B Lymphocytes in obesity-related adipose tissue inflammation and insulin resistance

Cellular and Molecular Life Sciences

Volumn 71, Issue 6, 2014, Pages 1033-1043

  Winer, Daniel A ^a,b   Winer, Shawn ^a,b   Chng, Melissa H Y ^c   Shen, Lei ^c   Engleman, Edgar G ^c  

^a TORONTO GENERAL HOSPITAL   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; B lymphocytes; Inflammation; Insulin resistance; Macrophages; T cells; Type 2 diabetes

Indexed keywords

ANTIBODY PRODUCTION; B LYMPHOCYTE; CELL MATURATION; DRUG TARGETING; GLUCOSE HOMEOSTASIS; HUMAN; IMMUNOMODULATION; INSULIN RESISTANCE; INTRAABDOMINAL FAT; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; REVIEW; SOFT TISSUE INFLAMMATION;

ANIMALS; B-LYMPHOCYTES; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; OBESITY;

EID: 84896726991     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1486-y     Document Type: Review

References (109)

1. Franks PW, Hanson RL, Knowler WC, Sievers ML, Bennett PH, Looker HC (2010) Childhood obesity, other cardiovascular risk factors, and premature death. N Engl J Med 362:485-493
2. Johnson AM, Olefsky JM (2013) The origins and drivers of insulin resistance. Cell 152:673-684
3. Xu H, Barnes GT, Yang Q et al (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821-1830
4. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796-1808
5. Winer S, Winer DA (2012) The adaptive immune system as a fundamental regulator of adipose tissue inflammation and insulin resistance. Immunol Cell Biol 90:755-762
6. Talukdar S, da Oh Y, Bandyopadhyay G et al (2012) Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 18:1407-1412
7. Ozcan U, Cao Q, Yilmaz E et al (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461
8. Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219-246
9. Odegaard JI, Chawla A (2013) Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339:172-177
10. Nishimura S, Manabe I, Nagasaki M et al (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15:914-920
11. Winer S, Chan Y, Paltser G et al (2009) Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15:921-929
12. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117:175-184
13. Wu D, Molofsky AB, Liang HE et al (2011) Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332:243-247
14. Feuerer M, Herrero L, Cipolletta D et al (2009) Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15:930-939
15. Molofsky AB, Nussbaum JC, Liang HE et al (2013) Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med 210:535-549
16. Lynch L, Nowak M, Varghese B et al (2012) Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 37:574-587
17. Yanaba K, Bouaziz JD, Matsushita T, Magro CM, St Clair EW, Tedder TF (2008) B-lymphocyte contributions to human autoimmune disease. Immunol Rev 223:284-299
18. Marino E, Grey ST (2012) B cells as effectors and regulators of autoimmunity. Autoimmunity 45:377-387
19. Duffaut C, Galitzky J, Lafontan M, Bouloumie A (2009) Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity. Biochem Biophys Res Commun 384:482-485
20. Winer DA, Winer S, Shen L et al (2011) B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 17:610-617
21. Defuria J, Belkina AC, Jagannathan-Bogdan M et al (2013) 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 110:5133-5138
22. Kaminski DA, Randall TD (2010) Adaptive immunity and adipose tissue biology. Trends Immunol 31:384-390
23. Haas KM, Poe JC, Steeber DA, Tedder TF (2005) B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23:7-18
24. Cui L, Johkura K, Liang Y et al (2002) Biodefense function of omental milky spots through cell adhesion molecules and leukocyte proliferation. Cell Tissue Res 310:321-330
25. Rangel-Moreno J, Moyron-Quiroz JE, Carragher DM et al (2009) Omental milky spots develop in the absence of lymphoid tissue-inducer cells and support B and T cell responses to peritoneal antigens. Immunity 30:731-743
26. Moro K, Yamada T, Tanabe M et al (2010) Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463:540-544
27. Ha SA, Tsuji M, Suzuki K et al (2006) Regulation of B1 cell migration by signals through Toll-like receptors. J Exp Med 203:2541-2550
