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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Mini-Review Article

Modulation of Vascular Function by Perivascular Adipose Tissue: Sex Differences

Author(s): Jamaira A. Victorio, Rafael M. da Costa, Rita C. Tostes and Ana P. Davel*

Volume 26, Issue 30, 2020

Page: [3768 - 3777] Pages: 10

DOI: 10.2174/1381612826666200701211912

Price: $65

Abstract

In addition to the endothelium, the perivascular adipose tissue (PVAT) has been described to be involved in the local modulation of vascular function by synthetizing and releasing vasoactive factors. Under physiological conditions, PVAT has anticontractile and anti-inflammatory effects. However, in the context of hypertension, obesity and type 2 diabetes, the PVAT pattern of anticontractile adipokines is altered, favoring oxidative stress, inflammation and, consequently, vascular dysfunction. Therefore, dysfunctional PVAT has become a target for therapeutic intervention in cardiometabolic diseases. An increasing number of studies have revealed sex differences in PVAT morphology and in the modulatory effects of PVAT on endothelial function and vascular tone. Moreover, distinct mechanisms underlying PVAT dysfunction may account for vascular abnormalities in males and females. Therefore, targeting sex-specific mechanisms of PVAT dysfunction in cardiovascular diseases is an evolving strategy for cardiovascular protection.

Keywords: Perivascular adipose tissue, sex differences, obesity, hypertension, diabetes, cardiovascular.

« Previous
[1]
Beery AK, Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 2011; 35(3): 565-72.
[http://dx.doi.org/10.1016/j.neubiorev.2010.07.002] [PMID: 20620164]
[2]
Shansky RM. Are hormones a “female problem” for animal research? Sciene 2019; 364(6443): 825-6.
[3]
Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature 2014; 509(7500): 282-3.
[http://dx.doi.org/10.1038/509282a] [PMID: 24834516]
[4]
Machida T, Yonezawa Y, Noumura T. Age-associated changes in plasma testosterone levels in male mice and their relation to social dominance or subordinance. Horm Behav 1981; 15(3): 238-45.
[http://dx.doi.org/10.1016/0018-506X(81)90013-1] [PMID: 7298026]
[5]
World Health Organization Obesity and overweight Available at:. https://www.who.int/en/news-room/fact-sheets/detail/obesity-andoverweight2019
[6]
World Health Organization Hypertension Available at:. https://www.who.int/news-room/fact-sheets/detail/hypertension2020
[7]
Lima R, Wofford M, Reckelhoff JF. Hypertension in postmenopausal women. Curr Hypertens Rep 2012; 14(3): 254-60.
[http://dx.doi.org/10.1007/s11906-012-0260-0] [PMID: 22427070]
[8]
Freedman RR, Sabharwal SC, Desai N. Sex differences in peripheral vascular adrenergic receptors. Circ Res 1987; 61(4): 581-5.
[http://dx.doi.org/10.1161/01.RES.61.4.581] [PMID: 3652401]
[9]
Christou DD, Jones PP, Jordan J, Diedrich A, Robertson D, Seals DR. Women have lower tonic autonomic support of arterial blood pressure and less effective baroreflex buffering than men. Circulation 2005; 111(4): 494-8.
[http://dx.doi.org/10.1161/01.CIR.0000153864.24034.A6] [PMID: 15687139]
[10]
Tipton AJ, Sullivan JC. Sex differences in T cells in hypertension. Clin Ther 2014; 36(12): 1882-900.
[http://dx.doi.org/10.1016/j.clinthera.2014.07.011] [PMID: 25134971]
[11]
Hamburg NM, Palmisano J, Larson MG, et al. Relation of brachial and digital measures of vascular function in the community: the Framingham heart study. Hypertension 2011; 57(3): 390-6.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.110.160812] [PMID: 21263120]
[12]
Mudrovcic N, Arefin S, Van Craenenbroeck AH, Kublickiene K. Endothelial maintenance in health and disease: Importance of sex differences. Pharmacol Res 2017; 119: 48-60.
[http://dx.doi.org/10.1016/j.phrs.2017.01.011] [PMID: 28108363]
[13]
Soltis EE, Cassis LA. Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin Exp Hypertens A 1991; 13(2): 277-96.
[http://dx.doi.org/10.3109/10641969109042063] [PMID: 2065467]
[14]
Gao YJ. Dual modulation of vascular function by perivascular adipose tissue and its potential correlation with adiposity/lipoatrophy-related vascular dysfunction. Curr Pharm Des 2007; 13(21): 2185-92.
[http://dx.doi.org/10.2174/138161207781039634] [PMID: 17627551]
[15]
Contreras GA, Thelen K, Ayala-Lopez N, Watts SW. The distribution and adipogenic potential of perivascular adipose tissue adipocyte progenitors is dependent on sexual dimorphism and vessel location. Physiol Rep 2016; 4(19): 4.
