The role of perivascular adipose tissue in vasoconstriction, arterial stiffness, and aneurysm

Hormone Molecular Biology and Clinical Investigation

Volumn 21, Issue 2, 2015, Pages 137-147

  Villacorta, Luis ^a   Chang, Lin ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

aneurysm; arterial stiffness; endothelial dysfunction; perivascular adipose tissue; vascular calcification

Indexed keywords

ADIPOSE TISSUE; ANEURYSM; ARTERIAL STIFFNESS; BLOOD VESSEL CALCIFICATION; CARDIOVASCULAR DISEASE; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; HEART MUSCLE CONTRACTILITY; HUMAN; NEOINTIMA; NONHUMAN; PERIVASCULAR ADIPOSE TISSUE; PRIORITY JOURNAL; REVIEW; VASOCONSTRICTION; ANIMAL; INFLAMMATION; METABOLISM; PATHOLOGY;

ADIPOSE TISSUE; ANEURYSM; ANIMALS; CARDIOVASCULAR DISEASES; HUMANS; INFLAMMATION; VASCULAR CALCIFICATION; VASCULAR STIFFNESS; VASOCONSTRICTION;

EID: 84928649039     PISSN: 18681883     EISSN: 18681891     Source Type: Journal    
DOI: 10.1515/hmbci-2014-0048     Document Type: Review

References (81)

1. Karpe F, Pinnick KE. Biology of upper-body and lower-body adipose tissue-link to whole-body phenotypes. Nat Rev Endocrinol 2015;11:90-100.
2. Bastien M, Poirier P, Lemieux I, Despres JP. Overview of epidemiology and contribution of obesity to cardiovascular disease. Prog Cardiovasc Dis 2014;56:369-81.
3. Fenzl A, Kiefer FW. Brown adipose tissue and thermogenesis. Horm Mol Biol Clin Investig 2014;19:25-37.
4. Cereijo R, Giralt M, Villarroya F. Thermogenic brown and beige/ brite adipogenesis in humans. Ann Med 2014:1-9. doi:10.3109/07853890.2014.952328.
5. Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P, Spiegelman BM. Beige adipocytes are a distinct type of thermo-genic fat cell in mouse and human. Cell 2012;150:366-76.
6. Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adi-pocytes: is beige the new brown? Genes Dev 2013;27:234-50.
7. Jespersen NZ, Larsen TJ, Peijs L, Daugaard S, Homoe P, Loft A, de Jong J, Mathur N, Cannon B, Nedergaard J, Pedersen BK, Moller K, Scheele C. A classical brown adipose tissue mrna signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab 2013;17:798-805.
8. Garg A. Gender differences in the prevalence of metabolic complications in familial partial lipodystrophy (Dunnigan variety). J Clin Endocrinol Metab 2000;85:1776-82.
9. Moitra J, Mason MM, Olive M, Krylov D, Gavrilova O, Marcus-Samuels B, Feigenbaum L, Lee E, Aoyama T, Eckhaus M, Reitman ML, Vinson C. Life without white fat: a transgenic mouse. Genes Dev 1998;12:3168-81.
10. Pajvani UB, Trujillo ME, Combs TP, Iyengar P, Jelicks L, Roth KA, Kitsis RN, Scherer PE. Fat apoptosis through targeted activation of caspase 8: a new mouse model of inducible and reversible lipoatrophy. Nat Med 2005;11:797-803.
11. Duan SZ, Ivashchenko CY, Whitesall SE, D'Alecy LG, Duquaine DC, Brosius FC 3rd, Gonzalez FJ, Vinson C, Pierre MA, Milstone DS, Mortensen RM. Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J Clin Invest 2007;117:812-22.
12. Vernochet C, Damilano F, Mourier A, Bezy O, Mori MA, Smyth G, Rosenzweig A, Larsson NG, Kahn CR. Adipose tissue mito-chondrial dysfunction triggers a lipodystrophic syndrome with insulin resistance, hepatosteatosis, and cardiovascular complications. FASEB J 2014;28:4408-19.
