The role of hydrogen sulphide in blood pressure regulation

Physiological Research

Volumn 65, Issue , 2016, Pages S273-S289

  Cacanyiova, S ^a   Berenyiova, A ^a   Kristek, F ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Hydrogen sulphide; Hypertension; Nitric oxide; Nitroso sulphide; Vascular tone

Indexed keywords

GASOTRANSMITTER; HYDROGEN SULFIDE; NITRIC OXIDE;

ADRENERGIC SYSTEM; ANIMAL; BLOOD PRESSURE; HYPERTENSION; MECHANOTRANSDUCTION; METABOLISM; PATHOPHYSIOLOGY; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION; VASODILATATION;

ANIMALS; BLOOD PRESSURE; GASOTRANSMITTERS; HYDROGEN SULFIDE; HYPERTENSION; MECHANOTRANSDUCTION, CELLULAR; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE; RATS; RATS, INBRED SHR; VASOCONSTRICTION; VASODILATION; VASOMOTOR SYSTEM;

EID: 84997426766     PISSN: 08628408     EISSN: 18029973     Source Type: Journal    
DOI: 10.33549/physiolres.933438     Document Type: Review

References (88)

1. ABE K, KIMURA H: The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16: 1066-1071, 1996.
2. ALI MY, PING CY, MOK YY, LING L, WHITEMAN M, BHATIA M, MOORE PK: Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol 149: 625-634, 2006.
3. BERENYIOVA A, CACANYIOVA S, KRISTEK F, MALEKOVA M: Vasoactive effect of NO and H2S interaction on thoracic aorta in young normotensive and spontaneously hypertensive rats. Cardiol Lett 22: 11S-12S, 2013.
4. BERENYIOVA A, GRMAN M, MIJUSJOVIC A, STASKO A, MISAK A, NAGY P, ONDRAISOVA E, CACANYIOVA S, BREZOVA V, FEELISCH M, ONDRIAS K: The reaction products of sulfide and S-nitrosoglutathione are potent vasorelaxants. Nitric Oxide 46: 123-130, 2015.
5. BERTOVA A, CACANYIOVA S, KRISTEK F, KRIZANOVA O, ONDRIAS K, TOMASKOVA Z: The hypothesis of the main role of H2S in coupled sulphide-nitroso signalling pathway. Gen Physiol Biophys 29: 402-410, 2010.
6. BOBKO AA, KHRAMTSOV VV: Mechanistic studies of oxidative decomposition of Angeli's salt and PAPA NONOate. Nitric Oxide 40: 92-98, 2014.
7. BOULANGER CM, HEYMES C, BENESSIANO J, GESKE RS, LEVY BI, VANHOUTTE PM: Neuronal nitric oxide synthase is expressed in rat vascular smooth muscle cells: activation by angiotensin II in hypertension. Circ Res 83: 1271-1278, 1998.
8. BUCCI M, PAPAPETROPOULOS A, VELLECCO V, ZHOU Z, PYRIOCHOU A, ROUSSOS C, ROVIEZZO F, BRANCALEONE V, CIRINO G: Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol 30: 1998-2004, 2010.
9. BUCHWALOW LB, CACANYIOVA S, NEUMANN J, SAMOILOVA VE, BOECKER W, KRISTEK F: The role of arterial smooth muscle in vasorelaxation. Biochem Biophy Res Commun 377: 504-507, 2008.
10. CACANYIOVA S, DOVINOVA I, KRISTEK F: The role of oxidative stress in acetylcholine-induced relaxation of endothelium-denuded arteries. J Physiol Pharmacol 64: 241-247, 2013.
11. CHARLES CJ, RADEMAKER MT, RICHARDS AM: Apelin 13 induces a biphasic haemodynamic response and hormonal activation in normal conscious sheep. J Endocrinol 189: 701-710, 2006.
12. CHEANG WS, WONG WT, SHEN B, LAU CW, TIAN XY, TSANG SY, YAO X, CHEN ZY, HUANG Y: 4-aminopyridine-sensitive K+ channels contribute to NaHS-induced membrane hyperpolarization and relaxation in the rat coronary artery. Vasc Pharmacol 53: 94-98, 2010.
