Fat-Resident Tregs: An Emerging Guard Protecting From Obesity-Associated Metabolic Disorders

Obesity Reviews

Volumn 14, Issue 7, 2013, Pages 568-578

  Chen, X ^a   Wu, Y ^a   Wang, L ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Obesity; PPAR ; Treg; VAT

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; 4 AMINOBUTYRIC ACID; ADIPONECTIN; ANTIDIABETIC AGENT; AUTOANTIGEN; CD3 ANTIBODY; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; EPIGALLOCATECHIN GALLATE; GLUCOSYLCERAMIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 10; JES 65H 4; JES6 5H4; L SELECTIN; LEPTIN; MAMMALIAN TARGET OF RAPAMYCIN; MONOCLONAL ANTIBODY; N (2 BENZOYLPHENYL) O [2 (METHYL 2 PYRIDINYLAMINO)ETHYL]TYROSINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; ROS; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; CELL DIFFERENTIATION; DISEASE ASSOCIATION; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; LEAN BODY WEIGHT; METABOLIC DISORDER; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; UPREGULATION;

DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; METABOLIC DISEASES; OBESITY; T-LYMPHOCYTES, REGULATORY;

EID: 84879506653     PISSN: 14677881     EISSN: 1467789X     Source Type: Journal    
DOI: 10.1111/obr.12033     Document Type: Article

References (85)

1. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 2011; 121: 2111-2117.
2. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006; 116: 1793-1801.
3. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest 1995; 95: 2409-2415.
4. Spiegelman BM, Hotamisligil GS. Through thick and thin: wasting, obesity, and TNF alpha. Cell 1993; 73: 625-627.
5. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259: 87-91.
6. Hotamisligil GS, Spiegelman BM. Tumor necrosis factor alpha: a key component of the obesity-diabetes link. Diabetes 1994; 43: 1271-1278.
7. Feuerer M, Herrero L, Cipolletta D etal. 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.
8. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012; 18: 363-374.
9. 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.
10. Xu H, Barnes GT, Yang Q etal. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
11. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184.
12. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 2007; 56: 16-23.
13. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH etal. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 2007; 447: 1116-1120.
14. Suganami T, Nishida J, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler Thromb Vasc Biol 2005; 25: 2062-2068.
15. Lumeng CN, Maillard I, Saltiel AR. T-ing up inflammation in fat. Nat Med 2009; 15: 846-847.
16. Nishimura S, Manabe I, Nagasaki M etal. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009; 15: 914-920.
17. Winer S, Chan Y, Paltser G etal. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 2009; 15: 921-929.
18. Winer DA, Winer S, Shen L etal. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011; 17: 610-U134.
19. Liu J, Divoux A, Sun J etal. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 2009; 15: 940-945.
20. Wu D, Molofsky AB, Liang HE etal. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011; 332: 243-247.
21. Lynch L, Nowak M, Varghese B etal. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012; 37: 574-587.
22. Schipper HS, Prakken B, Kalkhoven E, Boes M. Adipose tissue-resident immune cells: key players in immunometabolism. Trends Endocrinol Metab 2012; 23: 407-415.
23. Ilan Y, Maron R, Tukpah AM etal. Induction of regulatory T cells decreases adipose inflammation and alleviates insulin resistance in ob/ob mice. Proc Natl Acad Sci U S A 2010; 107: 9765-9770.
24. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155: 1151-1164.
25. Long SA, Buckner JH. CD4+FOXP3+ T regulatory cells in human autoimmunity: more than a numbers game. J Immunol 2011; 187: 2061-2066.
26. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008; 133: 775-787.
27. Battaglia M, Stabilini A, Roncarolo MG. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 2005; 105: 4743-4748.
28. Sakaguchi S, Miyara M, Costantino CM, Hafler DA. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 2010; 10: 490-500.
29. Sojka DK, Huang YH, Fowell DJ. Mechanisms of regulatory T-cell suppression - a diverse arsenal for a moving target. Immunology 2008; 124: 13-22.
30. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8: 523-532.
31. Soyka MB, Holzmann D, Akdis CA. Regulatory cells in allergen-specific immunotherapy. Immunotherapy 2012; 4: 389-396.
32. Mor A, Planer D, Luboshits G etal. Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscler Thromb Vasc Biol 2007; 27: 893-900.
33. Ait-Oufella H, Salomon BL, Potteaux S etal. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006; 12: 178-180.
34. Zeng C, Shi X, Zhang B etal. The imbalance of Th17/Th1/Tregs in patients with type 2 diabetes: relationship with metabolic factors and complications. J Mol Med (Berl) 2012; 90: 175-186.
35. Jagannathan-Bogdan M, McDonnell ME, Shin H etal. Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J Immunol 2011; 186: 1162-1172.
36. Deiuliis J, Shah Z, Shah N etal. Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers. PloS ONE 2011; 6: e16376.
37. Pettersson US, Walden TB, Carlsson PO, Jansson L, Phillipson M. Female mice are protected against high-fat diet induced metabolic syndrome and increase the regulatory T cell population in adipose tissue. PloS ONE 2012; 7: e46057.
38. Eller K, Kirsch A, Wolf AM etal. Potential role of regulatory T cells in reversing obesity-linked insulin resistance and diabetic nephropathy. Diabetes 2011; 60: 2954-2962.
39. Tian J, Dang HN, Yong J etal. Oral treatment with gamma-aminobutyric acid improves glucose tolerance and insulin sensitivity by inhibiting inflammation in high fat diet-fed mice. PloS ONE 2011; 6: e25338.
40. Cipolletta D, Feuerer M, Li A etal. PPAR-gamma is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 2012; 486: 549-553.
41. Svec P, Vasarhelyi B, Paszthy B etal. Do regulatory T cells contribute to Th1 skewness in obesity? Exp Clin Endocrinol Diabetes 2007; 115: 439-443.
42. Luczynski W, Stasiak-Barmuta A, Wawrusiewicz-Kurylonek N etal. Disturbances in some gene expression in T regulatory cells separated from children with metabolic syndrome. Scand J Immunol 2010; 71: 115-122.
43. van der Weerd K, Dik WA, Schrijver B etal. Morbidly obese human subjects have increased peripheral blood CD4+ T cells with skewing toward a Treg- and Th2-dominated phenotype. Diabetes 2012; 61: 401-408.
44. Luczynski W, Wawrusiewicz-Kurylonek N, Ilendo E etal. Generation of functional T-regulatory cells in children with metabolic syndrome. Arch Immunol Ther Exp (Warsz) 2012; 60: 487-495.