28. Choi YS, Baumgarth N (2008) Dual role for B-1a cells in immunity to influenza virus infection. J Exp Med 205:3053-3064
29. Morris DL, Cho KW, Delproposto JL et al (2013) Adipose tissue macrophages function as antigen-presenting cells and regulate adipose tissue CD4+ T cells in mice. Diabetes 62:2762-2772
30. Martin F, Kearney JF (2001) B1 cells: similarities and differences with other B cell subsets. Curr Opin Immunol 13:195-201
31. Kunisawa J, Kurashima Y, Gohda M et al (2007) Sphingosine 1-phosphate regulates peritoneal B-cell trafficking for subsequent intestinal IgA production. Blood 109:3749-3756
32. Kearney JF (2000) Immune recognition of OxLDL in atherosclerosis. J Clin Invest 105:1683-1685
33. Binder CJ, Silverman GJ (2005) Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin Immunopathol 26:385-404
34. Ait-Oufella H, Herbin O, Bouaziz JD et al (2010) B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 207:1579-1587
35. Kyaw T, Tay C, Khan A et al (2010) Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immunol 185:4410-4419
36. Mauri C, Ehrenstein MR (2008) The 'short' history of regulatory B cells. Trends Immunol 29:34-40
37. Griffin DO, Holodick NE, Rothstein TL (2011) Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+CD43+ CD70. J Exp Med 208:67-80
38. Allman D, Pillai S (2008) Peripheral B cell subsets. Curr Opin Immunol 20:149-157
39. Lund FE (2008) Cytokine-producing B lymphocytes-key regulators of immunity. Curr Opin Immunol 20:332-338
40. Ruprecht CR, Lanzavecchia A (2006) Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 36:810-816
41. LeBien TW, Tedder TF (2008) B lymphocytes: how they develop and function. Blood 112:1570-1580
42. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-563
43. Yoshida T, Mei H, Dorner T et al (2010) Memory B and memory plasma cells. Immunol Rev 237:117-139
44. Mauri C, Bosma A (2012) Immune regulatory function of B cells. Annu Rev Immunol 30:221-241
45. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF (2008) A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28:639-650
46. Yoshizaki A, Miyagaki T, DiLillo DJ et al (2012) Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491:264-268
47. Melchers F (2005) The pre-B-cell receptor: selector of fitting immunoglobulin heavy chains for the B-cell repertoire. Nat Rev Immunol 5:578-584
48. Lam KP, Kuhn R, Rajewsky K (1997) In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90:1073-1083
49. Trottier MD, Naaz A, Li Y, Fraker PJ (2012) Enhancement of hematopoiesis and lymphopoiesis in diet-induced obese mice. Proc Natl Acad Sci USA 109:7622-7629
50. Claycombe K, King LE, Fraker PJ (2008) A role for leptin in sustaining lymphopoiesis and myelopoiesis. Proc Natl Acad Sci USA 105:2017-2021
51. Chan ME, Adler BJ, Green DE, Rubin CT (2012) Bone structure and B-cell populations, crippled by obesity, are partially rescued by brief daily exposure to low-magnitude mechanical signals. FASEB J: Off Publ Fed Am Soc Exp Biol 26:4855-4863
52. Elgazar-Carmon V, Rudich A, Hadad N, Levy R (2008) Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. J Lipid Res 49:1894-1903
53. Nguyen MT, Favelyukis S, Nguyen AK et al (2007) 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 282:35279-35292
54. Duddy M, Niino M, Adatia F et al (2007) Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J Immunol 178:6092-6099
55. Mauri C, Gray D, Mushtaq N, Londei M (2003) Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 197:489-501
56. Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF (2008) Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 118:3420-3430
57. Hong EG, Ko HJ, Cho YR et al (2009) Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58:2525-2535
58. Kowalski GM, Nicholls HT, Risis S et al (2011) Deficiency of haematopoietic-cell-derived IL-10 does not exacerbate high-fat-diet-induced inflammation or insulin resistance in mice. Diabetologia 54:888-899
59. van Exel E, Gussekloo J, de Craen AJ, Frolich M, Bootsma-Van Der Wiel A, Westendorp RG (2002) Low production capacity of interleukin-10 associates with the metabolic syndrome and type 2 diabetes: the Leiden 85-plus study. Diabetes 51:1088-1092
