Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension

Circulation Journal

Volumn 77, Issue 1, 2013, Pages 11-18

  Chang, Lin ^a   Milton, Hamblin ^b   Eitzman, Daniel T ^a   Eugene Chen, Y ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Brown adipose tissue; Hypertension; Perivascular adipose tissue; White adipose tissue

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; ANGIOTENSIN II; ANGIOTENSIN II [1 SARCOSINE 8 ISOLEUCINE]; CHOLESTEROL; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; MYOSIN HEAVY CHAIN; NITRIC OXIDE; NORADRENALIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTACYCLIN; TRIACYLGLYCEROL; UNCOUPLING PROTEIN 1; VASCULAR ENDOTHELIAL CADHERIN;

ADIPOCYTE; ADIPOSE TISSUE; ATHEROSCLEROSIS; BLOOD PRESSURE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL FUNCTION; CELL INFILTRATION; CELL PROLIFERATION; ELECTROSTIMULATION; HUMAN; HYPERTENSION; INFLAMMATION; LIPID STORAGE; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; MUSCLE CONTRACTILITY; NONHUMAN; PERIVASCULAR ADIPOSE TISSUE; PROTEIN EXPRESSION; REVIEW; THERMOGENESIS; VASCULAR SMOOTH MUSCLE; WHITE ADIPOSE TISSUE;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; ATHEROSCLEROSIS; ENDOTHELIAL CELLS; ENERGY METABOLISM; HUMANS; HYPERTENSION; LIPID METABOLISM; MYOCYTES, SMOOTH MUSCLE; OBESITY; THERMOGENESIS;

EID: 84871677870     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-12-1393     Document Type: Review

References (74)

