Hydrogen sulfide in the pathogenesis of atherosclerosis and its therapeutic potential

References

• Wang R. Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J.16(13), 1792–1798 (2002).
   PubMed Web of Science ®Google Scholar
• Shibuya N, Mikami Y, Kimura Y, Nagahara N, Kimura H. Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J. Biochem.146(5), 623–626, (2009).
   PubMed Web of Science ®Google Scholar
• Shibuya N, Tanaka M, Yoshida M et al. 3-mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal.11(4), 703–714 (2009).
   PubMed Web of Science ®Google Scholar
• Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci.16(3), 1066–1071 (1996).
   PubMed Web of Science ®Google Scholar
• Zhao W, Zhang J, Lu Y, Wang R. The vasorelaxant effect of H2S as a novel endogenous gaseous K(ATP) channel opener. EMBO J.20(21), 6008–6016 (2001).
   PubMed Web of Science ®Google Scholar
• Toombs CF, Insko MA, Wintner EA et al. Detection of exhaled hydrogen sulphide gas in healthy human volunteers during intravenous administration of sodium sulphide. Br. J. Clin. Pharmacol.69(6), 626–636 (2010).
   PubMed Web of Science ®Google Scholar
• Zhu XY, Liu SJ, Liu YJ, Wang S, Ni X. Glucocorticoids suppress cystathionine γ-lyase expression and H2S production in lipopolysaccharide-treated macrophages. Cell. Mol. Life Sci.67(7), 1119–1132 (2010).
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhao X, Jin H et al. Role of hydrogen sulfide in the development of atherosclerotic lesions in apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol.29(2), 173–179 (2009).
   PubMed Web of Science ®Google Scholar
• Whiteman M, Armstrong JS, Chu SH et al. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite ‘scavenger’? J. Neurochem.90(3), 765–768 (2004).
   PubMed Web of Science ®Google Scholar
• Chang L, Geng B, Yu F et al. Hydrogen sulfide inhibits myocardial injury induced by homocysteine in rats. Amino Acids34(4), 573–585 (2008).
   PubMed Web of Science ®Google Scholar
• Muzaffar S, Shukla N, Bond M et al. Exogenous hydrogen sulfide inhibits superoxide formation, NOX-1 expression and Rac1 activity in human vascular smooth muscle cells. J. Vasc. Res.45(6), 521–528 (2008).
   PubMed Web of Science ®Google Scholar
• Whiteman M, Li L, Rose P, Tan CH, Parkinson DB, Moore PK. The effect of hydrogen sulfide donors on lipopolysaccharide-induced formation of inflammatory mediators in macrophages. Antioxid. Redox Signal.12(10), 1147–1154 (2010).
   PubMed Web of Science ®Google Scholar
• Jain SK, Bull R, Rains JL et al. Low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocin-treated rats causes vascular inflammation? Antioxid. Redox Signal.12(11), 1333–1337 (2010).
   PubMed Web of Science ®Google Scholar
• Li T, Zhao B, Wang C et al. Regulatory effects of hydrogen sulfide on IL-6, IL-8 and IL-10 levels in the plasma and pulmonary tissue of rats with acute lung injury. Exp. Biol. Med.233, 1081–1087 (2008).
   PubMed Web of Science ®Google Scholar
• Elrod JW, Calvert JW, Morrison J et al. Hydrogen sulphide attenuates myocardial ischemia–reperfusion injury by preservation of mitochondrial function. Proc. Natl Acad. Sci. USA104(39), 15560–15565 (2007).
   PubMed Web of Science ®Google Scholar
• Sen U, Mishra PK, Tyagi N, Tyagi SC. Homocysteine to hydrogen sulfide or hypertension. Cell. Biochem. Biophys.57(2–3), 49–58 (2010).
   PubMed Web of Science ®Google Scholar
• Zhang D, Jiang X, Fang P et al. Hyperhomocysteinemia promotes inflammatory monocyte generation and accelerates atherosclerosis in transgenic cystathionine β-synthase-deficient mice. Circulation120(19), 1893–1902 (2009).
   PubMed Web of Science ®Google Scholar
• Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulphide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J.20, E1411–E1418 (2006).
   Google Scholar
• Yusof M, Kamada K, Kalogeris T, Gaskin FS, Korthuis RJ. Hydrogen sulphide triggers late-phase preconditioning in postischemic small intestine by an NO- and p38 MAPK-dependent mechanism. Am. J. Physiol. Heart Circ. Physiol.296, H868–H876 (2009).
   PubMed Web of Science ®Google Scholar
• Yang G, Wu L, Jiang B et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science322(5901), 587–590 (2008).
   PubMed Web of Science ®Google Scholar
• Gupta S, Kühnisch J, Mustafa A et al. Mouse models of cystathionine β-synthase deficiency reveal significant threshold effects of hyperhomocysteinemia. FASEB J.23(3), 883–893 (2009).