13. Bartesaghi S, Hallen S, Huang L, Svensson PA, Momo RA, Wallin S, Carlsson EK, Forslow A, Seale P, Peng XR. Thermogenic activity of UCP1 in human white fat-derived beige adipocytes. Mol Endocrinol 2015;29:130-9.
14. Cherian S, Lopaschuk GD, Carvalho E. Cellular cross-talk between epicardial adipose tissue and myocardium in relation to the pathogenesis of cardiovascular disease. Am J Physiol Endocrinol Metab 2012;303:E937-49.
15. Iozzo P. Myocardial, perivascular, and epicardial fat. Diabetes Care 2011;34 Suppl 2:S371-9.
16. Chang L, Milton H, Eitzman DT, Chen YE. Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension. Circ J 2013;77:11-8.
17. Lim S, Meigs JB. Links between ectopic fat and vascular disease in humans. Arterioscler Thromb Vasc Biol 2014;34:1820-6.
18. Brown NK, Zhou Z, Zhang J, Zeng R, Wu J, Eitzman DT, Chen YE, Chang L. Perivascular adipose tissue in vascular function and disease: a review of current research and animal models. Arte-rioscler Thromb Vasc Biol 2014;34:1621-30.
19. Manka D, Chatterjee TK, Stoll LL, Basford JE, Konaniah ES, Srinivasan R, Bogdanov VY, Tang Y, Blomkalns AL, Hui DY, Weintraub NL. Transplanted perivascular adipose tissue accelerates injury-induced neointimal hyperplasia: role of monocyte chemoattractant protein-1. Arterioscler Thromb Vasc Biol 2014;34:1723-30.
20. Omar A, Chatterjee TK, Tang Y, Hui DY, Weintraub NL. Proinflam-matory phenotype of perivascular adipocytes. Arterioscler Thromb Vasc Biol 2014;34:1631-6.
21. Owen MK, Noblet JN, Sassoon DJ, Conteh AM, Goodwill AG, Tune JD. Perivascular adipose tissue and coronary vascular disease. Arterioscler Thromb Vasc Biol 2014;34:1643-9.
22. Tano JY, Schleifenbaum J, Gollasch M. Perivascular adipose tissue, potassium channels, and vascular dysfunction. Arterioscler Thromb Vasc Biol 2014;34:1827-30.
23. Withers SB, Bussey CE, Saxton SN, Melrose HM, Watkins AE, Heagerty AM. Mechanisms of adiponectin-associated perivas-cular function in vascular disease. Arterioscler Thromb Vasc Biol 2014;34:1637-42.
24. Egawa G, Miyachi Y, Kabashima K. Identification of perivascular adipose tissue in the mouse skin using two-photon microscopy. J Dermatol Sci 2013;70:139-40.
25. Chang L, Villacorta L, Li R, Hamblin M, Xu W, Dou C, Zhang J, Wu J, Zeng R, Chen YE. Loss of perivascular adipose tissue on peroxisome proliferator-activated receptor-gamma deletion in smooth muscle cells impairs intravascular thermoregulation and enhances atherosclerosis. Circulation 2012;126:1067-78.
26. 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:H1425-37.
27. Padilla J, Jenkins NT, Vieira-Potter VJ, Laughlin MH. Divergent phenotype of rat thoracic and abdominal perivascular adipose tissues. Am J Physiol Regul Integr Comp Physiol 2013;304:R543-52.
28. Mauro CR, Ilonzo G, Nguyen BT, Yu P, Tao M, Gao I, Seidman MA, Nguyen LL, Ozaki CK. Attenuated adiposopathy in perivascular adipose tissue compared with subcutaneous human adipose tissue. Am J Surg 2013;206:241-4.
