Role of T Lymphocytes in Type 2 Diabetes and Diabetes-Associated Inflammation

Journal of Diabetes Research

Volumn 2017, Issue , 2017, Pages

  Xia, Chang ^a,b   Rao, Xiaoquan ^b   Zhong, Jixin ^b  

^a WUHAN POLYTECHNIC UNIVERSITY   (China)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8+ T LYMPHOCYTE; CHRONIC INFLAMMATION; CYTOTOXIC T LYMPHOCYTE; GAMMA DELTA T LYMPHOCYTE; HUMAN; INFLAMMATION; NATURAL KILLER CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; IMMUNOLOGY; INSULIN RESISTANCE;

DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; T-LYMPHOCYTES;

EID: 85013344047     PISSN: 23146745     EISSN: 23146753     Source Type: Journal    
DOI: 10.1155/2017/6494795     Document Type: Review

References (75)

1. J. M. Guzmán-Flores and S. López-Briones, "Cells of the innate and adaptive immunity in type 2 diabetes mellitus and obesity," Gaceta Medica de Mexico, vol. 148, no. 4, pp. 381-389, 2012.
2. C. J. Shu, C. Benoist, and D. Mathis, "The immune system's involvement in obesity-driven type 2 diabetes," Seminars in Immunology, vol. 24, no. 6, pp. 436-442, 2012.
3. V. Guarner andM. E. Rubio-Ruiz, "Low-grade systemic inflammation connects aging, metabolic syndrome and cardiovascular disease," Aging and Health-A Systems Biology Perspective, vol. 40, pp. 99-106, 2014.
4. G. S. Hotamisligil, N. S. Shargill, and B. M. Spiegelman, "Adipose expression of tumor necrosis factor-direct role in obesity-linked insulin resistance," Science, vol. 259, no. 5091, pp. 87-91, 1993.
5. D. Mathis, "Immunological goings-on in visceral adipose tissue," Cell Metabolism, vol. 17, no. 6, pp. 851-859, 2013.
6. N. Ouchi, J. L. Parker, J. J. Lugus, and K.Walsh, "Adipokines in inflammation andmetabolic disease,"Nature Reviews Immunology, vol. 11, no. 2, pp. 85-97, 2011.
7. J. I. Odegaard, R. R. Ricardo-Gonzalez, M. H. Goforth et al., "Macrophage-specific PPAR controls alternative activation and improves insulin resistance," Nature, vol. 447, no. 7148, pp. 1116-1120, 2007.
8. S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante Jr., "Obesity is associated with macrophage accumulation in adipose tissue," Journal of Clinical Investigation, vol. 112, no. 12, pp. 1796-1808, 2003.
9. L. Boutens and R. Stienstra, "Adipose tissuemacrophages: going off track during obesity," Diabetologia, vol. 59, no. 5, pp. 879- 894, 2016.
10. K. Shirakawa, X. Yan, K. Shinmura et al., "Obesity accelerates T cell senescence in murine visceral adipose tissue," Journal of Clinical Investigation, vol. 126, no. 12, pp. 4626-4639, 2016.
11. T. Deng, C. J. Lyon, L. J. Minze et al., "Class II major histocompatibility complex plays an essential role in obesity-induced adipose inflammation," Cell Metabolism, vol. 17, no. 3, pp. 411- 422, 2013.
12. I. Raphael, S. Nalawade, T. N. Eagar, and T. G. Forsthuber, "T cell subsets and their signature cytokines in autoimmune and inflammatory diseases," Cytokine, vol. 74, no. 1, pp. 5-17, 2015.
13. S. E. Kahn, R. L. Hull, and K. M. Utzschneider, "Mechanisms linking obesity to insulin resistance and type 2 diabetes," Nature, vol. 444, no. 7121, pp. 840-846, 2006.
14. F. O. Martinez, "Macrophage activation and polarization," Frontiers in Bioscience, vol. 13, no. 13, p. 453, 2008.
15. D. E. Cintra, J. R. Pauli, E. P. Araújo et al., "Interleukin-10 is a protective factor against diet-induced insulin resistance in liver," Journal of Hepatology, vol. 48, no. 4, pp. 628-637, 2008.
16. C.N. Lumeng, J. L. Bodzin, andA. R. Saltiel, "Obesity induces a phenotypic switch in adipose tissue macrophage polarization," Journal of Clinical Investigation, vol. 117, no. 1, pp. 175-184, 2007.
17. S. Winer, Y. Chan, G. Paltser et al., "Normalization of obesityassociated insulin resistance through immunotherapy," Nature Medicine, vol. 15, no. 8, pp. 921-929, 2009.