13. CHEN L, INGRID S, DING YG, LIU Y, OI JG, TANG CS, DU JB: Imbalance of endogenous homocysteine and hydrogen sulfide metabolic pathway in essential hypertensive children. Chin Med J (Engl) 120: 389-393, 2007.
14. CHENG Y, NDISANG JF, TANG G, CAO K, WANG R: Hydrogen sulfide-induced relaxation of resistance mesenteric artery beds of rats. Am J Physiol Heart Circ Physiol 287: H2316-H2323, 2004.
15. COLETTA C, PAPAPETROPOULOS A, ERDELYI K, OLAH G, MóDIS K, PANOPOULOS P, ASIMAKOPOULOU A, GERö D, SHARINA I, MARTIN E, SZABO C: Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA 109: 9161-9166, 2012.
16. CORTESE-KROTT MM, FERNANDEZ BO, SANTOS JL, MERGIA E, GRMAN M, NAGY P, KELM M, BUTLER A, FEELISCH M: Nitrosopersulfide (SSNO-) accounts for sustained NO bioactivity of S-nitrosothiols following reaction with sulfide. Redox Biol 2: 234-244, 2014.
17. CORTESE-KROTT MM, KUHNLE GG, DYSON A, FERNANDEZ BO, GRMAN M, DUMOND JF, BAROWW MP, MCLEOD G, NAKAGAWA H, ONDRIAS K, NAGY P, KING SB, SAAVEDRA JE, KEEFER LK, SINGER M, KELM M, BUTLER AR, FEELISCH M: Key bioactive reaction products of the NO/H2S interaction are S/N-hybrid species, polysulfides, and nitroxyl. Proc Natl Acad Sci USA 112: E4651-E4660, 2015.
18. DAS UN: Essential fatty acids: biochemistry, physiology and pathology. Biotechnol J 1: 420-439, 2006.
19. DOELLER JE, ISBELL TS, BENAVIDES G, KOENITZER J, PATEL H, PATEL RP, LANCASTER JR, DARLEYUSMAR VM, KRAUS DW: Polarographic measurement of hydrogen sulfide production and consumption by mammalian tissues. Anal Biochem 341: 40-51, 2005.
20. DROBNA M, MISIAK A, HOLLAND T, KRISTEK F, GRMAN M, TOMASOVA M, BERENYIOVA A, CACANYIOVA S, ONDRIAS K: Captopril partially decreases the effect of H2S on rat blood pressure and inhibits H2S-induced nitric oxide release from S-nitrosoglutathione. Physiol Res 64: 479-486, 2015.
21. DURANTE W, JOHNSON FK, JOHNSON RA: Role of carbon monoxide in cardiovascular funcion. J Cell Mol Med 10: 672-686, 2006.
22. FILIPOVIC MR, MILJKOVIC J, NAUSER T, ROYZEN M, KLOS K, SHUBINA T, KOPPENOL WH, LIPPARD SJ, IVANOVIC-BURMAZOVIC I: Chemical characterization of the smallest S-nitrosothiol, HSNO; cellular cross-talk of H2S and S-nitrosothiols. J Am Chem Soc 134: 12016-12027, 2012.
23. FURCHGOTT RF, ZAWADZKI JV: The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376, 1980.
24. FURNE J, SPRINGFIELD J, KOENIG T, DEMASTER E, LEVITT MD: Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem Pharmacol 62: 255-259, 2001.
25. FURNE J, SAEED A, LEVITT MD: Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am J Physiol Regul Integr Comp Physiol 295: R1479-R1485, 2008.
26. GAO L, WANG W, LI YL, SCHULTZ HD, LIU D, CORNISH KG, ZUCKER IH: Sympathoexcitation by central ANG II: Roles for AT1 receptor upregulation and NAD(P)H oxidase in RVLM. Am J Physiol Heart Circ Physiol 288: H2271-H2279, 2005.
27. GARDINER SM, MARCH JE, KEMP PA, BENETT T: Bolus injection of human UII in conscious rats evokes a biphasic haemodynamic response. Br J Pharmacol 143: 422-430, 2004.
28. GENG B, YANG J, QI Y, ZHAO J, PANG Y, DU J, TANG C: H2S generated by heart in rat and its effects on cardiac function. Biochem Biophys Res Commun 313: 362-368, 2004.
29. 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 293: R1608-R1618, 2007.
