The role of infiltrating immune cells in dysfunctional adipose tissue

Cardiovascular Research

Volumn 113, Issue 9, 2017, Pages 1009-1023

  Guzik, Tomasz J ^a,b   Skiba, Dominik S ^a,b   Touyz, Rhian M ^a   Harrison, David G ^a,c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Adipose tissue; Atherosclerosis; Diabetes; Hypertension; Inflammation

Indexed keywords

ADIPOSE TISSUE; ATHEROSCLEROSIS; CELL FUNCTION; CELL INFILTRATION; CHRONIC INFLAMMATION; DIABETES MELLITUS; EVIDENCE BASED PRACTICE; HUMAN; HYPERTENSION; IMMUNOCOMPETENT CELL; IMMUNOPATHOLOGY; INFLAMMATORY DISEASE; INSULIN RESISTANCE; LIPID STORAGE; METABOLIC DISORDER; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; TISSUE REACTION; TRANSLATIONAL RESEARCH; VASCULAR DISEASE; ANIMAL; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; ENERGY METABOLISM; IMMUNE SYSTEM; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ADIPOCYTOKINE; AUTACOID; CYTOKINE;

ADIPOKINES; ADIPOSE TISSUE; ADIPOSITY; ANIMALS; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; CYTOKINES; ENERGY METABOLISM; HUMANS; IMMUNE SYSTEM; INFLAMMATION; INFLAMMATION MEDIATORS; OBESITY; SIGNAL TRANSDUCTION; TRANSLATIONAL MEDICAL RESEARCH;

EID: 85028428326     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvx108     Document Type: Review

References (217)

1. Stevens GA, Singh GM, Lu Y, Danaei G, Lin JK, Finucane MM, Bahalim AN, McIntire RK, Gutierrez HR, Cowan M, Paciorek CJ, Farzadfar F, Riley L, Ezzati M, Factors GBMR. National, regional, and global trends in adult overweight and obesity prevalences. Popul Health Metr 2012;10:22.
2. Newton R, Priyadharshini B, Turka LA. Immunometabolism of regulatory T cells. Nat Immunol 2016;17:618-625.
3. Norata GD, Caligiuri G, Chavakis T, Matarese G, Netea MG, Nicoletti A, O'neill LA, Marelli-Berg FM. The cellular and molecular basis of translational immunometabolism. Immunity 2015;43:421-434.
4. Guzik TJ, Cosentino F. Epigenetics and immunometabolism in diabetes and aging. Antioxid Redox Signal 2017; in revision.
5. Ronti T, Lupattelli G, Mannarino E. The endocrine function of adipose tissue: An update. Clin Endocrinol (Oxf) 2006;64:355-365.
6. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P. Functional brown adipose tissue in healthy adults. N Engl J Med 2009;360:1518-1525.
7. Ibrahim MM. Subcutaneous and visceral adipose tissue: Structural and functional differences. Obes Rev 2010;11:11-18.
8. Nosalski R, Guzik TJ. Perivascular adipose tissue inflammation in vascular disease. Br J Pharmacol 2017; doi: 10.1111/bph.13705.
9. Lim S, Meigs JB. Ectopic fat and cardiometabolic and vascular risk. Int J Cardiol 2013;169:166-176.
10. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-1808.
11. Xu HY, Barnes GT, Yang Q, Tan Q, Yang DS, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003;112: 1821-1830.
12. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumornecrosis-factor-alpha-direct role in obesity-linked insulin resistance. Science 1993;259:87-91.
13. 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.
14. Chatterjee TK, Aronow BJ, Tong WS, Manka D, Tang Y, Bogdanov VY, Unruh D, Blomkalns AL, Piegore MG, Jr., Weintraub DS, Rudich SM, Kuhel DG, Hui DY, Weintraub NL. Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis. Physiol Genomics 2013;45:697-709.
15. Brown NK, Zhou Z, Zhang JF, Zeng R, Wu JR, Eitzman DT, Chen YE, Chang L. Perivascular adipose tissue in vascular function and disease-a review of current research and animal models. Arterioscl Throm Vas 2014;34:1621-1630.
16. Watanabe K, Watanabe R, Konii H, Shirai R, Sato K, Matsuyama TA, Ishibashi-Ueda H, Koba S, Kobayashi Y, Hirano T, Watanabe T. Counteractive effects of omentin-1 against atherogenesisdagger. Cardiovasc Res 2016;110:118-128.
17. Hiramatsu-Ito M, Shibata R, Ohashi K, Uemura Y, Kanemura N, Kambara T, Enomoto T, Yuasa D, Matsuo K, Ito M, Hayakawa S, Ogawa H, Otaka N, Kihara S, Murohara T, Ouchi N. Omentin attenuates atherosclerotic lesion formation in apolipoprotein E-deficient mice. Cardiovasc Res 2016;110:107-117.
18. Kanneganti TD, Dixit VD. Immunological complications of obesity. Nat Immunol 2012;13:707-712.
19. Hong EG, Ko HJ, Cho YR, Kim HJ, Ma Z, Yu TY, Friedline RH, Kurt-Jones E, Finberg R, Fischer MA, Granger EL, Norbury CC, Hauschka SD, Philbrick WM, Lee CG, Elias JA, Kim JK. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 2009;58:2525-2535.
20. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117:175-184.
21. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the antiinflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004;323:630-635.
22. Cintra DE, Pauli JR, Araujo EP, Moraes JC, de Souza CT, Milanski M, Morari J, Gambero A, Saad MJ, Velloso LA. Interleukin-10 is a protective factor against dietinduced insulin resistance in liver. J Hepatol 2008;48:628-637.
23. Nguyen KD, Qiu Y, Cui X, Goh YP, Mwangi J, David T, Mukundan L, Brombacher F, Locksley RM, Chawla A. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 2011;480:104-108.
24. Qiu Y, Nguyen KD, Odegaard JI, Cui X, Tian X, Locksley RM, Palmiter RD, Chawla A. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 2014;157:1292-1308.
25. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee J, Goldfine AB, Benoist C, Shoelson S, Mathis D. 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. Guzik TJ, Marvar PJ, Czesnikiewicz-Guzik M, Korbut R. Perivascular adipose tissue as a messenger of the brain-vessel axis: Role in vascular inflammation and dysfunction. J Physiol Pharmacol 2007;58:591-610.
27. Ignacak A, Kasztelnik M, Sliwa T, Korbut RA, Rajda K, Guzik TJ. Prolactin-not only lactotrophin. A "new" view of the "old" hormone. J Physiol Pharmacol 2012;63:435-443.
28. Sun K, Tordjman J, Clement K, Scherer PE. Fibrosis and Adipose Tissue Dysfunction. Cell Metab 2013;18:470-477.
29. Guzik TJ, Mangalat D, Korbut R. Adipocytokines - novel link between inflammation and vascular function?. J Physiol Pharmacol 2006;57:505-528.
30. Hatem SN, Redheuil A, Gandjbakhch E. Cardiac adipose tissue and atrial fibrillation: The perils of adiposity. Cardiovasc Res 2016;109:502-509.
