Epicardial perivascular adipose tissue as a therapeutic target in obesity-related coronary artery disease

British Journal of Pharmacology

Volumn 165, Issue 3, 2012, Pages 659-669

  Payne, Gregory A ^a   Kohr, Meredith C ^a   Tune, Johnathan D ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

adipokines; adiponectin; coronary artery disease; coronary circulation; endothelial dysfunction; epicardial adipose tissue; inflammation; leptin; obesity; perivascular adipose tissue

Indexed keywords

ADIPONECTIN; ADRENOMEDULLIN; CHEMERIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR ALPHA; INTERLEUKIN 13; INTERLEUKIN 16; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEPTIN; MACROPHAGE MIGRATION INHIBITION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; NATRIURETIC PEPTIDE RECEPTOR C; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; RANTES; RESISTIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ADIPOSE TISSUE; ATHEROSCLEROSIS; BLOOD VESSEL REACTIVITY; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; EPICARDIAL PERIVASCULAR ADIPOSE TISSUE; HUMAN; INFLAMMATION; METABOLIC SYNDROME X; NONHUMAN; OBESITY; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; VASOCONSTRICTION;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; CORONARY ARTERY DISEASE; ENDOTHELIUM, VASCULAR; HUMANS; OBESITY;

EID: 84855682678     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01370.x     Document Type: Review

References (115)

1. Baker AR, Silva NF, Quinn DW, Harte AL, Pagano D, Bonser RS, et al,. (2006). Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc Diabetol 5: 1.
2. Barandier C, Montani JP, Yang Z, (2005). Mature adipocytes and perivascular adipose tissue stimulate vascular smooth muscle cell proliferation: effects of aging and obesity. Am J Physiol Heart Circ Physiol 289: H1807-H1813. (Pubitemid 41507326)
3. Beltowski J, Wojcicka G, Marciniak A, Jamroz A, (2004). Oxidative stress, nitric oxide production, and renal sodium handling in leptin-induced hypertension. Life Sci 74: 2987-3000. (Pubitemid 38402295)
4. Beltowski J, Jamroz-Wisniewska A, Widomska S, (2008). Adiponectin and its role in cardiovascular diseases. Cardiovasc Hematol Disord Drug Targets 8: 7-46.
5. Bohlen HG, (2004). Protein kinase betaII in Zucker obese rats compromises oxygen and flow-mediated regulation of nitric oxide formation. Am J Physiol Heart Circ Physiol 286: H492-H497. (Pubitemid 38140328)
6. Bouloumie A, Marumo T, Lafontan M, Busse R, (1999). Leptin induces oxidative stress in human endothelial cells. FASEB J 13: 1231-1238. (Pubitemid 29300368)
7. Bunker AK, Laughlin MH, (2010). Influence of exercise and perivascular adipose tissue on coronary artery vasomotor function in a familial hypercholesterolemic porcine atherosclerosis model. J Appl Physiol 108: 490-497.
8. Casellini CM, Barlow PM, Rice AL, Casey M, Simmons K, Pittenger G, et al,. (2007). A 6-month, randomized, double-masked, placebo-controlled study evaluating the effects of the protein kinase C-beta inhibitor ruboxistaurin on skin microvascular blood flow and other measures of diabetic peripheral neuropathy. Diabetes Care 30: 896-902. (Pubitemid 46556584)
9. Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G, et al,. (2009). Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding. Circ Res 104: 541-549.
10. Chen H, Montagnani M, Funahashi T, Shimomura I, Quon MJ, (2003). Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem 278: 45021-45026. (Pubitemid 37377262)
11. Cheng KH, Chu CS, Lee KT, Lin TH, Hsieh CC, Chiu CC, et al,. (2008). Adipocytokines and proinflammatory mediators from abdominal and epicardial adipose tissue in patients with coronary artery disease. Int J Obes (Lond) 32: 268-274.
12. Clement K, Basdevant A, Dutour A, (2009). Weight of pericardial fat on coronaropathy. Arterioscler Thromb Vasc Biol 29: 615-616.
13. Company JM, Booth FW, Laughlin MH, Arce-Esquivel AA, Sacks HS, Bahouth SW, et al,. (2010). Epicardial fat gene expression after aerobic exercise training in pigs with coronary atherosclerosis: relationship to visceral and subcutaneous fat. J Appl Physiol 109: 1904-1912.
14. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al,. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3: 301-313.
15. Deng G, Long Y, Yu YR, Li MR, (2010). Adiponectin directly improves endothelial dysfunction in obese rats through the AMPK-eNOS Pathway. Int J Obes (Lond) 34: 165-171.
16. Dick GM, Katz PS, Farias M, III, Morris M, James J, Knudson JD, et al,. (2006). Resistin impairs endothelium-dependent dilation to bradykinin, but not acetylcholine, in the coronary circulation. Am J Physiol Heart Circ Physiol 291: H2997-H3002. (Pubitemid 44904101)
17. Ding J, Hsu FC, Harris TB, Liu Y, Kritchevsky SB, Szklo M, et al,. (2009). The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Clin Nutr 90: 499-504.
18. Dubrovska G, Verlohren S, Luft FC, Gollasch M, (2004). Mechanisms of ADRF release from rat aortic adventitial adipose tissue. Am J Physiol Heart Circ Physiol 286: H1107-H1113. (Pubitemid 38248627)
19. Dutour A, Achard V, Sell H, Naour N, Collart F, Gaborit B, et al,. (2010). Secretory type II phospholipase A2 is produced and secreted by epicardial adipose tissue and overexpressed in patients with coronary artery disease. J Clin Endocrinol Metab 95: 963-967.
20. Eiras S, Teijeira-Fernandez E, Shamagian LG, Fernandez AL, Vazquez-Boquete A, Gonzalez-Juanatey JR, (2008). Extension of coronary artery disease is associated with increased IL-6 and decreased adiponectin gene expression in epicardial adipose tissue. Cytokine 43: 174-180.
21. Galili O, Versari D, Sattler KJ, Olson ML, Mannheim D, McConnell JP, et al,. (2007). Early experimental obesity is associated with coronary endothelial dysfunction and oxidative stress. Am J Physiol Heart Circ Physiol 292: H904-H911.
22. Galvez B, de Castro J, Herold D, Dubrovska G, Arribas S, Gonzalez MC, et al,. (2006). Perivascular adipose tissue and mesenteric vascular function in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 26: 1297-1302. (Pubitemid 44305373)
23. Gao YJ, Zeng ZH, Teoh K, Sharma AM, Abouzahr L, Cybulsky I, et al,. (2005). Perivascular adipose tissue modulates vascular function in the human internal thoracic artery. J Thorac Cardiovasc Surg 130: 1130-1136. (Pubitemid 41427351)
24. Gao YJ, Takemori K, Su LY, An WS, Lu C, Sharma AM, et al,. (2006). Perivascular adipose tissue promotes vasoconstriction: the role of superoxide anion. Cardiovasc Res 71: 363-373.
25. Gao YJ, Lu C, Su LY, Sharma AM, Lee RM, (2007). Modulation of vascular function by perivascular adipose tissue: the role of endothelium and hydrogen peroxide. Br J Pharmacol 151: 323-331. (Pubitemid 46842669)
26. Gnacinska M, Malgorzewicz S, Lysiak-Szydlowska W, Sworczak K, (2010). The serum profile of adipokines in overweight patients with metabolic syndrome. Endokrynol Pol 61: 36-41.
27. Gollasch M, Dubrovska G, (2004). Paracrine role for periadventitial adipose tissue in the regulation of arterial tone. Trends Pharmacol Sci 25: 647-653. (Pubitemid 39458171)
28. Goralski KB, McCarthy TC, Hanniman EA, Zabel BA, Butcher EC, Parlee SD, et al,. (2007). Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J Biol Chem 282: 28175-28188. (Pubitemid 47529521)
29. Gorter PM, van Lindert AS, de Vos AM, Meijs MF, van der GY, Doevendans PA, et al,. (2008). Quantification of epicardial and peri-coronary fat using cardiac computed tomography; reproducibility and relation with obesity and metabolic syndrome in patients suspected of coronary artery disease. Atherosclerosis 197: 896-903. (Pubitemid 351417890)
30. Gossl M, Versari D, Mannheim D, Ritman EL, Lerman LO, Lerman A, (2007). Increased spatial vasa vasorum density in the proximal LAD in hypercholesterolemia-implications for vulnerable plaque-development. Atherosclerosis 192: 246-252. (Pubitemid 46726324)
31. Greenstein AS, Khavandi K, Withers SB, Sonoyama K, Clancy O, Jeziorska M, et al,. (2009). Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 119: 1661-1670.