[http://dx.doi.org/10.14814/phy2.12993] [PMID: 27738018]
[16]
Ahmad AA, Randall MD, Roberts RE. Sex differences in the role of phospholipase A2 -dependent arachidonic acid pathway in the perivascular adipose tissue function in pigs. J Physiol 2017; 595(21): 6623-34.
[http://dx.doi.org/10.1113/JP274831] [PMID: 28877347]
[17]
Small HY, McNeilly S, Mary S, Sheikh AM, Delles C. Resistin mediates sex-dependent effects of perivascular adipose tissue on vascular function in the Shrsp. Sci Rep 2019; 9(1): 6897.
[http://dx.doi.org/10.1038/s41598-019-43326-z]
[18]
Friederich-Persson M, Nguyen Dinh Cat A, Persson P, Montezano AC, Touyz RM. Brown adipose tissue regulates small artery function through NADPH oxidase 4-derived hydrogen peroxide and redox-sensitive protein kinase G-1α. Arterioscler Thromb Vasc Biol 2017; 37(3): 455-65.
[http://dx.doi.org/10.1161/ATVBAHA.116.308659] [PMID: 28062507]
[19]
Brown NK, Zhou Z, Zhang J, et al. Perivascular adipose tissue in vascular function and disease: a review of current research and animal models. Arterioscler Thromb Vasc Biol 2014; 34(8): 1621-30.
[http://dx.doi.org/10.1161/ATVBAHA.114.303029] [PMID: 24833795]
[20]
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(7): R543-52.
[http://dx.doi.org/10.1152/ajpregu.00567.2012] [PMID: 23389108]
[21]
Chatterjee TK, Stoll LL, Denning GM, et al. Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding. Circ Res 2009; 104(4): 541-9.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.182998] [PMID: 19122178]
[22]
Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 2007; 92(3): 1023-33.
[http://dx.doi.org/10.1210/jc.2006-1055] [PMID: 17164304]
[23]
Kumar RKJY, Watts SW, Rockwell CE. Naïve, regulatory, activated, and memory immune cells co-exist in pvats that are comparable in density to non-pvat fats in health. Front Physiol 2020; 11: 58.
[24]
Gao YJ, Zeng ZH, Teoh K, et al. Perivascular adipose tissue modulates vascular function in the human internal thoracic artery. J Thorac Cardiovasc Surg 2005; 130(4): 1130-6.
[http://dx.doi.org/10.1016/j.jtcvs.2005.05.028] [PMID: 16214530]
[25]
Löhn M, Dubrovska G, Lauterbach B, Luft FC, Gollasch M, Sharma AM. Periadventitial fat releases a vascular relaxing factor. FASEB J 2002; 16(9): 1057-63.
[http://dx.doi.org/10.1096/fj.02-0024com] [PMID: 12087067]
[26]
Ayala-Lopez N, Thompson JM, Watts SW. Perivascular adipose tissue’s impact on norepinephrine-induced contraction of mesenteric resistance arteries. Front Physiol 2017; 8: 37.
[http://dx.doi.org/10.3389/fphys.2017.00037] [PMID: 28228728]
[27]
Gálvez B, de Castro J, Herold D, et al. Perivascular adipose tissue and mesenteric vascular function in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 2006; 26(6): 1297-302.
[http://dx.doi.org/10.1161/01.ATV.0000220381.40739.dd] [PMID: 16601235]
[28]
Owen MK, Witzmann FA, McKenney ML, et al. Perivascular adipose tissue potentiates contraction of coronary vascular smooth muscle: influence of obesity. Circulation 2013; 128(1): 9-18.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.112.001238] [PMID: 23685742]
[29]
Victorio JA, Fontes MT, Rossoni LV, Davel AP. Different anti contractile function and nitric oxide production of thoracic and abdominal perivascular adipose tissues. Front Physiol 2016; 7: 295.
[http://dx.doi.org/10.3389/fphys.2016.00295] [PMID: 27462277]
[30]
Bussey CE, Withers SB, Saxton SN, Bodagh N, Aldous RG, Heagerty AM. β3 -Adrenoceptor stimulation of perivascular adipocytes leads to increased fat cell-derived NO and vascular relaxation in small arteries. Br J Pharmacol 2018; 175(18): 3685-98.
[http://dx.doi.org/10.1111/bph.14433] [PMID: 29980164]
[31]
Fang L, Zhao J, Chen Y, et al. Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator. J Hypertens 2009; 27(11): 2174-85.
[http://dx.doi.org/10.1097/HJH.0b013e328330a900] [PMID: 19644389]
[32]
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(3): 323-31.
[http://dx.doi.org/10.1038/sj.bjp.0707228] [PMID: 17384669]
[33]
Lee RM, Lu C, Su LY, Gao YJ. Endothelium-dependent relaxation factor released by perivascular adipose tissue. J Hypertens 2009; 27(4): 782-90.
