The Vasoactive Role of Perivascular Adipose Tissue and the Sulfide Signaling Pathway in a Nonobese Model of Metabolic Syndrome
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
APVV-15-0565
Slovak Research and Development Agency
VEGA 2/0103/18, VEGA 2/0132/20, VEGA 2/0111/19
Scientific Grant Agency of The Ministry of Education, Science, Research and Sport of the Slovak Republic
IKEM, IN 00023001
Ministry of Health of the Czech Republic under the Conceptual Development of Research Organizations Program (Institute for Clinical and Experimental Medicine
PubMed
33467512
PubMed Central
PMC7829844
DOI
10.3390/biom11010108
PII: biom11010108
Knihovny.cz E-zdroje
- Klíčová slova
- H2S, HTG, Wistar, isolated artery, metabolic syndrome, perivascular adipose tissue,
- MeSH
- aorta thoracica patofyziologie MeSH
- cévní endotel patofyziologie MeSH
- cystathionin-gama-lyasa metabolismus MeSH
- hypertriglyceridemie metabolismus MeSH
- krysa rodu Rattus MeSH
- metabolický syndrom metabolismus patofyziologie MeSH
- modely nemocí na zvířatech MeSH
- noradrenalin farmakologie MeSH
- oxidace-redukce MeSH
- potkani Wistar MeSH
- signální transdukce * MeSH
- superoxiddismutasa metabolismus MeSH
- superoxidy metabolismus MeSH
- synthasa oxidu dusnatého, typ III metabolismus MeSH
- tuková tkáň metabolismus MeSH
- vazodilatace fyziologie MeSH
- vazokonstrikce účinky léků MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cystathionin-gama-lyasa MeSH
- noradrenalin MeSH
- superoxiddismutasa MeSH
- superoxidy MeSH
- synthasa oxidu dusnatého, typ III MeSH
The aim of this study was to evaluate the mutual relationship among perivascular adipose tissue (PVAT) and endogenous and exogenous H2S in vasoactive responses of isolated arteries from adult normotensive (Wistar) rats and hypertriglyceridemic (HTG) rats, which are a nonobese model of metabolic syndrome. In HTG rats, mild hypertension was associated with glucose intolerance, dyslipidemia, increased amount of retroperitoneal fat, increased arterial contractility, and endothelial dysfunction associated with arterial wall injury, which was accompanied by decreased nitric oxide (NO)-synthase activity, increased expression of H2S producing enzyme, and an altered oxidative state. In HTG, endogenous H2S participated in the inhibition of endothelium-dependent vasorelaxation regardless of PVAT presence; on the other hand, aortas with preserved PVAT revealed a stronger anticontractile effect mediated at least partially by H2S. Although we observed a higher vasorelaxation induced by exogenous H2S donor in HTG rats than in Wistar rats, intact PVAT subtilized this effect. We demonstrate that, in HTG rats, endogenous H2S could manifest a dual effect depending on the type of triggered signaling pathway. H2S within the arterial wall contributes to endothelial dysfunction. On the other hand, PVAT of HTG is endowed with compensatory vasoactive mechanisms, which include stronger anti-contractile action of H2S. Nevertheless, the possible negative impact of PVAT during hypertriglyceridemia on the activity of exogenous H2S donors needs to be taken into consideration.