1. Szasz T, Webb RC. Perivascular adipose tissue: More than just structural support. Clin Sci (Lond) 2012; 122: 1-12.
2. de Souza RR, Ferraz de Carvalho CA, Merluzzi Filho TJ, Andrade Vieira JA. Functional anatomy of the perivascular tissue in the adductor canal. Gegenbaurs Morphol Jahrb 1984; 130: 733-738.
3. Ouwens DM, Sell H, Greulich S, Eckel J. The role of epicardial and perivascular adipose tissue in the pathophysiology of cardiovascular disease. J Cell Mol Med 2010; 14: 2223-2234.
4. Calabro P, Yeh ET. Obesity, inflammation, and vascular disease: The role of the adipose tissue as an endocrine organ. Subcell Biochem 2007; 42: 63-91.
5. Iyama K, Ohzono K, Usuku G. Electron microscopical studies on the genesis of white adipocytes: Differentiation of immature pericytes into adipocytes in transplanted preadipose tissue. Virchows Arch B Cell Pathol Incl Mol Pathol 1979; 31: 143-155.
6. Bani-Sacchi T, Bianchi S, Bani G, Bigazzi M. Ultrastructural studies on white adipocyte differentiation in the mouse mammary gland following estrogen and relaxin. Acta Anat (Basel) 1987; 129: 1-9.
7. Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: Tracking obesity to its source. Cell 2007; 131: 242-256.
8. Yuan SM, Chen RL, Shen WM, Chen HN, Zhou XJ. Mesenchymal stem cells in infantile hemangioma reside in the perivascular region. Pediatr Dev Pathol 2012; 15: 5-12.
9. Guilak F, Lott KE, Awad HA, Cao Q, Hicok KC, Fermor B, et al. Clonal analysis of the differentiation potential of human adiposederived adult stem cells. J Cell Physiol 2006; 206: 229-237.
10. Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell 2008; 135: 240-249.
11. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, et al. White fat progenitor cells reside in the adipose vasculature. Science 2008; 322: 583-586.
12. Tran KV, Gealekman O, Frontini A, Zingaretti MC, Morroni M, Giordano A, et al. The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab 2012; 15: 222-229.
13. Gupta RK, Mepani RJ, Kleiner S, Lo JC, Khandekar MJ, Cohen P, et al. Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metab 2012; 15: 230-239.
14. Macotela Y, Emanuelli B, Mori MA, Gesta S, Schulz TJ, Tseng YH, et al. Intrinsic differences in adipocyte precursor cells from different white fat depots. Diabetes 2012; 61: 1691-1699.
15. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 2008; 454: 961-967.
16. Li L, Miano JM, Cserjesi P, Olson EN. SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ Res 1996; 78: 188-195.
17. Chang L, Villacorta L, Li R, Hamblin M, Xu W, Dou C, et al. Loss of perivascular adipose tissue on peroxisome proliferator-activated receptor-gamma deletion in smooth muscle cells impairs intravascular thermoregulation and enhances atherosclerosis. Circulation 2012; 126: 1067-1078.
18. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 2007; 293: E444-E452.
19. Sellayah D, Bharaj P, Sikder D. Orexin is required for brown adipose tissue development, differentiation, and function. Cell Metab 2011; 14: 478-490.
20. Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, et al. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012; 481: 463-468.
21. Sanchez-Gurmaches J, Hung CM, Sparks CA, Tang Y, Li H, Guertin DA. PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metab 2012; 16: 348-362.
22. Ortega-Molina A, Efeyan A, Lopez-Guadamillas E, Munoz-Martin M, Gomez-Lopez G, Canamero M, et al. PTEN positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab 2012; 15: 382-394.
23. Jimenez-Preitner M, Berney X, Uldry M, Vitali A, Cinti S, Ledford JG, et al. Plac8 is an inducer of C/EBPbeta required for brown fat differentiation, thermoregulation, and control of body weight. Cell Metab 2012; 14: 658-670.
24. Gburcik V, Cawthorn WP, Nedergaard J, Timmons JA, Cannon B. An essential role for Tbx15 in the differentiation of brown and "brite" but not white adipocytes. Am J Physiol Endocrinol Metab 2012; 303: E1053-E1060.
25. Ohno H, Shinoda K, Spiegelman BM, Kajimura S. PPARgamma agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab 2012; 15: 395-404.
26. Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012; 150: 366-376.
27. Aghamohammadzadeh R, Heagerty AM. Obesity-related hypertension: Epidemiology, pathophysiology, treatments, and the contribution of perivascular adipose tissue. Ann Med 2012; 44(Suppl 1): S74-S84.