32. Greif M, Becker A, von ZF, Lebherz C, Lehrke M, Broedl UC, et al,. (2009). Pericardial adipose tissue determined by dual source CT is a risk factor for coronary atherosclerosis. Arterioscler Thromb Vasc Biol 29: 781-786.
33. Gruen ML, Hao M, Piston DW, Hasty AH, (2007). Leptin requires canonical migratory signaling pathways for induction of monocyte and macrophage chemotaxis. Am J Physiol Cell Physiol 293: C1481-C1488. (Pubitemid 350085627)
34. Hergenc G, Schulte H, Assmann G, von EA, (1999). Associations of obesity markers, insulin, and sex hormones with HDL-cholesterol levels in Turkish and German individuals. Atherosclerosis 145: 147-156. (Pubitemid 29292710)
35. Herrmann J, Lerman LO, Rodriguez-Porcel M, Holmes DR, Jr, Richardson DM, Ritman EL, et al,. (2001). Coronary vasa vasorum neovascularization precedes epicardial endothelial dysfunction in experimental hypercholesterolemia. Cardiovasc Res 51: 762-766. (Pubitemid 32800717)
36. Huang F, Lezama MA, Ontiveros JA, Bravo G, Villafana S, del-Rio-Navarro BE, et al,. (2010). Effect of losartan on vascular function in fructose-fed rats: the role of perivascular adipose tissue. Clin Exp Hypertens 32: 98-104.
37. Iacobellis G, Sharma AM, (2007). Epicardial adipose tissue as new cardio-metabolic risk marker and potential therapeutic target in the metabolic syndrome. Curr Pharm Des 13: 2180-2184. (Pubitemid 47074050)
38. Iacobellis G, Pistilli D, Gucciardo M, Leonetti F, Miraldi F, Brancaccio G, et al,. (2005). Adiponectin expression in human epicardial adipose tissue in vivo is lower in patients with coronary artery disease. Cytokine 29: 251-255. (Pubitemid 40320925)
39. Iacobellis G, di Gioia CR, Di VM, Petramala L, Cotesta D, De S, et al,. (2009). Epicardial adipose tissue and intracoronary adrenomedullin levels in coronary artery disease. Horm Metab Res 41: 855-860.
40. Ishii T, Asuwa N, Masuda S, Ishikawa Y, (1998). The effects of a myocardial bridge on coronary atherosclerosis and ischaemia. J Pathol 185: 4-9. (Pubitemid 28266710)
41. Ishikawa Y, Ishii T, Asuwa N, Masuda S, (1997). Absence of atherosclerosis evolution in the coronary arterial segment covered by myocardial tissue in cholesterol-fed rabbits. Virchows Arch 430: 163-171. (Pubitemid 27121116)
42. Juge-Aubry CE, Henrichot E, Meier CA, (2005). Adipose tissue: a regulator of inflammation. Best Pract Res Clin Endocrinol Metab 19: 547-566. (Pubitemid 41823815)
43. Karastergiou K, Evans I, Ogston N, Miheisi N, Nair D, Kaski JC, et al,. (2010). Epicardial adipokines in obesity and coronary artery disease induce atherogenic changes in monocytes and endothelial cells. Arterioscler Thromb Vasc Biol 30: 1340-1346.
44. Kazumi T, Kawaguchi A, Hirano T, Yoshino G, (2003). C-reactive protein in young, apparently healthy men: associations with serum leptin, QTc interval, and high-density lipoprotein-cholesterol. Metabolism 52: 1113-1116. (Pubitemid 37203483)
45. Ketonen J, Shi J, Martonen E, Mervaala E, (2010). Periadventitial adipose tissue promotes endothelial dysfunction via oxidative stress in diet-induced obese C57Bl/6 mice. Circ J 74: 1479-1487.