60. Jagannathan M, McDonnell M, Liang Y et al (2010) Toll-like receptors regulate B cell cytokine production in patients with diabetes. Diabetologia 53:1461-1471
61. Jagannathan-Bogdan M, McDonnell ME, Shin H et al (2011) Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J Immunol 186:1162-1172
62. Azar Sharabiani MT, Vermeulen R, Scoccianti C et al (2011) Immunologic profile of excessive body weight. Biomarkers 16:243-251
63. Papathanassoglou E, El-Haschimi K, Li XC, Matarese G, Strom T, Mantzoros C (2006) Leptin receptor expression and signaling in lymphocytes: kinetics during lymphocyte activation, role in lymphocyte survival, and response to high-fat diet in mice. J Immunol 176:7745-7752
64. Agrawal S, Gollapudi S, Su H, Gupta S (2011) Leptin activates human B cells to secrete TNF-alpha, IL-6, and IL-10 via JAK2/STAT3 and p38MAPK/ERK1/2 signaling pathway. J Clin Immunol 31:472-478
65. Lam QL, Wang S, Ko OK, Kincade PW, Lu L (2010) Leptin signaling maintains B-cell homeostasis via induction of Bcl-2 and Cyclin D1. Proc Natl Acad Sci USA 107:13812-13817
66. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116:3015-3025
67. DiLillo DJ, Yanaba K, Tedder TF (2010) B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J Immunol 184:4006-4016
68. Bouaziz JD, Yanaba K, Venturi GM et al (2007) Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc Natl Acad Sci USA 104:20878-20883
69. Poggi M, Engel D, Christ A et al (2011) CD40L deficiency ameliorates adipose tissue inflammation and metabolic manifestations of obesity in mice. Arterioscler Thromb Vasc Biol 31:2251-2260
70. Wolf D, Jehle F, Ortiz Rodriguez A et al (2012) CD40L deficiency attenuates diet-induced adipose tissue inflammation by impairing immune cell accumulation and production of pathogenic IgG-antibodies. PLoS ONE 7:e33026
71. Guo CA, Kogan S, Amano SU et al (2013) CD40 deficiency in mice exacerbates obesity-induced adipose tissue inflammation, hepatic steatosis, and insulin resistance. Am J Physiol Endocrinol Metab 304:E951-E963
72. Hamada M, Abe M, Miyake T et al (2011) B cell-activating factor controls the production of adipokines and induces insulin resistance. Obesity (Silver Spring) 19:1915-1922
73. Tada F, Abe M, Kawasaki K et al (2013) B cell activating factor in obesity is regulated by oxidative stress in adipocytes. J Clin Biochem Nutr 52:120-127
74. Nikolajczyk BS, Jagannathan-Bogdan M, Shin H, Gyurko R (2011) State of the union between metabolism and the immune system in type 2 diabetes. Genes Immun 12:239-250
75. Mito N, Kaburagi T, Yoshino H, Imai A, Sato K (2006) Oral-tolerance induction in diet-induced obese mice. Life Sci 79:1056-1061
76. Palming J, Gabrielsson BG, Jennische E et al (2006) Plasma cells and Fc receptors in human adipose tissue-lipogenic and anti-inflammatory effects of immunoglobulins on adipocytes. Biochem Biophys Res Commun 343:43-48
77. Mamane Y, Chung Chan C, Lavallee G et al (2009) The C3a anaphylatoxin receptor is a key mediator of insulin resistance and functions by modulating adipose tissue macrophage infiltration and activation. Diabetes 58:2006-2017
78. Shulzhenko N, Morgun A, Hsiao W et al (2011) Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med 17:1585-1593
79. Tilg H, Kaser A (2011) Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest 121:2126-2132
80. Qin J, Li Y, Cai Z et al (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490:55-60
81. Lam YY, Ha CW, Campbell CR et al (2012) Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS ONE 7:e34233
82. Wang Y, Li J, Tang L, Charnigo R, de Villiers W, Eckhardt E (2010) T-lymphocyte responses to intestinally absorbed antigens can contribute to adipose tissue inflammation and glucose intolerance during high-fat feeding. PLoS ONE 5:e13951
83. Wang Y, Ghoshal S, Ward M, de Villiers W, Woodward J, Eckhardt E (2009) Chylomicrons promote intestinal absorption and systemic dissemination of dietary antigen (ovalbumin) in mice. PLoS ONE 4:e8442
84. Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E (2009) Chylomicrons promote intestinal absorption of lipopolysaccharides. J Lipid Res 50:90-97
85. Cani PD, Amar J, Iglesias MA et al (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761-1772