29. Claria J, Nguyen BT, Madenci AL, Ozaki CK, Serhan CN. Diversity of lipid mediators in human adipose tissue depots. Am J Physiol Cell Physiol 2013;304:C1141-9.
30. 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.
31. Lynch FM, Withers SB, Yao Z, Werner ME, Edwards G, Weston AH, Heagerty AM. Perivascular adipose tissue-derived adiponectin activates BK(Ca) channels to induce anticontractile responses. Am J Physiol Heart Circ Physiol 2013;304:H786-95.
32. Kohn C, Schleifenbaum J, Szijarto IA, Marko L, Dubrovska G, Huang Y, Gollasch M. Differential effects of cystathionine-gamma-lyase-dependent vasodilatory H2S in periadven-titial vasoregulation of rat and mouse aortas. PLoS ONE 2012;7:e41951.
33. Lee RM, Bader M, Alenina N, Santos RA, Gao YJ, Lu C. Mas receptors in modulating relaxation induced by perivascular adipose tissue. Life Sci 2011;89:467-72.
34. Lee YC, Chang HH, Chiang CL, Liu CH, Yeh JI, Chen MF, Chen PY, Kuo JS, Lee TJ. Role of perivascular adipose tissue-derived methyl palmitate in vascular tone regulation and pathogenesis of hypertension. Circulation 2011;124:1160-71.
35. Szasz T, Bomfim GF, Webb RC. The influence of perivascular adipose tissue on vascular homeostasis. Vasc Health Risk Manag 2013;9:105-16.
36. Beltowski J. Endogenous hydrogen sulfide in perivascular adipose tissue: role in the regulation of vascular tone in physiology and pathology. Can J Physiol Pharmacol 2013;91:889-98.
37. Aghamohammadzadeh R, Withers S, Lynch F, Greenstein A, Malik R, Heagerty A. Perivascular adipose tissue from human systemic and coronary vessels: the emergence of a new phar-macotherapeutic target. Br J Pharmacol 2012;165:670-82.
38. Malinowski M, Deja MA, Janusiewicz P, Golba KS, Roleder T, Wos S. Mechanisms of vasodilatatory effect of perivascular tissue of human internal thoracic artery. J Physiol Pharmacol 2013;64:309-16.
39. Ozen G, Topal G, Gomez I, Ghorreshi A, Boukais K, Benyahia C, Kanyinda L, Longrois D, Teskin O, Uydes-Dogan BS, Norel X. Control of human vascular tone by prostanoids derived from perivascular adipose tissue. Prostaglandins Other Lipid Mediat 2013;107:13-7.
40. Aghamohammadzadeh R, Greenstein AS, Yadav R, Jeziorska M, Hama S, Soltani F, Pemberton PW, Ammori B, Malik RA, Soran H, Heagerty AM. Effects of bariatric surgery on human small artery function: evidence for reduction in perivascular adipocyte inflammation, and the restoration of normal anticontractile activity despite persistent obesity. J Am Coll Cardiol 2013;62:128-35.
41. Withers SB, Simpson L, Fattah S, Werner ME, Heagerty AM. cGMP-dependent protein kinase (PKG) mediates the anticontractile capacity of perivascular adipose tissue. Cardiovasc Res 2014;101:130-7.
42. Weston AH, Egner I, Dong Y, Porter EL, Heagerty AM, Edwards G. Stimulated release of a hyperpolarizing factor (ADHF) from mesenteric artery perivascular adipose tissue: involvement of myocyte BKCa channels and adiponectin. Br J Pharmacol 2013;169:1500-9.
43. Chang L, Villacota L, Dou C, Chen E, Zhang J. Perivascular adipose tissue-derived prostaglandins constrict vessel [abstract]. Hypertension 2012;60:A662.
44. Wilson C. Recent advances in hypertension. Can Med Assoc J 1964;91:964-70.
45. Ayala-Lopez N, Martini M, Jackson WF, Darios E, Burnett R, Seitz B, Fink GD, Watts SW. Perivascular adipose tissue contains functional catecholamines. Pharmacol Res Perspect 2014;2:e00041.
