Perivascular adipose tissue: More than just structural support

Clinical Science

Volumn 122, Issue 1, 2012, Pages 1-12

  Szasz, Theodora ^a   Webb, R Clinton ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Adipokine; Atherosclerosis; Hypertension; Obesity; Perivascular adipose tissue; Vascular contraction

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; ADRENOMEDULLIN; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR; ANGIOTENSIN[1-7]; ANGIOTENSINOGEN; DIPEPTIDYL CARBOXYPEPTIDASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; LIPOXYGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PERIVASCULAR ADIPOSE TISSUE DERIVED RELAXING FACTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; PRORENIN RECEPTOR; PROTEIN; RANTES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESISTIN; SUPEROXIDE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ARTICLE; ATHEROSCLEROSIS; BROWN ADIPOSE TISSUE; CARDIOVASCULAR DISEASE; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE RELEASE; DIABETES MELLITUS; HUMAN; HYPERTENSION; INSULIN RESISTANCE; MUSCLE FIBER CONTRACTION; MUSCLE FORCE; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PERIVASCULAR ADIPOSE TISSUE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; VASCULITIS; WHITE ADIPOSE TISSUE; ANIMAL; BIOLOGICAL MODEL; BLOOD VESSEL; METABOLISM; PHYSIOLOGY; REVIEW; VASCULAR ENDOTHELIUM; VASOCONSTRICTION;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; BLOOD VESSELS; CARDIOVASCULAR DISEASES; ENDOTHELIUM, VASCULAR; HUMANS; MODELS, BIOLOGICAL; NITRIC OXIDE; VASOCONSTRICTION;

EID: 84856403083     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20110151     Document Type: Article

References (99)

1. Cinti, S. (2005) The adipose organ. Prostaglandins Leukotrienes Essent. Fatty Acids 73, 9-15
2. Berthoud, H. R., Fox, E. A. and Neuhuber, W. L. (2006) Vagaries of adipose tissue innervation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R1240-R1242
3. Lazar, M. A. (2008) Developmental biology. How now, brown fat? Science 321, 1048-1049
4. Richard, D., Carpentier, A. C., Dore, G., Ouellet, V. and Picard, F. (2010) Determinants of brown adipocyte development and thermogenesis. Int. J. Obes. 34 (Suppl. 2), S59-S66
5. Saito, M., Okamatsu-Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio-Kobayashi, J., Iwanaga, T., Miyagawa, M., Kameya, T., Nakada, K. et al. (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58, 1526-1531
6. Tilg, H. and Moschen, A. R. (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 6, 772-783
7. Kershaw, E. E. and Flier, J. S. (2004) Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 89, 2548-2556
8. Gao, Y. J. (2007) Dual modulation of vascular function by perivascular adipose tissue and its potential correlation with adiposity/lipoatrophy-related vascular dysfunction. Curr. Pharm. Des. 13, 2185-2192
9. Chatterjee, T. K., Stoll, L. L., Denning, G. M., Harrelson, A., Blomkalns, A. L., Idelman, G., Rothenberg, F. G., Neltner, B., Romig-Martin, S. A., Dickson, E.W. et al. (2009) Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding. Circ. Res. 104, 541-549
10. Galvez-Prieto, B., Bolbrinker, J., Stucchi, P., de Las Heras, A. I., Merino, B., Arribas, S., Ruiz-Gayo, M., Huber, M., Wehland, M., Kreutz, R. and Fernandez-Alfonso, M. S. (2008) Comparative expression analysis of the renin-angiotensin system components between white and brown perivascular adipose tissue. J. Endocrinol. 197, 55-64
11. Cao, R., Brakenhielm, E.,Wahlestedt, C., Thyberg, J. and Cao, Y. (2001) Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF. Proc. Natl. Acad. Sci. U.S.A. 98, 6390-6395