31. Naylor C, Petri WA. Jr. Leptin regulation of immune responses. Trends Mol Med 2016;22:88-98.
32. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011;11:85-97.
33. Shibata S, Tada Y, Hau CS, Mitsui A, Kamata M, Asano Y, Sugaya M, Kadono T, Masamoto Y, Kurokawa M, Yamauchi T, Kubota N, Kadowaki T, Sato S. Adiponectin regulates psoriasiform skin inflammation by suppressing IL-17 production from gammadelta-T cells. Nat Commun 2015;6:7687.
34. Cheng X, Folco EJ, Shimizu K, Libby P. Adiponectin induces pro-inflammatory programs in human macrophages and CD4+ T cells. J Biol Chem 2012;287:36896-36904.
35. Walcher D, Hess K, Berger R, Aleksic M, Heinz P, Bach H, Durst R, Hausauer A, Hombach V, Marx N. Resistin: A newly identified chemokine for human CD4-positive lymphocytes. Cardiovasc Res 2010;85:167-174.
36. Kukla M, Mazur W, Buldak RJ, Zwirska-Korczala K. Potential role of leptin, adiponectin and three novel adipokines-visfatin, chemerin and vaspin-in chronic hepatitis. Mol Med 2011;17:1397-1410.
37. Moraes-Vieira PM, Yore MM, Dwyer PM, Syed I, Aryal P, Kahn BB. RBP4 activates antigen-presenting cells, leading to adipose tissue inflammation and systemic insulin resistance. Cell Metab 2014;19:512-526.
38. Skiba DS, Nosalski R, Mikolajczyk TP, Siedlinski M, Rios FJ, Montezano AC, Jawien J, Olszanecki R, Korbut R, Czesnikiewicz-Guzik M, Touyz RM, Guzik TJ. Antiatherosclerotic effect of Ang- (1-7) non-peptide mimetic (AVE 0991) is mediated by inhibition of perivascular and plaque inflammation in early atherosclerosis. Br J Pharmacol 2016. doi: 10.1111/bph.13685.
39. Mikolajczyk TP, Nosalski R, Szczepaniak P, Budzyn K, Osmenda G, Skiba D, Sagan A, Wu J, Vinh A, Marvar PJ, Guzik B, Podolec J, Drummond G, Lob HE, Harrison DG, Guzik TJ. Role of chemokine RANTES in the regulation of perivascular inflammation, T-cell accumulation, and vascular dysfunction in hypertension. Faseb J 2016;30:1987-1999.
40. Bapat SP, Suh JM, Fang S, Liu SH, Zhang Y, Cheng A, Zhou C, Liang YQ, LeBlanc M, Liddle C, Atkins AR, Yu RT, Downes M, Evans RM, Zheng Y. Depletion of fat-resident T-reg cells prevents age-associated insulin resistance. Nature 2015;528:137. +.
41. Freemerman AJ, Johnson AR, Sacks GN, Milner JJ, Kirk EL, Troester MA, Macintyre AN, Goraksha-Hicks P, Rathmell JC, Makowski L. Metabolic reprogramming of macrophages: Glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem 2014;289:7884-7896.
42. Pamir N, Liu NC, Irwin A, Becker L, Peng YF, Ronsein GE, Bornfeldt KE, Duffield JS, Heinecke JW. Granulocyte/macrophage colony-stimulating factor-dependent dendritic cells restrain lean adipose tissue expansion. J Biol Chem 2015;290:14656-14667.
43. Bilkovski R, Schulte DM, Oberhauser F, Mauer J, Hampel B, Gutschow C, Krone W, Laudes M. Adipose tissue macrophages inhibit adipogenesis of mesenchymal precursor cells via wnt-5a in humans. Int J Obes Relat Metab Disord 2011;35:1450-1454.
44. Chen YH, Tian J, Tian XY, Tang XY, Rui K, Tong J, Lu LW, Xu HX, Wang SJ. Adipose tissue dendritic cells enhances inflammation by prompting the generation of Th17 cells. Plos One 2014;9.
45. Moore JP, Vinh A, Tuck KL, Sakkal S, Krishnan SM, Chan CT, Lieu M, Samuel CS, Diep H, Kemp-Harper BK, Tare M, Ricardo SD, Guzik TJ, Sobey CG, Drummond GR. M2 macrophage accumulation in the aortic wall during angiotensin II infusion in mice is associated with fibrosis, elastin loss, and elevated blood pressure. Am J Physiol Heart Circ Physiol 2015;309:H906-H917.
46. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009;15:914-920.
47. Wolf MJ, Adili A, Piotrowitz K, Abdullah Z, Boege Y, Stemmer K, Ringelhan M, Simonavicius N, Egger M, Wohlleber D, Lorentzen A, Einer C, Schulz S, Clavel T, Protzer U, Thiele C, Zischka H, Moch H, Tschop M, Tumanov AV, Haller D, Unger K, Karin M, Kopf M, Knolle P, Weber A, Heikenwalder M. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 2014;26:549-564.
48. Revelo XS, Tsai S, Lei H, Luck H, Ghazarian M, Tsui H, Shi SY, Schroer S, Luk CT, Lin GH, Mak TW, Woo M, Winer S, Winer DA. Perforin is a novel immune regulator of obesity-related insulin resistance. Diabetes 2015;64:90-103.
49. Ding W, Li J, Singh J, Alif R, Vazquez-Padron RI, Gomes SA, Hare JM, Shehadeh LA. miR-30e targets IGF2-regulated osteogenesis in bone marrow-derived mesenchymal stem cells, aortic smooth muscle cells, and ApoE-/- mice. Cardiovasc Res 2015;106:131-142.
50. Antonopoulos AS, Margaritis M, Coutinho P, Digby J, Patel R, Psarros C, Ntusi N, Karamitsos TD, Lee R, De Silva R, Petrou M, Sayeed R, Demosthenous M, Bakogiannis C, Wordsworth PB, Tousoulis D, Neubauer S, Channon KM, Antoniades C. Reciprocal effects of systemic inflammation and brain natriuretic peptide on adiponectin biosynthesis in adipose tissue of patients with ischemic heart disease. Arterioscler Thromb Vasc Biol 2014;34:2151-2159.
51. Mallat Z, Gojova A, Brun V, Esposito B, Fournier N, Cottrez F, Tedgui A, Groux H. Induction of a regulatory T cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice. Circulation 2003;108:1232-1237.
52. Ait-Oufella H, Taleb S, Mallat Z, Tedgui A. Recent advances on the role of cytokines in atherosclerosis. Arterioscler Thromb Vasc Biol 2011;31:969-979.
53. Zuniga LA, Shen WJ, Joyce-Shaikh B, Pyatnova EA, Richards AG, Thom C, Andrade SM, Cua DJ, Kraemer FB, Butcher EC. IL-17 regulates adipogenesis, glucose homeostasis, and obesity. J Immunol 2010;185:6947-6959.
54. van Bruggen N, Ouyang WJ. Th17 cells at the crossroads of autoimmunity, inflammation, and atherosclerosis. Immunity 2014;40:10-12.
55. Emamaullee JA, Davis J, Merani S, Toso C, Elliott JF, Thiesen A, Shapiro AM. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 2009;58:1302-1311.
