Emerging evidence suggests that perivascular adipose tissue (PVAT) has a relevant role in the control of vascular tone in physiology and pathology. Healthy PVAT has anticontractile, anti-inflammatory, and antioxidative actions. Accumulating data from both human and experimental animal models indicate that PVAT dysfunction is conceivably coupled to cardiovascular diseases, and it is associated with vascular inflammation, oxidative stress, and arterial remodeling. Therefore, “healthy” PVAT may constitute a novel therapeutic target for the prevention and treatment of cardiovascular diseases.
Recent Advances:
Hydrogen sulfide (H2S) has been recognized as a vascular anti-contractile factor released from PVAT. The enzymes deputed to H2S biosynthesis are variously expressed in PVAT and strictly dependent on the vascular bed and species. Metabolic and cardiovascular diseases can alter the morphological and secretory characteristics of PVAT, influencing also the H2S signaling. Here, we discuss the role of PVAT-derived H2S in healthy conditions and its relevance in alterations occurring in vascular disorders.
Critical Issues:
We discuss how a better understanding may help in the prevention of vascular dysfunction related to alteration in PVAT-released H2S as well as the importance of the interplay between PVAT and H2S.
Future Directions:
We propose future directions to evaluate the contribution of each enzyme involved in H2S biosynthesis and their alteration/switch occurring in vascular disorders and the remaining challenges in investigating the role of H2S. Antioxid. Redox Signal. 37, 84–97.
Get full access to this article
View all access options for this article.
References
1.
AalbaekF, BondeL, KimS, and BoedtkjerE. The Journal of Physiology Perivascular tissue inhibits rho-kinase-dependent smooth muscle Ca2+ sensitivity and endothelium-dependent H2S signalling in rat coronary arteries. J Physiol, 593: 4747–4764, 2015.
2.
AlmabroukTA, EwartMA, SaltIP, and KennedyS. Perivascular fat, AMP-activated protein kinase and vascular diseases. Br J Pharmacol, 171: 595–617, 2014.
3.
AritaY, KiharaS, OuchiN, TakahashiM, MaedaK, MiyagawaJ, HottaK, ShimomuraI, NakamuraT, MiyaokaK, KuriyamaH, NishidaM, YamashitaS, OkuboK, MatsubaraK, MuraguchiM, OhmotoY, FunahashiT, and MatsuzawaY. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun, 257: 79–83, 1999.
4.
AsimakopoulouA, PanopoulosP, ChasapisCT, ColettaC, ZhouZ, CirinoG, GiannisA, SzaboC, SpyrouliasGA, and PapapetropoulosA. Selectivity of commonly used pharmacological inhibitors for cystathionine β synthase (CBS) and cystathionine γ lyase (CSE). Br J Pharmacol, 169: 922–932, 2013.
BełtowskiJ, GuranowskiA, Jamroz-WiśniewskaA, WolskiA, and HałasK. Hydrogen-sulfide-mediated vasodilatory effect of nucleoside 5'-monophosphorothioates in perivascular adipose tissue. Can J Physiol Pharmacol, 93: 585–595, 2015.
7.
BeltowskiJ, Jamroz-WisniewskaA, and WidomskaS. Adiponectin and its role in cardiovascular diseases. Cardiovasc Hematol Disord Drug Targets, 8: 7–46, 2008.
8.
BibliSI, YangG, ZhouZ, WangR, TopouzisS, and PapapetropoulosA. Role of cGMP in hydrogen sulfide signaling. Nitric Oxide, 30: 7–13, 2015.
9.
BucciM, PapapetropoulosA, VelleccoV, ZhouZ, PyriochouA, RoussosC, RoviezzoF, BrancaleoneV, and CirinoG. Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol, 30: 1998–2004, 2010.
10.
BurnettMS, LeeCW, KinnairdTD, StabileE, DurraniS, DullumMK, DevaneyJM, FishmanC, StamouS, CanosD, ZbindenS, ClavijoLC, JangGJ, AndrewsJA, ZhuJ, and EpsteinSE. The potential role of resistin in atherogenesis. Atherosclerosis, 182: 241–248, 2005.
11.
CacanyiovaS, KrskovaK, ZoradS, FrimmelK, DrobnaM, ValaskovaZ, MisakA, GolasS, BrezaJ, BrezaJJr., and BerenyiovaA. Arterial hypertension and plasma glucose modulate the vasoactive effects of nitroso-sulfide coupled signaling in human intrarenal arteries. Molecules, 25: 2886, 2020.