[http://dx.doi.org/10.1097/HJH.0b013e328324ed86] [PMID: 19516177]
[34]
Fésüs G, Dubrovska G, Gorzelniak K, et al. Adiponectin is a novel humoral vasodilator. Cardiovasc Res 2007; 75(4): 719-27.
[http://dx.doi.org/10.1016/j.cardiores.2007.05.025] [PMID: 17617391]
[35]
Gálvez-Prieto B, Somoza B, Gil-Ortega M, et al. Anticontractile effect of perivascular adipose tissue and leptin are reduced in hypertension. Front Pharmacol 2012; 3: 103.
[http://dx.doi.org/10.3389/fphar.2012.00103] [PMID: 22679436]
[36]
Greenstein AS, Khavandi K, Withers SB, et al. Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 2009; 119(12): 1661-70.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.821181] [PMID: 19289637]
[37]
Wang N, Kuczmanski A, Dubrovska G, Gollasch M. Palmitic acid methyl ester and its relation to control of tone of human visceral arteries and rat aortas by perivascular adipose tissue. Front Physiol 2018; 9: 583.
[http://dx.doi.org/10.3389/fphys.2018.00583] [PMID: 29875688]
[38]
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(1): 130-7.
[http://dx.doi.org/10.1093/cvr/cvt229] [PMID: 24095868]
[39]
Köhn C, Schleifenbaum J, Szijártó IA, et al. Differential effects of cystathionine-γ-lyase-dependent vasodilatory H2S in periadventitial vasoregulation of rat and mouse aortas. PLoS One 2012; 7(8): e41951
[http://dx.doi.org/10.1371/journal.pone.0041951] [PMID: 22870268]
[40]
Zavaritskaya O, Zhuravleva N, Schleifenbaum J, et al. Role of KCNQ channels in skeletal muscle arteries and periadventitial vascular dysfunction. Hypertension 2013; 61(1): 151-9.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.112.197566] [PMID: 23184384]
[41]
Al-Jarallah A, Oriowo MA. Loss of anticontractile effect of perivascular adipose tissue on pregnant rats: a potential role of tumor necrosis factor-α. J Cardiovasc Pharmacol 2016; 67(2): 145-51.
[http://dx.doi.org/10.1097/FJC.0000000000000326] [PMID: 26848638]
[42]
Mann SE, Maille N, Clas D, Osol G. Perivascular adipose tissue: a novel regulator of vascular tone in the rat pregnancy. Reprod Sci 2015; 22(7): 802-7.
[http://dx.doi.org/10.1177/1933719114561556] [PMID: 25527422]
[43]
Wang D, Wang C, Wu X, et al. Endothelial dysfunction and enhanced contractility in microvessels from ovariectomized rats: roles of oxidative stress and perivascular adipose tissue. Hypertension 2014; 63(5): 1063-9.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.02284] [PMID: 24591333]
[44]
Meijer RI, Serné EH, Korkmaz HI, et al. Insulin-induced changes in skeletal muscle microvascular perfusion are dependent upon perivascular adipose tissue in women. Diabetologia 2015; 58(8): 1907-15.
[http://dx.doi.org/10.1007/s00125-015-3606-8] [PMID: 26003324]
[45]
Ahmad AA, Randall MD, Roberts RE. Sex differences in the regulation of porcine coronary artery tone by perivascular adipose tissue: a role of adiponectin? Br J Pharmacol 2017; 174(16): 2773-83.
[http://dx.doi.org/10.1111/bph.13902] [PMID: 28593738]
[46]
Kralova Lesna I, Kralova A, Cejkova S, et al. Characterisation and comparison of adipose tissue macrophages from human subcutaneous, visceral and perivascular adipose tissue. J Transl Med 2016; 14(1): 208.
[http://dx.doi.org/10.1186/s12967-016-0962-1] [PMID: 27400732]
[47]
El Khoudary SR, Shields KJ, Janssen I, et al. Cardiovascular fat, menopause, and sex hormones in women: The SWAN cardiovascular fat ancillary study. J Clin Endocrinol Metab 2015; 100(9): 3304-12.
[http://dx.doi.org/10.1210/JC.2015-2110] [PMID: 26176800]
[48]
Misso ML, Murata Y, Boon WC, Jones ME, Britt KL, Simpson ER. Cellular and molecular characterization of the adipose phenotype of the aromatase-deficient mouse. Endocrinology 2003; 144(4): 1474-80.
[http://dx.doi.org/10.1210/en.2002-221123] [PMID: 12639931]
[49]
Xu J, Xiang Q, Lin G, et al. Estrogen improved metabolic syndrome through down-regulation of VEGF and HIF-1α to inhibit hypoxia of periaortic and intra-abdominal fat in ovariectomized female rats. Mol Biol Rep 2012; 39(8): 8177-85.