Zobrazit více v PubMed
Schleifenbaum J., Kohn C., Voblova N., Dubrovska G., Zavarirskaya O., Gloe T., Crean C.S., Luft F.C., Huang Y., Schubert R., et al. Systemic peripheral artery relaxation by KCNQ channel openers and hydrogen sulfide. J. Hypertens. 2010;28:1875–1882. doi: 10.1097/HJH.0b013e32833c20d5. PubMed DOI
Fang L., Zhao J., Chen Y., Ma T., Xu G., Tang C., Liu X., Geng B. Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator. J. Hypertens. 2009;27:2174–2185. doi: 10.1097/HJH.0b013e328330a900. PubMed DOI
Zhao W., Zhang J., Lu Y., Wang R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J. 2001;20:6008–6016. doi: 10.1093/emboj/20.21.6008. PubMed DOI PMC
Mustafa A.K., Sikka G., Gazi S.K., Steppan J., Jung S.M., Bhunia A.K., Barodka V.M., Gazi F.K., Barrow R.K., Wang R., et al. Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 2011;109:1259–1268. doi: 10.1161/CIRCRESAHA.111.240242. PubMed DOI PMC
Liu Y.H., Lu M., Hu L.F., Wong P.T.-H., Webb G.D., Bian J.-S. Hydrogen sulfide in the mammalian cardiovascular system. Antioxid. Redox. Signal. 2012;17:141–185. doi: 10.1089/ars.2011.4005. PubMed DOI
Coletta C., Papapetropoulos A., Erdelyi K., Olah G., Modis K., Panopoulos P., Asimakopoulou A., Gero D., Sharina I., Martin E., et al. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc. Natl. Acad. Sci. USA. 2012;109:9161–9166. doi: 10.1073/pnas.1202916109. PubMed DOI PMC
Kubo S., Doe I., Kurokawa Y., Nishikawa H., Kawabata A. Direct inhibition of endothelial nitric oxide synthase by hydrogen sulfide: Contribution to dual modulation of vascular tension. Toxicology. 2007;232:138–146. doi: 10.1016/j.tox.2006.12.023. PubMed DOI
Xie Z.Z., Liu Y., Bian J.S. Hydrogen Sulfide and Cellular Redox Homeostasis. Oxid. Med. Cell. Longev. 2016;2016:6043038. doi: 10.1155/2016/6043038. PubMed DOI PMC
Cacanyiova S., Majzunova M., Golas S., Berenyiova A. 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. 2019;70 doi: 10.26402/jpp.2019.2.13. PubMed DOI
Beltowski J., Jamroz-Wisniewska A. Hydrogen Sulfide in the Adipose Tissue-Physiology, Pathology and a Target for Pharmacotherapy. Molecules. 2017;22:63. doi: 10.3390/molecules22010063. PubMed DOI PMC
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;91:889–898. doi: 10.1139/cjpp-2013-0001. PubMed DOI
Vrana A., Kazdova L. The hereditary hypertriglyceridemic nonobese rat: An experimental model of human hypertriglyceridemia. Transplant. Proc. 1990;22:2579. PubMed
Zicha J., Pechanova O., Cacanyiova S., Cebova M., Kristek F., Torok J., Simko F., Dobesova Z., Kunes J. Hereditary hypertriglyceridemic rat: A suitable model of cardiovascular disease and metabolic syndrome? Physiol. Res. 2006;55(Suppl. 1):S49–S63. PubMed
Skottova N., Kazdova L., Oliyarnyk O., Vecera R., Sobolova L., Ulrichova J. Phenolics-rich extracts from Silybum marianum and Prunella vulgaris reduce a high-sucrose diet induced oxidative stress in hereditary hypertriglyceridemic rats. Pharmacol. Res. 2004;50:123–130. doi: 10.1016/j.phrs.2003.12.013. PubMed DOI
Cacanyiova S., Cebova M., Kunes J., Kristek F. Comparison of vascular function and structure of iliac artery in spontaneously hypertensive and hereditary hypertriglyceridemic rats. Physiol. Res. 2006;55(Suppl. 1):S73–S80. PubMed
Pechanova O., Bernatova I., Pelouch V., Simko F. Protein remodelling of the heart in NO-deficient hypertension: The effect of captopril. J. Mol. Cell. Cardiol. 1997;29:3365–3374. doi: 10.1006/jmcc.1997.0566. PubMed DOI
Skop V.C., Malinska H., Trnovska J., Huttl M., Cahova M., Blachnio-Zabielska A., Baranowski M., Burian M., Oliyarnyk O., Kazdova L. Positive effects of voluntary running on metabolic syndrome-related disorders in non-obese hereditary hypertriacylglycerolemic rats. PLoS ONE. 2015;10:e0122768. doi: 10.1371/journal.pone.0122768. PubMed DOI PMC
