, G. S., Arner, P., Caro, J. F., Atkinson, R. L. & Spiegelman, B. M. Increased adipose tissue expression of tumor necrosis factor-α in human obesity and insulin resistance. J. Clin. Invest. 95, 2409-2415 (1995).
22. Kern, P. A. et al. 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 (1995).
23. Saghizadeh, M., Ong, J. M., Garvey, W. T., Henry, R. R. & Kern, P. A. The expression of TNFα by human muscle: relationship to insulin resistance. J. Clin. Invest. 97, 1111-1116 (1996).
24. Krogh-Madsen, R., Plomgaard, P., Moller, K., Mittendorfer, B. & Pedersen, B. K. Influence of TNF-α and IL-6 infusions on insulin sensitivity and expression of IL-18 in humans. Am. J. Physiol. Endocrinol. Metab. 291, E108-E114 (2006).
25. Ofei, F., Hurel, S., Newkirk, J., Sopwith, M. & Taylor, K. Effects of an engineered human anti-TNF-α antibody (CDP571) on insulin sensitivity and glycemic control in patients with NIDDM. Diabetes 45, 881-885 (1996).
26. Gonzalez-Gay, M. A. et al. Anti-tumor necrosis factor-α blockade improves insulin resistance in patients with rheumatoid arthritis. Clin. Exp. Rheumatol. 24, 83-86 (2006).
27. Kiortsis, D. N., Mavridis, A. K., Vasakos, S., Nikas, S. N. & Drosos, A. A. Effects of infliximab treatment on insulin resistance in patients with rheumatoid arthritis and ankylosing spondylitis. Ann. Rheum. Dis. 64, 765-766 (2005).
28. Weisberg, S. P. et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796-1808 (2003).
29. Xu, H. et al. Chronic inflammation in fat plays a crucial role in the development of obesityrelated insulin resistance. J. Clin. Invest. 112, 1821-1830 (2003).
30. Cinti, S. et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46, 2347-2355 (2005).
31. Arkan, M. C. et al. IKK-β links inflammation to obesity-induced insulin resistance. Nature Med. 11, 191-198 (2005).
32. Baumgartl, J. et al. Myeloid lineage cell-restricted insulin resistance protects apolipoproteinE-deficient mice against atherosclerosis. Cell Metab. 3, 247-256 (2006).
33. Han, S. et al. Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell Metab. 3, 257-266 (2006).
34. Yu, C. et al. 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 (2002).
35. Chawla, A., Repa, J. J., Evans, R. M. & Mangelsdorf, D. J. Nuclear receptors and lipid physiology: opening the X-files. Science 294, 1866-1870 (2001).
36. Glass, C. K. & Ogawa, S. Combinatorial roles of nuclear receptors in inflammation and immunity. Nature Rev. Immunol. 6, 44-55 (2006).
37. Lee, C. H., Olson, P. & Evans, R. M. Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144, 2201-2207 (2003).
38. Joseph, S. B., Castrillo, A., Laffitte, B. A., Mangelsdorf, D. J. & Tontonoz, P. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nature Med. 9, 213-219 (2003).
39. Castrillo, A. et al. Crosstalk between LXR and Toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol. Cell 12, 805-816 (2003).
40. Lin, Y. et al. The lipopolysaccharide-activated Toll-like receptor (TLR)-4 induces synthesis of the closely related receptor TLR-2 in adipocytes. J. Biol. Chem. 275, 24255-24263 (2000).
41. Bookout, A. L. et al. Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126, 789-799 (2006).
42. Ogawa, S. et al. Molecular determinants of crosstalk between nuclear receptors and Tolllike receptors. Cell 122, 707-721 (2005).
43. Makowski, L. et al. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nature Med. 7, 699-705 (2001).
44. Rosen, E. D. & Spiegelman, B. M. PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth. J. Biol. Chem. 276, 37731-37734 (2001).
45. Hotamisligil, G. S. et al. Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science 274, 1377-1379 (1996).
46. Maeda, K. et al. Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metab. 1, 107-119 (2005).
47. Tuncman, G. et al. A genetic variant at the fatty acid-binding protein aP2 locus reduces the risk for hypertriglyceridemia, type 2 diabetes, and cardiovascular disease. Proc. Natl Acad. Sci. USA 103, 6970-6975 (2006).
48. Shum, B. O. et al. The adipocyte fatty acid-binding protein aP2 is required in allergic airway inflammation. J. Clin. Invest. 116, 2183-2192 (2006).
49. Makowski, L. & Hotamisligil, G. S. Fatty acid binding proteins - the evolutionary crossroads of inflammatory and metabolic responses. J. Nutr. 134, 2464S-2468S (2004).
50. Taniguchi, C. M., Emanuelli, B. & Kahn, C. R. Critical nodes in signalling pathways: insights into insulin action. Nature Rev. Mol. Cell Biol. 7, 85-96 (2006).
51. White, M. F. IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283, E413-E422 (2002).
52. Hotamisligil, G. S. et al. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-α- and obesity-induced insulin resistance. Science 271, 665-668 (1996).
53. 307. J. Biol. Chem. 275, 9047-9054 (2000).
54. Paz, K. et al. 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 (1997).
55. Emanuelli, B. et al. SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-α in the adipose tissue of obese mice. J. Biol. Chem. 276, 47944-47949 (2001).