46. Kimura K, Tsuda K, Baba A, Kawabe T, Boh-oka S, Ibata M, et al,. (2000). Involvement of nitric oxide in endothelium-dependent arterial relaxation by leptin. Biochem Biophys Res Commun 273: 745-749. (Pubitemid 30599054)
47. Knudson JD, Dincer UD, Zhang C, Swafford, AN, Jr, Koshida R, Picchi A, et al,. (2005). Leptin receptors are expressed in coronary arteries and hyperleptinemia causes significant coronary endothelial dysfunction. Am J Physiol Heart Circ Physiol 289: H48-H56. (Pubitemid 40934081)
48. Knudson JD, Dincer UD, Bratz IN, Sturek M, Dick GM, Tune JD, (2007). Mechanisms of coronary dysfunction in obesity and insulin resistance. Microcirculation 14: 317-338. (Pubitemid 47050025)
49. Knudson JD, Payne GA, Borbouse L, Tune JD, (2008). Leptin and mechanisms of endothelial dysfunction and cardiovascular disease. Curr Hypertens Rep 10: 434-439.
50. Korda M, Kubant R, Patton S, Malinski T, (2008). Leptin-induced endothelial dysfunction in obesity. Am J Physiol Heart Circ Physiol 295: H1514-H1521.
51. Kougias P, Chai H, Lin PH, Lumsden AB, Yao Q, Chen C, (2005). Adipocyte-derived cytokine resistin causes endothelial dysfunction of porcine coronary arteries. J Vasc Surg 41: 691-698. (Pubitemid 40637670)
52. Kourliouros A, Karastergiou K, Nowell J, Gukop P, Tavakkoli HM, Valencia O, et al,. (2010). Protective effect of epicardial adiponectin on atrial fibrillation following cardiac surgery. Eur J Cardiothorac Surg 39: 228-232.
53. Langheim S, Dreas L, Veschini L, Maisano F, Foglieni C, Ferrarello S, et al,. (2010). Increased expression and secretion of resistin in epicardial adipose tissue of patients with acute coronary syndrome. Am J Physiol Heart Circ Physiol 298: H746-H753.
54. Lau DC, Dhillon B, Yan H, Szmitko PE, Verma S, (2005). Adipokines: molecular links between obesity and atheroslcerosis. Am J Physiol Heart Circ Physiol 288: H2031-H2041. (Pubitemid 40604084)
55. Lee RM, Ding L, Lu C, Su LY, Gao YJ, (2009). Alteration of perivascular adipose tissue function in angiotensin II-induced hypertension. Can J Physiol Pharmacol 87: 944-953.
56. Lehman SJ, Massaro JM, Schlett CL, O'Donnell CJ, Hoffmann U, Fox CS, (2010). Peri-aortic fat, cardiovascular disease risk factors, and aortic calcification: the Framingham Heart Study. Atherosclerosis 210: 656-661.
57. Lembo G, Vecchione C, Fratta L, Marino G, Trimarco V, Amati G, et al,. (2000). Leptin induces direct vasodilation through distinct endothelial mechanisms. Diabetes 49: 293-297. (Pubitemid 30071008)
58. Li R, Wang WQ, Zhang H, Yang X, Fan Q, Christopher TA, et al,. (2007). Adiponectin improves endothelial function in hyperlipidemic rats by reducing oxidative/nitrative stress and differential regulation of eNOS/iNOS activity. Am J Physiol Endocrinol Metab 293: E1703-E1708. (Pubitemid 350255122)
59. Lohn M, Dubrovska G, Lauterbach B, Luft FC, Gollasch M, Sharma AM, (2002). Periadventitial fat releases a vascular relaxing factor. FASEB J 16: 1057-1063. (Pubitemid 34753512)
60. Lu C, Su LY, Lee RM, Gao YJ, (2008). Superoxide anion mediates angiotensin II-induced potentiation of contractile response to sympathetic stimulation. Eur J Pharmacol 589: 188-193.
61. Ma L, Ma S, He H, Yang D, Chen X, Luo Z, et al,. (2010). Perivascular fat-mediated vascular dysfunction and remodeling through the AMPK/mTOR pathway in high-fat diet-induced obese rats. Hypertens Res 33: 446-453.