12.
CacanyiovaS, MajzunovaM, GolasS, and BerenyiovaA. The role of perivascular adipose tissue and endogenous hydrogen sulfide in vasoactive responses of isolated mesenteric arteries in normotensive and spontaneously hypertensive rats. J Physiol Pharmacol, 70: 295–306, 2019.
13.
ChaiQ, LuT, WangXL, and LeeHC. Hydrogen sulfide impairs shear stress-induced vasodilatation in mouse coronary arteries. Pflugers Arch, 467: 329–340, 2015.
14.
ChangJ, LiY, HuangY, LamKS, HooRL, WongWT, ChengKK, WangY, VanhouttePM, and XuA. Adiponectin prevents diabetic premature senescence of endothelial progenitor cells and promotes endothelial repair by suppressing the p38 MAP kinase/p16INK4A signaling pathway. Diabetes, 59: 2949–2959, 2010.
15.
ChangL, Garcia-BarrioMT, and ChenYE. Perivascular adipose tissue regulates vascular function by targeting vascular smooth muscle cells. Arterioscler Thromb Vasc Biol, 40: 1094–1109, 2020.
16.
ChenC, JiangJ, LüJ-M, ChaiH, WangX, LinPH, and YaoQ. Resistin decreases expression of endothelial nitric oxide synthase through oxidative stress in human coronary artery endothelial cells. Am J Physiol Heart Circ Physiol, 299: H193–H201, 2010.
17.
ChengKK, LamKS, WangY, HuangY, CarlingD, WuD, WongC, and XuA. Adiponectin-induced endothelial nitric oxide synthase activation and nitric oxide production are mediated by APPL1 in endothelial cells. Diabete, 56: 1387–1394, 2007.
18.
ChuS, DingW, LiK, PangY, and TangC. Plasma resistin associated with myocardium injury in patients with acute coronary syndrome. Circ J, 72: 1249–1253, 2008.
19.
ColettaC, PapapetropoulosA, ErdelyiK, OlahG, MódisK, PanopoulosP, AsimakopoulouA, GeröD, SharinaI, MartinE, and SzaboC. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci U S A, 109: 9161–9166, 2012.
20.
d'Emmanuele di Villa BiancaR, SorrentinoR, ColettaC, MitidieriE, RossiA, VelleccoV, PintoA, CirinoG, and SorrentinoR. Hydrogen sulfide-induced dual vascular effect involves arachidonic acid cascade in rat mesenteric arterial bed. J Pharmacol Exp Ther, 337: 59–64, 2011.
DongóE, Beliczai-MarosiG, DybvigAS, and KissL. The mechanism of action and role of hydrogen sulfide in the control of vascular tone. Nitric Oxide, 81: 75–87, 2018.
23.
DonovanJ, WongPS, GarleMJ, AlexanderSPH, DunnWR, and RalevicV. Coronary artery hypoxic vasorelaxation is augmented by perivascular adipose tissue through a mechanism involving hydrogen sulphide and cystathionine-β-synthase. Acta Physiol, 224: 13126, 2018.
24.
DonovanJ, WongPS, RobertsR, GarleMJ, AlexanderSPH, DunnWR, and RalevicV. A critical role for cystathionine-β-synthase in hydrogen sulfide-mediated hypoxic relaxation of the coronary artery. Vasc Pharmacol, 93–95: 20–32, 2017.
25.
EmilovaR, DimitrovaD, MladenovM, DanevaT, SchubertR, and GagovH. Cystathionine gamma-lyase of perivascular adipose tissue with reversed regulatory effect in diabetic rat artery. Biotechnol Biotechnol Equip, 29: 147–151, 2015.
26.
FangL, ZhaoJ, ChenY, MaT, XuG, TangC, LiuX, and GengB. Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator. J Hypertens, 27: 2174–2185, 2009.
27.
FésüsG, DubrovskaG, GorzelniakK, KlugeR, HuangY, LuftFC, and GollaschM. Adiponectin is a novel humoral vasodilator. Cardiovasc Res, 75: 719–727, 2007.
28.
FilkováM, HaluzíkM, GayS, and SenoltL. The role of resistin as a regulator of inflammation: implications for various human pathologies. Clin Immunol, 133: 157–170, 2009.
29.