[http://dx.doi.org/10.1007/s11033-012-1665-1] [PMID: 22570111]
[50]
Osikoya O, Ahmed H, Panahi S, Bourque SL, Goulopoulou S. Uterine perivascular adipose tissue is a novel mediator of uterine artery blood flow and reactivity in rat pregnancy. J Physiol 2019; 597(15): 3833-52.
[http://dx.doi.org/10.1113/JP277643] [PMID: 31165480]
[51]
Al-Jarallah A, Oommen E, Chacko Verghese L, Oriowo MA. Role of extracellular calcium and calcium sensitization in the anti contractile effect of perivascular adipose tissue in pregnant rat aorta. Pharmacology 2019; 104(5-6): 359-67.
[http://dx.doi.org/10.1159/000502504] [PMID: 31484179]
[52]
Boydens C, Pauwels B, Van de Voorde J. Effect of resveratrol and orchidectomy on the vasorelaxing influence of perivascular adipose tissue. Heart Vessels 2016; 31(4): 608-15.
[http://dx.doi.org/10.1007/s00380-015-0664-2] [PMID: 25822805]
[53]
Lerchbaum E, Schwetz V, Rabe T, Giuliani A, Obermayer-Pietsch B. Hyperandrogenemia in polycystic ovary syndrome: exploration of the role of free testosterone and androstenedione in metabolic phenotype. PLoS One 2014; 9(10): e108263
[http://dx.doi.org/10.1371/journal.pone.0108263] [PMID: 25310562]
[54]
Nestler JE. Insulin resistance and the polycystic ovary syndrome: Recent advances 2020; 8: F1000 Faculty Rev-565.
[55]
Rojas J, Chávez M, Olivar L, et al. Polycystic ovary syndrome, insulin resistance, and obesity: navigating the pathophysiologic labyrinth. Int J Reprod Med 2014; 2014: 719050
[http://dx.doi.org/10.1155/2014/719050] [PMID: 25763405]
[56]
Nofer JR. Estrogens and atherosclerosis: insights from animal models and cell systems. J Mol Endocrinol 2012; 48(2): R13-29.
[http://dx.doi.org/10.1530/JME-11-0145] [PMID: 22355098]
[57]
Lopes RA, Neves KB, Carneiro FS, Tostes RC. Testosterone and vascular function in aging. Front Physiol 2012; 3: 89.
[http://dx.doi.org/10.3389/fphys.2012.00089] [PMID: 22514541]
[58]
Lopes RA, Neves KB, Pestana CR, et al. Testosterone induces apoptosis in vascular smooth muscle cells via extrinsic apoptotic pathway with mitochondria-generated reactive oxygen species involvement. Am J Physiol Heart Circ Physiol 2014; 306(11): H1485-94.
[http://dx.doi.org/10.1152/ajpheart.00809.2013] [PMID: 24658017]
[59]
Costa TJ, Ceravolo GS, dos Santos RA, et al. Association of testosterone with estrogen abolishes the beneficial effects of estrogen treatment by increasing ROS generation in aorta endothelial cells. Am J Physiol Heart Circ Physiol 2015; 308(7): H723-32.
[http://dx.doi.org/10.1152/ajpheart.00681.2014] [PMID: 25637546]
[60]
da Costa RM, Fais RS, Dechandt CRP, et al. Increased mitochondrial ROS generation mediates the loss of the anti-contractile effects of perivascular adipose tissue in high-fat diet obese mice. Br J Pharmacol 2017; 174(20): 3527-41.
[http://dx.doi.org/10.1111/bph.13687] [PMID: 27930804]
[61]
Filgueira FP, Lobato NS, DosSantos RA, et al. Endogenous testosterone increases leukocyte-endothelial cell interaction in spontaneously hypertensive rats. Life Sci 2012; 90(17-18): 689-94.
[http://dx.doi.org/10.1016/j.lfs.2012.03.009] [PMID: 22498877]
[62]
Chignalia AZ, Oliveira MA, Debbas V, et al. Testosterone induces leucocyte migration by NADPH oxidase-driven ROS- and COX2-dependent mechanisms. Clin Sci (Lond) 2015; 129(1): 39-48.
[http://dx.doi.org/10.1042/CS20140548] [PMID: 25700020]
[63]
Akyürek N, Atabek ME, Eklioglu BS, Alp H. The relationship of periaortic fat thickness and cardiovascular risk factors in children with Turner syndrome. Pediatr Cardiol 2015; 36(5): 925-9.
[http://dx.doi.org/10.1007/s00246-015-1098-4] [PMID: 25601134]
[64]
Granato S, Barbaro G, Di Giorgio MR, et al. Epicardial fat: the role of testosterone and lipid metabolism in a cohort of patients with Klinefelter syndrome. Metabolism 2019; 95: 21-6.