12. Ohashi, K., Ouchi, N. and Matsuzawa, Y. (2011) Adiponectin and hypertension. Am. J. Hypertens. 24, 263-269
13. Bhalla, V., Kalogeropoulos, A., Georgiopoulou, V. and Butler, J. (2010) Serum resistin: physiology, pathophysiology and implications for heart failure. Biomark. Med. 4, 445-452
14. Rajsheker, S., Manka, D., Blomkalns, A. L., Chatterjee, T. K., Stoll, L. L. and Weintraub, N. L. (2010) Crosstalk between perivascular adipose tissue and blood vessels. Curr. Opin. Pharmacol. 10, 191-196
15. Yamawaki, H. (2011) Vascular effects of novel adipocytokines: focus on vascular contractility and inflammatory responses. Biol. Pharm. Bull. 34, 307-310
16. Thalmann, S. and Meier, C. A. (2007) Local adipose tissue depots as cardiovascular risk factors. Cardiovasc. Res. 75, 690-701
17. Lu, C., Su, L. Y., Lee, R. M. and Gao, Y. J. (2010) Mechanisms for perivascular adipose tissue-mediated potentiation of vascular contraction to perivascular neuronal stimulation: the role of adipocyte-derived angiotensin II. Eur. J. Pharmacol. 634, 107-112
18. Fang, L., Zhao, J., Chen, Y., Ma, T., Xu, G., Tang, C., Liu, X. and Geng, B (2009) Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator. J. Hypertens. 27, 2174-2185
19. Gao, Y. J., Lu, C., Su, L. Y., Sharma, A. M. and Lee, R. M. (2007) Modulation of vascular function by perivascular adipose tissue: the role of endothelium and hydrogen peroxide. Br. J. Pharmacol. 151, 323-331
20. Ketonen, J., Shi, J., Martonen, E. and Mervaala, E. (2010) Periadventitial adipose tissue promotes endothelial dysfunction via oxidative stress in diet-induced obese C57Bl/6 mice. Circ. J. 74, 1479-1487
21. Guzik, T. J., Marvar, P. J., Czesnikiewicz-Guzik, M. and Korbut, R. (2007) Perivascular adipose tissue as a messenger of the brain-vessel axis: role in vascular inflammation and dysfunction. J. Physiol. Pharmacol. 58, 591-610
22. Henrichot, E., Juge-Aubry, C. E., Pernin, A., Pache, J. C., Velebit, V., Dayer, J. M.,Meda, P., Chizzolini, C. andMeier, C. A. (2005) Production of chemokines by perivascular adipose tissue: a role in the pathogenesis of atherosclerosis? Arterioscler. Thromb. Vasc. Biol. 25, 2594-2599
23. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L. and Ferrante, Jr, A. W. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796-1808
24. Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A. and Chen, H. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112, 1821-1830
25. Withers, S. B., Agabiti-Rosei, C., Livingstone, D. M., Little, M. C., Aslam, R., Malik, R. A. and Heagerty, A. M. (2011) Macrophage activation is responsible for loss of anticontractile function in inflamed perivascular fat. Arterioscler. Thromb. Vasc. Biol. 31, 908-913
26. Soltis, E. E. and Cassis, L. A. (1991) Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin. Exp. Hypertens. A 13, 277-296
27. Dubrovska, G., Verlohren, S., Luft, F. C. and Gollasch, M. (2004) Mechanisms of ADRF release from rat aortic adventitial adipose tissue. Am. J. Physiol. Heart Circ. Physiol. 286, H1107-H1113
28. Löhn, M., Dubrovska, G., Lauterbach, B., Luft, F. C., Gollasch, M. and Sharma, A. M. (2002) Periadventitial fat releases a vascular relaxing factor. FASEB J. 16, 1057-1063
29. Verlohren, S., Dubrovska, G., Tsang, S. Y., Essin, K., Luft, F. C., Huang, Y. and Gollasch, M. (2004) Visceral periadventitial adipose tissue regulates arterial tone of mesenteric arteries. Hypertension 44, 271-276
30. Gollasch, M. and Dubrovska, G. (2004) Paracrine role for periadventitial adipose tissue in the regulation of arterial tone. Trends Pharmacol. Sci. 25, 647-653