   PubMed Web of Science ®Google Scholar
• Zhao W, Wang R. H2S-induced vasorelaxation and underlying cellular and molecular mechanisms. Am. J. Physiol. Heart Circ. Physiol.283(2), H474–H480 (2002).
   PubMed Web of Science ®Google Scholar
• Laggner H, Hermann M, Esterbauer H et al. The novel gaseous vasorelaxant hydrogen sulfide inhibits angiotensin-converting enzyme activity of endothelial cells. J. Hypertens.25(10), 2100–2104 (2007).
   PubMed Web of Science ®Google Scholar
• Hosoki R, Matsuki N, Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem. Biophys. Res. Commun.237(3), 527–531 (1997).
   PubMed Web of Science ®Google Scholar
• Yong QC, Hu LF, Wang S, Huang D, Lee HS, Bian JS. Hydrogen sulfide interacts with nitric oxide in the heart – possible involvement of nitroxyl. Cardiovasc. Res.88(3), 482–491 (2010).
   PubMed Web of Science ®Google Scholar
• Oh GS, Pae HO, Lee BS et al. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic. Biol. Med.41(1), 106–119 (2006).
   PubMed Web of Science ®Google Scholar
• 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. Toxicology232(1–2), 138–146 (2007).
   PubMed Web of Science ®Google Scholar
• DeGraba TJ. Expression of inflammatory mediators and adhesion molecules in human atherosclerotic plaque. Neurology49(5 Suppl. 4), S15–S19 (1997).
   PubMed Web of Science ®Google Scholar
• Blankenberg S, Barbaux S, Tiret L. Adhesion molecules and atherosclerosis. Atherosclerosis170(2), 191–203 (2003).
   PubMed Web of Science ®Google Scholar
• Clarke R, Daly L, Robinson K et al. Hyperhomocysteinemia: an independent risk factor for vascular disease. N. Engl. J. Med.324(17), 1149–1155 (1991).
   PubMed Web of Science ®Google Scholar
• Boushey CJ, Beresford SA, Omenn GS, Motulsky AG. A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. JAMA274(13), 1049–1057 (1995).
   PubMed Web of Science ®Google Scholar
• Eikelboom JW, Lonn E, Genest J Jr, Hankey G, Yusuf S. Homocyst(e)ine and cardiovascular disease: a critical review of the epidemiologic evidence. Ann. Intern. Med.131(5), 363–375 (1999).
   PubMed Web of Science ®Google Scholar
• Wang H, Jiang XH, Yang F et al. Hyperhomocysteinemia accelerates atherosclerosis in cystathionine β-synthase and apolipoprotein E double knock-out mice with and without dietary perturbation. Blood101(10), 3901–3907 (2003).
   PubMed Web of Science ®Google Scholar
• Dayal S, Bottiglieri T, Arning E et al. Endothelial dysfunction and elevation of S-adenosylhomocysteine in cystathionine β-synthase-deficient mice. Circ. Res.88, 1203–1209 (2001).
   PubMed Web of Science ®Google Scholar
• Eberhardt RT, Forgione MA, Cap A et al. Endothelial dysfunction in a murine model of mild hyperhomocyst(e)inemia. J. Clin. Invest.106(4), 483–491 (2000).
   PubMed Web of Science ®Google Scholar
• Weiss N, Heydrick S, Zhang Y-Y, Cierl C, Cap A, Loscalzo J. Cellular redox state and endothelial dysfunction in mildly hyperhomocysteinemic cystathionine β-synthase-deficient mice. Arterioscler. Thromb. Vasc. Biol.2, 34–41 (2001).
   Google Scholar
• Weiss N, Zhang Y-Y, Heydrick S, Bierl C, Loscalzo J. Overexpression of cellular glutathionine peroxidise rescues homocyst(e)ine-induced endothelial dysfunction. Proc. Natl Acad. Sci. USA98(22), 12503–12508 (2001).
   PubMed Web of Science ®Google Scholar
• Dickhout JG, Sood SK, Austin RC. Role of endoplasmic reticulum calcium disequilibria in the mechanism of homocysteine-induced ER stress. Antioxid. Redox Signal.9, 1863–1873 (2007).
   PubMed Web of Science ®Google Scholar
• Werstuck GH, Lentz SR, Dayal S et al. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J. Clin. Invest.107, 1263–1273 (2001).
   PubMed Web of Science ®Google Scholar
• Wei H, Zhang R, Jin H et al. Hydrogen sulfide attenuates hyperhomocysteinemia-induced cardiomyocytic endoplasmic reticulum stress in rats. Antioxid. Redox Signal.12(9), 1079–1091 (2010).