62. Mahabadi AA, Massaro JM, Rosito GA, Levy D, Murabito JM, Wolf PA, et al,. (2009). Association of pericardial fat, intrathoracic fat, and visceral abdominal fat with cardiovascular disease burden: the Framingham Heart Study. Eur Heart J 30: 850-856.
63. Malinowski M, Deja MA, Golba KS, Roleder T, Biernat J, Wos S, (2008). Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor. Eur J Cardiothorac Surg 33: 225-231.
64. Marchesi C, Ebrahimian T, Angulo O, Paradis P, Schiffrin EL, (2009). Endothelial nitric oxide synthase uncoupling and perivascular adipose oxidative stress and inflammation contribute to vascular dysfunction in a rodent model of metabolic syndrome. Hypertension 54: 1384-1392.
65. Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, et al,. (2003). Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108: 2460-2466. (Pubitemid 37444406)
66. Mehta NN, Sheetz M, Price K, Comiskey L, Amrutia S, Iqbal N, et al,. (2009). Selective PKC beta inhibition with ruboxistaurin and endothelial function in type-2 diabetes mellitus. Cardiovasc Drugs Ther 23: 17-24.
67. Montani JP, Carroll JF, Dwyer TM, Antic V, Yang Z, Dulloo AG, (2004). Ectopic fat storage in heart, blood vessels and kidneys in the pathogenesis of cardiovascular diseases. Int J Obes Relat Metab Disord 28: S58-S65. (Pubitemid 40143850)
68. Monzillo LU, Hamdy O, Horton ES, Ledbury S, Mullooly C, Jarema C, et al,. (2003). Effect of lifestyle modification on adipokine levels in obese subjects with insulin resistance. Obes Res 11: 1048-1054. (Pubitemid 41151581)
69. Moreno PR, Purushothaman KR, Zias E, Sanz J, Fuster V, (2006). Neovascularization in human atherosclerosis. Curr Mol Med 6: 457-477.
70. Okamoto E, Couse T, De LH, Vinten-Johansen J, Goodman RB, Scott NA, et al,. (2001). Perivascular inflammation after balloon angioplasty of porcine coronary arteries. Circulation 104: 2228-2235. (Pubitemid 33043305)
71. O'Rourke L, Yeaman SJ, Shepherd PR, (2001). Insulin and leptin acutely regulate cholesterol ester metabolism in macrophages by novel signaling pathways. Diabetes 50: 955-961. (Pubitemid 32374524)
72. Ouwens DM, Sell H, Greulich S, Eckel J, (2010). The role of epicardial and perivascular adipose tissue in the pathophysiology of cardiovascular disease. J Cell Mol Med 14: 2223-2234.
73. Payne GA, Borbouse L, Bratz IN, Roell WC, Bohlen HG, Dick GM, et al,. (2008). Endogenous adipose-derived factors diminish coronary endothelial function via inhibition of nitric oxide synthase. Microcirculation 15: 417-426. (Pubitemid 351927730)
74. Payne GA, Bohlen HG, Dincer UD, Borbouse L, Tune JD, (2009). Periadventitial adipose tissue impairs coronary endothelial function via PKC-beta-dependent phosphorylation of nitric oxide synthase. Am J Physiol Heart Circ Physiol 297: H460-H465.
75. Payne GA, Borbouse L, Kumar S, Neeb Z, Alloosh M, Sturek M, et al,. (2010). Epicardial perivascular adipose-derived leptin exacerbates coronary endothelial dysfunction in metabolic syndrome via a protein kinase C-beta pathway. Arterioscler Thromb Vasc Biol 30: 1711-1717.
76. Picchi A, Gao X, Belmadani S, Potter BJ, Focardi M, Chilian WM, et al,. (2006). Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res 99: 69-77. (Pubitemid 44297057)
77. Police SB, Thatcher SE, Charnigo R, Daugherty A, Cassis LA, (2009). Obesity promotes inflammation in periaortic adipose tissue and angiotensin II-induced abdominal aortic aneurysm formation. Arterioscler Thromb Vasc Biol 29: 1458-1464.