56. Taleb S, Romain M, Ramkhelawon B, Uyttenhove C, Pasterkamp G, Herbin O, Esposito B, Perez N, Yasukawa H, Van Snick J, Yoshimura A, Tedgui A, Mallat Z. Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J Exp Med 2009;206:2067-2077.
57. Taleb S, Tedgui A, Mallat Z. IL-17 and Th17 cells in atherosclerosis: Subtle and contextual roles. Arterioscler Thromb Vasc Biol 2015;35:258-264.
58. Wang L, Gao S, Xu W, Zhao S, Zhou J, Wang N, Yuan Z. Allergic asthma accelerates atherosclerosis dependent on Th2 and Th17 in apolipoprotein E deficient mice. J Mol Cell Cardiol 2014;72:20-27.
59. Xiong Q, Jin L, Li J, Fan H, Cao R, Wu J, Li T, Liu J. A Th2 immune shift to heat shock protein 65 fails to arrest atherosclerosis: Proatherogenic role of Th2-deviated autoantibodies. Autoimmunity 2009;42:475-483.
60. Daugherty A, Rateri DL. T lymphocytes in atherosclerosis: The yin-yang of Th1 and Th2 influence on lesion formation. Circ Res 2002;90:1039-1040.
61. Mehta P, Nuotio-Antar AM, Smith CW. gammadelta T cells promote inflammation and insulin resistance during high fat diet-induced obesity in mice. J Leukoc Biol 2015;97:121-134.
62. Caillon A, Mian MO, Fraulob-Aquino JC, Huo KG, Barhoumi T, Ouerd S, Sinnaeve PR, Paradis P, Schiffrin EL. Gamma delta T cells mediate angiotensin ii-induced hypertension and vascular injury. Circulation 2017;135:2155-2162.
63. Cheng HY, Wu R, Hedrick CC. Gammadelta (gammadelta) T lymphocytes do not impact the development of early atherosclerosis. Atherosclerosis 2014; 234:265-269.
64. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee J, Goldfine A, Benoist C, Shoelson S, Mathis D. Fat T(reg) cells: A liaison between the immune and metabolic systems. Nat Med 2009;15:930-939.
65. Qi L. Tipping the balance in metabolic regulation: Regulating regulatory T cells by costimulation. Diabetes 2014;63:1179-1181.
66. Caligiuri G, Rudling M, Ollivier V, Jacob MP, Michel JB, Hansson GK, Nicoletti A. Interleukin-10 deficiency increases atherosclerosis, thrombosis, and low-density lipoproteins in apolipoprotein E knockout mice. Mol Med 2003;9:10-17.
67. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006;12:178-180.
68. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G, Tsui H, Wu P, Davidson MG, Alonso MN, Leong HX, Glassford A, Caimol M, Kenkel JA, Tedder TF, McLaughlin T, Miklos DB, Dosch HM, Engleman EG. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011;17:610-U134.
69. Wensveen FM, Jelencic V, Valentic S, Sestan M, Wensveen TT, Theurich S, Glasner A, Mendrila D, Stimac D, Wunderlich FT, Bruning JC, Mandelboim O, Polic B. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat Immunol 2015;16:376-385.
70. Caspar-Bauguil S, Cousin B, Galinier A, Segafredo C, Nibbelink M, Andre A, Casteilla L, Penicaud L. Adipose tissues as an ancestral immune organ: Site-specific change in obesity. Febs Lett 2005;579:3487-3492.
71. Kossmann S, Schwenk M, Hausding M, Karbach SH, Schmidgen MI, Brandt M, Knorr M, Hu H, Kroller-Schon S, Schonfelder T, Grabbe S, Oelze M, Daiber A, Munzel T, Becker C, Wenzel P. Angiotensin II-induced vascular dysfunction depends on interferon-gamma-driven immune cell recruitment and mutual activation of monocytes and NK-cells. Arterioscler Thromb Vasc Biol 2013;33:1313-1319.
72. Wu L, Parekh VV, Gabriel CL, Bracy DP, Marks-Shulman PA, Tamboli RA, Kim S, Mendez-Fernandez YV, Besra GS, Lomenick JP, Williams B, Wasserman DH, Van Kaer L. Activation of invariant natural killer T cells by lipid excess promotes tissue inflammation, insulin resistance, and hepatic steatosis in obese mice. P Natl Acad Sci USA 2012;109:E1143-E1152.
73. Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A, Locksley RM. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011;332:243-247.
74. Withers SB, Forman R, Meza-Perez S, Sorobetea D, Sitnik K, Hopwood T, Lawrence CB, Agace WW, Else KJ, Heagerty AM, Svensson-Frej M, Cruickshank SM. Eosinophils are key regulators of perivascular adipose tissue and vascular functionality. Sci Rep 2017;7:44571.
75. 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.
76. Talukdar S, Oh DY, Bandyopadhyay G, Li D, Xu J, McNelis J, Lu M, Li P, Yan Q, Zhu Y, Ofrecio J, Lin M, Brenner MB, Olefsky JM. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012;18:1407-1412.
77. Scheiermann C, Frenette PS, Hidalgo A. Regulation of leucocyte homeostasis in the circulation. Cardiovasc Res 2015;107:340-351.
78. Rossaint J, Zarbock A. Platelets in leucocyte recruitment and function. Cardiovasc Res 2015;107:386-395.
79. Bornstein SR, Abu-Asab M, Glasow A, Path G, Hauner H, Tsokos M, Chrousos GP, Scherbaum WA. Immnohistochemical and ultrastructural localization of leptin and leptin receptor in human white adipose tissue and differentiating human adipose cells in primary culture. Diabetes 2000;49:532-538.
80. Gordon S. The role of the macrophage in immune regulation. Res Immunol 1998;149:685-688.
81. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K, Charo I, Leibel RL, Ferrante AW. Jr. CCR2 modulates inflammatory and metabolic effects of highfat feeding. J Clin Invest 2006;116:115-124.
82. Wentworth JM, Naselli G, Brovvn WA, Doyle L, Phipson B, Smyth GK, Wabitsch M, O'brien PE, Harrison LC. Pro-inflammatory CD11c(+)CD206(+) adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes 2010;59:1648-1656.
83. Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS. Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat dietinduced obesity in mice. Diabetes 2010;59:1171-1181.
84. Oh DY, Morinaga H, Talukdar S, Bae EJ, Olefsky JM. Increased macrophage migration into adipose tissue in obese mice. Diabetes 2012;61:346-354.
85. Weber C, Shantsila E, Hristov M, Caligiuri G, Guzik T, Heine GH, Hoefer IE, Monaco C, Peter K, Rainger E, Siegbahn A, Steffens S, Wojta J, Lip GY. Role and analysis of monocyte subsets in cardiovascular disease. Joint consensus document of the European Society of Cardiology (ESC) Working Groups "Atherosclerosis & Vascular Biology". Thromb Haemost 2016;116:626-637.
86. Eerenberg ES, Teunissen PF, van den Born BJ, Meijers JC, Hollander MR, Jansen M, Tijssen R, Belien JA, van de Ven PM, Aly MF, Kamp O, Niessen HW, Kamphuisen PW, Levi M, van Royen N. The role of ADAMTS13 in acute myocardial infarction: Cause or consequence?. Cardiovasc Res 2016;111:194-203.