46. Meyer MR, Fredette NC, Barton M, Prossnitz ER. Regulation of vascular smooth muscle tone by adipose-derived contracting factor. PLoS ONE 2013;8:e79245.
47. Mendizabal Y, Llorens S, Nava E. Vasoactive effects of pros-taglandins from the perivascular fat of mesenteric resistance arteries in WKY and SHROB rats. Life Sci 2013;93:1023-32.
48. Owen MK, Witzmann FA, McKenney ML, Lai X, Berwick ZC, Moberly SP, Alloosh M, Sturek M, Tune JD. Perivascular adipose tissue potentiates contraction of coronary vascular smooth muscle: influence of obesity. Circulation 2013;128:9-18.
49. Lee MH, Chen SJ, Tsao CM, Wu CC. Perivascular adipose tissue inhibits endothelial function of rat aortas via caveolin-1. PLoS ONE 2014;9:e99947.
50. Watts SW, Dorrance AM, Penfold ME, Rourke JL, Sinal CJ, Seitz B, Sullivan TJ, Charvat TT, Thompson JM, Burnett R, Fink GD. Chemerin connects fat to arterial contraction. Arterioscler Thromb Vasc Biol 2013;33:1320-8.
51. Hai-Mei L, Song-Yin H, Run-Mei L, Xiao-Huang X, Le-Quan Z, Xiao-Ping L, Jin-Wen X. Andrographolide protects against lipopolysaccharide-induced vascular hyporeactivity by suppressing the expression of inducible nitric oxide in periaortic adipose. J Cardiovasc Pharmacol 2013;62:154-9.
52. Gil-Ortega M, Condezo-Hoyos L, Garcia-Prieto CF, Arribas SM, Gonzalez MC, Aranguez I, Ruiz-Gayo M, Somoza B, Fernandez-Alfonso MS. Imbalance between pro and anti-oxidant mechanisms in perivascular adipose tissue aggravates long-term high-fat diet-derived endothelial dysfunction. PLoS ONE 2014;9:e95312.
53. Chen Y, Wang X, Mai J, Zhao X, Liang Y, Gu M, Chen Z, Nie R, Wang J. C-reactive protein promotes vascular endothelial dysfunction partly via activating adipose tissue inflammation in hyperlipidemic rabbits. Int J Cardiol 2013;168:2397-403.
54. Virdis A, Duranti E, Rossi C, Dell'agnello U, Santini E, Anselmino M, Chiarugi M, Taddei S, Solini A. Tumour necrosis factor-alpha participates on the endothelin-1/nitric oxide imbalance in small arteries from obese patients: role of perivascular adipose tissue. Eur Heart J 2014. doi: 10.1093/eurheartj/ehu072.
55. Wang D, Wang C, Wu X, Zheng W, Sandberg K, Ji H, Welch WJ, Wilcox CS. Endothelial dysfunction and enhanced contractility in microvessels from ovariectomized rats: roles of oxidative stress and perivascular adipose tissue. Hypertension 2014;63:1063-9.
56. Schrammel A, Mussbacher M, Wolkart G, Stessel H, Pail K, Winkler S, Schweiger M, Haemmerle G, Al Zoughbi W, Hofler G, Lametschwandtner A, Zechner R, Mayer B. Endothelial dysfunction in adipose triglyceride lipase deficiency. Biochim Biophys Acta 2014;1841:906-17.
57. Bhattacharya I, Dragert K, Albert V, Contassot E, Damjanovic M, Hagiwara A, Zimmerli L, Humar R, Hall MN, Battegay EJ, Haas E. Rictor in perivascular adipose tissue controls vascular function by regulating inflammatory molecule expression. Arterioscler Thromb Vasc Biol 2013;33:2105-11.