56. Rui, L., Yuan, M., Frantz, D., Shoelson, S. & White, M. F. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J. Biol. Chem. 277, 42394-42398 (2002).
57. Howard, J. K. et al. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nature Med. 10, 734-738 (2004).
58. Gao, Z. et al. Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J. Biol. Chem. 277, 48115-48121 (2002).
59. Griffin, M. E. et al. 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 (1999).
60. Hotamisligil, G. S.et al. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-α- and obesity-induced insulin resistance. Science 271, 665-668 (1996).
61. Zick, Y. Ser/Thr phosphorylation of IRS proteins: a molecular basis for insulin resistance. Sci. STKE 2005 pe4 (2005).
62. Baud, V. & Karin, M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol. 11, 372-377 (2001).
63. Hirosumi, J. et al. A central role for JNK in obesity and insulin resistance. Nature 420, 333-336 (2002).
64. ser307 phosphorylation in a tissue-specific fashion. Endocrinology 146, 1576-1587 (2005).
65. Ozcan, U. et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461 (2004).
66. Tuncman, G. et al. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc. Natl Acad. Sci. USA 103, 10741-10746 (2006).
67. Ricci, R. et al. Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science 306, 1558-1561 (2004).
68. Kaneto, H. N. Y. et al. Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nature Med. 10, 1128-1132 (2004).
69. Liu, G. & Rondinone, C. M. JNK: bridging the insulin signaling and inflammatory pathway. Curr. Opin. Investig. Drugs 6, 979-987 (2005).
70. Yuan, M. et al. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted distruption of Ikkβ. Science 293, 1673-1677 (2001).
71. Hundal, R. S. et al. Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J. Clin. Invest. 109, 1321-1326 (2002).
72. Cai, D. et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-β and NF-κB. Nature Med. 11, 183-190 (2005).
73. Kim, J. K. et al. PKC-theta knockout mice are protected from fat-induced insulin resistance. J. Clin. Invest. 114, 823-827 (2004).
74. Boden, G. et al. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappaB pathway in rat liver. Diabetes 54, 3458-3465 (2005).
75. Liu, J. et al. NF-κB is required for UV-induced JNK activation via induction of PKCδ. Mol. Cell 21, 467-480 (2006).
76. Marciniak, S. J. & Ron, D. Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86, 1133-1149 (2006).
77. Schroder, M. & Kaufman, R. J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789 (2005).
78. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H. & Ron, D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904 (2000).
79. Harding, H. P., Zhang, Y. & Ron, D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274 (1999).
80. Urano, F. et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666 (2000).
81. Deng, J. L.P. et al. Translational repression mediates activation of nuclear factor κ B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 24, 10161-10168 (2004).
82. Hu, P. H. Z., Couvillon, A. D., Kaufman, R. J. & Exton, J. H. Autocrine tumor necrosis factor α links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1α-mediated NF-κB activation and down-regulation of TRAF2 expression. Mol. Cell. Biol. 26, 3071-3084 (2006).
83. Ozawa, K. et al. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes. Diabetes 54, 657-663 (2005).
84. Nakatani, Y. et al. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J. Biol. Chem. 280, 847-851 (2005).
85. Ozcan, U. et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140 (2006).
86. Zhang, K. S. X. et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124, 587-599 (2006).
87. Cullinan, S. B. & Diehl, J. A. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 38, 317-332 (2006).
88. Xue, X. P. J. et al. Tumor necrosis factor α (TNFα) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFα. J. Biol. Chem. 280, 33917-33925 (2005).
89. Furukawa, S. et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114, 1752-1761 (2004).
90. Lin, Y. et al. The hyperglycemia-induced inflammatory response in adipocytes: the role of reactive oxygen species. J. Biol. Chem. 280, 4617-4626 (2005).
91. Houstis, N., Rosen, E. D. & Lander, E. S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440, 944-948 (2006).
92. Brownlee, M. Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820 (2001).
93. Lowell, B. B. & Shulman, G. I. Mitochondrial dysfunction and type 2 diabetes. Science 307, 384-387 (2005).
94. Steen, E. et al. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease - is this type 3 diabetes? J. Alzheimers Dis. 7, 63-80 (2005).
95. Mootha, V. K. et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature Genet. 34, 267-273 (2003).
96. St-Pierre, J. et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127, 397-408 (2006).
97. Gao, Z., Zuberi, A., Quon, M. J., Dong, Z. & Ye, J. Aspirin inhibits serine phosphorylation of insulin receptor substrate 1 in tumor necrosis factor-treated cells through targeting multiple serine kinases. J. Biol. Chem. 278, 24944-24950 (2003).
98. Waeber, G. et al. The gene MAPK8IP1, encoding islet-brain-1, is a candidate for type 2 diabetes. Nature Genet. 24, 291-295 (2000).
99. Kliewer, S. A., Xu, H. E., Lambert, M. H. & Wilson, T. M. Peroxisome proliferator-activated receptors: from genes to physiology. Recent Prog. Horm. Res. 56, 239-263 (2001).
100. Mahata, B., Mukherjee, S., Mishra, S., Bandyopadhyay, A. & Adhya, S. Functional delivery of a cytosolic tRNA into mutant mitochondria of human cells. Science 314, 471-474 (2006).