FriedmanJM and HalaasJL. Leptin and the regulation of body weight in mammals. Nature, 395: 763–770, 1998.
30.
GalvezB, de CastroJ, HeroldD, DubrovskaG, ArribasS, GonzàlezMC, AranguezI, LuftFC, RamosMP, GollaschM, and AlfonsoMSF. Perivascular adipose tissue and mesenteric vascular function in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol, 26: 1297–1302, 2006.
31.
Galvez-PrietoB, BolbrinkerJ, StucchiP, de Las HerasAI, MerinoB, ArribasS, Ruiz-GayoM, HuberM, WehlandM, KreutzM, and Fernandez-AlfonsoMS. Comparative expression analysis of the renin-angiotensin system components between white and brown perivascular adipose tissue. J Endocrinol, 197: 55–64, 2008.
32.
Gálvez-PrietoB, SomozaB, Gil-OrtegaM, García-PrietoCF, de Las HerasAI, GonzálezMC, ArribasS, AranguezI, BolbrinkerJ, KreutzR, Ruiz-GayoM, and Fernández-AlfonsoMS. Anticontractile effect of perivascular adipose tissue and leptin are reduced in hypertension. Front Pharmacol, 3: 103, 2012.
GuzikT, MangalatD, and KorbutR. Adipocytokines - novel link between inflammation and vascular function?. J Physiol Pharmacol, 54: 505–528, 2007.
36.
HottaK, FunahashiT, AritaY, TakahashiM, MatsudaM, OkamotoY, IwahashiH, KuriyamaH, OuchiN, MaedaK, NishidaM, KiharaS, SakaiN, NakajimaT, HasegawaK, MuraguchiM, OhmotoY, NakamuraT, YamashitaS, HanafusaT, and MatsuzawaY. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol, 20: 1595–1599, 2000.
37.
HuangF, LezamaMAR, OntiverosJAP, BravoG, VillafanaS, Estela del-Rio-NavarroB, and HongE. Effect of losartan on vascular function in fructose-fed rats: the role of perivascular adipose tissue. Clin Exp Hypertens, 32: 98–104, 2010.
38.
HulsmansM, Van DoorenE, MathieuC, and HolvoetP. Decrease of miR-146b-5p in monocytes during obesity is associated with loss of the anti-inflammatory but not insulin signaling action of adiponectin. PLoS One, 7: 32794, 2012.
39.
JiangB, TangG, CaoK, WuL, and WangR. Molecular mechanism for H2S-inducedactivation of KATP channels. Antioxid Redox Signal, 12: 1–2, 2010.
40.
KawahitoH, YamadaH, IrieD, KatoT, AkakabeY, KishidaS, TakataH, WakanaN, OgataT, IkedaK, UeyamaT, MatobaS, MoriY, and MatsubaraH. Periaortic adipose tissue-specific activation of the renin-angiotensin system contributes to atherosclerosis development in uninephrectomized apoE-/- mice. Am J Physiol Heart Circ Physiol, 305: 667–675, 2013.
41.
KawanamiD, MaemuraK, TakedaN, HaradaT, NojiriT, ImaiY, ManabeI, UtsunomiyaK, and NagaiR. Direct reciprocal effects of resistin and adiponectin on vascular endothelial cells: a new insight into adipocytokine-endothelial cell interactions. Biochem Biophys Res Commun, 314: 415–419, 2004.
42.
KazamaK, OkadaM, HaraY, and YamawakiH. A novel adipocytokine, omentin, inhibits agonists-induced increases of blood pressure in rats. J Vet Med Sci, 75: 1029–1034, 2013.
43.
KazamaK, OkadaM, and YamawakiH. A novel adipocytokine, omentin, inhibits platelet-derived growth factor-BB-induced vascular smooth muscle cell migration through antioxidative mechanism. Am J Physiol Heart Circ Physiol, 306: 1714–1719, 2014.
44.
KazamaK, OkadaM, and YamawakiH. A novel adipocytokine, omentin, inhibits monocrotaline-induced pulmonary arterial hypertension in rats. Biochem Biophys Res Commun, 452: 142–146, 2014.
45.
KimS and IwaoH. Molecular and cellular mechanisms of angiotensin II-mediated cardiovascular and renal diseases. Pharmacol Rev, 52: 11–34, 2000.