[http://dx.doi.org/10.1016/j.metabol.2019.03.002] [PMID: 30878494]
[65]
Schlett CL, Massaro JM, Lehman SJ, et al. Novel measurements of periaortic adipose tissue in comparison to anthropometric measures of obesity, and abdominal adipose tissue. Int J Obes 2009; 33(2): 226-32.
[http://dx.doi.org/10.1038/ijo.2008.267] [PMID: 19139753]
[66]
Wagner R, Machann J, Lehmann R, et al. Exercise-induced albuminuria is associated with perivascular renal sinus fat in individuals at increased risk of type 2 diabetes. Diabetologia 2012; 55(7): 2054-8.
[http://dx.doi.org/10.1007/s00125-012-2551-z] [PMID: 22526613]
[67]
Britton KA, Pedley A, Massaro JM, et al. Prevalence, distribution, and risk factor correlates of high thoracic periaortic fat in the Framingham heart study. J Am Heart Asso 2012; 1(6): e004200.
[68]
Park SY, Kim KH, Seo KW, et al. Resistin derived from diabetic perivascular adipose tissue up-regulates vascular expression of osteopontin via the AP-1 signalling pathway. J Pathol 2014; 232(1): 87-97.
[http://dx.doi.org/10.1002/path.4286] [PMID: 24089355]
[69]
Han F, Li K, Pan R, et al. Calycosin directly improves perivascular adipose tissue dysfunction by upregulating the adiponectin/AMPK/eNOS pathway in obese mice. Food Funct 2018; 9(4): 2409-15.
[http://dx.doi.org/10.1039/C8FO00328A] [PMID: 29595858]
[70]
Xia N, Horke S, Habermeier A, et al. Uncoupling of endothelial nitric oxide synthase in perivascular adipose tissue of diet-induced obese mice. Arterioscler Thromb Vasc Biol 2016; 36(1): 78-85.
[http://dx.doi.org/10.1161/ATVBAHA.115.306263] [PMID: 26586660]
[71]
Ma L, Ma S, He H, et al. Perivascular fat-mediated vascular dysfunction and remodeling through the AMPK/mTOR pathway in high-fat diet-induced obese rats. Hypertens Res 2010; 33(5): 446-53.
[http://dx.doi.org/10.1038/hr.2010.11] [PMID: 20186150]
[72]
Xu X, Liu C, Xu Z, et al. Altered adipocyte progenitor population and adipose-related gene profile in adipose tissue by long-term high-fat diet in mice. Life Sci 2012; 90(25-26): 1001-9.
[http://dx.doi.org/10.1016/j.lfs.2012.05.016] [PMID: 22683431]
[73]
Gil-Ortega M, Stucchi P, Guzmán-Ruiz R, et al. Adaptative nitric oxide overproduction in perivascular adipose tissue during early diet-induced obesity. Endocrinology 2010; 151(7): 3299-306.
[http://dx.doi.org/10.1210/en.2009-1464] [PMID: 20410199]
[74]
Withers SB, Forman R, Meza-Perez S, et al. Eosinophils are key regulators of perivascular adipose tissue and vascular functionality. Sci Rep 2017; 7: 44571.
[http://dx.doi.org/10.1038/srep44571] [PMID: 28303919]
[75]
Gil-Ortega M, Condezo-Hoyos L, García-Prieto CF, et al. Imbalance between pro and anti-oxidant mechanisms in perivascular adipose tissue aggravates long-term high-fat diet-derived endothelial dysfunction. PLoS One 2014; 9(4): e95312
[http://dx.doi.org/10.1371/journal.pone.0095312] [PMID: 24760053]
[76]
Wang H, Luo W, Wang J, et al. Obesity-induced endothelial dysfunction is prevented by deficiency of p-selectin glycoprotein ligand-1. Diabetes 2012; 3219-27.
[http://dx.doi.org/10.2337/db12-0162]
[77]
Agabiti-Rosei C, De Ciuceis C, Rossini C, et al. Anticontractile activity of perivascular fat in obese mice and the effect of long-term treatment with melatonin. J Hypertens 2014; 32(6): 1264-74.
[http://dx.doi.org/10.1097/HJH.0000000000000178] [PMID: 24751595]
[78]
Cybularz M, Langbein H, Zatschler B, et al. Endothelial function and gene expression in perivascular adipose tissue from internal mammary arteries of obese patients with coronary artery disease. Atheroscler Suppl 2017; 30: 149-58.
[http://dx.doi.org/10.1016/j.atherosclerosissup.2017.05.042] [PMID: 29096831]
[79]
Withers SB, Bussey CE, Saxton SN, Melrose HM, Watkins AE, Heagerty AM. Mechanisms of adiponectin-associated perivascular function in vascular disease. Arterioscler Thromb Vasc Biol 2014; 34(8): 1637-42.