86. Mohammed N, Tang L, Jahangiri A, de Villiers W, Eckhardt E (2012) Elevated IgG levels against specific bacterial antigens in obese patients with diabetes and in mice with diet-induced obesity and glucose intolerance. Metabolism 61:1211-1214
87. Hotamisligil GS (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140:900-917
88. Alkhouri N, Gornicka A, Berk MP et al (2010) Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J Biol Chem 285:3428-3438
89. Wueest S, Rapold RA, Schumann DM et al (2010) Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J Clin Invest 120:191-202
90. Gomez-Tourino I, Camina-Darriba F, Otero-Romero I et al (2010) Autoantibodies to glial fibrillary acid protein and S100beta in diabetic patients. Diabet Med 27:246-248
91. Yi CX, Tschop MH, Woods SC, Hofmann SM (2012) High-fat-diet exposure induces IgG accumulation in hypothalamic microglia. Dis Model Mech 5:686-690
92. Winer S, Tsui H, Lau A et al (2003) Autoimmune islet destruction in spontaneous type 1 diabetes is not beta-cell exclusive. Nat Med 9:198-205
93. Aran A, Weiner K, Lin L et al (2010) Post-streptococcal auto-antibodies inhibit protein disulfide isomerase and are associated with insulin resistance. PLoS ONE 5:e12875
94. Chen R, Mias GI, Li-Pook-Than J et al (2012) Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell 148:1293-1307
95. Fredrikson GN, Anand DV, Hopkins D et al (2009) Associations between autoantibodies against apolipoprotein B-100 peptides and vascular complications in patients with type 2 diabetes. Diabetologia 52:1426-1433
96. Zimering MB, Pan Z (2009) Autoantibodies in type 2 diabetes induce stress fiber formation and apoptosis in endothelial cells. J Clin Endocrinol Metab 94:2171-2177
97. Hempel P, Karczewski P, Kohnert KD et al (2009) Sera from patients with type 2 diabetes contain agonistic autoantibodies against G protein-coupled receptors. Scand J Immunol 70:159-160
98. Gabriel CL, Smith PB, Mendez-Fernandez YV, Wilhelm AJ, Ye AM, Major AS (2012) Autoimmune-mediated glucose intolerance in a mouse model of systemic lupus erythematosus. Am J Physiol Endocrinol Metab 303:E1313-E1324
99. Arai S, Maehara N, Iwamura Y et al (2013) Obesity-associated autoantibody production requires AIM to retain the immunoglobulin m immune complex on follicular dendritic cells. Cell Rep 3:1187-1198
100. Tuomi T, Groop LC, Zimmet PZ, Rowley MJ, Knowles W, Mackay IR (1993) Antibodies to glutamic acid decarboxylase reveal latent autoimmune diabetes mellitus in adults with a non-insulin-dependent onset of disease. Diabetes 42:359-362
101. Larsen CM, Faulenbach M, Vaag A et al (2007) Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356:1517-1526
102. Goldfine AB, Fonseca V, Jablonski KA, Pyle L, Staten MA, Shoelson SE (2010) The effects of salsalate on glycemic control in patients with type 2 diabetes: a randomized trial. Ann Intern Med 152:346-357
103. Tesfa D, Ajeganova S, Hagglund H et al (2011) Late-onset neutropenia following rituximab therapy in rheumatic diseases: association with B lymphocyte depletion and infections. Arthritis Rheum 63:2209-2214
104. Rauch M, Tussiwand R, Bosco N, Rolink AG (2009) Crucial role for BAFF-BAFF-R signaling in the survival and maintenance of mature B cells. PLoS ONE 4:e5456
105. Kyaw T, Tay C, Hosseini H et al (2012) Depletion of B2 but not B1a B cells in BAFF receptor-deficient ApoE mice attenuates atherosclerosis by potently ameliorating arterial inflammation. PLoS ONE 7:e29371
106. Sage AP, Tsiantoulas D, Baker L et al (2012) BAFF receptor deficiency reduces the development of atherosclerosis in mice: brief report. Arterioscler Thromb Vasc Biol 32:1573-1576
107. Kawasaki K, Abe M, Tada F et al (2013) Blockade of B-cell-activating factor signaling enhances hepatic steatosis induced by a high-fat diet and improves insulin sensitivity. Lab Invest 93:311-321
108. Mingrone G, Panunzi S, De Gaetano A et al (2012) Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med 366:1577-1585
109. Zhang H, Wang Y, Zhang J, Potter BJ, Sowers JR, Zhang C (2011) Bariatric surgery reduces visceral adipose inflammation and improves endothelial function in type 2 diabetic mice. Arterioscler Thromb Vasc Biol 31:2063-2069