Adipose tissue as an immunological organ

Obesity

Volumn 23, Issue 3, 2015, Pages 512-518

  Grant, Ryan W ^a   Dixit, Vishwa Deep ^b  

^a PURDUE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ADIPOCYTE; ADIPOSE TISSUE; ARTICLE; B LYMPHOCYTE; CELL INTERACTION; CHRONIC INFLAMMATION; COMORBIDITY; DISEASE PREDISPOSITION; ENDOCRINE FUNCTION; HEMATOPOIETIC CELL; HOST RESISTANCE; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; INFECTION; INFORMATION RETRIEVAL; INNATE IMMUNITY; INSULIN RESISTANCE; LEUKOCYTE; LEUKOCYTOSIS; MACROPHAGE; MEDLINE; METABOLIC DISORDER; METABOLIC SYNDROME X; METABOLISM; NEUTROPHIL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PARACRINE SIGNALING; T LYMPHOCYTE; IMMUNOLOGY; INFLAMMATION; PATHOPHYSIOLOGY;

ADAPTIVE IMMUNITY; ADIPOSE TISSUE; DIABETES MELLITUS, TYPE 2; HUMANS; IMMUNITY, INNATE; INFLAMMATION; METABOLIC SYNDROME X; OBESITY;

EID: 84925273129     PISSN: 19307381     EISSN: 1930739X     Source Type: Journal    
DOI: 10.1002/oby.21003     Document Type: Article

References (78)