18. F. C. McGillicuddy, E. H. Chiquoine, C. C. Hinkle et al., "Interferon γ attenuates insulin signaling, lipid storage, and differentiation in human adipocytes via activation of the JAK/ STAT pathway,"The Journal of Biological Chemistry, vol. 284, no. 46, pp. 31936-31944, 2009.
19. M. Feuerer, L.Herrero, D. Cipolletta et al., "Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affectmetabolic parameters," Nature Medicine, vol. 15, no. 8, pp. 930-939, 2009.
20. A. Chatzigeorgiou, K. P. Karalis, S. R. Bornstein, and T. Chavakis, "Lymphocytes in obesity-related adipose tissue inflammation," Diabetologia, vol. 55, no. 10, pp. 2583-2592, 2012.
21. S. Nishimura, I. Manabe, M. Nagasaki et al., "CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity," Nature Medicine, vol. 15, no. 8, pp. 914-920, 2009.
22. T. McLaughlin, L. Liu, C. Lamendola et al., "T-cell profile in adipose tissue is associated with insulin resistance and systemic inflammation in humans," Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 34, no. 12, pp. 2637-2643, 2014.
23. C. Zeng, X. Shi, B. Zhang et al., "The imbalance of Th17/Th1/ Tregs in patients with type 2 diabetes: relationship with metabolic factors and complications," Journal ofMolecularMedicine, vol. 90, no. 2, pp. 175-186, 2012.
24. M. P.Nekoua, R. Fachinan, A. K. Atchamou et al., "Modulation of immune cells andTh1/Th2 cytokines in insulin-treated type 2 diabetes mellitus," African Health Sciences, vol. 16, no. 3, pp. 712-724, 2016.
25. Y. S. Lee, P. Li, J. Y. Huh et al., "Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance," Diabetes, vol. 60, no. 10, pp. 2474-2483, 2011.
26. K. A. Harford, C. M. Reynolds, F. C. McGillicuddy, and H. M. Roche, "Fats, inflammation and insulin resistance: insights to the role of macrophage and T-cell accumulation in adipose tissue," Proceedings of the Nutrition Society, vol. 70, no. 4, pp. 408-417, 2011.
27. J. F. Navarro and C. Mora, "Diabetes, inflammation, proinflammatory cytokines, and diabetic nephropathy,"TheScientific- WorldJournal, vol. 6, pp. 908-917, 2006.
28. S. Abouzeid and N. Sherif, "Role of alteration in Treg/Th17 cells' balance in nephropathic patients with Type 2 diabetesmellitus," Electronic physician, vol. 7, no. 8, pp. 1613-1618, 2015.
29. D. Wu, A. B. Molofsky, H.-E. Liang et al., "Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis," Science, vol. 332, no. 6026, pp. 243-247, 2011.
30. C. Francisco, A. Catai, S.Moura-Tonello et al., "Cytokine profile and lymphocyte subsets in type 2 diabetes," Brazilian Journal of Medical and Biological Research, vol. 49, no. 4, 2016.
31. S. Mocellin, F. Marincola, C. R. Rossi, D. Nitti, and M. Lise, "The multifaceted relationship between IL-10 and adaptive immunity: putting together the pieces of a puzzle," Cytokine and Growth Factor Reviews, vol. 15, no. 1, pp. 61-76, 2004.
32. Y. Ilan, R.Maron, A.-M. Tukpah et al., "Induction of regulatory T cells decreases adipose inflammation and alleviates insulin resistance in ob/ob mice," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 21, pp. 9765-9770, 2010.
33. C. Zhang, C. Xiao, P. Wang et al., "The alteration of Th1/Th2/ Th17/Treg paradigm in patients with type 2 diabetes mellitus: relationship with diabetic nephropathy," Human Immunology, vol. 75, no. 4, pp. 289-296, 2014.
34. L. A. Zuniga, W. Shen, B. Joyce-Shaikh et al., "IL-17 regulates adipogenesis, glucose homeostasis, and obesity," The Journal of Immunology, vol. 185, no. 11, pp. 6947-6959, 2010.
35. L. Garidou, C. Pomié, P. Klopp et al., "The gut microbiota regulates intestinal CD4 T cells expressing RORγ and controls metabolic disease," Cell Metabolism, vol. 22, no. 1, pp. 100-112, 2015.
36. M. K.Hamilton, G. Boudry, D. G. Lemay, and H. E. Raybould, "Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent," American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 308, no. 10, pp.G840-G851, 2015.