28. Fitzgibbons TP, Kogan S, Aouadi M, Hendricks GM, Straubhaar J, Czech MP. Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation. Am J Physiol Heart Circ Physiol 2011; 301: H1425-H1437.
29. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med 2012; 17: 200-205.
30. Ross R. The pathogenesis of atherosclerosis: A perspective for the 1990 s. Nature 1993; 362: 801-809.
31. Scott NA, Cipolla GD, Ross CE, Dunn B, Martin FH, Simonet L, et al. Identification of a potential role for the adventitia in vascular lesion formation after balloon overstretch injury of porcine coronary arteries. Circulation 1996; 93: 2178-2187.
32. Wilcox JN, Okamoto EI, Nakahara KI, Vinten-Johansen J. Perivascular responses after angioplasty which may contribute to postangioplasty restenosis: A role for circulating myofibroblast precursors? Ann NY Acad Sci 2001; 947: 68-90; Discussion 90-92.
33. Okamoto E, Couse T, De Leon H, Vinten-Johansen J, Goodman RB, Scott NA, et al. Perivascular inflammation after balloon angioplasty of porcine coronary arteries. Circulation 2001; 104: 2228-2235.
34. Takaoka M, Suzuki H, Shioda S, Sekikawa K, Saito Y, Nagai R, et al. Endovascular injury induces rapid phenotypic changes in perivascular adipose tissue. Arterioscler Thromb Vasc Biol 2010; 30: 1576-1582.
35. Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G, et al. Proinflammatory phenotype of perivascular adipocytes: Influence of high-fat feeding. Circ Res 2009; 104: 541-549.
36. Henrichot E, Juge-Aubry CE, Pernin A, Pache JC, Velebit V, Dayer JM, et al. Production of chemokines by perivascular adipose tissue: A role in the pathogenesis of atherosclerosis? Arterioscler Thromb Vasc Biol 2005; 25: 2594-2599.
37. Ohman MK, Luo W, Wang H, Guo C, Abdallah W, Russo HM, et al. Perivascular visceral adipose tissue induces atherosclerosis in apolipoprotein E deficient mice. Atherosclerosis 2011; 219: 33-39.
38. Verhagen SN, Vink A, van der Graaf Y, Visseren FL. Coronary perivascular adipose tissue characteristics are related to atherosclerotic plaque size and composition: A post-mortem study. Atherosclerosis 2012; 225: 99-104.
39. Rittig K, Dolderer JH, Balletshofer B, Machann J, Schick F, Meile T, et al. The secretion pattern of perivascular fat cells is different from that of subcutaneous and visceral fat cells. Diabetologia 2012; 55: 1514-1525.
40. Hennig B, Chow CK. Lipid peroxidation and endothelial cell injury: Implications in atherosclerosis. Free Radic Biol Med 1988; 4: 99-106.
41. Balogh L, Donhoffer S, Mestyan G, Pap T, Toth I. The effect of environmental temperature on the O2-consumption and body temperature of rats under the acute action of some drugs affecting en ergy exchange and body temperature. Acta Physiol Hung 1952; 3: 367-375.
42. Dawkins MJ, Scopes JW. Non-shivering thermogenesis and brown adipose tissue in the human new-born infant. Nature 1965; 206: 201-202.
43. Drettner B. Vascular reactions on the intake of food and drink of various temperatures. Acta Otolaryngol Suppl 1964; 188(Suppl): 249+.
44. Robinson S. Physiological effects of heat and cold. Annu Rev Physiol 1952; 14: 73-96.
45. Zeman V, Novak J, Holecek V. Blood pressure response to swimming in icy and warm water in individuals adapted to cold. Cas Lek Cesk 1982; 121: 1035-1038.(in Czech).
46. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009; 360: 1500-1508.
47. Verhagen SN, Visseren FL. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis 2011; 214: 3-10.
48. Takemori K, Gao YJ, Ding L, Lu C, Su LY, An WS, et al. Elevated blood pressure in transgenic lipoatrophic mice and altered vascular function. Hypertension 2007; 49: 365-372.
49. Marchesi C, Ebrahimian T, Angulo O, Paradis P, Schiffrin EL. Endothelial nitric oxide synthase uncoupling and perivascular adipose oxidative stress and inflammation contribute to vascular dysfunction in a rodent model of metabolic syndrome. Hypertension 2009; 54: 1384-1392.
50. Gil-Ortega M, Stucchi P, Guzman-Ruiz R, Cano V, Arribas S, Gonzalez MC, et al. Adaptative nitric oxide overproduction in perivascular adipose tissue during early diet-induced obesity. Endocrinology 2010; 151: 3299-3306.
51. Ma L, Ma S, He H, Yang D, Chen X, Luo Z, et al. Perivascular fatmediated vascular dysfunction and remodeling through the AMPK/mTOR pathway in high-fat diet-induced obese rats. Hypertens Res 2010; 33: 446-453.