1. Masters RK, Reither EN, Powers DA, Yang YC, Burger AE, Link BG,. The Impact of Obesity on US Mortality Levels: The Importance of Age and Cohort Factors in Population Estimates. AM J Public Health 2013; 103: 1895-1901.
2. Grant R, Youm YH, Ravussin A, Dixit VD,. Quantification of adipose tissue leukocytosis in obesity. Methods Mol Biol 2013; 1040: 195-209.
3. Knowler WC, Barrett-Connor E, Fowler SE, et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002; 346: 393-403.
4. Sims EA,. Are there persons who are obese, but metabolically healthy? Metabolism 2001; 50: 1499-1504.
5. Phillips CM, Perry IJ,. Does inflammation determine metabolic health status in obese and nonobese adults? J Clin Endocrinol Metab 2013; 98: E1610-1619.
6. Perez-Martinez P, Alcala-Diaz J, Delgado-Lista J, et al. Metabolical phenotypes of obesity influence triglyceride and inflammation homeostasis. Eur J Clin Invest 2014; 44: 1053-1064.
7. Lackey DE, Burk DH, Ali MR, et al. Contributions of adipose tissue architectural and tensile properties toward defining healthy and unhealthy obesity. Am J Physiol Endocrinol Metab 2014; 306: E233-246.
8. Swinburn BA, Nyomba BL, Saad MF, et al. Insulin resistance associated with lower rates of weight gain in Pima Indians. J Clin Invest 1991; 88: 168-173.
9. Zurlo F, Lillioja S, Esposito-Del Puente A, et al. Low ratio of fat to carbohydrate oxidation as predictor of weight gain: Study of 24-h RQ. Am J Physiol 1990; 259: E650-657.
10. Marra M, Scalfi L, Covino A, Esposito-Del Puente A, Contaldo F,. Fasting respiratory quotient as a predictor of weight changes in non-obese womenInt J Obes Relat Metab Disord 1998; 22: 601-603.
11. Shi LZ, Wang R, Huang G, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011; 208: 1367-1376.
12. Tannahill GM, Curtis AM, Adamik J, et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 2013; 496: 238-242.
13. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW, Jr,. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796-1808.
14. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
15. Winer DA, Winer S, Shen L, et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011; 17: 610-617.
16. Nishimura S, Manabe I, Nagasaki M, et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009; 15: 914-920.
17. Elgazar-Carmon V, Rudich A, Hadad N, Levy R,. Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. J Lipid Res 2008; 49: 1894-1903.
18. Talukdar S, Oh da Y, Bandyopadhyay G, et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012; 18: 1407-1412.
19. Wu D, Molofsky AB, Liang HE, et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011; 332: 243-247.
20. Hellman B, Larsson S, Westman S,. Mast cell content and fatty acid metabolism in the epididymal fat pad of obese mice. Acta Physiol Scand 1963; 58: 255-262.
21. Liu J, Divoux A, Sun J, et al. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 2009; 15: 940-945.
22. Nguyen KD, Qiu Y, Cui X, et al. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 2011; 480: 104-108.
23. Kosteli A, Sugaru E, Haemmerle G, et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest 2010; 120: 3466-3479.
24. Lumeng CN, Bodzin JL, Saltiel AR,. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184.
25. Feuerer M, Herrero L, Cipolletta D, et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 2009; 15: 930-939.
26. Arner E, Westermark PO, Spalding KL, et al. Adipocyte turnover: Relevance to human adipose tissue morphology. Diabetes 2010; 59: 105-109.
27. Hardy OT, Perugini RA, Nicoloro SM, et al. Body mass index-independent inflammation in omental adipose tissue associated with insulin resistance in morbid obesity. Surg Obes Relat Dis 2011; 7: 60-67.
28. Khan T, Muise ES, Iyengar P, et al. Metabolic dysregulation and adipose tissue fibrosis: Role of collagen VI. Mol Cell Biol 2009; 29: 1575-1591.
29. Strissel KJ, Stancheva Z, Miyoshi H, et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007; 56: 2910-2918.
30. Giordano A, Murano I, Mondini E, et al. Obese adipocytes show ultrastructural features of stressed cells and die of pyroptosis. J Lipid Res 2013; 54: 2423-2436.
31. Wen H, Gris D, Lei Y, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 2011; 12: 408-415.
32. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J,. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010; 11: 136-140.
33. Mariathasan S, Weiss DS, Newton K, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006; 440: 228-232.
34. Vandanmagsar B, Youm YH, Ravussin A, et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 2011; 17: 179-188.
35. Duewell P, Kono H, Rayner KJ, et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010; 464: 1357-1361.
36. Youm YH, Kanneganti TD, Vandanmagsar B, et al. The Nlrp3 inflammasome promotes age-related thymic demise and immunosenescence. Cell Rep 2012; 1: 56-68.
37. Tsushima Y, Nishizawa H, Tochino Y, et al. Uric acid secretion from adipose tissue and its increase in obesity. J Biol Chem 2013; 288: 27138-27149.
38. Ebke LA, Nestor-Kalinoski AL, Slotterbeck BD, et al. Tight association between macrophages and adipocytes in obesity: Implications for adipocyte preparation. Obesity (Silver Spring) 2014; 22: 1246-1255.
39. Kopp A, Buechler C, Neumeier M, et al. Innate immunity and adipocyte function: Ligand-specific activation of multiple Toll-like receptors modulates cytokine, adipokine, and chemokine secretion in adipocytes. Obesity (Silver Spring) 2009; 17: 648-656.
40. Pal D, Dasgupta S, Kundu R, et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med 2012; 18: 1279-1285.