30. GEROVá M, MESAROŠ S, KITTOVá M, HATRIK S, KRISTEK F, MALINSKI T: Nitric oxide in the periendothelial area of femoral vein of the dog assessed in vivo by a porphyrinic sensor. Physiol Res 45: 285-289, 1996.
31. GINES FF, VINCENTE KE, RICCA R: Right ventricle systolic pressure increase following intravenous acetylcholine injection. Acta Physiol Pharmacol Ther Latinoam 44: 77-84, 1994.
32. GREINER R, PáLINKáS Z, BäSELL K, BECHER D, ANTELMANN H, NAGY P, DICK TP: Polysulfides link H2S to protein thiol oxidation. Antioxid Redox Signal 19: 1749-1765, 2013.
33. GRMAN M, MISAK A, JACOB C, TOMASKOVA Z, BERTOVA A, BURKHOLZ T, DOCOLOMANSKY P, HABALA L, ONDRIAS K: Low molecular thiols, pH and O2 modulate H2S-induced S-nitrosoglutathione decomposition - NO release. Gen Physiol Biophys 32: 429-444, 2013.
34. 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: 527-531, 1997.
35. ISHIGAMI M, HIRAKI K, UMEMURA K, OGASAWARA Y, ISHII K, KIMURA H: Hydrogen sulfide and a mechanism of its release in the brain. Antioxid Redox Signal 11: 205-214, 2009.
36. 2+ sparks. Am J Physiol Heart Circ Physiol 304: H1446-H1454, 2013.
37. KIMURA H: Hydrogen sulfide: its production, release and functions. Amino Acids 43: 113-121, 2010.
38. KIMURA H: Hydrogen sulfide and polysulfides as biological mediators, Molecules 19: 16146-16157, 2015.
39. KING AJ, PFEFFER JM, PFEFFER MA, BRENNER BM: Systemic hemodynamic effects of endothelin in rats. Am J Physiol 258: H787-H792, 1990.
40. 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 232: 138-146, 2007.
41. LAGGNER H, HERMANN M, ESTERBAUER H, MUELLNER MK, EXNER M, GMEINER BM, KAPIOTIS S: The novel gaseous vasorelaxant hydrogen sulfide inhibits angiotensin-converting enzyme activity of endothelial cells. J Hypertens 25: 2100-2104, 2007.
42. LEE SW, CHENG Y, MOORE PK, BIAN JS: Hydrogen sulphide regulates intracellular pH in vascular smooth muscle cells. Biochem Biophys Res Commun 358: 1142-1147, 2007.
43. LEVITT MD, ABDEL-REHIM MS, FURNE J: Free and acid labile hydrogen sulfide concentrations in mouse tissues: anomalously high free hydrogen sulfide in aortic tissue. Antioxid Redox Signal 15: 373-378, 2011.
44. LI L, WHITEMAN M, GUAN YY, NEO KL, CHENG Y, LEE SW, ZHAO Y, BASKAR R, TAN CH, MOORE PK: Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117: 2351-2360, 2008.
45. LI S, PING NN, CAO L, MI YN, CAO YX: H2S induces vasoconstriction of rat cerebral arteries via cAMP/adenylyl cyclase pathway Toxicol Appl Pharmacol 289: 389-396, 2015.
46. LIM JJ, LIU YH, KHIN ES, BIAN JS: Vasoconstrictive effect of hydrogen sulfide involves downregulation of cAMP in vascular smooth muscle cells. Am J Physiol Cell Physiol 295: C1261-C1270, 2008.
47. LIU YH, BIAN JS: Bicarbonate-dependent effect of hydrogen sulfide on vascular contractility in rat aortic rings. Am J Physiol Cell Physiol 299: C866-C872, 2010.
48. LIU YH, LU M, HU LF, WONG PT, WEBB DG, BIAN JS: Hydrogen sulphide in the mammalian cardiovascular system. Antioxid Redox Signal 17: 141-185, 2012.
49. LU M, LIU YH, GOH HS, WANG JJ, YONG QC, WANG R, BIAN JS: Hydrogen sulfide inhibits plasma renin activity. J Am Soc Nephrol 21: 993-1002, 2010.
50. LU M, LIU YH, HO CY, TIONG CX, BIAN JS: Hydrogen sulfide regulates cAMP homeostasis and renin degranulation in As4.1 and rat renin-rich kidney cells. Am J Physiol Cell Physiol 302: C59-C66, 2012.