KingAL, PolhemusDJ, BhushanS, OtsukaH, KondoK, NicholsonCK, BradleyJM, IslamKN, CalvertJW, TaoYX, DugasTR, KelleyEE, ElrodJW, HuangPL, WangR, and LeferDJ. Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent. Proc Natl Acad Sci U S A, 111: 3182–3187, 2014.
48.
KissL, DeitchEA, and SzabóC. Hydrogen sulfide decreases adenosine triphosphate levels in aortic rings and leads to vasorelaxation via metabolic inhibition. Life Sci, 83: 589–594, 2008.
49.
KoenitzerJR, IsbellTS, PatelHD, BenavidesGA, DickinsonDA, PatelRP, Darley-UsmarVM, Lancaster JrJR, DoellerJE, and KrausDW. Hydrogen sulfide mediates vasoactivity in an O2-dependent manner. Am J Physiol Heart Circ Physiol, 292: 1953–1960, 2007.
50.
KohnC, SchleifenbaumJ, SzijartoIA, MarkoL, DubrovskaG, HuangY, and GollaschM. Differential effects of cystathionine-gamma-lyase dependent vasodilatory H2S in periadventitial vasoregulation of rat and mouse aortas. PLoS One, 7: 41951, 2012.
51.
KuboS, KajiwaraM, and KawabataA. Dual modulation of the tension of isolated gastric artery and gastric mucosal circulation by hydrogen sulfide in rats. Inflammopharmacology, 15: 288–292, 2007.
KuoMM, KimDH, JanduS, BergmanY, TanS, WangH, PandeyDR, AbrahamTP, ShoukasAA, BerkowitzDE, and SanthanamL. MPST but not CSE is the primary regulator of hydrogen sulfide production and function in the coronary artery. Am J Physiol Heart Circ Physiol, 310: H71–H79, 2016.
54.
LeeRM, LuC, SuLY, and GaoYJ. Endothelium-dependent relaxation factor released by perivascular adipose tissue. J Hypertens, 27: 782–790, 2009.
55.
LeeYC, ChangHH, ChiangCL, LiuCH, YehJI, ChenMF, ChenPY, KuoJS, and LeeTJ. Role of perivascular adipose tissue-derived methyl palmitate in vascular tone regulation and pathogenesis of hypertension. Circulation, 124: 1160–1171, 2011.
56.
LiH, WangYP, ZhangLN, and TianG. Perivascular adipose tissue-derived leptin promotes vascular smooth muscle cell phenotypic switching via p38 mitogen-activated protein kinase in metabolic syndrome rats. Exp Biol Med (Maywood), 239: 954–965, 2014.
57.
LiL, HsuA, and MoorePK.Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation—a tale of three gases!. Pharmacol Ther, 123: 386–400, 2009.
58.
LiL, MamputuJC, WiernspergerN, and RenierG. Signaling pathways involved in human vascular smooth muscle cell proliferation and matrix metalloproteinase-2 expression induced by leptin: inhibitory effect of metformin. Diabetes, 54: 2227–2234, 2005.
59.
LiR, AndersenI, AlekeJ, GolubinskayaV, GustafssonH, and NilssonH. Reduced anti-contractile effect of perivascular adipose tissue on mesenteric small arteries from spontaneously hypertensive rats: role of Kv7 channels. Eur J Pharmacol, 698: 310–315, 2013.
60.
LiS, PingNN, CaoL, MiYN, and CaoYX. H2S induces vasoconstriction of rat cerebral arteries via cAMP/adenylyl cyclase pathway. Toxicol Appl Pharmacol, 289: 389–396, 2015.
61.
LimJJ, LiuYH, KhinES, and BianJS. Vasoconstrictive effect of hydrogen sulfide involves downregulation of cAMP in vascular smooth muscle cells. Am J Physiol Cell Physiol, 295: C1261–C1270, 2008.
62.
LimaPO, CalilCM, and MarcondesFK. Influence of gender and stress on the volatile sulfur compounds and stress biomarkers production. Oral Dis, 19: 366–373, 2013.
63.
LiuR, WangX, and BuP. Omentin-1 is associated with carotid atherosclerosis in patients with metabolic syndrome. Diabetes Res Clin Pract, 93: 21–25, 2011.
64.
LiuYH, YanCD, and BianJS. Hydrogen sulfide: a novel signaling molecule in the vascular system. J Cardiovasc Pharmacol, 58: 560–569, 2011.
65.
LöhnM, DubrovskaG, LauterbachB, LuftFC, GollaschM, and SharmaAM. Periadventitial fat releases a vascular relaxing factor. FASEB J, 16: 1057–1063, 2002.