58. Moe KT, Naylynn TM, Yin NO, Khairunnisa K, Allen JC, Wong MC, Chin-Dusting J, Wong P. Tumor necrosis factor-alpha induces aortic intima-media thickening via perivascular adipose tissue inflammation. J Vasc Res 2013;50:228-37.
59. Schroeter MR, Eschholz N, Herzberg S, Jerchel I, Leifheit-Nestler M, Czepluch FS, Chalikias G, Konstantinides S, Schafer K. Leptin-dependent and leptin-independent paracrine effects of perivascular adipose tissue on neointima formation. Arterio-scler Thromb Vasc Biol 2013;33:980-7.
60. Tian Z, Miyata K, Tazume H, Sakaguchi H, Kadomatsu T, Horio E, Takahashi O, Komohara Y, Araki K, Hirata Y, Tabata M, Takanashi S, Takeya M, Hao H, Shimabukuro M, Sata M, Kawasuji M, Oike Y. Perivascular adipose tissue-secreted angiopoietin-like protein 2 (Angptl2) accelerates neointimal hyperplasia after endovascular injury. J Mol Cell Cardiol 2013;57:1-12.
61. Bailey-Downs LC, Tucsek Z, Toth P, Sosnowska D, Gautam T, Sonntag WE, Csiszar A, Ungvari Z. Aging exacerbates obesity-induced oxidative stress and inflammation in perivascular adipose tissue in mice: a paracrine mechanism contributing to vascular redox dysregulation and inflammation. J Gerontol A Biol Sci Med Sci 2013;68:780-92.
62. Leopold JA. MicroRNAs regulate vascular medial calcification. Cells 2014;3:963-80.
63. Greenland P, Bonow RO, Brundage BH, Budoff MJ, Eisenberg MJ, Grundy SM, Lauer MS, Post WS, Raggi P, Redberg RF, Rodgers GP, Shaw LJ, Taylor AJ, Weintraub WS, Harrington RA, Abrams J, Anderson JL, Bates ER, Grines CL, Hlatky MA, Lichtenberg RC, Lindner JR, Pohost GM, Schofield RS, Shubrooks SJ Jr, Stein JH, Tracy CM, Vogel RA, Wesley DJ; American College of Cardiology Foundation Clinical Expert Consensus Task Force; Society of Atherosclerosis Imaging and Prevention; Society of Cardiovascular Computed Tomography. ACCF/AHA 2007 clinical expert consensus document on coronary artery calcium scoring by computed tomography in global cardiovascular risk assessment and in evaluation of patients with chest pain: a report of the American College of Cardiology Foundation Clinical Expert Consensus Task Force (ACCF/AHA Writing Committee to update the 2000 expert consensus document on electron beam computed tomography). Circulation 2007;115:402-26.
64. Paloian NJ, Giachelli CM. A current understanding of vascular calcification in CKD. Am J Physiol Renal Physiol 2014;307: F891-900.
65. Lehman SJ, Massaro JM, Schlett CL, O'Donnell CJ, Hoffmann U, Fox CS. Peri-aortic fat, cardiovascular disease risk factors, and aortic calcification: the Framingham Heart Study. Atherosclerosis 2010;210:656-61.
66. Shields KJ, Barinas-Mitchell E, Gingo MR, Tepper P, Goodpaster BH, Kao AH, Manzi S, Sutton-Tyrrell K. Perivascular adipose tissue of the descending thoracic aorta is associated with systemic lupus erythematosus and vascular calcification in women. Atherosclerosis 2013;231:129-35.
67. Longenecker CT, Jiang Y, Yun CH, Debanne S, Funderburg NT, Lederman MM, Storer N, Labbato DE, Bezerra HG, McComsey GA. Perivascular fat, inflammation, and cardiovascular risk in HIV-infected patients on antiretroviral therapy. Int J Cardiol 2013;168:4039-45.
68. Seifalian AM, Filippatos TD, Joshi J, Mikhailidis DP. Obesity and arterial compliance alterations. Curr Vasc Pharmacol 2010;8:155-68.
