Potential role of hydrogen sulfide in the pathogenesis of vascular dysfunction in septic shock

Current Vascular Pharmacology

Volumn 11, Issue 2, 2013, Pages 208-221

  Coletta, Ciro ^a   Szabo, Csaba ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Blood flow; cGMP; Circulatory shock; Endothelium; Endotoxin; Nitric oxide; Peroxynitrite; Sepsis; Smooth muscle; Superoxide; Vascular

Indexed keywords

5 HYDROXYDECANOIC ACID; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CAPSAZEPINE; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYSTATHIONINE BETA LYASE; CYSTATHIONINE GAMMA LYASE; DEXAMETHASONE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIUM DERIVED RELAXING FACTOR; GLIBENCLAMIDE; HEME OXYGENASE 1; HYDROGEN SULFIDE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.1; MYELOPEROXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA; VANILLOID RECEPTOR 1;

BIOSYNTHESIS; BURN; HUMAN; NEUROGENIC INFLAMMATION; NONHUMAN; PANCREATITIS; PATHOPHYSIOLOGY; PAW EDEMA; REVIEW; SEPTIC SHOCK; VASCULAR DISEASE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; PRINCIPAL COMPONENT ANALYSIS; SHOCK, SEPTIC; VASCULAR DISEASES; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

ANIMALS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HUMANS; HYDROGEN SULFIDE; MUSCLE, SMOOTH, VASCULAR; PRINCIPAL COMPONENT ANALYSIS; SHOCK, SEPTIC; VASCULAR DISEASES;

EID: 84875327172     PISSN: 15701611     EISSN: 18756212     Source Type: Journal    
DOI: 10.2174/1570161111311020010     Document Type: Review

References (116)