37. A. Bertola, T. Ciucci, D. Rousseau et al., "Identification of adipose tissue dendritic cells correlated with obesity-associated insulin-resistance and inducing Th17 responses in mice and patients," Diabetes, vol. 61, no. 9, pp. 2238-2247, 2012.
38. B.-C. Lee and J. Lee, "Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance," Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1842, no. 3, pp. 446-462, 2014.
39. E. Dalmas, N. Venteclef, C. Caer et al., "T cell-derived IL-22 amplifies IL-1-driven inflammation in human adipose tissue: relevance to obesity and type 2 diabetes," Diabetes, vol. 63, no. 6, pp. 1966-1977, 2014.
40. R. Zhao, D. Tang, S. Yi et al., "Elevated peripheral frequencies of Th22 cells: a novel potent participant in obesity and type 2 diabetes," PLoS ONE, vol. 9, no. 1,Article ID e85770, 2014.
41. B. C. Ip, A. E. Hogan, and B. S. Nikolajczyk, "Lymphocyte roles in metabolic dysfunction: of men and mice," Trends in Endocrinology and Metabolism, vol. 26, no. 2, pp. 91-100, 2015.
42. Y. Zheng and A.Y. Rudensky, "Foxp3 in control of the regulatory T cell lineage," Nature Immunology, vol. 8, no. 5, pp. 457-462, 2007.
43. S. Sakaguchi, T. Yamaguchi, T. Nomura, and M. Ono, "Regulatory T cells and immune tolerance," Cell, vol. 133, no. 5, pp. 775-787, 2008.
44. T. J. Murphy, N. N. Choileain, Y. Zang, J. A. Mannick, and J. A. Lederer, "CD4+CD25+ regulatory T cells control innate immune reactivity after injury," Journal of Immunology, vol. 174, no. 5, pp. 2957-2963, 2005.
45. L. T. Nguyen, J. Jacobs, D. Mathis, and C. Benoist, "Where FoxP3-dependent regulatory T cells impinge on the development of inflammatory arthritis," Arthritis & Rheumatism, vol. 56, no. 2, pp. 509-520, 2007.
46. M. Jagannathan-Bogdan,M. E.McDonnell, H. Shin et al., "Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes," Journal of Immunology, vol. 186, no. 2, pp. 1162-1172, 2011.
47. J. M. Guzmán-Flores and D. P. Portales-Pérez, "Mechanisms of suppression by regulatory T cells (Treg)," Gaceta Medica de Mexico, vol. 149, no. 6, pp. 630-638, 2013.
48. M. F. Gregor and G. S. Hotamisligil, "Inflammatory mechanisms in obesity," Annual Review of Immunology, vol. 29, pp. 415-445, 2011.
49. L. Zeng, H. Lu, H. Deng, P. Mu, X. Li, and M. Wang, "Noninferiority effects on glycemic control and -cell function improvement in newly diagnosed type 2 diabetes patients: basal insulin monotherapy versus continuous subcutaneous insulin infusion treatment," Diabetes Technology andTherapeutics, vol. 14, no. 1, pp. 35-42, 2012.
50. V.Della Latta, M. Cabiati, S. Rocchiccioli, S.Del Ry, and M.-A. Morales, "The role of the adenosinergic systemin lung fibrosis," Pharmacological Research, vol. 76, pp. 182-189, 2013.
51. J. Gu, X. Ni, X. Pan et al., "Human CD39hi regulatory T cells present stronger stability and function under inflammatory conditions," Cellular & Molecular Immunology, vol. 13, pp. 1-8, 2016.
52. Y. Sun, W.-Z. Liu, T. Liu, X. Feng, N. Yang, and H.-F. Zhou, "Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis," Journal of Receptors and Signal Transduction, vol. 35, no. 6, pp. 600-604, 2015.
53. U. Kintscher, M. Hartge, K. Hess et al., "T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance," Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 7, pp. 1304-1310, 2008.
54. H. Luck, S. Tsai, J. Chung et al., "Regulation of obesity-related insulin resistance with gut anti-inflammatory agents," Cell Metabolism, vol. 21, no. 4, pp. 527-542, 2015.
55. D. S. Vinay and B. S. Kwon, "Role of 4-1BB in immune responses," Seminars in Immunology, vol. 10, no. 6, pp. 481-489, 1998.
56. T. H. Tu,C.-S.Kim, J.-H.Kang et al., "Levels of 4-1BB transcripts and soluble 4-1BB protein are elevated in the adipose tissue of human obese subjects and are associated with inflammatory andmetabolic parameters," International Journal ofObesity, vol. 38, no. 8, pp. 1075-1082, 2014.