69. Selcuk A, Bulucu F, Kalafat F, Cakar M, Demirbas S, Karaman M, Ay SA, Saglam K, Balta S, Demirkol S, Arslan E. Skinfold thickness as a predictor of arterial stiffness: obesity and fatness linked to higher stiffness measurements in hypertensive patients. Clin Exp Hypertens 2013;35:459-64.
70. Thanassoulis G, Massaro JM, Corsini E, Rogers I, Schlett CL, Meigs JB, Hoffmann U, O'Donnell CJ, Fox CS. Periaortic adipose tissue and aortic dimensions in the Framingham Heart Study. J Am Heart Assoc 2012;1:e000885.
71. Fox CS, Massaro JM, Schlett CL, Lehman SJ, Meigs JB, O'Donnell CJ, Hoffmann U, Murabito JM. Periaortic fat deposition is associated with peripheral arterial disease: the Framingham Heart Study. Circ Cardiovasc Imaging 2010;3:515-9.
72. Liu Y, Dang C, Garcia M, Gregersen H, Kassab GS. Surrounding tissues affect the passive mechanics of the vessel wall: theory and experiment. Am J Physiol Heart Circ Physiol 2007;293:H3290-300.
73. Kim J, Peruski B, Hunley C, Kwon S, Baek S. Influence of surrounding tissues on biomechanics of aortic wall. Int J Exp Comput Biomech 2013;2:105-17.
74. Aroor AR, Demarco VG, Jia G, Sun Z, Nistala R, Meininger GA, Sowers JR. The role of tissue renin-angiotensin-aldosterone system in the development of endothelial dysfunction and arterial stiffness. Front Endocrinol (Lausanne) 2013;4:161.
75. Fleenor BS, Eng JS, Sindler AL, Pham BT, Kloor JD, Seals DR. Superoxide signaling in perivascular adipose tissue promotes age-related artery stiffness. Aging Cell 2014;13:576-8.
76. Chen JY, Tsai PJ, Tai HC, Tsai RL, Chang YT, Wang MC, Chiou YW, Yeh ML, Tang MJ, Lam CF, Shiesh SC, Li YH, Tsai WC, Chou CH, Lin LJ, Wu HL, Tsai YS. Increased aortic stiffness and attenuated lysyl oxidase activity in obesity. Arterioscler Thromb Vasc Biol 2013;33:839-46.
77. Britton KA, Wang N, Palmisano J, Corsini E, Schlett CL, Hoffmann U, Larson MG, Vasan RS, Vita JA, Mitchell GF, Benjamin EJ, Hamburg NM, Fox CS. Thoracic periaortic and visceral adipose tissue and their cross-sectional associations with measures of vascular function. Obesity (Silver Spring) 2013;21:1496-503.
78. Blomkalns AL, Gavrila D, Thomas M, Neltner BS, Blanco VM, Benjamin SB, McCormick ML, Stoll LL, Denning GM, Collins SP, Qin Z, Daugherty A, Cassis LA, Thompson RW, Weiss RM, Lindower PD, Pinney SM, Chatterjee T, Weintraub NL. CD14 directs adventitial macrophage precursor recruitment: role in early abdominal aortic aneurysm formation. J Am Heart Assoc 2013;2:e000065.
79. Li MW, Mian MO, Barhoumi T, Rehman A, Mann K, Paradis P, Schiffrin EL. Endothelin-1 overexpression exacerbates atherosclerosis and induces aortic aneurysms in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 2013;33:2306-15.
80. 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;204:2449-60.
81. Kurobe H, Hirata Y, Matsuoka Y, Sugasawa N, Higashida M, Nakayama T, Maxfield MW, Yoshida Y, Shimabukuro M, Kitagawa T, Sata M. Protective effects of selective mineralocorticoid receptor antagonist against aortic aneurysm progression in a novel murine model. J Surg Res 2013;185:455-62.