78. Porreca E, Di FC, Moretta V, Angelini A, Guglielmi MD, Di NM, et al,. (2004). Circulating leptin is associated with oxidized LDL in postmenopausal women. Atherosclerosis 175: 139-143. (Pubitemid 38746920)
79. Rainwater DL, Comuzzie AG, VandeBerg JL, Mahaney MC, Blangero J, (1997). Serum leptin levels are independently correlated with two measures of HDL. Atherosclerosis 132: 237-243. (Pubitemid 27311016)
80. Rajsheker S, Manka D, Blomkalns AL, Chatterjee TK, Stoll LL, Weintraub NL, (2010). Crosstalk between perivascular adipose tissue and blood vessels. Curr Opin Pharmacol 10: 191-196.
81. Reifenberger MS, Turk JR, Newcomer SC, Booth FW, Laughlin MH, (2007). Perivascular fat alters reactivity of coronary artery: effects of diet and exercise. Med Sci Sports Exerc 39: 2125-2134. (Pubitemid 350211504)
82. Rhoads RP, Johnson RM, Rathbone CR, Liu X, Temm-Grove C, Sheehan SM, et al,. (2009). Satellite cell-mediated angiogenesis in vitro coincides with a functional hypoxia-inducible factor pathway. Am J Physiol Cell Physiol 296: C1321-C1328.
83. Rosito GA, Massaro JM, Hoffmann U, Ruberg FL, Mahabadi AA, Vasan RS, et al,. (2008). Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study. Circulation 117: 605-613.
84. Ross R, (1993a). Atherosclerosis: current understanding of mechanisms and future strategies in therapy. Transplant Proc 25: 2041-2043. (Pubitemid 23125199)
85. Ross R, (1993b). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362: 801-809. (Pubitemid 23132154)
86. Ross R, Glomset JA, (1973). Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 180: 1332-1339.
87. Ruan CC, Zhu DL, Chen QZ, Chen J, Guo SJ, Li XD, et al,. (2010). Perivascular adipose tissue-derived complement 3 is required for adventitial fibroblast functions and adventitial remodeling in deoxycorticosterone acetate-salt hypertensive rats. Arterioscler Thromb Vasc Biol 30: 2568-2574.
88. Sacks HS, Fain JN, (2007). Human epicardial adipose tissue: a review. Am Heart J 153: 907-917. (Pubitemid 46809849)
89. Sacks HS, Fain JN, Holman B, Cheema P, Chary A, Parks F, et al,. (2009). Uncoupling protein-1 and related messenger ribonucleic acids in human epicardial and other adipose tissues: epicardial fat functioning as brown fat. J Clin Endocrinol Metab 94: 3611-3615.
90. Sade LE, Eroglu S, Bozbas H, Ozbicer S, Hayran M, Haberal A, et al,. (2009). Relation between epicardial fat thickness and coronary flow reserve in women with chest pain and angiographically normal coronary arteries. Atherosclerosis 204: 580-585.
91. Sarin S, Wenger C, Marwaha A, Qureshi A, Go BD, Woomert CA, et al,. (2008). Clinical significance of epicardial fat measured using cardiac multislice computed tomography. Am J Cardiol 102: 767-771.
92. Schlett CL, Massaro JM, Lehman SJ, Bamberg F, O'Donnell CJ, Fox CS, et al,. (2009). Novel measurements of periaortic adipose tissue in comparison to anthropometric measures of obesity, and abdominal adipose tissue. Int J Obes (Lond) 33: 226-232.
93. Shamsuzzaman AS, Winnicki M, Wolk R, Svatikova A, Phillips BG, Davison DE, et al,. (2004). Independent association between plasma leptin and C-reactive protein in healthy humans. Circulation 109: 2181-2185. (Pubitemid 38625394)
94. Shibasaki I, Nishikimi T, Mochizuki Y, Yamada Y, Yoshitatsu M, Inoue Y, et al,. (2010). Greater expression of inflammatory cytokines, adrenomedullin, and natriuretic peptide receptor-C in epicardial adipose tissue in coronary artery disease. Regul Pept 165: 210-217.
95. Silha JV, Krsek M, Skrha JV, Sucharda P, Nyomba BL, Murphy LJ, (2003). Plasma resistin, adiponectin and leptin levels in lean and obese subjects: correlations with insulin resistance. Eur J Endocrinol 149: 331-335. (Pubitemid 37304704)
96. Skilton MR, Serusclat A, Sethu AH, Brun S, Bernard S, Balkau B, et al,. (2009). Noninvasive measurement of carotid extra-media thickness: associations with cardiovascular risk factors and intima-media thickness. JACC Cardiovasc Imaging 2: 176-182.