31. Fesus, G., Dubrovska, G., Gorzelniak, K., Kluge, R., Huang, Y., Luft, F. C. and Gollasch, M. (2007) Adiponectin is a novel humoral vasodilator. Cardiovasc. Res. 75, 719-727
32. Gao, Y. J., Takemori, K., Su, L. Y., An, W. S., Lu, C., Sharma, A. M. and Lee, R. M. (2006) Perivascular adipose tissue promotes vasoconstriction: the role of superoxide anion. Cardiovasc. Res. 71, 363-373
33. Gao, Y. J., Zeng, Z. H., Teoh, K., Sharma, A. M., Abouzahr, L., Cybulsky, I., Lamy, A., Semelhago, L. and Lee, R. M. (2005) Perivascular adipose tissue modulates vascular function in the human internal thoracic artery. J. Thorac. Cardiovasc. Surg. 130, 1130-1136
34. Lee, R. M., Ding, L., Lu, C., Su, L. Y. and Gao, Y. J. (2009) Alteration of perivascular adipose tissue function in angiotensin II-induced hypertension. Can. J. Physiol. Pharmacol. 87, 944-953
35. Lee, R. M., Lu, C., Su, L. Y. and Gao, Y. J. (2009) Endothelium-dependent relaxation factor released by perivascular adipose tissue. J. Hypertens. 27, 782-790
36. Lee, R.M., Lu,C., Su, L. Y., Werstuck,G. and Gao, Y. J. (2009) Effects of hyperglycemia on the modulation of vascular function by perivascular adipose tissue. J. Hypertens. 27, 118-131
37. Lu, C., Su, L. Y., Lee, R. M. and Gao, Y. J. (2011) Alterations in perivascular adipose tissue structure and function in hypertension. Eur. J. Pharmacol. 656, 68-73
38. Lu, C., Zhao, A. X., Gao, Y. J. and Lee, R. M. (2011) Modulation of vein function by perivascular adipose tissue. Eur. J. Pharmacol. 657, 111-116
39. Brandes, R. P. (2007) The fatter the better? Perivascular adipose tissue attenuates vascular contraction through different mechanisms. Br. J. Pharmacol. 151, 303-304
40. Girouard, H., Bonev, A. D., Hannah, R. M., Meredith, A., Aldrich, R. W. and Nelson, M. T. (2010) Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc. Natl. Acad. Sci. U.S.A. 107, 3811-3816
41. Dashwood, M. R., Dooley, A., Shi-Wen, X., Abraham, D. J., Dreifaldt, M. and Souza, D. S. (2007) Perivascular fat-derived leptin: a potential role in improved vein graft performance in coronary artery bypass surgery. Interact. Cardiovasc. Thorac. Surg. 12, 170-173
42. Mohammed, M. M., Myers, D. S., Sofola, O. A., Hainsworth, R. and Drinkhill, M. J. (2007) Vasodilator effects of leptin on canine isolated mesenteric arteries and veins. Clin. Exp. Pharmacol. Physiol. 34, 771-774
43. Sahin, A. S. and Bariskaner, H. (2007) The mechanisms of vasorelaxant effect of leptin on isolated rabbit aorta. Fundam. Clin. Pharmacol. 21, 595-600
44. Nakagawa, K., Higashi, Y., Sasaki, S., Oshima, T., Matsuura, H. and Chayama, K. (2002) Leptin causes vasodilation in humans. Hypertens. Res. 25, 161-165
45. Kimura, K., Tsuda, K., Baba, A., Kawabe, T., Boh-oka, S., Ibata, M., Moriwaki, C., Hano, T. and Nishio, I. (2000) Involvement of nitric oxide in endothelium-dependent arterial relaxation by leptin. Biochem. Biophys. Res. Commun. 273, 745-749
46. Rahmouni, K. and Haynes, W. G. (2005) Endothelial effects of leptin: implications in health and diseases. Curr. Diab. Rep. 5, 260-266
47. Fortuno, A., Rodriguez, A., Gomez-Ambrosi, J., Muniz, P., Salvador, J., Diez, J. and Fruhbeck, G. (2002) Leptin inhibits angiotensin II-induced intracellular calcium increase and vasoconstriction in the rat aorta. Endocrinology 143, 3555-3560
48. Rodriguez, A., Fortuno, A., Gomez-Ambrosi, J., Zalba, G., Diez, J. and Fruhbeck, G. (2007) The inhibitory effect of leptin on angiotensin II-induced vasoconstriction in vascular smooth muscle cells is mediated via a nitric oxide-dependent mechanism. Endocrinology 148, 324-331