41. Nguyen MT, Favelyukis S, Nguyen AK, et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem 2007; 282: 35279-35292.
42. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS,. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006; 116: 3015-3025.
43. Schroder K, Tschopp J,. The inflammasomes. Cell 2010; 140: 821-832.
44. Heneka MT, Kummer MP, Stutz A, et al. NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 2013; 493: 674-678.
45. Halle A, Hornung V, Petzold GC, et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 2008; 9: 857-865.
46. Busso N, So A,. Mechanisms of inflammation in gout. Arthritis Res Ther 2010; 12: 206.
47. Franklin BS, Bossaller L, De Nardo D, et al. The adaptor ASC has extracellular and 'prionoid' activities that propagate inflammation. Nat Immunol 2014; 15: 727-737.
48. Baroja-Mazo A, Martin-Sanchez F, Gomez AI, et al. The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol 2014; 15: 738-748.
49. Munoz-Planillo R, Kuffa P, Martinez-Colon G, Smith BL, Rajendiran TM, Nunez G,. K(+) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 2013; 38: 1142-1153.
50. Sheedy FJ, Grebe A, Rayner KJ, et al. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat Immunol 2013; 14: 812-820.
51. Yan Y, Jiang W, Spinetti T, et al. Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation. Immunity 2013; 38: 1154-1163.
52. Stienstra R, van Diepen JA, Tack CJ, et al. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc Natl Acad Sci USA 2011; 108: 15324-15329.
53. Lee HM, Kim JJ, Kim HJ, Shong M, Ku BJ, Jo EK,. Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes 2013; 62: 194-204.
54. Henao-Mejia J, Elinav E, Jin C, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179-185.
55. Vats D, Mukundan L, Odegaard JI, et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab 2006; 4: 13-24.
56. Kovacikova M, Sengenes C, Kovacova Z, et al. Dietary intervention-induced weight loss decreases macrophage content in adipose tissue of obese women. Int J Obes (Lond) 2011; 35: 91-98.
57. Cancello R, Henegar C, Viguerie N, 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 2005; 54: 2277-2286.
58. Morris DL, Cho KW, Delproposto JL, et al. Adipose tissue macrophages function as antigen-presenting cells and regulate adipose tissue CD4+ T cells in mice. Diabetes 2013; 62: 2762-2772.
59. Deng T, Lyon CJ, Minze LJ, et al. Class II major histocompatibility complex plays an essential role in obesity-induced adipose inflammation. Cell Metab 2013; 17: 411-422.
60. Cipolletta D, Feuerer M, Li A, et al. PPAR-gamma is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 2012; 486: 549-553.
61. Lira FS, Rosa JC, Pimentel GD, et al. Both adiponectin and interleukin-10 inhibit LPS-induced activation of the NF-kappaB pathway in 3T3-L1 adipocytes. Cytokine 2012; 57: 98-106.
62. Yang H, Youm YH, Vandanmagsar B, et al. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J Immunol 2010; 185: 1836-1845.
63. Priceman SJ, Kujawski M, Shen S, et al. Regulation of adipose tissue T cell subsets by Stat3 is crucial for diet-induced obesity and insulin resistance. Proc Natl Acad Sci USA 2013; 110: 13079-13084.
64. Guarda G, Zenger M, Yazdi AS, et al. Differential expression of NLRP3 among hematopoietic cells. J Immunol 2011; 186: 2529-2534.
65. Defuria J, Belkina AC, Jagannathan-Bogdan M, et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc Natl Acad Sci USA 2013; 110: 5133-5138.
66. Nishimura S, Manabe I, Takaki S, et al. Adipose natural regulatory B cells negatively control adipose tissue inflammation. Cell Metab 2013; 18: 759-766.
67. Pond CM, Mattacks CA,. Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro. J Lipid Res 1995; 36: 2219-2231.
68. Rangel-Moreno J, Moyron-Quiroz JE, Carragher DM, et al. Omental milky spots develop in the absence of lymphoid tissue-inducer cells and support B and T cell responses to peritoneal antigens. Immunity 2009; 30: 731-743.
69. Mohanta SK, Yin C, Peng L, et al. Artery tertiary lymphoid organs contribute to innate and adaptive immune responses in advanced mouse atherosclerosis. Circ Res 2014; 114: 1772-1787.
70. Moro K, Yamada T, Tanabe M, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010; 463: 540-544.
71. Qiu YF, Nguyen KD, Odegaard JI, et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 2014; 157: 1292-1308.
72. Smith AG, Sheridan PA, Harp JB, Beck MA,. Diet-induced obese mice have increased mortality and altered immune responses when infected with influenza virus. J Nutr 2007; 137: 1236-1243.
73. Karlsson EA, Sheridan PA, Beck MA,. Diet-induced obesity in mice reduces the maintenance of influenza-specific CD8+ memory T cells. J Nutr 2010; 140: 1691-1697.
74. Karlsson EA, Sheridan PA, Beck MA,. Diet-induced obesity impairs the T cell memory response to influenza virus infection. J Immunol 2010; 184: 3127-3133.
75. O'Brien KB, Vogel P, Duan S, et al. Impaired wound healing predisposes obese mice to severe influenza virus infection. J Infect Dis 2012; 205: 252-261.
76. Zhang AJ, To KK, Li C, et al. Leptin mediates the pathogenesis of severe 2009 pandemic influenza A(H1N1) infection associated with cytokine dysregulation in mice with diet-induced obesity. J Infect Dis 2013; 207: 1270-1280.
77. Kanneganti TD, Dixit VD,. Immunological complications of obesity. Nat Immunol 2012; 13: 707-712.
78. Milner JJ, Sheridan PA, Karlsson EA, Schultz-Cherry S, Shi Q, Beck MA,. Diet-induced obese mice exhibit altered heterologous immunity during a secondary 2009 pandemic H1N1 infection. J Immunol 2013; 191: 2474-2485.