66.
LuC, SuL-Y, LeeRMKW, and GaoY-J. 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, 2010.
67.
LynchFM, WithersSB, YaoZ, WernerME, EdwardsG, WestonAH, and HeagertyAM. Perivascular adipose tissue-derived adiponectin activates BK(Ca) channels to induce anticontractile responses. Am J Physiol Heart Circ Physiol, 304: 786–795, 2013.
68.
MahadevK, WuX, DonnellyS, OuedraogoR, EckhartA, and GoldsteinB. Adiponectin inhibits vascular endothelial growth factor-induced migration of human coronary artery endothelial cells. Cardiovasc Res, 78: 376–384, 2008.
69.
MalinowskiM, DejaMA, GolbaKS, RolederT, BiernatJ, and WosS. Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor. Eur J Cardiothorac Surg, 33: 225–231, 2008.
70.
MargaritisM, AntonopoulosAS, DigbyJ, LeeR, ReillyS, CoutinhoP, ShirodariaC, SayeedR, PetrouM, De SilvaR, JalilzadehS, DemosthenousM, BakogiannisC, TousoulisD, StefanadisC, ChoudhuryRP, CasadeiB, ChannonKM, and AntoniadesC. Interactions between vascular wall and perivascular adipose tissue reveal novel roles for adiponectin in the regulation of endothelial nitric oxide synthase function in human vessels. Circulation, 127: 2209–2221, 2013.
71.
MartelliA, CitiV, and CalderoneV. Vascular Effects of H(2)S-Donors: fluorimetric detection of H2S generation and ion channel activation in human aortic smooth muscle cells. Methods Mol Biol, 2007: 79–87, 2019.
72.
MartelliA, TestaiL, Breschi MC LawsonK, McKayNG, MicelliF, TaglialatelaM, and CalderoneV. Vasorelaxation by hydrogen sulphide involves activation of Kv7 potassium channels. Pharmacol Res, 70: 27–34, 2013.
73.
MatsudaM, ShimomuraI, SataM, AritaY, NishidaM, MaedaN, KumadaM, OkamotoY, NagaretaniH, NishizawaH, KishidaK, KomuroR, OuchiN, KiharaS, NagaiR, FunahashiT, and MatsuzawaY. Role of adiponectin in preventing vascular stenosis. The missing link of adipo-vascular axis. J Biol Chem, 277: 37487–37491, 2002.
74.
MellemkjaerS and Nielsen-KudskJE. Glibenclamide inhibits hypoxic relaxation of isolated porcine coronary arteries under conditions of impaired glycolysis. Eur J Pharmacol, 270: 307–312, 1994.
75.
MiaoCY and LiZY. The role of perivascular adipose tissue in vascular smooth muscle cell growth. Br J Pharmacol, 165: 43–658, 2012.
76.
MikamiY, ShibuyaN, KimuraY, NagaharaN, OgasawaraY, and KimuraH. Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J, 439: 479–485, 2011.
77.
MitidieriE, GurgoneD, CaiazzoE, TramontanoT, CicalaC, SorrentinoR, and d'Emmanuele di Villa BiancaR. L-cysteine/cystathionine-β-synthase-induced relaxation in mouse aorta involves a L-serine/sphingosine-1-phosphate/NO pathway. Br J Pharmacol, 177: 734–744, 2020.
78.
MitidieriE, TramontanoT, GurgioneD, CitiV, CalderoneV, BrancaleoneV, KatsoudaA, NagaharaN, PapapetropoulosA, CirinoG, d'Emmanuele di VillaBianca, and SorrentinoR. Mercaptopyruvate acts as endogenous vasodilator independently of 3-mercaptopyruvate sulfurtransferase activity. Nitric Oxide, 75: 53–59, 2018.
79.
MitidieriE, VelleccoV, BrancaleoneV, VanacoreD, ManzoOL, MartinE, SharinaI, KrutsenkoY, MontiMC, MorrettaE, PapapetropoulosA, CaliendoG, FrecenteseF, CirinoG, SorrentinoR, d'Emmanuele di Villa BiancaR, and BucciM. Involvement of 3',5'cyclic inosine monophosphate in cystathionine γ-lyase -dependent regulation of the vascular tone. Br J Pharmacol, 178: 3765–3782, 2021.
80.