49. Knudson, J. D., Dincer, U. D., Zhang, C., Swafford, Jr, A. N., Koshida, R., Picchi, A., Focardi, M., Dick, G. M. and Tune, J. D. (2005) Leptin receptors are expressed in coronary arteries, and hyperleptinemia causes significant coronary endothelial dysfunction. Am. J. Physiol. Heart Circ. Physiol. 289, H48-H56
50. Shek, E.W., Brands, M. W. and Hall, J. E. (1998) Chronic leptin infusion increases arterial pressure. Hypertension 31, 409-414
51. Zhu, W., Cheng, K. K., Vanhoutte, P. M., Lam, K. S. and Xu, A. (2008) Vascular effects of adiponectin: molecular mechanisms and potential therapeutic intervention. Clin. Sci. 114, 361-374
52. Okamoto, Y., Arita, Y., Nishida, M., Muraguchi, M., Ouchi, N., Takahashi, M., Igura, T., Inui, Y., Kihara, S., Nakamura, T. et al. (2000) An adipocyte-derived plasma protein, adiponectin, adheres to injured vascular walls. Horm. Metab. Res. 32, 47-50
53. Lam, K. S. and Xu, A. (2005) Adiponectin: protection of the endothelium. Curr. Diab. Rep. 5, 254-259
54. Cho, Y., Lee, S. E., Lee, H. C., Hur, J., Lee, S., Youn, S. W., Lee, J., Lee, H. J., Lee, T. K., Park, J. et al. (2010) Adipokine resistin is a key player to modulate monocytes, endothelial cells, and smooth muscle cells, leading to progression of atherosclerosis in rabbit carotid artery. J. Am. Coll. Cardiol. 57, 99-109
55. Shyu, K. G., Lien, L. M.,Wang, B.W., Kuan, P. and Chang, H. (2011) Resistin contributes to neointimal formation via oxidative stress after vascular injury. Clin. Sci. 120, 121-129
56. Wang, P., Xu, T. Y., Guan, Y. F., Su, D. F., Fan, G. R. and Miao, C. Y. (2009) Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc. Res. 81, 370-380
57. Maenhaut, N., Boydens, C. and Van de Voorde, J. (2010) Hypoxia enhances the relaxing influence of perivascular adipose tissue in isolated mice aorta. Eur. J. Pharmacol. 641, 207-212
58. Malinowski, M., Deja, M. A., Golba, K. S., Roleder, T., Biernat, J. and 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
59. Greenstein, A. S., Khavandi, K., Withers, S. B., Sonoyama, K., Clancy, O., Jeziorska, M., Laing, I., Yates, A. P., Pemberton, P.W., Malik, R. A. and Heagerty, A. M. (2009) Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 119, 1661-1670
60. Achike, F. I., To, N. H., Wang, H. and Kwan, C. Y. (2011) Obesity, metabolic syndrome, adipocytes and vascular function: A holistic viewpoint. Clin. Exp. Pharmacol. Physiol. 38, 1-10
61. Payne, G. A., Bohlen, H. G., Dincer, U. D., Borbouse, L. and Tune, J. D. (2009) Periadventitial adipose tissue impairs coronary endothelial function via PKC-β-dependent phosphorylation of nitric oxide synthase. Am. J. Physiol. Heart Circ. Physiol. 297, H460-H465
62. Payne, G. A., Borbouse, L., Kumar, S., Neeb, Z., Alloosh, M., Sturek, M. and Tune, J. D. (2010) Epicardial perivascular adipose-derived leptin exacerbates coronary endothelial dysfunction in metabolic syndrome via a protein kinase C-β pathway. Arterioscler. Thromb. Vasc. Biol. 30, 1711-1717
63. Barandier, C., Montani, J. P. and 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
64. Engeli, S. (2005) Is there a pathophysiological role for perivascular adipocytes? Am. J. Physiol. Heart Circ. Physiol. 289, H1794-H1795
65. Lamers, D., Schlich, R., Greulich, S., Sasson, S., Sell, H. and Eckel, J. (2011) Oleic acid and adipokines synergize in inducing proliferation and inflammatory signaling in human vascular smooth muscle cells. J. Cell. Mol. Med. 15, 1177-1188
66. Wang, Y., Lam, K. S., Xu, J. Y., Lu, G., Xu, L. Y., Cooper, G. J. and Xu, A. (2005) Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J. Biol. Chem. 280, 18341-18347
