Adaptive immunity in obesity and insulin resistance (original) (raw)

• Ouchi, N., Parker, J. L., Lugus, J. J. & Walsh, K. Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11, 85–97 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Després, J. P. & Lemieux, I. Abdominal obesity and metabolic syndrome. Nature 444, 881–887 (2006).
  Article CAS PubMed Google Scholar
• Olefsky, J. M. & Glass, C. K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219–246 (2010).
  Article CAS PubMed Google Scholar
• Hotamisligil, G. S. Inflammation and metabolic disorders. Nature 444, 860–867 (2006).
  Article CAS PubMed Google Scholar
• Weisberg, S. P. et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796–1808 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, H. et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112, 1821–1830 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Murano, I. et al. Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice. J. Lipid Res. 49, 1562–1568 (2008).
  Article CAS PubMed Google Scholar
• Fischer-Posovszky, P., Wang, Q. A., Asterholm, I. W., Rutkowski, J. M. & Scherer, P. E. Targeted deletion of adipocytes by apoptosis leads to adipose tissue recruitment of alternatively activated M2 macrophages. Endocrinology 152, 3074–3081 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Trayhurn, P. & Wood, I. S. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br. J. Nutr. 92, 347–355 (2004).
  Article CAS PubMed Google Scholar
• Chen, B. et al. Hypoxia dysregulates the production of adiponectin and plasminogen activator inhibitor-1 independent of reactive oxygen species in adipocytes. Biochem. Biophys. Res. Commun. 341, 549–556 (2006).
  Article CAS PubMed Google Scholar
• Hosogai, N. et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 56, 901–911 (2007).
  Article CAS PubMed Google Scholar
• Pasarica, M. et al. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes 58, 718–725 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Goossens, G. H. et al. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation 124, 67–76 (2011).
  Article CAS PubMed Google Scholar
• Sun, K., Kusminski, C. M. & Scherer, P. E. Adipose tissue remodeling and obesity. J. Clin. Invest. 121, 2094–2101 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Lumeng, C. N., Bodzin, J. L. & Saltiel, A. R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117, 175–184 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Fleming, B. D. & Mosser, D. M. Regulatory macrophages: setting the threshold for therapy. Eur. J. Immunol. 41, 2498–2502 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Meijer, K. et al. Human primary adipocytes exhibit immune cell function: adipocytes prime inflammation independent of macrophages. PLoS ONE 6, e17154 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Strissel, K. J. et al. T-cell recruitment and Th1 polarization in adipose tissue during diet-induced obesity in C57BL/6 mice. Obesity (Silver Spring) 18, 1918–1925 (2010).
  Article CAS Google Scholar
• Caspar-Bauguil, S. et al. Adipose tissue lymphocytes: types and roles. J. Physiol. Biochem. 65, 423–436 (2009).
  Article CAS PubMed Google Scholar
• Kaminski, D. A. & Randall, T. D. Adaptive immunity and adipose tissue biology. Trends Immunol. 31, 384–390 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Feuerer, M. et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15, 930–939 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Caspar-Bauguil, S. et al. Adipose tissues as an ancestral immune organ: site-specific change in obesity. FEBS Lett. 579, 3487–3492 (2005).
  Article CAS PubMed Google Scholar
• Winer, S. et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 15, 921–929 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Zúñiga, L. A. et al. IL-17 regulates adipogenesis, glucose homeostasis, and obesity. J. Immunol. 185, 6947–6959 (2010).
  Article CAS PubMed Google Scholar
• Duffaut, C. et al. Interplay between human adipocytes and T lymphocytes in obesity: CCL20 as an adipochemokine and T lymphocytes as lipogenic modulators. Arterioscler. Thromb. Vasc. Biol. 29, 1608–1614 (2009).
  Article CAS PubMed Google Scholar
• Wu, H. et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 115, 1029–1038 (2007).
  Article CAS PubMed Google Scholar
• O'Rourke, R. W. et al. Depot-specific differences in inflammatory mediators and a role for NK cells and IFN-γ in inflammation in human adipose tissue. Int. J. Obes. (Lond.) 33, 978–990 (2009).
  Article CAS Google Scholar
• Rocha, V. Z. & Folco, E. J. Inflammatory concepts of obesity. Int. J. Inflam. 2011, 529061 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kintscher, U. et al. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler. Thromb. Vasc. Biol. 28, 1304–1310 (2008).
  Article CAS PubMed Google Scholar
• Odegaard, J. I. et al. Macrophage-specific PPARγ controls alternative activation and improves insulin resistance. Nature 447, 1116–1120 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Tiemessen, M. M. et al. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc. Natl Acad. Sci. USA 104, 19446–19451 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Foryst-Ludwig, A. et al. PPARγ activation attenuates T-lymphocyte-dependent inflammation of adipose tissue and development of insulin resistance in obese mice. Cardiovasc. Diabetol. 9, 64 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Stienstra, R. et al. Peroxisome proliferator-activated receptor γ activation promotes infiltration of alternatively activated macrophages into adipose tissue. J. Biol. Chem. 283, 22620–22627 (2008).