97. Soltis EE, Cassis LA, (1991). Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin Exp Hypertens A 13: 277-296.
98. Spiroglou SG, Kostopoulos CG, Varakis JN, Papadaki HH, (2010). Adipokines in periaortic and epicardial adipose tissue: differential expression and relation to atherosclerosis. J Atheroscler Thromb 17: 115-130.
99. Staub D, Schinkel AF, Coll B, Coli S, van der Steen AF, Reed JD, et al,. (2010). Contrast-enhanced ultrasound imaging of the vasa vasorum: from early atherosclerosis to the identification of unstable plaques. JACC Cardiovasc Imaging 3: 761-771.
100. Takaoka M, Nagata D, Kihara S, Shimomura I, Kimura Y, Tabata Y, et al,. (2009). Periadventitial adipose tissue plays a critical role in vascular remodeling. Circ Res 105: 906-911.
101. Takaoka M, Suzuki H, Shioda S, Sekikawa K, Saito Y, Nagai R, et al,. (2010). Endovascular injury induces rapid phenotypic changes in perivascular adipose tissue. Arterioscler Thromb Vasc Biol 30: 1576-1582.
102. Tao L, Gao E, Jiao X, Yuan Y, Li S, Christopher TA, et al,. (2007). Adiponectin cardioprotection after myocardial ischemia/reperfusion involves the reduction of oxidative/nitrative stress. Circulation 115: 1408-1416. (Pubitemid 46648376)
103. Thalmann S, Meier CA, (2007). Local adipose tissue depots as cardiovascular risk factors. Cardiovasc Res 75: 690-701. (Pubitemid 47238732)
104. Tinsley JH, Hunter FA, Childs EW, (2008). PKC and MLCK-dependent, cytokine-induced rat coronary endothelial dysfunction. J Surg Res 152: 76-83.
105. Trayhurn P, Wood IS, (2005). Signalling role of adipose tissue: adipokines and inflammation in obesity. Biochem Soc Trans 33: 1078-1081. (Pubitemid 41659117)
106. Tune JD, Considine RV, (2007). Effects of leptin on cardiovascular physiology. J Am Soc Hypertens 1: 231-241. (Pubitemid 47091544)
107. Vela D, Buja LM, Madjid M, Burke A, Naghavi M, Willerson JT, et al,. (2007). The role of periadventitial fat in atherosclerosis. Arch Pathol Lab Med 131: 481-487.
108. Verhagen SN, Visseren FL, (2011). Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis 214: 3-10.
109. Verlohren S, Dubrovska G, Tsang SY, Essin K, Luft FC, Huang Y, et al,. (2004). Visceral periadventitial adipose tissue regulates arterial tone of mesenteric arteries. Hypertension 44: 271-276. (Pubitemid 39167221)
110. Wang P, Xu TY, Guan YF, Su DF, Fan GR, Miao CY, (2009). Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc Res 81: 370-380.
111. Xu A, Wang Y, Lam KS, Vanhoutte PM, (2010). Vascular actions of adipokines molecular mechanisms and therapeutic implications. Adv Pharmacol 60: 229-255.
112. Yamawaki H, Hara N, Okada M, Hara Y, (2009). Visfatin causes endothelium-dependent relaxation in isolated blood vessels. Biochem Biophys Res Commun 383: 503-508.
113. Yamawaki H, Tsubaki N, Mukohda M, Okada M, Hara Y, (2010). Omentin, a novel adipokine, induces vasodilation in rat isolated blood vessels. Biochem Biophys Res Commun 393: 668-672.
114. Zhang H, Zhang C, (2009). Regulation of microvascular function by adipose tissue in obesity and type 2 diabetes: evidence of an adipose-vascular loop. Am J Biomed Sci 1: 133-142.
115. Zhang H, Park Y, Wu J, Chen X, Lee S, Yang J, et al,. (2009). Role of TNF-alpha in vascular dysfunction. Clin Sci (Lond) 116: 219-230.