45. Yun JM, Jialal I, Devaraj S. Effects of epigallocatechin gallate on regulatory T cell number and function in obese v. lean volunteers. Br J Nutr 2010; 103: 1771-1777.
46. Zeyda M, Huber J, Prager G, Stulnig TM. Inflammation correlates with markers of T-cell subsets including regulatory T cells in adipose tissue from obese patients. Obesity (Silver Spring) 2011; 19: 743-748.
47. Miyara M, Yoshioka Y, Kitoh A etal. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 2009; 30: 899-911.
48. Liston A, Rudensky AY. Thymic development and peripheral homeostasis of regulatory T cells. Curr Opin Immunol 2007; 19: 176-185.
49. Rosenblum MD, Gratz IK, Paw JS, Lee K, Marshak-Rothstein A, Abbas AK. Response to self antigen imprints regulatory memory in tissues. Nature 2011; 480: 538-542.
50. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 2010; 11: 11-18.
51. Forster R, Davalos-Misslitz AC, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 2008; 8: 362-371.
52. Eksteen B, Miles A, Curbishley SM etal. Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J Immunol 2006; 177: 593-603.
53. Zou L, Barnett B, Safah H etal. Bone marrow is a reservoir for CD4+CD25+ regulatory T cells that traffic through CXCL12/CXCR4 signals. Cancer Res 2004; 64: 8451-8455.
54. Benoist C, Mathis D. Treg cells, life history, and diversity. Cold Spring Harb Perspect Biol 2012; 4: a007021.
55. Liu L, Callahan MK, Huang D, Ransohoff RM. Chemokine receptor CXCR3: an unexpected enigma. Curr Top Dev Biol 2005; 68: 149-181.
56. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011; 11: 85-97.
57. Ouchi N, Walsh K. Adiponectin as an anti-inflammatory factor. Clin Chim Acta 2007; 380: 24-30.
58. Hirose H, Yamamoto Y, Seino-Yoshihara Y, Kawabe H, Saito I. Serum high-molecular-weight adiponectin as a marker for the evaluation and care of subjects with metabolic syndrome and related disorders. J Atheroscler Thromb 2010; 17: 1201-1211.
59. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004; 323: 630-635.
60. Kumada M, Kihara S, Ouchi N etal. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation 2004; 109: 2046-2049.
61. Murai M, Turovskaya O, Kim G etal. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 2009; 10: 1178-1184.
62. Tsang JY, Li D, Ho D etal. Novel immunomodulatory effects of adiponectin on dendritic cell functions. Int Immunopharmacol 2011; 11: 604-609.
63. Wong VW, Rustad KC, Akaishi S etal. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med 2012; 18: 148-152.
64. De Rosa V, Procaccini C, Cali G etal. A key role of leptin in the control of regulatory T cell proliferation. Immunity 2007; 26: 241-255.
65. Procaccini C, De Rosa V, Galgani M etal. An oscillatory switch in mTOR kinase activity sets regulatory T cell responsiveness. Immunity 2010; 33: 929-941.
66. Procaccini C, Jirillo E, Matarese G. Leptin as an immunomodulator. Mol Aspects Med 2012; 33: 35-45.
67. Matarese G, Carrieri PB, La Cava A etal. Leptin increase in multiple sclerosis associates with reduced number of CD4(+)CD25+ regulatory T cells. Proc Natl Acad Sci U S A 2005; 102: 5150-5155.
68. Procaccini C, Galgani M, De Rosa V, Matarese G. Intracellular metabolic pathways control immune tolerance. Trends Immunol 2012; 33: 1-7.
69. Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res 2005; 96: 939-949.
70. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ. Nuclear receptors and lipid physiology: opening the X-files. Science 2001; 294: 1866-1870.
71. Hamaguchi M, Sakaguchi S. Regulatory T cells expressing PPAR-gamma control inflammation in obesity. Cell Metab 2012; 16: 4-6.
72. Balint BL, Nagy L. Selective modulators of PPAR activity as new therapeutic tools in metabolic diseases. Endocr Metab Immune Disord Drug Targets 2006; 6: 33-43.
73. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010; 72: 219-246.
74. Anbalagan M, Huderson B, Murphy L, Rowan BG. Post-translational modifications of nuclear receptors and human disease. Nucl Recept Signal 2012; 10: e001.
75. Rangwala SM, Rhoades B, Shapiro JS etal. Genetic modulation of PPAR gamma phosphorylation regulates insulin sensitivity. Dev Cell 2003; 5: 657-663.
76. Choi JH, Banks AS, Estall JL etal. Anti-diabetic drugs inhibit obesity-linked phosphorylation of PPAR gamma by Cdk5. Nature 2010; 466: 451-U451.
77. Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes (Lond) 2009; 33: 54-66.
78. He Q, Gao Z, Yin J, Zhang J, Yun Z, Ye J. Regulation of HIF-1{alpha} activity in adipose tissue by obesity-associated factors: adipogenesis, insulin, and hypoxia. Am J Physiol Endocrinol Metab 2011; 300: E877-E885.
79. Dang EV, Barbi J, Yang HY etal. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 2011; 146: 772-784.
80. Shi LZ, Wang R, Huang G etal. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011; 208: 1367-1376.
81. Darce J, Rudra D, Li L etal. An N-terminal mutation of the Foxp3 transcription factor alleviates arthritis but exacerbates diabetes. Immunity 2012; 36: 731-741.
82. Bettini ML, Pan F, Bettini M etal. Loss of epigenetic modification driven by the Foxp3 transcription factor leads to regulatory T cell insufficiency. Immunity 2012; 36: 717-730.
83. Boyman O, Kovar M, Rubinstein MP, Surh CD, Sprent J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 2006; 311: 1924-1927.
84. Hevener AL, Olefsky JM, Reichart D etal. Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest 2007; 117: 1658-1669.
85. Parker VE, Savage DB, O'Rahilly S, Semple RK. Mechanistic insights into insulin resistance in the genetic era. Diabet Med 2011; 28: 1476-1486.