67. Zhang, H. and 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
68. Yudkin, J. S., Eringa, E. and Stehouwer, C. D. (2005) 'Vasocrine' signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet 365, 1817-1820
69. Montani, J. P., Carroll, J. F., Dwyer, T. M., Antic, V., Yang, Z. and Dulloo, A. G. (2004) Ectopic fat storage in heart, blood vessels and kidneys in the pathogenesis of cardiovascular diseases. Int. J. Obes. Relat. Metab. Disord. 28(Suppl. 4), S58-S65
70. Marchesi, C., Ebrahimian, T., Angulo, O., Paradis, P. and Schiffrin, E. L. (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
71. Ma, L., Ma, S., He, H., Yang, D., Chen, X., Luo, Z., Liu, D. and Zhu, Z. (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
72. Rittig, K., Staib, K., Machann, J., Bottcher, M., Peter, A., Schick, F., Claussen, C., Stefan, N., Fritsche, A., Haring, H. U. and Balletshofer, B. (2008) Perivascular fatty tissue at the brachial artery is linked to insulin resistance but not to local endothelial dysfunction. Diabetologia 51, 2093-2099
73. Lehman, S. J., Massaro, J. M., Schlett, C. L., O'Donnell, C. J., Hoffmann, U. and Fox, C. S. (2010) Peri-aortic fat, cardiovascular disease risk factors, and aortic calcification: the Framingham Heart Study. Atherosclerosis 210, 656-661
74. Meijer, R. I., Serne, E. H., Smulders, Y. M., van Hinsbergh, V. W., Yudkin, J. S. and Eringa, E. C. (2011) Perivascular adipose tissue and its role in type 2 diabetes and cardiovascular disease. Curr. Diab. Rep. 11, 211-217
75. Gil-Ortega, M., Stucchi, P., Guzman-Ruiz, R., Cano, V., Arribas, S., Gonzalez, M. C., Ruiz-Gayo, M., Fernandez-Alfonso, M. S. and Somoza, B. (2010) Adaptative nitric oxide overproduction in perivascular adipose tissue during early diet-induced obesity. Endocrinology 151, 3299-3306
76. Rebolledo, A., Rebolledo, O. R., Marra, C. A., Garcia, M. E., Roldan Palomo, A. R., Rimorini, L. and Gagliardino, J. J. (2010) Early alterations in vascular contractility associated to changes in fatty acid composition and oxidative stress markers in perivascular adipose tissue. Cardiovasc. Diabetol. 9, 65
77. Huang, F., Lezama, M. A., Ontiveros, J. A., Bravo, G., Villafana, S., del-Rio-Navarro, B. E. and Hong, E. (2010) Effect of losartan on vascular function in fructose-fed rats: the role of perivascular adipose tissue. Clin. Exp. Hypertens. 32, 98-104
78. Zhang, H. and Zhang, C. (2010) Adipose 'talks' to distant organs to regulate insulin sensitivity and vascular function. Obesity 18, 2071-2076
79. Galvez, B., de Castro, J., Herold, D., Dubrovska, G., Arribas, S., Gonzalez, M. C., Aranguez, I., Luft, F. C., Ramos, M. P., Gollasch, M. and Fernandez Alfonso, M. S. (2006) Perivascular adipose tissue and mesenteric vascular function in spontaneously hypertensive rats. Arterioscler. Thromb. Vasc. Biol. 26, 1297-1302
80. Ruan, C. C., Zhu, D. L., Chen, Q. Z., Chen, J., Guo, S. J., Li, X. D. and Gao, P. J. (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
81. Galvez-Prieto, B., Dubrovska, G., Cano, M. V., Delgado, M., Aranguez, I., Gonzalez, M. C., Ruiz-Gayo, M., Gollasch, M. and Fernandez-Alfonso, M. S. (2008) A reduction in the amount and anti-contractile effect of periadventitial mesenteric adipose tissue precedes hypertension development in spontaneously hypertensive rats. Hypertens. Res. 31, 1415-1423
82. Zeng, Z. H., Zhang, Z. H., Luo, B. H., He,W. K., Liang, L. Y., He, C. C. and Su, C. J. (2009) The functional changes of the perivascular adipose tissue in spontaneously hypertensive rats and the effects of atorvastatin therapy. Clin. Exp. Hypertens. 31, 355-363