87. Duca L, Blaise S, Romier B, Laffargue M, Gayral S, El Btaouri H, Kawecki C, Guillot A, Martiny L, Debelle L, Maurice P. Matrix ageing and vascular impacts: Focus on elastin fragmentation. Cardiovasc Res 2016;110:298-308.
88. Di Gregoli K, George SJ, Jackson CL, Newby AC, Johnson JL. Differential effects of tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2 on atherosclerosis and monocyte/macrophage invasion. Cardiovasc Res 2016;109:318-330.
89. De Caterina R, Madonna R. Von Willebrand factor, ADAMTS13, and coronary microvascular obstruction: Beautiful hypotheses, ugly facts. Cardiovasc Res 2016;111:169-171.
90. Ensan S, Li A, Besla R, Degousee N, Cosme J, Roufaiel M, Shikatani EA, El-Maklizi M, Williams JW, Robins L, Li C, Lewis B, Yun TJ, Lee JS, Wieghofer P, Khattar R, Farrokhi K, Byrne J, Ouzounian M, Zavitz CC, Levy GA, Bauer CM, Libby P, Husain M, Swirski FK, Cheong C, Prinz M, Hilgendorf I, Randolph GJ, Epelman S, Gramolini AO, Cybulsky MI, Rubin BB, Robbins CS. Self-renewing resident arterial macrophages arise from embryonic CX3CR1(+) precursors and circulating monocytes immediately after birth. Nat Immunol 2016;17:159-168.
91. Robbins CS, Hilgendorf I, Weber GF, Theurl I, Iwamoto Y, Figueiredo JL, Gorbatov R, Sukhova GK, Gerhardt LM, Smyth D, Zavitz CC, Shikatani EA, Parsons M, van Rooijen N, Lin HY, Husain M, Libby P, Nahrendorf M, Weissleder R, Swirski FK. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 2013;19:1166-1172.
92. Wu J, Grassia G, Cambrook H, Ialenti A, MacRitchie N, Carberry J, Wadsworth RM, Lawrence C, Kennedy S, Maffia P. Perivascular mast cells regulate vein graft neointimal formation and remodeling. PeerJ 2015;3:e1192.
93. Bot I, de Jager SC, Zernecke A, Lindstedt KA, van Berkel TJ, Weber C, Biessen EA. Perivascular mast cells promote atherogenesis and induce plaque destabilization in apolipoprotein E-deficient mice. Circulation 2007;115:2516-2525.
94. Layne K, Di Giosia P, Ferro A, Passacquale G. Anti-platelet drugs attenuate the expansion of circulating CD14highCD16+ monocytes under pro-inflammatory conditions. Cardiovasc Res 2016;111:26-33.
95. Gerhardt T, Ley K. Monocyte trafficking across the vessel wall. Cardiovasc Res 2015;107:321-330.
96. Hu D, Mohanta SK, Yin C, Peng L, Ma Z, Srikakulapu P, Grassia G, MacRitchie N, Dever G, Gordon P, Burton FL, Ialenti A, Sabir SR, McInnes IB, Brewer JM, Garside P, Weber C, Lehmann T, Teupser D, Habenicht L, Beer M, Grabner R, Maffia P, Weih F, Habenicht AJ. Artery tertiary lymphoid organs control aorta immunity and protect against atherosclerosis via vascular smooth muscle cell lymphotoxin beta receptors. Immunity 2015;42:1100-1115.
97. Akhavanpoor M, Wangler S, Gleissner CA, Korosoglou G, Katus HA, Erbel C. Adventitial inflammation and its interaction with intimal atherosclerotic lesions. Front Physiol 2014;5:296.
98. Bertola A, Ciucci T, Rousseau D, Bourlier V, Duffaut C, Bonnafous S, Blin-Wakkach C, Anty R, Iannelli A, Gugenheim J, Tran A, Bouloumie A, Gual P, Wakkach A. Identification of adipose tissue dendritic cells correlated with obesity-associated insulin-resistance and inducing Th17 responses in mice and patients. Diabetes 2012;61:2238-2247.
99. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL, Sweeney JF, Peterson LE, Chan L, Smith CW, Ballantyne CM. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 2007;115:1029-1038.
100. Han JM, Wu D, Denroche HC, Yao Y, Verchere CB, Levings MK. IL-33 reverses an obesity-induced deficit in visceral adipose tissue ST2+ T regulatory cells and ameliorates adipose tissue inflammation and insulin resistance. JI 2015;194:4777-4783.
101. Ilan Y, Maron R, Tukpah AM, Maioli TU, Murugaiyan G, Yang K, Wu HY, Weiner HL. Induction of regulatory T cells decreases adipose inflammation and alleviates insulin resistance in ob/ob mice. Proc Natl Acad Sci USA 2010;107:9765-9770.
102. Li Y, Kanellakis P, Hosseini H, Cao A, Deswaerte V, Tipping P, Toh BH, Bobik A, Kyaw T. A CD1d-dependent lipid antagonist to NKT cells ameliorates atherosclerosis in ApoE-/- mice by reducing lesion necrosis and inflammation. Cardiovasc Res 2016;109:305-317.
103. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol 2007;25:297-336.
104. Lynch L, O'shea D, Winter DC, Geoghegan J, Doherty DG, O'farrelly C. Invariant NKT cells and CD1d(+) cells amass in human omentum and are depleted in patients with cancer and obesity. Eur J Immunol 2009;39:1893-1901.
105. Vieth JA, Das J, Ranaivoson FM, Comoletti D, Denzin LK, Sant'angelo DB. TCRalpha-TCRbeta pairing controls recognition of CD1d and directs the development of adipose NKT cells. Nat Immunol 2017;18:36-44.
106. Li Y, Wu Y, Zhang C, Li P, Cui W, Hao J, Ma X, Yin Z, Du J. gammadeltaT Cellderived interleukin-17A via an interleukin-1beta-dependent mechanism mediates cardiac injury and fibrosis in hypertension. Hypertension 2014;64:305-314.
107. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 2011;17:179-188.
108. Exley MA, Hand L, O'shea D, Lynch L. Interplay between the immune system and adipose tissue in obesity. J Endocrinol 2014;223:R41-R48.
109. Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 2007;92:1023-1033.
110. McEver RP. Selectins: Initiators of leucocyte adhesion and signalling at the vascular wall. Cardiovasc Res 2015;107:331-339.
111. Kosteli A, Sugaru E, Haemmerle G, Martin JF, Lei J, Zechner R, Ferrante AW. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest 2010;120:3466-3479.
112. 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.
113. Ye JP, Gao ZG, Yin J, He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J Physiol Endocrinol Metab 2007;293:E1118-E1128.
114. O'Rourke RW, White AE, Metcalf MD, Olivas AS, Mitra P, Larison WG, Cheang EC, Varlamov O, Corless CL, Roberts CT, Marks DL. Hypoxia-induced inflammatory cytokine secretion in human adipose tissue stromovascular cells. Diabetologia 2011;54:1480-1490.