Markova I., Miklankova D., Huttl M., Kacer P., Skibova J., Kucera J., Sedlacek R., Kacerova T., Kazdova L., Malinska H. The Effect of Lipotoxicity on Renal Dysfunction in a Nonobese Rat Model of Metabolic Syndrome: A Urinary Proteomic Approach. J. Diabetes Res. 2019;2019:8712979. doi: 10.1155/2019/8712979. PubMed DOI PMC
Liu K., Ren X.M., You Q.S., Gu M.M., Wang F., Wang S., Ma C.H., Li W.N., Ye Q. Ameliorative Effect of Dangguibuxue Decoction against Cyclophosphamide- Induced Heart Injury in Mice. Biomed. Res. Int. 2018;2018:8503109. doi: 10.1155/2018/8503109. PubMed DOI PMC
Trovato F.M., Castrogiovanni P., Szychlinska M.A., Purrello F., Musumeci G. Impact of Western and Mediterranean Diets and Vitamin D on Muscle Fibers of Sedentary Rats. Nutrients. 2018;10:231. doi: 10.3390/nu10020231. PubMed DOI PMC
Zicha J., Kunes J., Devynck M.A. Abnormalities of membrane function and lipid metabolism in hypertension: A review. Am. J. Hypertens. 1999;12:315–331. doi: 10.1016/S0895-7061(98)00178-2. PubMed DOI
Emilova R., Dimitrova D., Mladenov M., Daneva T., Schubert R., Gagov H. Cystathionine gamma-lyase of perivascular adipose tissue with reversed regulatory effect in diabetic rat artery. Biotechnol. Biotechnol. Equip. 2015;29:147–151. doi: 10.1080/13102818.2014.991565. PubMed DOI PMC
Kaprinay B., Liptak B., Slovak L., Svik K., Knezl V., Sotnikova R., Gasparova Z. Hypertriglyceridemic rats fed high fat diet as a model of metabolic syndrome. Physiol. Res. 2016;65:S515–S518. doi: 10.33549/physiolres.933524. PubMed DOI
Torok J., Koprdova R., Cebova M., Kunes J., Kristek F. Functional and structural pattern of arterial responses in hereditary hypertriglyceridemic and spontaneously hypertensive rats in early stage of experimental hypertension. Physiol. Res. 2006;55(Suppl. 1):S65–S71. PubMed
Lu C., Su L.Y., Lee R.M.K.W., Gao Y.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. 2010;634:107–112. doi: 10.1016/j.ejphar.2010.02.006. PubMed DOI
Gao Y.J., Takemori K., Su L.Y., An W.S., Lu C., Sharma A.M., Lee R.M.K.W. Perivascular adipose tissue promotes vasoconstriction: The role of superoxide anion. Cardiovasc. Res. 2006;71:363–373. doi: 10.1016/j.cardiores.2006.03.013. PubMed DOI
Knapp L.T., Klann E. Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. J. Neurosci. 2002;22:674–683. doi: 10.1523/JNEUROSCI.22-03-00674.2002. PubMed DOI PMC
Lewis T.V., Dart A.M., Chin-Dusting J.P. Endothelium-dependent relaxation by acetylcholine is impaired in hypertriglyceridemic humans with normal levels of plasma LDL cholesterol. J. Am. Coll. Cardiol. 1999;33:805–812. doi: 10.1016/S0735-1097(98)00667-6. PubMed DOI
Gustafson B., Hammarstedt A., Andersson C.X., Smith U. Inflamed adipose tissue: A culprit underlying the metabolic syndrome and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2007;27:2276–2283. doi: 10.1161/ATVBAHA.107.147835. PubMed DOI
Rizvi A.A. Cytokine biomarkers, endothelial inflammation, and atherosclerosis in the metabolic syndrome: Emerging concepts. Am. J. Med. Sci. 2009;338:310–318. doi: 10.1097/MAJ.0b013e3181a4158c. PubMed DOI
Malinska H., Skop V., Trnovska J., Markova I., Svoboda P., Kazdova L., Haluzik M. Metformin attenuates myocardium dicarbonyl stress induced by chronic hypertriglyceridemia. Physiol. Res. 2018;67:181–189. doi: 10.33549/physiolres.933606. PubMed DOI
Kristek F., Edelsteinova S., Sebokova E., Kyselovic J., Klimes I. Structural changes in the aorta of the hereditary hypertriglyceridemic rat. Ann. N. Y. Acad. Sci. 1997;827:514–520. doi: 10.1111/j.1749-6632.1997.tb51862.x. PubMed DOI
Simko F., Pelouch V., Torok J., Luptak I., Matuskova J., Pechanova O., Babal P. Protein remodeling of the heart ventricles in hereditary hypertriglyceridemic rat: Effect of ACE-inhibition. J. Biomed. Sci. 2005;12:103–111. doi: 10.1007/s11373-004-8173-9. PubMed DOI