  Article CAS PubMed Google Scholar
• Winer, D. A. et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17, 610–617 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Korn, T. et al. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 13, 423–431 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• De Rosa, V. et al. A key role of leptin in the control of regulatory T cell proliferation. Immunity 26, 241–255 (2007).
  Article CAS PubMed Google Scholar
• Deiuliis, J. et al. Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers. PLoS ONE 6, e16376 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Nishimura, S. et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15, 914–920 (2009).
  Article CAS PubMed Google Scholar
• Ohmura, K. et al. Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arterioscler. Thromb. Vasc. Biol. 30, 193–199 (2010).
  Article CAS PubMed Google Scholar
• Van Kaer, L., Parekh, V. V. & Wu, L. Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res. 343, 43–55 (2011).
  Article CAS PubMed Google Scholar
• Van Kaer, L. NKT cells: T lymphocytes with innate effector functions. Curr. Opin. Immunol. 19, 354–364 (2007).
  Article CAS PubMed Google Scholar
• Duffaut, C., Galitzky, J., Lafontan, M. & Bouloumie, A. Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity. Biochem. Biophys. Res. Commun. 384, 482–485 (2009).
  Article CAS PubMed Google Scholar
• Jagannathan, M. et al. Toll-like receptors regulate B cell cytokine production in patients with diabetes. Diabetologia 53, 1461–1471 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Rocha, V. Z. et al. Interferon-γ, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ. Res. 103, 467–476 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Suganami, T. et al. Role of the Toll-like receptor 4/NF-kappaB pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler. Thromb. Vasc. Biol. 27, 84–91 (2007).
  Article CAS PubMed Google Scholar
• Shi, H. et al. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015–3025 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).
  Article PubMed Google Scholar
• Vijay-Kumar, M. et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328, 228–231 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Ding, S. et al. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS ONE 5, e12191 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Tilg, H. & Kaser, A. Gut microbiome, obesity, and metabolic dysfunction. J. Clin. Invest. 121, 2126–2132 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Delzenne, N. M., Neyrinck, A. M. & Cani, P. D. Modulation of the gut microbiota by nutrients with prebiotic properties: consequences for host health in the context of obesity and metabolic syndrome. Microb. Cell Fact. 10 (Suppl. 1), S10 (2011).
  Article PubMed PubMed Central Google Scholar
• Kvietys, P. R., Specian, R. D., Grisham, M. B. & Tso, P. Jejunal mucosal injury and restitution: role of hydrolytic products of food digestion. Am. J. Physiol. 261, G384–G391 (1991).
  CAS PubMed Google Scholar
• Wang, Y. et al. Chylomicrons promote intestinal absorption and systemic dissemination of dietary antigen (ovalbumin) in mice. PLoS ONE 4, e8442 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ghoshal, S., Witta, J., Zhong, J., de Villiers, W. & Eckhardt, E. Chylomicrons promote intestinal absorption of lipopolysaccharides. J. Lipid Res. 50, 90–97 (2009).
  Article CAS PubMed Google Scholar
• Bickerton, A. S. et al. Preferential uptake of dietary Fatty acids in adipose tissue and muscle in the postprandial period. Diabetes 56, 168–176 (2007).
  Article CAS PubMed Google Scholar
• Karpe, F., Humphreys, S. M., Samra, J. S., Summers, L. K. & Frayn, K. N. Clearance of lipoprotein remnant particles in adipose tissue and muscle in humans. J. Lipid Res. 38, 2335–2343 (1997).
  CAS PubMed Google Scholar
• Wang, Y. et al. T-lymphocyte responses to intestinally absorbed antigens can contribute to adipose tissue inflammation and glucose intolerance during high fat feeding. PLoS ONE 5, e13951 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Chehade, M. & Mayer, L. Oral tolerance and its relation to food hypersensitivities. J. Allergy Clin. Immunol. 115, 3–12; quiz 13 (2005).
  Article PubMed Google Scholar
• Mingrone, G. & Castagneto-Gissey, L. Mechanisms of early improvement/resolution of type 2 diabetes after bariatric surgery. Diabetes Metab. 35, 518–523 (2009).
  Article CAS PubMed Google Scholar
• Clément, K. Bariatric surgery, adipose tissue and gut microbiota. Int. J. Obes. (Lond.) 35 (Suppl. 3), S7–S15 (2011).
  Article Google Scholar
• Furet, J. P. et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59, 3049–3057 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Delzenne, N. M., Neyrinck, A. M., Backhed, F. & Cani, P. D. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat. Rev. Endocrinol. 7, 639–646 (2011).