[http://dx.doi.org/10.1161/ATVBAHA.114.303031] [PMID: 24855062]
[80]
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(4): H1425-37.
[http://dx.doi.org/10.1152/ajpheart.00376.2011] [PMID: 21765057]
[81]
Bełtowski J, Guranowski A, Jamroz-Wiśniewska A, Wolski A, Hałas K. Hydrogen-sulfide-mediated vasodilatory effect of nucleoside 5′-monophosphorothioates in perivascular adipose tissue. Can J Physiol Pharmacol 2015; 93(7): 585-95.
[http://dx.doi.org/10.1139/cjpp-2014-0543] [PMID: 26120822]
[82]
Candela J, Wang R, White C. Microvascular endothelial dysfunction in obesity is driven by macrophage-dependent hydrogen sulfide depletion. Arterioscler Thromb Vasc Biol 2017; 37(5): 889-99.
[http://dx.doi.org/10.1161/ATVBAHA.117.309138] [PMID: 28336559]
[83]
Mendizábal Y, Llorens S, Nava E. Vasoactive effects of prostaglandins from the perivascular fat of mesenteric resistance arteries in WKY and SHROB rats. Life Sci 2013; 93(25-26): 1023-32.
[http://dx.doi.org/10.1016/j.lfs.2013.10.021] [PMID: 24200844]
[84]
Chen JY, Tsai PJ, Tai HC, et al. Increased aortic stiffness and attenuated lysyl oxidase activity in obesity. Arterioscler Thromb Vasc Biol 2013; 33(4): 839-46.
[http://dx.doi.org/10.1161/ATVBAHA.112.300036] [PMID: 23413430]
[85]
Manka D, Chatterjee TK, Stoll LL, et al. Transplanted perivascular adipose tissue accelerates injury-induced neointimal hyperplasia: role of monocyte chemoattractant protein-1. Arterioscler Thromb Vasc Biol 2014; 34(8): 1723-30.
[http://dx.doi.org/10.1161/ATVBAHA.114.303983] [PMID: 24947528]
[86]
Horimatsu T, Kim HW, Weintraub NL. The role of perivascular adipose tissue in non-atherosclerotic vascular disease. Front Physiol 2017; 8: 969.
[http://dx.doi.org/10.3389/fphys.2017.00969] [PMID: 29234289]
[87]
Sowers JR, Habibi J, Aroor AR, et al. Epithelial sodium channels in endothelial cells mediate diet-induced endothelium stiffness and impaired vascular relaxation in obese female mice. Metabolism 2019; 99: 57-66.
[http://dx.doi.org/10.1016/j.metabol.2019.153946] [PMID: 31302199]
[88]
Tilley MA, Hatcher AS, Chantler PD, Asano S. Perivascular adipose tissue mediated aortic reactivity data: Female lean and obese Zucker rats. Data Brief 2020; 29: 105290
[http://dx.doi.org/10.1016/j.dib.2020.105290] [PMID: 32140508]
[89]
DeVallance E, Branyan KW, Lemaster K, et al. Aortic dysfunction in metabolic syndrome mediated by perivascular adipose tissue TNFα- and NOX2-dependent pathway. Exp Physiol 2018; 103(4): 590-603.
[http://dx.doi.org/10.1113/EP086818] [PMID: 29349831]
[90]
Vieira-Potter VJ, Lee S, Bayless DS, et al. Disconnect between adipose tissue inflammation and cardiometabolic dysfunction in Ossabaw pigs. Obesity (Silver Spring) 2015; 23(12): 2421-9.
[http://dx.doi.org/10.1002/oby.21252] [PMID: 26524201]
[91]
Ruan CC, Zhu DL, Chen QZ, et al. 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 2010; 30(12): 2568-74.
[http://dx.doi.org/10.1161/ATVBAHA.110.215525] [PMID: 20864665]
[92]
Sheng LJ, Ruan CC, Ma Y, et al. Beta3 adrenergic receptor is involved in vascular injury in deoxycorticosterone acetate-salt hypertensive mice. FEBS Lett 2016; 590(6): 769-78.
[http://dx.doi.org/10.1002/1873-3468.12107] [PMID: 26910302]
[93]
Lu C, Su LY, Lee RM, Gao YJ. Alterations in perivascular adipose tissue structure and function in hypertension. Eur J Pharmacol 2011; 656(1-3): 68-73.
[http://dx.doi.org/10.1016/j.ejphar.2011.01.023] [PMID: 21277297]
[94]
Zeng ZH, Zhang ZH, Luo BH, 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(4): 355-63.
[http://dx.doi.org/10.1080/10641960902977916] [PMID: 19811363]
[95]
Lynch FM, Withers SB, Yao Z, et al. Perivascular adipose tissue derived adiponectin activates BK(Ca) channels to induce anticontractile responses. Am J Physiol Heart Circ Physiol 2013; 304(6): H786-95.