MominAU, MelikianN, ShahAM, GrieveDJ, WheatcroftSB, JohnL, El GamelA, DesaiJB, NelsonT, DriverC, SherwoodRA, and KearneyMT. Leptin is an endothelial-independent vasodilator in humans with coronary artery disease: evidence for tissue specificity of leptin resistance. Eur Heart J, 27: 2294–2299, 2006.
81.
MuH, OhashiR, YanS, ChaiH, YangH, LinP, YaoQ, and ChenC. Adipokine resistin promotes in vitro angiogenesis of human endothelial cells. Cardiovasc Res, 70: 146–157, 2006.
82.
MustafaAK, GadallaMM, SenN, KimS, MuW, GaziSK, BarrowRK, YangG, WangR, and SnyderSH. H2S signal throughprotein S-sulfhydration. Sci Signal, 2: 1–8, 2009.
83.
NóbregaN, AraújoNF, ReisD, FacineLM, MirandaCAS, MotaGC, AiresRD, CapettiniLDSA, CruzJDS, and BonaventuraD. Hydrogen peroxide and nitric oxide induce anticontractile effect of perivascular adipose tissue via renin angiotensin system activation. Nitric Oxide, 84: 50–59, 2019.
84.
PayneGA, BohlenHG, DincerUD, BorbouseL, and TuneJD. Periadventitial adipose tissue impairs coronary endothelial function via PKC-beta-dependent phosphorylation of nitric oxide synthase. Am J Physiol Heart Circ Physiol, 297: 460–465, 2009.
85.
Peri-OkonnyPA, AyersC, MaaloufN, DasSR, de LemosJA, BerryJD, TurerAT, NeelandIJ, SchererPE, and VongpatanasinW. Adiponectin protects against incident hypertension independent of body fat distribution: observations from the Dallas Heart Study. Diabetes Metab Res Rev, 33: 10.1002, 2016.
86.
RamirezJG, O'MalleyEJ, and HoWSV. Pro-contractile effects of perivascular fat in health and disease. Br J Pharmacol, 174: 3482–3495, 2017.
87.
ReifenbergerMS, TurkJR, NewcomerSC, BoothFW, and LaughlinMH. Perivascular fat alters reactivity of coronary artery: effects of diet and exercise. Med Sci Sports Exerc, 39: 2125–2134, 2007.
88.
ReillyMP, LehrkeM, WolfeML, RohatgiA, LazarMA, and RaderDJ. Resistin is an inflammatory marker of atherosclerosis in humans. Circulation, 111: 932–939, 2005.
89.
SarvottamK, MaganD, YadavRK, MehtaN, and MahapatraSC. Adiponectin, interleukin-6, and cardiovascular disease risk factors are modified by a short-term yoga-based lifestyle intervention in overweight and obese men. J Altern Complement Med, 19: 397–402, 2013.
90.
SchleifenbaumJ, KöhnC, VoblovaN, DubrovskaG, ZavarirskayaO, GloeT, CreanCS, LuftFC, HuangY, SchubertR, and GollaschM. Systemic peripheral artery relaxation by KCNQ channel openers and hydrogen sulfide. J Hypertens, 28: 1875–1882, 2010.
91.
ShenL, EvansIM, SouzaD, DreifaldtM, DashwoodMR, and VidyaM-A. Adiponectin: an endothelium-derived vasoprotective factor?. Curr Vasc Pharmacol, 14: 168–174, 2016.
92.
ShibataR, OuchiN, KikuchiR, TakahashiR, TakeshitaK, KataokaY, OhashiK, IkedaN, KiharaS, and MuroharaT. Circulating omentin is associated with coronary artery disease in men. Atherosclerosis, 219: 811–814, 2011.
93.
ShibuyaN, MikamiY, KimuraY, NagaharaN, and KimuraH. Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J Biochem, 146: 623–626, 2009.
94.
ShibuyaN, TanakaM, YoshidaM, OgasawaraY, TogawaT, IshiiK, and KimuraH. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal, 11: 703–714, 2009.
95.
SmagliyLV, GusakovaSV, BirulinaYG, KovalevIV, and OrlovSN. The role of hydrogen sulfide in volume-dependent mechanisms of regulation of vascular smooth muscle cells contractile activity. Ross Fiziol Zh Im I M Sechenova, 101: 441–450, 2015.
96.
SmithRE and RobertsJC. Thermogenesis of brown adipose tissue in cold-acclimated rats. Am J Physiol, 206: 143–148, 1964.