52. Payne GA, Borbouse L, Kumar S, Neeb Z, Alloosh M, Sturek M, et al. Epicardial perivascular adipose-derived leptin exacerbates coronary endothelial dysfunction in metabolic syndrome via a protein kinase C-beta pathway. Arterioscler Thromb Vasc Biol 2010; 30: 1711-1717.
53. Bunker AK, Laughlin MH. Influence of exercise and perivascular adipose tissue on coronary artery vasomotor function in a familial hypercholesterolemic porcine atherosclerosis model. J Appl Physiol 2010; 108: 490-497.
54. Galvez-Prieto B, Somoza B, Gil-Ortega M, Garcia-Prieto CF, de Las Heras AI, Gonzalez MC, et al. Anticontractile effect of perivascular adipose tissue and leptin are reduced in hypertension. Front Pharmacol 2012; 3: 103.
55. Lu C, Su LY, Lee RM, Gao YJ. Alterations in perivascular adipose tissue structure and function in hypertension. Eur J Pharmacol 2011; 656: 68-73.
56. Zeng ZH, Zhang ZH, Luo BH, He WK, Liang LY, He CC, et al. The functional changes of the perivascular adipose tissue in spontaneously hypertensive rats and the effects of atorvastatin therapy. Clin Exp Hypertens 2009; 31: 355-363.
57. Galvez B, de Castro J, Herold D, Dubrovska G, Arribas S, Gonzalez MC, et al. Perivascular adipose tissue and mesenteric vascular function in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 2006; 26: 1297-1302.
58. Fesus G, Dubrovska G, Gorzelniak K, Kluge R, Huang Y, Luft FC, et al. Adiponectin is a novel humoral vasodilator. Cardiovasc Res 2007; 75: 719-727.
59. Xu A, Wang Y, Lam KS, Vanhoutte PM. Vascular actions of adipokines molecular mechanisms and therapeutic implications. Adv Pharmacol 2010; 60: 229-255.
60. Wojcicka G, Jamroz-Wisniewska A, Atanasova P, Chaldakov GN, Chylinska-Kula B, Beltowski J. Differential effects of statins on endogenous H2S formation in perivascular adipose tissue. Pharmacol Res 2011; 63: 68-76.
61. Gao YJ, Lu C, Su LY, Sharma AM, Lee RM. Modulation of vascular function by perivascular adipose tissue: The role of endothelium and hydrogen peroxide. Br J Pharmacol 2007; 151: 323-331.
62. Lee RM, Lu C, Su LY, Gao YJ. Endothelium-dependent relaxation factor released by perivascular adipose tissue. J Hypertens 2009; 27: 782-790.
63. Lee YC, Chang HH, Chiang CL, Liu CH, Yeh JI, Chen MF, et al. Role of perivascular adipose tissue-derived methyl palmitate in vascular tone regulation and pathogenesis of hypertension. Circulation 2011; 124: 1160-1171.
64. Hermenegildo C, Oviedo PJ, Garcia-Perez MA, Tarin JJ, Cano A. Effects of phytoestrogens genistein and daidzein on prostacyclin production by human endothelial cells. J Pharmacol Exp Ther 2005; 315: 722-728.
65. -/- knockout mice. J Cardiovasc Pharmacol 2005; 46: 761-765.
66. Galvez-Prieto B, Bolbrinker J, Stucchi P, de Las Heras AI, Merino B, Arribas S, et al. Comparative expression analysis of the reninangiotensin system components between white and brown perivascular adipose tissue. J Endocrinol 2008; 197: 55-64.
67. Soltis EE, Cassis LA. Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin Exp Hypertens A 1991; 13: 277-296.
68. Lu C, Su LY, Lee RM, Gao YJ. Mechanisms for perivascular adipose tissue-mediated potentiation of vascular contraction to perivascular neuronal stimulation: The role of adipocyte-derived angiotensin II. Eur J Pharmacol 2010; 634: 107-112.
69. Mamiya Y, Suzuki M, Namima M, Ouno H. The influence of the sympathetic nervous system on brown adipose tissue: An experimental and histopathologic study on aging. Nihon Naibunpi Gakkai Zasshi 1991; 67: 1252-1262. (in Japanese).
70. Gao YJ, Takemori K, Su LY, An WS, Lu C, Sharma AM, et al. Perivascular adipose tissue promotes vasoconstriction: The role of superoxide anion. Cardiovasc Res 2006; 71: 363-373.
71. Moitra J, Mason MM, Olive M, Krylov D, Gavrilova O, Marcus-Samuels B, et al. Life without white fat: A transgenic mouse. Genes Dev 1998; 12: 3168-3181.
72. Duan SZ, Ivashchenko CY, Whitesall SE, D'Alecy LG, Duquaine DC, Brosius FC 3rd, et al. Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J Clin Invest 2007; 117: 812-822.
73. Wang N, Yang G, Jia Z, Zhang H, Aoyagi T, Soodvilai S, et al. Vascular PPARgamma controls circadian variation in blood pressure and heart rate through Bmal1. Cell Metab 2008; 8: 482-491.
74. Halabi CM, Beyer AM, de Lange WJ, Keen HL, Baumbach GL, Faraci FM, et al. Interference with PPAR gamma function in smooth muscle causes vascular dysfunction and hypertension. Cell Metab 2008; 7: 215-226.