[http://dx.doi.org/10.1152/ajpheart.00697.2012] [PMID: 23292715]
[96]
Ahmad MF, Ferland D, Ayala-Lopez N, et al. Perivascular Adipocytes Store Norepinephrine by Vesicular Transport. Arterioscler Thromb Vasc Biol 2019; 39(2): 188-99.
[http://dx.doi.org/10.1161/ATVBAHA.118.311720] [PMID: 30567483]
[97]
Costa RM, Filgueira FP, Tostes RC, Carvalho MH, Akamine EH, Lobato NS. H2O2 generated from mitochondrial electron transport chain in thoracic perivascular adipose tissue is crucial for modulation of vascular smooth muscle contraction. Vascul Pharmacol 2016; 84: 28-37.
[http://dx.doi.org/10.1016/j.vph.2016.05.008] [PMID: 27252154]
[98]
Zemančíková A, Török J. Influence of age on anticontractile effect of perivascular adipose tissue in normotensive and hypertensive rats. Oxid Med Cell Longev 2019; 2019: 9314260
[http://dx.doi.org/10.1155/2019/9314260] [PMID: 30800212]
[99]
Gálvez-Prieto B, Dubrovska G, Cano MV, et al. A reduction in the amount and anti-contractile effect of periadventitial mesenteric adipose tissue precedes hypertension development in spontaneously hypertensive rats. Hypertens Res 2008; 31(7): 1415-23.
[http://dx.doi.org/10.1291/hypres.31.1415] [PMID: 18957813]
[100]
Li R, Andersen I, Aleke J, Golubinskaya V, Gustafsson H, Nilsson H. Reduced anti-contractile effect of perivascular adipose tissue on mesenteric small arteries from spontaneously hypertensive rats: role of Kv7 channels. Eur J Pharmacol 2013; 698(1-3): 310-5.
[http://dx.doi.org/10.1016/j.ejphar.2012.09.026] [PMID: 23059186]
[101]
Lee YC, Chang HH, Chiang CL, et al. Role of perivascular adipose tissue-derived methyl palmitate in vascular tone regulation and pathogenesis of hypertension. Circulation 2011; 124(10): 1160-71.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.111.027375] [PMID: 21844078]
[102]
Lee RM, Ding L, Lu C, Su LY, Gao YJ. Alteration of perivascular adipose tissue function in angiotensin II-induced hypertension. Can J Physiol Pharmacol 2009; 87(11): 944-53.
[http://dx.doi.org/10.1139/Y09-088] [PMID: 19935902]
[103]
Mikolajczyk TP, Nosalski R, Szczepaniak P, et al. Role of chemokine RANTES in the regulation of perivascular inflammation, T-cell accumulation, and vascular dysfunction in hypertension. FASEB J 2016; 30(5): 1987-99.
[http://dx.doi.org/10.1096/fj.201500088R] [PMID: 26873938]
[104]
Caillon A, Mian MOR, Fraulob-Aquino JC, et al. γδ T Cells mediate angiotensin ii-induced hypertension and vascular injury. Circulation 2017; 135(22): 2155-62.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.116.027058] [PMID: 28330983]
[105]
Spradley FT, Ho DH, Pollock JS. Dahl SS rats demonstrate enhanced aortic perivascular adipose tissue-mediated buffering of vasoconstriction through activation of NOS in the endothelium. Am J Physiol Regul Integr Comp Physiol 2016; 310(3): R286-96.
[http://dx.doi.org/10.1152/ajpregu.00469.2014] [PMID: 26608658]
[106]
Ji H, Zheng W, Li X, et al. Sex-specific T-cell regulation of angiotensin II-dependent hypertension. Hypertension 2014; 64(3): 573-82.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.114.03663] [PMID: 24935938]
[107]
Aghamohammadzadeh R, Unwin RD, Greenstein AS, Heagerty AM. Effects of obesity on perivascular adipose tissue vasorelaxant function: nitric oxide, inflammation and elevated systemic blood pressure. J Vasc Res 2015; 52(5): 299-305.
[http://dx.doi.org/10.1159/000443885] [PMID: 26910225]
[108]
Amor S, González-Hedström D, Martín-Carro B, et al. Beneficial effects of an aged black garlic extract in the metabolic and vascular alterations induced by a high fat/sucrose diet in male rats. Nutrients 2019; 11(1): 11.
[http://dx.doi.org/10.3390/nu11010153] [PMID: 30642033]
[109]
Rosei CA, Withers SB, Belcaid L, De Ciuceis C, Rizzoni D, Heagerty AM. Blockade of the renin-angiotensin system in small arteries and anticontractile function of perivascular adipose tissue. J Hypertens 2015; 33(5): 1039-45.