97.
SoltisEE and CassisLA. Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin Exp Hypertens A, 13: 277–296, 1991.
98.
Souza-PaulaE, PolonioLCC, ZochioGP, Pinho da SilvaK, KushimaH, and Dias-JuniorCA. Anticontractile effect of perivascular adipose tissue but not of endothelium is enhanced by hydrogen sulfide stimulation in hypertensive pregnant rat aortae. J Cardiovasc Pharmacol, 76: 715–729, 2020.
99.
SteppanCM, BaileyST, BhatS, BrownEJ, BanerjeeRR, WrightCM, PatelHR, AhimaRS, and LazarMA. The hormone resistin links obesity to diabetes. Nature, 409: 307–312, 2001.
100.
SunY, XunK, WangC, ZhaoH, BiH, ChenX, and WangY. Adiponectin, an unlocking adipocytokine. Cardiovasc Ther, 27: 59–75, 2009.
101.
SzaboC.Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov, 6: 917–935, 2007.
102.
SzaszT and WebbRC. Perivascular adipose tissue: more than just structural support. Clin Sci (Lond), 122: 1–12, 2012.
103.
TahergorabiZ and KhazaeiM. Leptin and its cardiovascular effects: focus on angiogenesis. Adv Biomed Res, 4: 79, 2015.
104.
TanoJY, SchleifenbaumJ, and GollaschM. Perivascular adipose tissue, potassium channels, and vascular dysfunction. Arterioscler Thromb Vasc Biol, 34: 1827–1830, 2014.
105.
TestaiL, BarreseV, SoldovieriMV, AmbrosinoP, MartelliA, VinciguerraI, MiceliF, GreenwoodIA, CurtisMJ, BreschiMC, SisalliMJ, ScorzielloA, CanduelaMJ, GrandesP, CalderoneV, and TaglialatelaM. Expression and function of Kv7.4 channels in rat cardiac mitochondria: possible targets for cardioprotection. Cardiovasc Res, 110: 40–50, 2016.
106.
TorokJ, ZemancikovaA, and KocianovaZ. Interaction of perivascular adipose tissue and sympathetic nerves in arteries from normotensive and hypertensive rats. Physiol Res, 65: 391–399, 2016.
107.
UemuraY, ShibataR, KanemuraN, OhashiK, KambaraT, Hiramatsu-ItoM, EnomotoT, YuasaD, JokiY, MatsuoK, ItoM, HayakawaS, OgawaH, MuroharaT, and OuchiN. Adipose-derived protein omentin prevents neointimal formation after arterial injury. FASEB J, 29: 141–151, 2015.
108.
Van de VoordeJ, BoydensC, PauwelsB, and DecaluweK. Perivascular adipose tissue, inflammation and vascular dysfunction in obesity. Curr Vasc Pharmacol, 12: 403–411, 2014.
109.
VecchioneC, MaffeiA, ColellaS, AretiniA, PouletR, FratiG, GentileMT, FrattaL, TrimarcoV, TrimarcoB, and LemboG. Leptin effect on endothelial nitric oxide is mediated through Akt-endothelial nitric oxide synthase phosphorylation pathway. Diabetes, 51: 168–173, 2002.
110.
VerlohrenS, DubrovskaG, TsangSY, EssinK, LuftFC, HuangY, and GollaschM. Visceral periadventitial adipose tissue regulates arterial tone of mesenteric arteries. Hypertension, 44: 271–276, 2004.
111.
WangP, XuTY, GuanYF, SuDF, FanGR, and MiaoCY. Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc Res, 81: 370–380, 2009.
112.
WangR.Hydrogen sulphide: a new EDRF. Kidney Int, 76: 700–704, 2009.
113.
WebbGD, LimLH, OhVMS, YeoSB, CheongYP, AliMY, OakleyRE, LeeCN, WongPS, CalebMG, Salto-TellezM, BhatiaM, ChanESY, TaylorEA, and MoorePK. Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. J Pharmacol Exp Ther, 324: 876–88, 20082.
114.
WestonAH, EgnerI, DongY, PorterEL, HeagertyAM, and EdwardsG. Stimulated release of a hyperpolarizing factor (ADHF) from mesenteric artery perivascular adipose tissue: involvement of myocyte BKCa channels and adiponectin. Br J Pharmacol, 169: 1500–1509, 2013.
115.