51. LYKAKIS YN, FERRERI C, CHATGILIALOGLU C: The sulfhydryl radical (HS./HS.-): a contender for the isomerization of double bonds in membrane lipids. Angew Chem 119: 1946-1948, 2007.
52. MA S, ZHU XY, EIRIN A, WOOLLARD JR, JORDAN KL, TANG H, LERMAN A, LERMAN LO: Perirenal fat promotes renal arterial endothelial dysfunction in obese swine through tumor necrosis factor-a. J Urol 195: 1152-1159, 2016.
53. MALEKOVA L, KRIZANOVA O, ONDRIAS K: H2S and HS-donor NaHS inhibits intracellular chloride channels. Gen Physiol Biophys 28: 190-194, 2009.
54. MARKS GS, BRIEN JF, NAKATSU K, MCLAUGHLIN BE: Does carbon monoxide have a physiological function? Trends Pharmacol Sci 12: 185-188, 1991.
55. MIERSCH S, MUTUS B: Protein S-nitrosation: Biochemistry and characterization of protein thiol-NO interactions as cellular signaling. Clin Biochem 38: 777-791, 2005.
56. MUELLNER MK, SCHREIER SM, LAGGER M, HERMANN H, ESTERBAUER H, EXNER BM, GMEINER BM, KAPIOTIS S: Hydrogen sulfide destroys lipid hydoperoxides in oxidized LDL. Biochem J 420: 277-281, 2009.
57. MUSTAFA AK, SIKKA G, GAZI SK, STEPPAN J, JUNG SM, BHUNIA AK, BARODKA VM, GAZI FK, BARROW RK, WANG R, AMZEL LM, BERKOWITZ DE, SNYDER SH: Hydrogen sulfide as endotheliumderived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 109: 1259-1268, 2011.
58. NG ES, CHENG ZJ, ELLIS A, DING H, JIANG Y, LI Y, HOLLENBERG MD, TRIGGLE CR: Nitrosothiol stores in vascular tissue: modulation by ultraviolet light, acetylcholine and ionomycin. Eur J Pharmacol 560: 183-192, 2007.
59. ONDRIAS K, STASKO A, CACANYIOVA S, SULOVA Z, KRIZANOVA O, KRISTEK F, MALEKOVA L, KNEZL V, BEIER A: H2S and HS-donor NaHS releases nitric oxide from nitrosothiols, metal nitrosyl complex, brain homogenate and murine L1210 leukaemia cells. Pflugers Arch 457: 271-279, 2008.
60. PALMER RM, FERRIGE AG, MONCADA S: Nitric oxide release accounts for the biological activity of endotheliumderived relaxing factor. Nature 327: 524-526, 1987.
61. PEERS C, BAUER CC, BOYLE JP, SCRAGG JL, DALLAS ML: Modulation of ion channels by hydrogen sulfide. Antioxid Redox Signal 17: 95-105, 2012.
62. PECHáNOVá O: Contribution of captopril thiol group to the prevention of spontaneous hypertension. Physiol Res 56 (Suppl 2): S41-S48, 2007.
63. 2+ influx. Acta Physiol 214: 88-96, 2015.
64. RAM CV: Renovascular hypertension. Cardiol Clin 6: 483-508, 1988.
65. RICHARDSON CJ, MAGEE EA, CUMMINGS JH: A new method for the determination of sulphide in gastrointestinal contents and whole blood by microdistillation and ion chromatography. Clin Chim Acta 293: 115-125, 2000.
66. SHI YX, CHEN Y, ZHU YZ, HUANG GY, MOORE PK, HUANG SH, YAO T, ZHU YC: Chronic sodium hydrosulfide treatment decreases medial thickening of intramyocardial coronary arterioles, interstitial fibrosis, and ROS production in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 293: H2093-H2100, 2007.
67. SHIBUYA N, MIKAMI Y, KIMURA Y, NAGAHARA N, KIMURA H: Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J Biochem 146: 623-626, 2009.
68. SCHLEIFENBAUM J, KOHN C, VOBLOVA N, DUBROVSKA G, ZAVARIRSKAYA O, GLOE T, CREAN CS, LUFT FC, HUANG Y, SCHUBERT R, GOLLASCH M: Systemic peripheral artery relaxation by KCNQ channel openers and hydrogen sulfide. J Hypertens 28: 1875-1882, 2010.