[http://dx.doi.org/10.1097/HJH.0000000000000506] [PMID: 25909701]
[110]
Briones AM, Nguyen Dinh Cat A, Callera GE, et al. Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension 2012; 59(5): 1069-78.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.111.190223] [PMID: 22493070]
[111]
Lefranc C, Friederich-Persson M, Braud L, et al. MR (Mineralocorticoid Receptor) induces adipose tissue senescence and mitochondrial dysfunction leading to vascular dysfunction in obesity. Hypertension 2019; 73(2): 458-68.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.118.11873] [PMID: 30624990]
[112]
Xia N, Weisenburger S, Koch E, et al. Restoration of perivascular adipose tissue function in diet-induced obese mice without changing bodyweight. Br J Pharmacol 2017; 174(20): 3443-53.
[http://dx.doi.org/10.1111/bph.13703] [PMID: 28055105]
[113]
Zhu B, Li Y, Mei W, et al. Alogliptin improves endothelial function by promoting autophagy in perivascular adipose tissue of obese mice through a GLP-1-dependent mechanism. Vascul Pharmacol 2019; 115: 55-63.
[http://dx.doi.org/10.1016/j.vph.2018.11.003] [PMID: 30447331]
[114]
Han F, Hou N, Liu Y, et al. Liraglutide improves vascular dysfunction by regulating a cAMP-independent PKA-AMPK pathway in perivascular adipose tissue in obese mice. Biomedicine pharmacotherapy 2019; 10: 109537
[http://dx.doi.org/10.1016/j.biopha.2019.109537]
[115]
Hou N, Du G, Han F, Zhang J, Jiao X, Sun X. Irisin regulates heme oxygenase-1/adiponectin axis in perivascular adipose tissue and improves endothelial dysfunction in diet-induced obese mice. Cell Physiol Biochem 2017; 42(2): 603-14.
[http://dx.doi.org/10.1159/000477864] [PMID: 28595178]
[116]
Bussey CE, Withers SB, Aldous RG, Edwards G, Heagerty AM. Obesity-related perivascular adipose tissue damage is reversed by sustained weight loss in the rat. Arterioscler Thromb Vasc Biol 2016; 36(7): 1377-85.
[http://dx.doi.org/10.1161/ATVBAHA.116.307210] [PMID: 27174097]
[117]
DeVallance E, Branyan KW, Lemaster KC, et al. Exercise training prevents the perivascular adipose tissue-induced aortic dysfunction with metabolic syndrome. Redox Biol 2019; 26: : 101285
[http://dx.doi.org/10.1016/j.redox.2019.101285] [PMID: 31374361]
[118]
Meziat C, Boulghobra D, Strock E, et al. Exercise training restores eNOS activation in the perivascular adipose tissue of obese rats: Impact on vascular function. Nitric Oxide 2019; 86: 63-7.
[http://dx.doi.org/10.1016/j.niox.2019.02.009] [PMID: 30836135]
[119]
Sousa AS, Sponton ACS, Trifone CB, Delbin MA. Aerobic exercise training prevents perivascular adipose tissue-induced endothelial dysfunction in thoracic aorta of obese mice. Front Physiol 2019; 10: 1009.
[http://dx.doi.org/10.3389/fphys.2019.01009] [PMID: 31474873]
[120]
Araujo HN, Victório JA, Valgas da Silva CP, et al. Anti-contractile effects of perivascular adipose tissue in thoracic aorta from rats fed a high-fat diet: role of aerobic exercise training. Clin Exp Pharmacol Physiol 2018; 45(3): 293-302.
[http://dx.doi.org/10.1111/1440-1681.12882] [PMID: 29265399]
[121]
Wang X, Lin Y, Luo N, et al. Short-term intensive atorvastatin therapy improves endothelial function partly via attenuating perivascular adipose tissue inflammation through 5-lipoxygenase pathway in hyperlipidemic rabbits. Chin Med J (Engl) 2014; 127(16): 2953-9.
[PMID: 25131234]
[122]
Wójcicka G, Jamroz-Wiśniewska A, Atanasova P, Chaldakov GN, Chylińska-Kula B, Bełtowski J. Differential effects of statins on endogenous H2S formation in perivascular adipose tissue. Pharmacol Res 2011; 63(1): 68-76.
[http://dx.doi.org/10.1016/j.phrs.2010.10.011] [PMID: 20969959]
[123]
Rubba P. Effects of atorvastatin on the different phases of atherogenesis. Drugs 2007; 67(Suppl. 1): 17-27.
[http://dx.doi.org/10.2165/00003495-200767001-00003] [PMID: 17910518]
[124]
Peng S, Xu LW, Che XY, et al. Atorvastatin inhibits inflammatory response, attenuates lipid deposition, and improves the stability of vulnerable atherosclerotic plaques by modulating autophagy. Front Pharmacol 2018; 9: 438.
[http://dx.doi.org/10.3389/fphar.2018.00438] [PMID: 29773990]

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