   PubMed Web of Science ®Google Scholar
• Zhou J, Lhotak S, Hilditch BA, Austin RC. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apoplipoprotein E-deficient mice. Circulation111, 1814–1821 (2005).
   PubMed Web of Science ®Google Scholar
• Zulli A, Lau E, Wijaya BP et al. High dietary taurine reduces apoptosis and atherosclerosis in the left main coronary artery: association with reduced CCAAT/enhancer binding protein homologous protein and total plasma homocysteine but not lipidemia. Hypertension53, 1017–1022 (2009).
   PubMed Web of Science ®Google Scholar
• Sen U, Basu P, Abe OA et al. Hydrogen sulfide ameliorates hyperhomocysteinemia-associated chronic renal failure. Am. J. Physiol. Renal Physiol.2, F410–F419 (2009).
   Google Scholar
• Tyagi N, Moshal KS, Sen U et al. H2S protects against methionine-induced oxidative stress in brain endothelial cells. Antioxid. Redox Signal.11, 25–33 (2009).
   PubMed Web of Science ®Google Scholar
• Yang G, Yang W, Wu L, Wang R. H2S, endoplasmic reticulum stress, and apoptosis of insulin-secreting b cells. J. Biol. Chem.282(22), 16567–16576 (2007).
   PubMed Web of Science ®Google Scholar
• Yan SK, Chang T, Wang H, Wu L, Wang R, Meng QH. Effects of hydrogen sulfide on homocysteine-induced oxidative stress in vascular smooth muscle cells. Biochem. Biophys. Res. Commun.351(2), 485–491 (2006).
   PubMed Web of Science ®Google Scholar
• Calvert JW, Jha S, Gundewar S et al. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ. Res.105(4), 365–374 (2009).
   PubMed Web of Science ®Google Scholar
• Itoh K, Chiba T, Takahashi S et al. An Nrf2/small Maf heterodimer mediates the induction of Phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun.236(2), 313–322 (1997).
   PubMed Web of Science ®Google Scholar
• Zhu H, Itoh K, Yamamoto M, Zweier JL, Li Y. Role of Nrf2 signaling in regulation of antioxidants and Phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett.579(14), 3029–3036 (2005).
   PubMed Web of Science ®Google Scholar
• Benavides GA, Squadrito GL, Mills RW et al. Hydrogen sulfide mediates the vasoactivity of garlic. Proc. Natl Acad. Sci. USA104(46), 17977–17982 (2007).
   PubMed Web of Science ®Google Scholar
• Fisher CD, Augustine LM, Maher JM et al. Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2. Drug Metab. Dispos.35(6), 995–1000 (2007).
   PubMed Web of Science ®Google Scholar
• Lonn E, Yusuf S, Arnold MJ et al. Homocysteine lowering with folic acid and B vitamins in vascular disease. N. Engl. J. Med.354(15), 1567–1577 (2006).
   PubMed Web of Science ®Google Scholar
• Clarke R, Halsey J, Lewington S et al. Effects of lowering homocysteine levels with B vitamins on cardiovascular disease, cancer, and cause-specific mortality: Meta-analysis of 8 randomized trials involving 37 485 individuals. Arch. Intern. Med.170(18), 1622–1631 (2010).
   PubMed Web of Science ®Google Scholar
• Du J, Hui Y, Cheung Y et al. The possible role of hydrogen sulfide as a smooth muscle cell proliferation inhibitor in rat cultured cells. Heart Vessels19(2), 75–80 (2004).
   PubMed Web of Science ®Google Scholar
• Yang G, Cao K, Wu L, Wang R. Cystathionine γ-lyase overexpression inhibits cell proliferation via a H2S-dependent modulation of ERK1/2 phosphorylation and p21Cip/WAK-1. J. Biol. Chem.279(47), 49199–49205 (2004).
   PubMed Web of Science ®Google Scholar
• Yang G, Wu L, Bryan S, Khaper N, Mani S, Wang R. Cystathionine γ-lyase deficiency and overproliferation of smooth muscle cells. Cardiovasc. Res.86(3), 487–495 (2010).
   PubMed Web of Science ®Google Scholar
• Baskar R, Sparatore A, Del Soldato P, Moore PK. Effect of S-diclofenac, a novel hydrogen sulfide releasing derivative inhibit rat vascular smooth muscle cell proliferation. Eur. J. Pharmacol.594(1–3), 1–8 (2008).
   PubMed Web of Science ®Google Scholar
• Yang G, Wu L, Wang R. Pro-apoptotic effect of endogenous H2S on human aorta smooth muscle cells. FASEB J.20(3), 553–555 (2006).
   PubMed Web of Science ®Google Scholar
• Geng B, Chang L, Pan C et al. Endogenous hydrogen sulphide regulation of myocardial injury induced by isoproterenol. Biochem. Biophys. Res. Commun.318(3), 756–763 (2004).