69. STAMLER JS, LAMAS S, FANG FC: Nitrosylation: The prototypic redox-based signaling mechanism. Cell 106: 675-683, 2001.
70. - donor. Free Radic Res 43: 581-593, 2009.
71. TANG G, WU L, LIANG W, WANG R: Direct stimulation of KATP channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells. Mol Pharmacol 68: 1757-1764, 2005.
72. TOMASKOVA Z, CACANYIOVA S, BENCO A, KRISTEK F, DUGOVICOVA L, HRBAC J, ONDRIAS K: Lipids modulate H2S/HS-induced NO release from S-nitrosoglutathione. Biochem Biophys Res Commun 390: 1241-1244, 2009.
73. TOMASOVA L, PAVLOVICOVA M, MALEKOVA L, MISAK A, KRISTEK F, GRMAN M, CACANYIOVA S, TOMASEK M, TOMASKOVA Z, PERRY A, WOOD ME, LACINOVA L, ONDRIAS K, WHITEMAN M: Effects of AP39, a novel triphenylphosphonium derivatised anethole dithiolethione hydrogen sulfide donor, on rat haemodynamic parameters and chloride and calcium Cav3 and RyR2 channels. Nitric Oxide 46: 131-144, 2015.
74. WANG R: Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798, 2002.
75. WANG R: Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92: 791-896, 2012.
76. WHITEMAN M, GOODING KM, WHATMORE JL, BALL CI, MAWSON D, SKINNER K, TOOKE JE, SHORE AC: Adiposity is a major determinant of plasma levels of the novel vasodilator hydrogen sulphide. Diabetologia 53: 1722-1726, 2010.
77. WHITFIELD NL, KREIMIER EL, VERDIAL FC, SKOVGAARD N, OLSON KR: Reappraisal of H2S/sulfide concentration in vertebrate blood and its potential significance in ischemic preconditioning and vascular signaling. Am J Physiol Regul Integr Comp Physiol 294: R1930-R1937, 2008.
78. WU CC, YEN MH: Higher level of plasma nitric oxide in spontaneously hypertensive rats. Am J Hypertens 12: 476-482, 1999.
79. XIA M, CHEN L, MUH RW, LI PL, LI N: Production and actions of hydrogen sulfide, a novel gaseous bioactive substance, in the kidneys. J Pharmacol Exp Ther 329: 1056-1062, 2009.
80. YAN H, DU J, TANG C: The possible role of hydrogen sulfide on the pathogenesis of spontaneous hypertension in rats. Biochem Biophys Res Commun 313: 22-27, 2004.
81. YANG G, WU L, JIANG B, YANG W, QI J, CAO K, MENG Q, MUSTAFA AK, MU W, ZHANG S, SNYDER SH, WANG R: H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gammalyase. Science 322: 587-590, 2008.
82. YONG QC, CHOO CH, TAN BH, LOW CM, BIAN JS: Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells. Neurochem Int 56: 508-515, 2010.
83. ZHANG Y, HOGG N: S-Nitrosothiols: cellular formation and transport. Free Radic Biol Med 38: 831-838, 2005.
84. ZHAO W, WANG R: H2S-induced vasorelaxation and underlying cellular and molecular mechanisms. Am J Physiol Heart Circ Physiol 283: H474-H480, 2002.
85. 2S as a novel endogenous gaseous KATP channel opener. EMBO J 20: 6008-6016, 2001.
86. ZHAO W, NDISANG JF, WANG R: Modulation of endogenous production of H2S in rat tissues. Can J Physiol Pharmacol 81: 848-853, 2003.
87. ZHAO X, ZHANG LK, ZHANG CY, ZENG XJ, YAN H, JIN HF, TANG CS, DU JB: Regulatory effect of hydrogen sulfide on vascular collagen content in spontaneously hypertensive rats. Hypertens Res 31: 1619-1630, 2008.
88. ZHAO Y, VANHOUTTE PM, LEUNG SWS: Endothelial nitric oxide synthase-independent release of nitric oxide in the aorta of the spontaneously hypertensive rat. J Pharmacol Exp Ther 344: 15-22, 2012.