  Article CAS PubMed Google Scholar
• Cani, P. D. & Delzenne, N. M. The gut microbiome as therapeutic target. Pharmacol. Ther. 130, 202–212 (2011).
  Article CAS PubMed Google Scholar
• Sultan, A. et al. T cell-mediated inflammation in adipose tissue does not cause insulin resistance in hyperlipidemic mice. Circ. Res. 104, 961–968 (2009).
  Article CAS PubMed Google Scholar
• Lee, Y. S. et al. Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance. Diabetes 60, 2474–2483 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Thewissen, M. M. et al. Abdominal fat mass is associated with adaptive immune activation: the CODAM Study. Obesity (Silver Spring) 19, 1690–1698 (2011).
  Article CAS Google Scholar
• Viardot, A., Grey, S. T., Mackay, F. & Chisholm, D. Potential antiinflammatory role of insulin via the preferential polarization of effector T cells toward a T helper 2 phenotype. Endocrinology 148, 346–353 (2007).
  Article CAS PubMed Google Scholar
• Viardot, A., Lord, R. V. & Samaras, K. The effects of weight loss and gastric banding on the innate and adaptive immune system in type 2 diabetes and prediabetes. J. Clin. Endocrinol. Metab. 95, 2845–2850.
• Jagannathan-Bogdan, M. et al. Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J. Immunol. 186, 1162–1172.
• Surendar, J., Mohan, V., Rao, M. M., Babu, S. & Aravindhan, V. Increased levels of both TH1 and TH2 cytokines in subjects with metabolic syndrome (CURES-103). Diabetes Technol. Ther. 13, 477–482 (2011).
  Article CAS PubMed Google Scholar
• Liu, Z., Stanojevic, V., Avadhani, S., Yano, T. & Habener, J. F. Stromal cell-derived factor-1 (SDF-1)/chemokine (C-X-C motif) receptor 4 (CXCR4) axis activation induces intra-islet glucagon-like peptide-1 (GLP-1) production and enhances β cell survival. Diabetologia 54, 2067–2076 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kang, K. et al. Adipocyte-derived Th2 cytokines and myeloid PPARδ regulate macrophage polarization and insulin sensitivity. Cell. Metab. 7, 485–495 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Wellen, K. E. & Hotamisligil, G. S. Inflammation, stress, and diabetes. J. Clin. Invest. 115, 1111–1119 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Arkan, M. C. et al. IKK-β links inflammation to obesity-induced insulin resistance. Nat. Med. 11, 191–198 (2005).
  Article CAS PubMed Google Scholar
• Hirosumi, J. et al. A central role for JNK in obesity and insulin resistance. Nature 420, 333–336 (2002).
  Article CAS PubMed Google Scholar
• Coletta, D. K. & Mandarino, L. J. Mitochondrial dysfunction and insulin resistance from the outside in: extracellular matrix, the cytoskeleton, and mitochondria. Am. J. Physiol. Endocrinol. Metab. 301, E749–E755 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Clynes, R. B cell therapy is β-tested: Rituximab puts a pause on β-cell destruction. Islets 2, 130–132 (2010).
  Article PubMed Google Scholar
• Scott, D. L., Wolfe, F. & Huizinga, T. W. Rheumatoid arthritis. Lancet 376, 1094–1098 (2010).
  Article PubMed Google Scholar
• Kanakasabai, S. et al. Peroxisome proliferator-activated receptor delta agonists inhibit T helper type 1 (Th1) and Th17 responses in experimental allergic encephalomyelitis. Immunology 130, 572–588 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Miller, A. M. et al. Interleukin-33 induces protective effects in adipose tissue inflammation during obesity in mice. Circ. Res. 107, 650–658 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Kowalski, G. M. et al. Deficiency of haematopoietic-cell-derived IL-10 does not exacerbate high-fat-diet-induced inflammation or insulin resistance in mice. Diabetologia 54, 888–899 (2011).
  Article CAS PubMed Google Scholar
• Hong, E. G. et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58, 2525–2535 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Deiuliis, J. A., Kampfrath, T., Ying, Z., Maiseyeu, A. & Rajagopalan, S. Lipoic acid attenuates innate immune infiltration and activation in the visceral adipose tissue of obese insulin resistant mice. Lipids 46, 1021–1032 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Bruun, J. M., Helge, J. W., Richelsen, B. & Stallknecht, B. Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am. J. Physiol. Endocrinol. Metab. 290, E961–E967 (2006).
  Article CAS PubMed Google Scholar
• Klöting, N. et al. Insulin-sensitive obesity. Am. J. Physiol. Endocrinol. Metab. 299, E506–E515 (2010).
  Article CAS PubMed Google Scholar
• Cancello, R. et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 54, 2277–2286 (2005).
  Article CAS PubMed Google Scholar
• Wu, D. et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332, 243–247 (2011).
  Article CAS PubMed PubMed Central Google Scholar