83. Gao, Y. J., Holloway, A. C., Su, L. Y., Takemori, K., Lu, C. and Lee, R. M. (2008) Effects of fetal and neonatal exposure to nicotine on blood pressure and perivascular adipose tissue function in adult life. Eur. J. Pharmacol. 590, 264-268
84. Rodriguez, A., Fruhbeck, G., Gomez-Ambrosi, J., Catalan, V., Sainz, N., Diez, J., Zalba, G. and Fortuno, A. (2006) The inhibitory effect of leptin on angiotensin II-induced vasoconstriction is blunted in spontaneously hypertensive rats. J. Hypertens. 24, 1589-1597
85. Verhagen, S. N. and Visseren, F. L. (2011) Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis 214, 3-10
86. Vela, D., Buja, L. M., Madjid, M., Burke, A., Naghavi, M., Willerson, J. T., Casscells, S.W. and Litovsky, S. (2007) The role of periadventitial fat in atherosclerosis. Arch. Pathol. Lab. Med. 131, 481-487
87. Sacks, H. S. and Fain, J. N. (2007) Human epicardial adipose tissue: a review. Am. Heart J. 153, 907-917
88. Spiroglou, S. G., Kostopoulos, C. G., Varakis, J. N. and Papadaki, H. H. (2010) Adipokines in periaortic and epicardial adipose tissue: differential expression and relation to atherosclerosis. J. Atheroscler. Thromb. 17, 115-130
89. Hug, C. and Lodish, H. F. (2005) The role of the adipocyte hormone adiponectin in cardiovascular disease. Curr. Opin. Pharmacol. 5, 129-134
90. Silaghi, A., Achard, V., Paulmyer-Lacroix, O., Scridon, T., Tassistro, V., Duncea, I., Clement, K., Dutour, A. and Grino, M. (2007) Expression of adrenomedullin in human epicardial adipose tissue: role of coronary status. Am. J. Physiol. Endocrinol. Metab. 293, E1443-E1450
91. Baker, A. R., Silva, N. F., Quinn, D. W., Harte, A. L., Pagano, D., Bonser, R. S., Kumar, S. and McTernan, P. G. (2006) Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc. Diabetol. 5, 1
92. Cheng, K. H., Chu, C. S., Lee, K. T., Lin, T. H., Hsieh, C. C., Chiu, C. C., Voon, W. C., Sheu, S. H. and Lai,W. T. (2008) Adipocytokines and proinflammatory mediators from abdominal and epicardial adipose tissue in patients with coronary artery disease. Int. J. Obes. 32, 268-274
93. Eiras, S., Teijeira-Fernandez, E., Shamagian, L. G., Fernandez, A. L., Vazquez-Boquete, A. and Gonzalez-Juanatey, J. R. (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
94. Mazurek, T., Zhang, L., Zalewski, A., Mannion, J. D., Diehl, J. T., Arafat, H., Sarov-Blat, L., O'Brien, S., Keiper, E. A., Johnson, A. G. et al. (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108, 2460-2466
95. Ishikawa, Y., Akasaka, Y., Ito, K., Akishima, Y., Kimura, M., Kiguchi, H., Fujimoto, A. and Ishii, T. (2006) Significance of anatomical properties of myocardial bridge on atherosclerosis evolution in the left anterior descending coronary artery. Atherosclerosis 186, 380-389
96. Bunker, A. K. and Laughlin, M. H. (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
97. Takaoka, M., Suzuki, H., Shioda, S., Sekikawa, K., Saito, Y., Nagai, R. and Sata, M. (2010) Endovascular injury induces rapid phenotypic changes in perivascular adipose tissue. Arterioscler. Thromb. Vasc. Biol. 30, 1576-1582
98. Lohmann, C., Schafer, N., von Lukowicz, T., Sokrates Stein, M. A., Boren, J., Rutti, S., Wahli, W., Donath, M. Y., Luscher, T. F. and Matter, C. M. (2009) Atherosclerotic mice exhibit systemic inflammation in periadventitial and visceral adipose tissue, liver, and pancreatic islets. Atherosclerosis 207, 360-367
99. Schleifenbaum, J., Kohn, C., Voblova, N., Dubrovska, G., Zavarirskaya, O., Gloe, T., Crean, C. S., Luft, F. C., Huang, Y., Schubert, R. and Gollasch, M. (2010) Systemic peripheral artery relaxation by KCNQ channel openers and hydrogen sulfide. J. Hypertens. 28, 1875-1882