115. Amano SU, Cohen JL, Vangala P, Tencerova M, Nicoloro SM, Yawe JC, Shen YF, Czech MP, Aouadi M. Local proliferation of macrophages contributes to obesityassociated adipose tissue inflammation. Cell Metab 2014;19:162-171.
116. Zheng C, Yang Q, Cao J, Xie N, Liu K, Shou P, Qian F, Wang Y, Shi Y. Local proliferation initiates macrophage accumulation in adipose tissue during obesity. Cell Death Dis 2016;7.
117. Charriere G, Cousin B, Arnaud E, Andre M, Bacou F, Penicaud L, Casteilla L. Preadipocyte conversion to macrophage - evidence of plasticity. J Biol Chem 2003;278:9850-9855.
118. Nguyen MTA, Favelyukis S, Nguyen AK, Reichart D, Scott PA, Jenn A, Liu-Bryan R, Glass CK, Neels JG, Olefsky JM. 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.
119. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Eagle AR, Vats D, Brombacher F, Ferrante AW, Chawla A. Macrophage-specific PPAR gamma controls alternative activation and improves insulin resistance. Nature 2007;447:1116-U1112.
120. Ito A, Suganami T, Yamauchi A, Degawa-Yamauchi M, Tanaka M, Kouyama R, Kobayashi Y, Nitta N, Yasuda K, Hirata Y, Kuziel WA, Takeya M, Kanegasaki S, Kamei Y, Ogawa Y. Role of CC chemokine receptor 2 in bone marrow cells in the recruitment of macrophages into obese adipose tissue. J Biol Chem 2008;283:35715-35723.
121. Patsouris D, Li PP, Thapar D, Chapman J, Olefsky JM, Neels JG. Ablation of CD11cpositive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab 2008;8:301-309.
122. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C, Coupaye M, Pelloux V, Hugol D, Bouillot JL, Bouloumie A, Barbatelli G, Cinti S, Svensson PA, Barsh GS, Zucker JD, Basdevant A, Langin D, Clement K. 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.
123. Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes Relat Metab Disord 2008;32:451-463.
124. Monney L, Sabatos CA, Gaglia JL, Ryu A, Waldner H, Chernova T, Manning S, Greenfield EA, Coyle AJ, Sobel RA, Freeman GJ, Kuchroo VK. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 2002;415:536-541.
125. Harford KA, Reynolds CM, McGillicuddy FC, Roche HM. Fats, inflammation and insulin resistance: Insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 2011;70:408-417.
126. Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, Fischer-Posovszky P, Barth TFE, Dragun D, Skurk T, Hauner H, Bluher M, Unger T, Wolf AM, Knippschild U, Hombach V, Marx N. T-lymphocyte infiltration in visceral adipose tissue - A primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscl Throm Vas 2008;28:1304-1310.
127. Meshkani R, Vakili S. Tissue resident macrophages: Key players in the pathogenesis of type 2 diabetes and its complications. Clin Chim Acta 2016;462:77-89.
128. Shirakawa K, Yan XX, Shinmura K, Endo J, Kataoka M, Katsumata Y, Yamamoto T, Anzai A, Isobe S, Yoshida N, Itoh H, Manabe I, Sekai M, Hamazaki Y, Fukuda K, Minato N, Sano M. Obesity accelerates T cell senescence in murine visceral adipose tissue. J Clin Invest 2016;126:4626-4639.
129. Wei K, Diaz-Trelles R, Liu Q, Diez-Cunado M, Scimia MC, Cai W, Sawada J, Komatsu M, Boyle JJ, Zhou B, Ruiz-Lozano P, Mercola M. Developmental origin of age-related coronary artery disease. Cardiovasc Res 2015;107:287-294.
130. Jourdan T, Godlewski G, Cinar R, Bertola A, Szanda G, Liu J, Tam J, Han T, Mukhopadhyay B, Skarulis MC, Ju C, Aouadi M, Czech MP, Kunos G. Activation of the Nlrp3 inflammasome in infiltrating macrophages by endocannabinoids mediates beta cell loss in type 2 diabetes. Nat Med 2013;19:1132-1140.
131. DeFuria J, Belkina AC, Jagannathan-Bogdan M, Snyder-Cappione J, Carr JD, Nersesova YR, Markham D, Strissel KJ, Watkins AA, Zhu M, Allen J, Bouchard J, Toraldo G, Jasuja R, Obin MS, McDonnell ME, Apovian C, Denis GV, Nikolajczyk BS. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. P Natl Acad Sci USA 2013;110:5133-5138.
132. Molofsky AB, Nussbaum JC, Liang HE, Van Dyken SJ, Cheng LE, Mohapatra A, Chawla A, Locksley RM. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med 2013;210:535-549.
133. Lynch L, Nowak M, Varghese B, Clark J, Hogan AE, Toxavidis V, Balk SP, O'shea D, O'farrelly C, Exley MA. Adipose tissue invariant NKT cells protect against dietinduced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012;37:574-587.
134. Youn JY, Siu KL, Lob HE, Itani H, Harrison DG, Cai H. Role of vascular oxidative stress in obesity and metabolic syndrome. Diabetes 2014;63:2344-2355.
135. Guzik TJ, Olszanecki R, Sadowski J, Kapelak B, Rudzinski P, Jopek A, Kawczynska A, Ryszawa N, Loster J, Jawien J, Czesnikiewicz-Guzik M, Channon KM, Korbut R. Superoxide dismutase activity and expression in human venous and arterial bypass graft vessels. J Physiol Pharmacol 2005;56:313-323.
136. Xia C, Rao X, Zhong J. Role of T lymphocytes in type 2 diabetes and diabetesassociated inflammation. J Diabetes Res 2017;2017:6.
137. Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, Sai Y, Takamura T, Yamamoto H, Miyamoto K, Ginsberg HN, Mukaida N, Kaneko S, Ota T. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 2012;61:1680-1690.
138. McLaughlin T, Liu LF, Lamendola C, Shen L, Morton J, Rivas H, Winer D, Tolentino L, Choi O, Zhang H, Chng MHY, Engleman E. T-cell profile in adipose tissue is associated with insulin resistance and systemic inflammation in humans. Arterioscl Throm Vas 2014;34:2637-2643.
139. Seijkens T, Kusters P, Engel D, Lutgens E. CD40-CD40L: Linking pancreatic, adipose tissue and vascular inflammation in type 2 diabetes and its complications. Diabetes Vasc Dis Re 2013;10:115-122.
140. Poggi M, Engel D, Christ A, Beckers L, Wijnands E, Boon L, Driessen A, Cleutjens J, Weber C, Gerdes N, Lutgens E. CD40L deficiency ameliorates adipose tissue inflammation and metabolic manifestations of obesity in mice. Arterioscl Throm Vas 2011;31:2251-U2248.
141. Donath MY. Targeting inflammation in the treatment of type 2 diabetes: Time to start. Nat Rev Drug Discov 2014;13:465-476.