WeyerC, FunahashiT, TanakaS, HottaK, MatsuzawaY, PratleyRE, and TataranniPA. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab, 86: 1930–1935, 2001.
116.
WithersSB, BusseyCE, SaxtonSN, MelroseHM, WatkinsAE, and HeagertyAM. Mechanisms of adiponectin-associated perivascular function in vascular disease. Arterioscler Thromb Vasc Biol, 34: 1637–1642, 2014.
117.
WolkR and SomersVK. Leptin and vascular function: friend or foe?. Eur Heart J, 27: 2263–2265, 2006.
118.
XuA and VanhouttePM. Adiponectin and adipocyte fatty acid binding protein in the pathogenesis of cardiovascular disease. Am J Physiol Heart Circ Physiol, 302: 1231–1240, 2012.
119.
YadavPK, YamadaK, ChikuT, KoutmosM, and BanerjeeR. Structure and kinetic analysis of H2S production by human mercaptopyruvate sulfurtransferase. J Biol Chem, 288: 20002–20013, 2013.
120.
YamawakiH, TsubakiN, MukohdaM, OkadaM, and HaraY. Omentin, a novel adipokine, induces vasodilation in rat isolated blood vessels. Biochem Biophys Res Commun, 393: 668–672, 2010.
121.
YangG and WangR. H2S and blood vessels: an overview. Handb Exp Pharmacol, 230: 85–110, 2015.
122.
YangG, WuL, JiangB, YangW, QiJ, CaoK, MengQ, MustafaAK, MuW, ZhangS, SnyderSH, and WangR. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science, 322: 587–590, 2008.
123.
YangRZ, LeeMJ, HuH, PrayJ, WuHB, HansenBC, ShuldinerAR, FriedSK, McLenithanJC, and GongDW. Identification of omentin as a novel depot-specific adipokine in human adipose tissue: possible role in modulating insulin action. Am J Physiol Endocrinol Metab, 290: 1253–1261, 2006.
124.
YaturuS, DaberryRP, RainsJ, and JainS. Resistin and adiponectin levels in subjects with coronary artery disease and type 2 diabetes. Cytokine, 34: 219–223, 2006.
125.
YuPL, WangC, LiW, and ZhangFX. Visfatin level and the risk of hypertension and cerebrovascular accident: a systematic review and meta-analysis. Horm Metab Res, 51: 220–229, 2019.
126.
ZavaritskayaO, ZhuravlevaN, SchleifenbaumJ, GloeT, DevermannL, KlugeR, MladenovM, FreyM, GagovH, FésusG, GalloschM, and SchubertR. Role of KCNQ channels in skeletal muscle arteries and periadventitial vascular dysfunction. Hypertension, 61: 151–159, 2013.
ZhangP, WangY, FanY, TangZ, and WangN. Overexpression of adiponectin receptors potentiates the antiinflammatory action of subeffective dose of globular adiponectin in vascular endothelial cells. Arterioscler Thromb Vasc Biol, 29: 67–74, 2009.
129.
ZhangW, ShuC, LiQ, LiM, and LiX. Adiponectin affects vascular smooth muscle cell proliferation and apoptosis through modulation of the mitofusin-2-mediated Ras-Raf-Erk1/2 signaling pathway. Mol Med Rep, 12: 4703–4707, 2015.
130.
ZhangYY, ShiYN, ZhuN, ZhaoTJ, Yi-JieGuo, LiaoDF, DaiAG, and QinL. PVAT targets VSMCs to regulate vascular remodeling: angel or demon. J Drug Target, 3: 1–38, 2020.
131.
ZhaoW, NdisangJF, and WangR. Modulation of endogenous production of H2S in rat tissues. Can J Physiol Pharmacol, 81: 848–853, 2003.
132.
ZhaoW and WangR. H2S-induced vasorelaxation and underlying cellular and molecular mechanisms. Am J Physiol Heart Circ Physiol, 283: H474–H480, 2002.
133.
ZhaoW, ZhangJ, LuY, and WangR. The vasorelaxant effect of H2S as a novel endogenous gaseous K(ATP) channel opener. EMBO J, 20: 6008–6016, 2001.
134.
ZhouZ, MartinE, SharinaI, EspositoI, SzaboC, BucciM, CirinoG, and PapapetropoulosA. Regulation of soluble guanylyl cyclase redox state by hydrogen sulfide. Pharmacol Res, 111: 556–562, 2016.