57. T. H. Tu, C.-S. Kim, T. Goto, T. Kawada, B.-S. Kim, and R. Yu, "4-1BB/4-1BBL interaction promotes obesity-induced adipose inflammation by triggering bidirectional inflammatory signaling in adipocytes/macrophages," Mediators of Inflammation, vol. 2012, Article ID 972629, 10 pages, 2012.
58. C. S.Kim, J. G.Kim, B. J. Lee et al., "Deficiency for costimulatory receptor 4-1BB protects against obesity-induced inflammation andmetabolic disorders," Diabetes, vol. 60,no. 12,pp. 3159-3168, 2011.
59. K. A. Rhodes, E. M. Andrew, D. J. Newton, D. Tramonti, and S. R. Carding, "A subset of IL-10-producing T cells protect the liver from Listeria-elicited, CD8+ T cell-mediated injury," European Journal of Immunology, vol. 38, no. 8, pp. 2274-2283, 2008.
60. K. D. C. Jensen, X. Su, S. Shin et al., "Thymic selection determines T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon ," Immunity, vol. 29, no. 1, pp. 90-100, 2008.
61. D. E. Lackey and J. M. Olefsky, "Regulation of metabolism by the innate immune system," Nature Reviews Endocrinology, vol. 12, no. 1, pp. 15-20, 2016.
62. T. Dimova, M. Brouwer, F. Gosselin et al., "Effector V9V2 T cells dominate the human fetal T-cell repertoire," Proceedings of the National Academy of Sciences, vol. 112, no. 6, pp. E556- E565, 2015.
63. A. E. Costanzo, K. R. Taylor, S. Dutt, P. P. Han, K. Fujioka, and J. M. Jameson, "Obesity impairs T cell homeostasis and antiviral function in humans," PLoS ONE, vol. 10, no. 3, Article ID e0120918, 2015.
64. L. A. Lynch, J. M. O'Connell, A. K. Kwasnik, T. J. Cawood, C. O'Farrelly, and D. B. O'Shea, "Are natural killer cells protecting the metabolically healthy obese patient?" Obesity, vol. 17, no. 3, pp. 601-605, 2009.
65. L. Lynch, D. O'Shea, D. C.Winter, J. Geoghegan, D. G. Doherty, and C. O'Farrelly, "Invariant NKT cells and CD1d+ cells amass in human omentum and are depleted in patients with cancer and obesity," European Journal of Immunology, vol. 39, no. 7, pp. 1893-1901, 2009.
66. L. Lynch, M.Nowak, B.Varghese et al., "Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production," Immunity, vol. 37, no. 3, pp. 574-587, 2012.
67. M. Brigl and M. B. Brenner, "CD1: antigen presentation and T cell function," Annual Review of Immunology, vol. 22, pp. 817- 890, 2004.
68. E. M. Beckman, S. A. Porcelli, C. T. Morita, S. M. Behar, S. T. Furlong, and M. B. Brenner, "Recognition of a lipid antigen by GDI-restricted + T cells," Nature, vol. 372, no. 6507, pp. 691- 694, 1994.
69. L. Lynch, X. Michelet, S. Zhang et al., "Regulatory iNKT cells lack expression of the transcription factor PLZF and control the homeostasis of T cells and macrophages in adipose tissue," Nature Immunology, vol. 16, no. 1, pp. 85-95, 2015.
70. H. S. Schipper, M. Rakhshandehroo, S. F. J. Van De Graaf et al., "Natural killer T cells in adipose tissue prevent insulin resistance," Journal of Clinical Investigation, vol. 122, no. 9, pp. 3343- 3354, 2012.
71. J. Y. Huh, J. I. Kim, Y. J. Park et al., "A novel function of adipocytes in lipid antigen presentation to iNKT cells," Molecular and Cellular Biology, vol. 33, no. 2, pp. 328-339, 2013.
72. E. Hams, R. M. Locksley, A. N. J.McKenzie, and P. G. Fallon, "Cutting edge: IL-25 elicits innate lymphoid type 2 and type II NKT cells that regulate obesity in mice," The Journal of Immunology, vol. 191, no. 11, pp. 5349-5353, 2013.
73. Y. Ji, S. Sun, A. Xu et al., "Activation of natural killer T cells promotes M2 macrophage polarization in adipose tissue and improves systemic glucose tolerance via interleukin-4 (IL- 4)/STAT6 protein signaling axis in obesity," Journal of Biological Chemistry, vol. 287, no. 17, pp. 13561-13571, 2012.
74. A. Kohlgruber and L. Lynch, "Adipose tissue inflammation in the pathogenesis of type 2 diabetes," Current Diabetes Reports, vol. 15, no. 11, article no. 92, 2015.
75. S. Tsai, X. Clemente-Casares, X. S. Revelo, S. Winer, and D. A. Winer, "Are obesity-related insulin resistance and type 2 diabetes autoimmune diseases?" Diabetes, vol. 64, no. 6, pp. 1886-1897, 2015.