142. Poggi M, Jager J, Paulmyer-Lacroix O, Peiretti F, Gremeaux T, Verdier M, Grino M, Stepanian A, Msika S, Burcelin R, de Prost D, Tanti JF, Alessi MC. The inflammatory receptor CD40 is expressed on human adipocytes: Contribution to crosstalk between lymphocytes and adipocytes. Diabetologia 2009;52:1152-1163.
143. Missiou A, Wolf D, Platzer I, Ernst S, Walter C, Rudolf P, Zirlik K, Kostlin N, Willecke FK, Munkel C, Schonbeck U, Libby P, Bode C, Varo N, Zirlik A. CD40L induces inflammation and adipogenesis in adipose cells - A potential link between metabolic and cardiovascular disease. Thromb Haemost 2010;103:788-796.
144. de Hoog VC, Bovens SM, de Jager SC, van Middelaar BJ, van Duijvenvoorde A, Doevendans PA, Pasterkamp G, de Kleijn DP, Timmers L. BLT1 antagonist LSN2792613 reduces infarct size in a mouse model of myocardial ischaemiareperfusion injury. Cardiovasc Res 2015;108:367-376.
145. Harrison DG, Guzik TJ, Lob HE, Madhur MS, Marvar PJ, Thabet SR, Vinh A, Weyand CM. Inflammation, immunity, and hypertension. Hypertension 2011;57:132-140.
146. Itani HA, McMaster WG, Jr., Saleh MA, Nazarewicz RR, Mikolajczyk TP, Kaszuba AM, Konior A, Prejbisz A, Januszewicz A, Norlander AE, Chen W, Bonami RH, Marshall AF, Poffenberger G, Weyand CM, Madhur MS, Moore DJ, Harrison DG, Guzik TJ. Activation of human T cells in hypertension: Studies of humanized mice and hypertensive humans. Hypertension 2016;68:123-132.
147. Guzik TJ, Mikolajczyk T. In search of the T cell involved in hypertension and target organ damage. Hypertension 2014;64:224-226.
148. Carnevale D, Pallante F, Fardella V, Fardella S, Iacobucci R, Federici M, Cifelli G, De Lucia M, Lembo G. The angiogenic factor PlGF mediates a neuroimmune interaction in the spleen to allow the onset of hypertension. Immunity 2014; 41:737-752.
149. Marvar PJ, Thabet SR, Guzik TJ, Lob HE, McCann LA, Weyand C, Gordon FJ, Harrison DG. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res 2010;107:263-270.
150. Wilk G, Osmenda G, Matusik P, Nowakowski D, Jasiewicz-Honkisz B, Ignacak A, Czesnikiewicz-Guzik M, Guzik TJ. Endothelial function assessment in atherosclerosis: Comparison of brachial artery flow-mediated vasodilation and peripheral arterial tonometry. Pol Arch Med Wewn 2013;123:443-452.
151. Nus M, Martinez-Poveda B, MacGrogan D, Chevre R, Amato G, Sbroggio M, Rodriguez C, Martinez-Gonzalez J, Andres V, Hidalgo A, Luis de la Pompa J. Endothelial Jag1-RBPJ signalling promotes inflammatory leucocyte recruitment and atherosclerosis. Cardiovasc Res 2016;112:568-580.
152. Minami T, Satoh K, Nogi M, Kudo S, Miyata S, Tanaka S, Shimokawa H. Statins upregulate SmgGDS through beta1-integrin/Akt1 pathway in endothelial cells. Cardiovasc Res 2016;109:151-161.
153. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 2007;204:2449-2460.
154. West NEJ, Qian HS, Guzik TJ, Black E, Cai S, George SE, Channon KM. Nitric oxide synthase (nNOS) gene transfer modifies venous bypass graft remodeling: Effects on vascular smooth muscle cell differentiation and superoxide production. Circulation 2001;104:1526-1532.
155. Madhur MS, Lob HE, McCann LA, Iwakura Y, Blinder Y, Guzik TJ, Harrison DG. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 2010;55:500-507.
156. Wu J, Thabet SR, Kirabo A, Trott DW, Saleh MA, Xiao L, Madhur MS, Chen W, Harrison DG. Inflammation and mechanical stretch promote aortic stiffening in hypertension through activation of p38 mitogen-activated protein kinase. Circ Res 2014;114:616-625.
157. Matrougui K, Zakaria AE, Kassan M, Choi S, Nair D, Gonzalez-Villalobos RA, Chentoufi AA, Kadowitz P, Belmadani S, Partyka M. Natural regulatory T cells control coronary arteriolar endothelial dysfunction in hypertensive mice. Am J Pathol 2011;178:434-441.
158. Barhoumi T, Kasal DA, Li MW, Shbat L, Laurant P, Neves MF, Paradis P, Schiffrin EL. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 2011;57:469-476.
159. Chan CT, Sobey CG, Lieu M, Ferens D, Kett MM, Diep H, Kim HA, Krishnan SM, Lewis CV, Salimova E, Tipping P, Vinh A, Samuel CS, Peter K, Guzik TJ, Kyaw TS, Toh BH, Bobik A, Drummond GR. Obligatory role for B cells in the development of angiotensin II-dependent hypertension. Hypertension 2015;66:1023-1033.
160. Chan CT, Moore JP, Budzyn K, Guida E, Diep H, Vinh A, Jones ES, Widdop RE, Armitage JA, Sakkal S, Ricardo SD, Sobey CG, Drummond GR. Reversal of vascular macrophage accumulation and hypertension by a CCR2 antagonist in deoxycorticosterone/salt-treated mice. Hypertension 2012;60:1207-1212.
161. Saleh MA, McMaster WG, Wu J, Norlander AE, Funt SA, Thabet SR, Kirabo A, Xiao L, Chen W, Itani HA, Michell D, Huan TX, Zhang YH, Takaki S, Titze J, Levy D, Harrison DG, Madhur MS. Lymphocyte adaptor protein LNK deficiency exacerbates hypertension and end-organ inflammation. J Clin Invest 2015;125:1189-1202.
162. Kirabo A, Fontana V, de Faria APC, Loperena R, Galindo CL, Wu J, Bikineyeva AT, Dikalov S, Xiao L, Chen W, Saleh MA, Trott DW, Itani HA, Vinh A, Amarnath V, Amarnath K, Guzik TJ, Bernstein KE, Shen XZ, Shyr Y, Chen SC, Mernaugh RL, Laffer CL, Elijovich F, Davies SS, Moreno LH, Madhur MS, Roberts J, Harrison DG. DC isoketal-modified proteins activate T cells and promote hypertension. J Clin Invest 2014;124:4642-4656.
163. Vinh A, Chen W, Blinder Y, Weiss D, Taylor WR, Goronzy JJ, Weyand CM, Harrison DG, Guzik TJ. Inhibition and genetic ablation of the B7/CD28 T-cell costimulation axis prevents experimental hypertension. Circulation 2010;122:2529-2537.
164. Lumeng CN, Deyoung SM, Saltiel AR. Macrophages block insulin action in adipocytes by altering expression of signaling and glucose transport proteins. Am J Physiol Endocrinol Metab 2007;292:E166-E174.