   PubMed Web of Science ®Google Scholar
• Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulphide (H2S) protects against regional myocardial ischemia–reperfusion injury – evidence for a role of KATP channels. Basic Res. Cardiol.101(1), 53–60 (2006).
   PubMed Web of Science ®Google Scholar
• Bian JS, Yong QC, Pan TT et al. Role of hydrogen sulphide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes. J. Pharmacol. Exp. Ther.316(2), 670–678 (2006).
   PubMed Web of Science ®Google Scholar
• Abedin M, Tintut Y, Demer LL. Vascular calcification: mechanisms and clinical ramifications. Arterioscler. Thromb. Vasc. Biol.24(7), 1161–1170 (2004).
   PubMed Web of Science ®Google Scholar
• Wu SY, Pan CS, Geng B et al. Hydrogen sulfide ameliorates vascular calcification induced by vitamin D3 plus nicotine in rats. Acta Pharmacol. Sin.27(3), 299–306 (2006).
   PubMedGoogle Scholar
• Li J, Chai S, Tang C, Du J. Homocysteine potentiates calcification of cultured rat aortic smooth muscle cells. Life Sci.74(4), 451–461 (2003).
   PubMed Web of Science ®Google Scholar
• Predmore BL, Alendy MJ, Ahmed KI, Leeuwenburgh C, Julian D. The hydrogen sulphide signalling system: changes during aging and the benefits of caloric restriction. Age32(4), 467–481 (2010).
   PubMedGoogle Scholar
• Zhang X-H, Lowe D, Giles P, Fell S, Connock MJ, Maslin DJ. Gender may affect the action of garlic oil on plasma cholesterol and glucose levels of normal subjects. J. Nutr.131, 1471–1478 (2001).
   PubMed Web of Science ®Google Scholar
• Cai W-J, Wang M-J, Moore PK, Jin H-M, Yao T, Zhu Y-C. The novel proangiogenic effect of hydrogen sulphide is dependent on Akt phosphorylation. Cardiovasc. Res.76, 29–40 (2007).
   PubMed Web of Science ®Google Scholar
• Papapetropoulos A, Pyriochou A, Altaany Z et al. Hydrogen sulphide is an endogenous stimulator of angiogenesis. Proc. Natl Acad. Sci. USA106(51), 21972–21977 (2009).
   PubMed Web of Science ®Google Scholar
• Jacobs RL, House JD, Brosnan ME, Brosnan JT. Efects of streptozotocin-induced diabetes and of insulin treatment on homocysteine metabolism in the rat. Diabetes47, 1967–1970 (1998).
   PubMed Web of Science ®Google Scholar
• Yusuf M, Huat BT, Hsu A, Whiteman M, Bhatia M, Moore PK. Streptozotocin-induced diabetes in the rat is associated with enhanced tissue hydrogen sulphide biosynthesis. Biochem. Biophys. Res. Commun.333, 1146–1152 (2005).
   PubMed Web of Science ®Google Scholar
• Yang W, Yang G, Jia X, Wu L, Wang R. Activation of KATP channels by H2S in rat insulin-secreting cells and the underlying mechanisms. J. Physiol.569(2), 519–531 (2005).
   PubMed Web of Science ®Google Scholar
• Laggner H, Muellner MK, Schreier S et al. Hydrogen sulphide: a novel physiological inhibitor of LDL atherogenic modification by HOCl. Free Radic. Res.41(7), 741–747 (2007).
   PubMed Web of Science ®Google Scholar
• Jeney V, Komodi E, Nagy E et al. Supression of hemin-mediated oxidation of low-density lipoprotein and subsequent endothelial reactions by hydrogen sulphide (H2S). Free Radic. Res.46, 616–623 (2009).
   Google Scholar
• Muellner MK, Schreier SM, Laggner H et al. Hydrogen sulphide destroys lipid hydroperoxides in oxidized LDL. Biochem. J.420, 277–281 (2009).
   PubMed Web of Science ®Google Scholar
• Li L, Salto-Tellez M, Tan CH, Whiteman M, Moore PK. GYY4137, a novel hydrogen sulfide-releasing molecule, protects against endotoxic shock in the rat. Free Radic. Biol. Med.47(1), 103–113 (2009).
   PubMed Web of Science ®Google Scholar
• Yanfei W, Lin S, Junbao D, Chaoshu T. Impact of L-arginine on hydrogen sulphide/cystathionine-γ-lyase pathway in rats with high blood flow-induced pulmonary hypertension. Biochem. Biophys. Res. Commun.345, 851–857 (2006).
   PubMed Web of Science ®Google Scholar
• Derwall M, Westerkamp M, Lower C et al. Hydrogen sulphide does not increase resuscitability in a porcine model of prolonged cardiac arrest. Shock34(2), 190–195 (2010).
   PubMed Web of Science ®Google Scholar