Banos G., Carvajal K., Cardoso G., Zamora J., Franco M. Vascular reactivity and effect of serum in a rat model of hypertriglyceridemia and hypertension. Am. J. Hypertens. 1997;10:379–388. doi: 10.1016/S0895-7061(97)90520-3. PubMed DOI
Kusterer K., Pohl T., Fortmeyer H.P., Marz W., Scharnagl H., Oldenburg A., Angermuller S., Fleming I., Usadel K.H., Busse R. Chronic selective hypertriglyceridemia impairs endothelium-dependent vasodilatation in rats. Cardiovasc. Res. 1999;42:783–793. doi: 10.1016/S0008-6363(98)00331-9. PubMed DOI
Bartus M., Lomnicka M., Lorkowska B., Franczyk M., Kostogrys R.B., Pisulewski P.M., Chlopicki S. Hypertriglyceridemia but not hypercholesterolemia induces endothelial dysfunction in the rat. Pharmacol. Rep. 2005;57:127–137. PubMed
Pechanova O., Bernatová I., Babal P., Martinez C.M., Kysela S., Stvrtina S., Andriantsitohaina R. Red wine polyphenols prevent cardiovascular alterations in L-NAME-induced hypertension. J. Hypertens. 2004;22:1551–1559. doi: 10.1097/01.hjh.0000133734.32125.c7. PubMed DOI
Chait A., Brazg R.L., Tribble D.L., Krauss R.M. Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am. J. Med. 1993;94:350–356. doi: 10.1016/0002-9343(93)90144-E. PubMed DOI
Payne G.A., Bohlen H.G., Dincer U.D., Borbouse L., Tune J.D. Periadventitial adipose tissue impairs coronary endothelial function via PKC-beta-dependent phosphorylation of nitric oxide synthase. Am. J. Physiol. Heart. Circ. Physiol. 2009;297:H460–H465. doi: 10.1152/ajpheart.00116.2009. PubMed DOI PMC
Ketonen J., Shi J., Martonen E., Mervaala E. Periadventitial adipose tissue promotes endothelial dysfunction via oxidative stress in diet-induced obese C57Bl/6 mice. Circ. J. 2010;74:1479–1487. doi: 10.1253/circj.CJ-09-0661. PubMed DOI
Kwaifa I.K., Bahari H., Yong Y.K., Noor S.M. Endothelial Dysfunction in Obesity-Induced Inflammation: Molecular Mechanisms and Clinical Implications. Biomolecules. 2020;10:291. doi: 10.3390/biom10020291. PubMed DOI PMC
Brancaleone V., Roviezzo F., Vellecco V., De Gruttola L., Bucci M., Cirino G. Biosynthesis of H2S is impaired in non-obese diabetic (NOD) mice. Br. J. Pharmacol. 2008;155:673–680. doi: 10.1038/bjp.2008.296. PubMed DOI PMC
Zaorska E., Tomasova L., Koszelewski D., Ostaszewski R., Ufnal M. Hydrogen Sulfide in Pharmacotherapy, Beyond the Hydrogen Sulfide-Donors. Biomolecules. 2020;10:323. doi: 10.3390/biom10020323. PubMed DOI PMC
Torok J., Babal P., Matuskova J., Luptak I., Klimes I., Simko F. Impaired endothelial function of thoracic aorta in hereditary hypertriglyceridemic rats. Ann. N. Y. Acad. Sci. 2002;967:469–475. doi: 10.1111/j.1749-6632.2002.tb04304.x. PubMed DOI
Cacanyiova S., Berenyiova A., Kristek F., Drobna M., Ondrias K., Grman M. The adaptive role of nitric oxide and hydrogen sulphide in vasoactive responses of thoracic aorta is triggered already in young spontaneously hypertensive rats. J. Physiol. Pharmacol. 2016;67:501–512. PubMed
Berenyiova A., Drobna M., Cebova M., Kristek F., Cacanyiova S. Changes in the vasoactive effects of nitric oxide, hydrogen sulfide and the structure of the rat thoracic aorta: The role of age and essential hypertension. J. Physiol. Pharmacol. 2018;69 doi: 10.26402/jpp.2018.4.05. PubMed DOI
Szijarto I.A., Marko L., Filipovic M.R., Miljkovic J.L., Tabeling C., Tsvetkov D., Wang N., Rabelo L.A., Witzenrath M., Diedrich A., et al. Cystathionine gamma-Lyase-Produced Hydrogen Sulfide Controls Endothelial NO Bioavailability and Blood Pressure. Hypertension. 2018;71:1210–1217. doi: 10.1161/HYPERTENSIONAHA.117.10562. PubMed DOI
Geng B., Cui Y., Zhao J., Yu F., Zhu Y., Xu G., Zhang Z., Tang C., Du J. Hydrogen sulfide downregulates the aortic L-arginine/nitric oxide pathway in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007;293:R1608–R1618. doi: 10.1152/ajpregu.00207.2006. PubMed DOI