165. Pietrowski E, Bender B, Huppert J, White R, Luhmann HJ, Kuhlmann CR. Pro-inflammatory effects of interleukin-17A on vascular smooth muscle cells involve NAD(P)H- oxidase derived reactive oxygen species. J Vasc Res 2011;48:52-58.
166. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-238.
167. Roussel L, Houle F, Chan C, Yao Y, Berube J, Olivenstein R, Martin JG, Huot J, Hamid Q, Ferri L, Rousseau S. IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation. J Immunol 2010;184:4531-4537.
168. Nguyen H, Chiasson VL, Chatterjee P, Kopriva SE, Young KJ, Mitchell BM. Interleukin-17 causes Rho-kinase-mediated endothelial dysfunction and hypertension. Cardiovasc Res 2013;97:696-704.
169. Nosalski R, McGinnigle E, Siedlinski M, Guzik TJ. Novel immune mechanisms in hypertension and cardiovascular risk. Curr Cardiovasc Risk Rep 2017;11:12.
170. Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, Furuyama N, Kondo H, Takahashi M, Arita Y, Komuro R, Ouchi N, Kihara S, Tochino Y, Okutomi K, Horie M, Takeda S, Aoyama T, Funahashi T, Matsuzawa Y. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med 2002;8:731-737.
171. Fasshauer M, Kralisch S, Klier M, Lossner U, Bluher M, Klein J, Paschke R. Adiponectin gene expression and secretion is inhibited by interleukin-6 in 3T3-L1 adipocytes. Biochem Biophys Res Commun 2003;301:1045-1050.
172. Noh M. Interleukin-17A increases leptin production in human bone marrow mesenchymal stem cells. Biochem Pharmacol 2012;83:661-670.
173. La Cava A, Matarese G. The weight of leptin in immunity. Nat Rev Immunol 2004;4:371-379.
174. Bokarewa M, Nagaev I, Dahlberg L, Smith U, Tarkowski A. Resistin, an adipokine with potent proinflammatory properties. J Immunol 2005;174:5789-5795.
175. Spiroglou SG, Kostopoulos CG, Varakis JN, Papadaki HH. Adipokines in periaortic and epicardial adipose tissue: Differential expression and relation to atherosclerosis. JAT 2010;17:115-130.
176. Durpes MC, Morin C, Paquin-Veillet J, Beland R, Pare M, Guimond MO, Rekhter M, King GL, Geraldes P. PKC-beta activation inhibits IL-18-binding protein causing endothelial dysfunction and diabetic atherosclerosis. Cardiovasc Res 2015;106:303-313.
177. Planavila A, Redondo-Angulo I, Ribas F, Garrabou G, Casademont J, Giralt M, Villarroya F. Fibroblast growth factor 21 protects the heart from oxidative stress. Cardiovasc Res 2015;106:19-31.
178. Podolec J, Kopec G, Niewiara L, Komar M, Guzik B, Bartus K, Tomkiewicz-Pajak L, Guzik TJ, Plazak W, Zmudka K. Chemokine RANTES is increased at early stages of coronary artery disease. J Physiol Pharmacol 2016;67:321-328.
179. Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J Exp Med 2006;203:1273-1282.
180. Moos MPW, John N, Grabner R, Nossmann S, Gunther B, Vollandt D, Funk CD, Kaiser B, Habenicht AJR. The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005;25:2386-2391.
181. Lohmann C, Schafer N, von Lukowicz T, Stein MAS, Boren J, Rutti S, Wahli W, Donath MY, Luscher TF, Matter CM. Atherosclerotic mice exhibit systemic inflammation in periadventitial and visceral adipose tissue, liver, and pancreatic islets. Atherosclerosis 2009;207:360-367.
182. Ketelhuth DF, Hansson GK. Adaptive response of T and B cells in atherosclerosis. Circ Res 2016;118:668-678.
183. Henrichot E, Juge-Aubry CE, Pernin AS, Pache JC, Velebit V, Dayer JM, Meda P, Chizzolini C, Meier CA. Production of chemokines by perivascular adipose tissue - A role in the pathogenesis of atherosclerosis?. Arterioscl Throm Vas 2005;25:2594-2599.
184. Smith E, Prasad KM, Butcher M, Dobrian A, Kolls JK, Ley K, Galkina E. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation 2010;121:1746-1755.
185. Dobrian AD, Hatcher MA, Brotman JJ, Galkina EV, Taghavie-Moghadam P, Pei H, Haynes BA, Nadler JL. STAT4 contributes to adipose tissue inflammation and atherosclerosis. J Endocrinol 2015;227:13-24.
186. Foks AC, Van Puijvelde GH, Wolbert J, Kroner MJ, Frodermann V, Van Der Heijden T, Van Santbrink PJ, Boon L, Bot I, Kuiper J. CD11b+Gr-1+ myeloid-derived suppressor cells reduce atherosclerotic lesion development in LDLr deficient mice. Cardiovasc Res 2016;111:252-261.
187. Tay C, Liu YH, Hosseini H, Kanellakis P, Cao A, Peter K, Tipping P, Bobik A, Toh BH, Kyaw T. B-cell-specific depletion of tumour necrosis factor alpha inhibits atherosclerosis development and plaque vulnerability to rupture by reducing cell death and inflammation. Cardiovasc Res 2016;111:385-397.
188. Nus M, Mallat Z. Immune-mediated mechanisms of atherosclerosis and implications for the clinic. Expert Rev Clin Immunol 2016;12:1217-1237.
189. Malkic Salihbegovic E, Hadzigrahic N, Cickusic AJ. Psoriasis and metabolic syndrome. Med Arh 2015;69:85-87.
190. Hjuler KF, Gormsen LC, Vendelbo MH, Egeberg A, Nielsen J, Iversen L. Increased global arterial and subcutaneous adipose tissue inflammation in patients with moderate-to-severe psoriasis. Br J Dermatol 2017;176:732-740.
191. Kontny E, Prochorec-Sobieszek M. Articular adipose tissue resident macrophages in rheumatoid arthritis patients: Potential contribution to local abnormalities. Rheumatology (Oxford) 2013;52:2158-2167.
192. Procaccini C, Carbone F, Galgani M, La Rocca C, De Rosa V, Cassano S, Matarese G. Obesity and susceptibility to autoimmune diseases. Expert Rev Clin Immunol 2011;7:287-294.
193. Graner M, Nyman K, Siren R, Pentikainen MO, Lundbom J, Hakkarainen A, Lauerma K, Lundbom N, Nieminen MS, Taskinen MR. Ectopic fat depots and left ventricular function in nondiabetic men with nonalcoholic fatty liver disease. Circ Cardiovasc Imaging 2015;8:e001979.
194. He Q, Li F, Li J, Li R, Zhan G, Li G, Du W, Tan H. MicroRNA-26a-interleukin (IL)-6-IL-17 axis regulates the development of non-alcoholic fatty liver disease in a murine model. Clin Exp Immunol 2017;187:174-184.
195. Crippa S, Nemir M, Ounzain S, Ibberson M, Berthonneche C, Sarre A, Boisset G, Maison D, Harshman K, Xenarios I, Diviani D, Schorderet D, Pedrazzini T. Comparative transcriptome profiling of the injured zebrafish and mouse hearts identifies miRNA-dependent repair pathways. Cardiovasc Res 2016;110:73-84.
196. Vacca M, Di Eusanio M, Cariello M, Graziano G, D'amore S, Petridis FD, D'orazio A, Salvatore L, Tamburro A, Folesani G, Rutigliano D, Pellegrini F, Sabba C, Palasciano G, Di Bartolomeo R, Moschetta A. Integrative miRNA and wholegenome analyses of epicardial adipose tissue in patients with coronary atherosclerosis. Cardiovasc Res 2016;109:228-239.
197. Iaconetti C, De Rosa S, Polimeni A, Sorrentino S, Gareri C, Carino A, Sabatino J, Colangelo M, Curcio A, Indolfi C. Down-regulation of miR-23b induces phenotypic switching of vascular smooth muscle cells in vitro and in vivo. Cardiovasc Res 2015;107:522-533.
198. Hu W, Wang M, Yin H, Yao C, He Q, Yin L, Zhang C, Li W, Chang G, Wang S. MicroRNA-1298 is regulated by DNA methylation and affects vascular smooth muscle cell function by targeting connexin 43. Cardiovasc Res 2015;107:534-545.
199. Duygu B, Da Costa Martins PA. miR-21: A star player in cardiac hypertrophy. Cardiovasc Res 2015;105:235-237.
200. Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, Sarov-Blat L, O'brien S, Keiper EA, Johnson AG, Martin J, Goldstein BJ, Shi Y. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 2003;108:2460-2466.
201. Gaborit B, Venteclef N, Ancel P, Pelloux V, Gariboldi V, Leprince P, Amour J, Hatem SN, Jouve E, Dutour A, Clement K. Human epicardial adipose tissue has a specific transcriptomic signature depending on its anatomical peri-atrial, peri-ventricular, or peri-coronary location. Cardiovasc Res 2015;108:62-73.
202. Baragetti A, Pisano G, Bertelli C, Garlaschelli K, Grigore L, Fracanzani AL, Fargion S, Norata GD, Catapano AL. Subclinical atherosclerosis is associated with epicardial fat thickness and hepatic steatosis in the general population. Nutr Metab Cardiovasc Dis 2016;26:141-153.
203. Harman-Boehm I, Bluher M, Redel H, Sion-Vardy N, Ovadia S, Avinoach E, Shai I, Kloting N, Stumvoll M, Bashan N, Rudich A. Macrophage infiltration into omental versus subcutaneous fat across different populations: Effect of regional adiposity and the comorbidities of obesity. J Clin Endocrinol Metab 2007;92:2240-2247.
204. Zeyda M, Farmer D, Todoric J, Aszmann O, Speiser M, Gyori G, Zlabinger GJ, Stulnig TM. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int J Obes Relat Metab Disord 2007;31:1420-1428.
205. Antonopoulos AS, Margaritis M, Coutinho P, Shirodaria C, Psarros C, Herdman L, Sanna F, De Silva R, Petrou M, Sayeed R, Krasopoulos G, Lee R, Digby J, Reilly S, Bakogiannis C, Tousoulis D, Kessler B, Casadei B, Channon KM, Antoniades C. Adiponectin as a link between type 2 diabetes and vascular NADPH oxidase activity in the human arterial wall: The regulatory role of perivascular adipose tissue. Diabetes 2015;64:2207-2219.
206. Antonopoulos AS, Margaritis M, Verheule S, Recalde A, Sanna F, Herdman L, Psarros C, Nasrallah H, Coutinho P, Akoumianakis I, Brewer AC, Sayeed R, Krasopoulos G, Petrou M, Tarun A, Tousoulis D, Shah AM, Casadei B, Channon KM, Antoniades C. Mutual regulation of epicardial adipose tissue and myocardial redox state by PPAR-gamma/adiponectin signalling. Circ Res 2016;118:842-855.
207. Larsen CM, Faulenbach M, Vaag A, Ehses JA, Donath MY, Mandrup-Poulsen T. Sustained effects of interleukin-1 receptor antagonist treatment in type 2 diabetes. Diabetes Care 2009;32:1663-1668.
208. Cavelti-Weder C, Babians-Brunner A, Keller C, Stahel MA, Kurz-Levin M, Zayed H, Solinger AM, Mandrup-Poulsen T, Dinarello CA, Donath MY. Effects of gevokizumab on glycemia and inflammatory markers in type 2 diabetes. Diabetes Care 2012;35:1654-1662.
209. Hensen J, Howard CP, Walter V, Thuren T. Impact of interleukin-1 beta antibody (canakinumab) on glycaemic indicators in patients with type 2 diabetes mellitus: Results of secondary endpoints from a randomized, placebo-controlled trial. Diabetes Metab 2013;39:524-531.
210. Sloan-Lancaster J, Abu-Raddad E, Polzer J, Miller JW, Scherer JC, De Gaetano A, Berg JK, Landschulz WH. Double-blind, randomized study evaluating the glycemic and anti-inflammatory effects of subcutaneous LY2189102, a neutralizing IL-1 beta antibody, in patients with type 2 diabetes. Diabetes Care 2013; 36:2239-2246.
211. Ofei F, Hurel S, Newkirk J, Sopwith M, Taylor R. Effects of an engineered human anti-TNF-alpha antibody (CDP571) on insulin sensitivity and glycemic control in patients with NIDDM. Diabetes 1996;45:881-885.
212. Paquot N, Castillo MJ, Lefebvre PJ, Scheen AJ. No increased insulin sensitivity after a single intravenous administration of a recombinant human tumor necrosis factor receptor: Fc fusion protein in obese insulin-resistant patients. J Clin Endocrinol Metab 2000;85:1316-1319.
213. Dominguez H, Storgaard H, Rask-Madsen C, Hermann TS, Ihlemann N, Nielsen DB, Spohr C, Kober L, Vaag A, Torp-Pedersen C. Metabolic and vascular effects of tumor necrosis factor-alpha blockade with etanercept in obese patients with type 2 diabetes. J Vasc Res 2005;42:517-525.
214. Goldfine AB, Fonseca V, Jablonski KA, Chen YDI, Tipton L, Staten MA, Shoelson SE, Salsa TIU. Salicylate (Salsalate) in patients with type 2 diabetes. Ann Intern Med 2013;159:1.
215. Passacquale G, Di Giosia P, Ferro A. The role of inflammatory biomarkers in developing targeted cardiovascular therapies: Lessons from the cardiovascular inflammation reduction trials. Cardiovasc Res 2016;109:9-23.
216. Lewis DR, Petersen LK, York AW, Ahuja S, Chae H, Joseph LB, Rahimi S, Uhrich KE, Haser PB, Moghe PV. Nanotherapeutics for inhibition of atherogenesis and modulation of inflammation in atherosclerotic plaques. Cardiovasc Res 2016;109:283-293.
217. Giles JT, Ferrante AW, Broderick R, Zartoshti A, Rose J, Downer K, Zhang HZ, Winchester RJ. Adipose tissue macrophages in rheumatoid arthritis: Prevalence, disease related indicators, and associations with cardiometabolic risk factors. Arthritis Care Res (Hoboken) 2017; doi: 10.1002/acr.23253.