1. Vincent JL. Cardiovascular alterations in septic shock. J Antimicrob Chemother 1998;41:S9-15.
2. Ruokonen E, Parviainen I, Uusaro A. Treatment of impaired perfusion in septic shock. Ann Med 2002;34:590-7.
3. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003;348:1546-54.
4. Assreuy J. Nitric oxide and cardiovascular dysfunction in sepsis. Endocr Metab Immune Disord Drug Targets. 2006;6:165-73.
5. Vincent JL. Clinical sepsis and septic shock--definition, diagnosis and management principles. Langenbecks Arch Surg 2008;393: 817-24.
6. Myburgh JA. Catecholamines for shock: the quest for high-quality evidence. Crit Care Resusc 2007;9:352-6.
7. Dellinger RP, Levy MM, Carlet JM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med 2008;36:296-327.
8. Leone M, Martin C. Vasopressor use in septic shock: an update. Curr Opin Anaesthesiol 2008;21:141-7.
9. Russel JA. The current management of septic shock. Minerva Med 2008;99:431-58.
10. Dünser MW, Hasibeder WR. Sympathetic overstimulation during critical illness: adverse effects of adrenergic stress. J Intensive Care Med 2009;24:293-316.
11. Levy B, Dusang B, Annane D, Gibot S, Bollaert PE; College Interregional des Réanimateurs du Nord-Est. Cardiovascular response to dopamine and early prediction of outcome in septic shock: a prospective multiple-center study. Crit Care Med 2005;33: 2172-7.
12. Micek ST, Shah P, Hollands JM, Shah RA, Shannon WD, Kollef MH. Addition of vasopressin to norepinephrine as independent predictor of mortality in patients with refractory septic shock: an observational study. Surg Infect (Larchmt) 2007;8:189-200.
13. Drexler H. Endothelial dysfunction: clinical implications. Prog Cardiovasc Dis 1997;39:287-324.
14. Hein OV, Misterek K, Tessmann JP, van Dossow V, Krimphove M, Spies C. Time course of endothelial damage in septic shock: prediction of outcome. Crit Care 2005;9:R323-30.
15. Grandel U, Grimminger F. Endothelial responses to bacterial toxins in sepsis. Crit Rev Immunol 2003;23:267-99.
16. Matsuda N, Hattori Y. Vascular biology in sepsis: pathophysiological and therapeutic significance of vascular dysfunction. J Smooth Muscle Res 2007;43:117-37.
17. Lucas R, Verin AD, Black SM, Catravas JD. Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochem Pharmacol 2009;77:1763-72.
18. Gando S. Microvascular thrombosis and multiple organ dysfunction syndrome. Crit Care Med 2010;38:S35-42.
19. Legrand M, Klijn E, Payen D, Ince C. The response of the host microcirculation to bacterial sepsis: does the pathogen matter? J Mol Med 2010;88:127-33.
20. Szabó C, Módis K. Pathophysiological roles of peroxynitrite in circulatory shock. Shock 2010;34 (Suppl 1):1-14.
21. Szabó C. Alterations in the production of nitric oxide in various forms of circulatory shock. New Horizons 1995;3:3-32.
22. Huet O, Dupic L, Harrois A, Duranteau J. Oxidative stress and endothelial dysfunction during sepsis. Front Biosci 2011;16:1986-95.
23. Levy B, Collin S, Sennoun N, et al. Vascular hyporesponsiveness to vasopressors in septic shock: from bench to bedside. Intensive Care Med 2010;36:2019-29.
24. Parratt JR. Nitric oxide in sepsis and endotoxaemia. J Antimicrob Chemother 1998;41 (Suppl A):31-9.
25. Cobb JP. Nitric oxide synthase inhibition as therapy for sepsis: a decade of promise. Surg Infect (Larchmt) 2001; 2:93-100.
26. Szabó C, Wu CC. Role of nitric oxide in the development of vascular contractile dysfunction in circulatory shock. J Med Sci 2011;31:1-16.
27. Beauchamp RO Jr, Bus JS, Popp JA, Boreiko CJ, Andjelkovich DA. A critical review of the literature on hydrogen sulfide toxicity. Crit Rev Toxicol 1984;13:25-97.
28. Turner RM, Fairhurst S. Toxicology of substances in relation to major hazards: hydrogen sulphide. London: HSE Books; 1980.
29. Reiffenstein RJ, Hulbert WC, Roth SH: Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 1992;32:109-134.
30. Munke M, Kraus JP, Ohura T and Francke U. The gene for cystathionine b-synthase (CBS) maps to the subtelomeric region on human chromosome 21q and to proximal mouse chromosome 17. Am J Hum Genet 1988;42:550-559.
31. Kery V, Poneleit L and Kraus JP. Trypsin cleavage of human cystathionine b-synthase into an evolutionary conserved active core: structural and functional consequences. Arch Biochem Biophys 1998;355:222-232.
32. Meier M, Janosik M, Kery V, Kraus JP, Burkhard P. Structure of human cystathionine beta-synthase: a unique pyridoxal 5'-phosphate-dependent heme protein. EMBO J 2001;20:3910-6.
33. Kabil O, Zhou Y and Banerjee R. Human cystathionine b-synthase is a target for sumoylation. Biochemsitry 2006;45:13528-13536.
34. Agrawal N, Banerjee R. Human polycomb 2 protein is a SUMO E3 ligase and alleviates substrate-induced inhibition of cystathionine b-synthase sumoylation. PLoS One 2008;3:e4032.
35. Kraus JP, Janosík M, et al. Cystathionine beta-synthase mutations in homocystinuria. Hum Mutat 1999;13:362-75.
36. Meier M, Oliveriusova J, Kraus JP, Burkhard P. Structural insights into mutations of cystathionine beta-synthase. Biochim Biophys Acta 2003;1647:206-13.
37. Chiku T, Padovani D, Zhu W, Singh S, Vitvitsky V, Banerjee R.J. H2S biogenesis by human cystathionine gamma-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. Biol Chem 2009;284:11601-12.
38. Yang G, Wu L, Jiang B, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008;322:587-590.
39. Mustafa AK, Gadalla MM, Snyder SH. Signaling by gasotransmitters. Sci Signal 2009;2:re2.
40. Mustafa AK, Gadalla MM, Sen N, et al. H2S signals through protein S-sulfhydration. Sci Signal 2009;2:ra72.
41. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 1996;16:1066-1071.
42. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 2009;11:703-14.
43. Shibuya N, Mikami Y, Kimura Y, Nagahara N, Kimura H. Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J Biochem 2009;146:623-6.
44. Nagahara N, Katayama A. Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteinesulfenate in the maintenance of redox homeostasis. J Biol Chem 2005;280:34569-76.
45. Nagahara N, Yoshii T, Abe Y, Matsumura T. Thioredoxindependent enzymatic activation of mercaptopyruvate sulfurtransferase. An intersubunit disulfide bond serves as a redox switch for activation. J Biol Chem 2007 282:1561-9.
46. Zottola MA, Beigel K, Soni SD, Lawrence R. Disulfides as cyanide antidotes: evidence for a new in vivo oxidative pathway for cyanide detoxification. Chem Res Toxicol 2009;22:1948-53.
47. Belardinelli MC, Chabli A, Chadefaux-Vekemans B, Kamoun P. Urinary sulfur compounds in Down syndrome. Clin Chem 2001;47:1500-1.
48. 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 2001;62:255-259.
49. Levitt MD, Furne J, Springfield J, Suarez F, DeMaster E: Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest 1999;104:1107-1114.
50. Picton R, Eggo MC, Merrill GA, Langman MJ, Singh S. Mucosal protection against sulphide: importance of the enzyme rhodanese. Gut 2002;50:201-205.
51. Suzuki K, Olah G, Modis K, et al. Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci USA 2011;108:13829-34.
52. Lawrence NS, Davis J and Compton RG. Analytical strategies for the detection of sulfide: a review. Talanta 2000;52:771-784.
53. Richardson CJ, Magee EA and Cummings JH. A new method for the determination of sulphide in gastrointestinal contents and whole blood by microdistillation and ion chromatography. Clin Chim Acta 2000;293:115-125.
54. Chen L, Ingrid S, Ding YG, et al. Imbalance of endogenous homocysteine and hydrogen sulfide metabolic pathway in essential hypertensive children. Chin Med J 2000;120:389-393.
55. 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 2008;295: R1479-R1485.
56. Wintner, EA, Deckwerth TL, Langston W, et al. A monobromobimane-based assay to measure the pharmacokinetic profile of reactive sulphide species in blood. Br J Pharmacol 2010:160:941-957.
57. Hosoki R, Matsuki N and Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 1997;237:527-531.
58. Cheng Y, Ndisang JF, Tang G, Cao K and Wang R. Hydrogen sulfide-induced relaxation of resistance mesenteric artery beds of rats. Am J Physiol Heart Circ Physiol 2004;287:H2316-H2323.
59. Zhao W, Zhang J, Lu Y, Wang R. The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 2001;20:6008-6016.
60. Bucci M, Papapetropoulos A, Vellecco V, et al. cGMP-Dependent Protein Kinase Contributes to Hydrogen Sulfide-Stimulated Vasorelaxation. PLoS One 2012;7:e53319.
61. Bucci M, Cirino G. Hydrogen sulphide in heart and systemic circulation. Inflamm Allergy Drug Targets 2011;10:103-8.
62. Shesely EG, Maeda N, Kim HS, et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 1996;93:13176-81.
63. Ishii I, Akahoshi N, Yamada H, Nakano S, Izumi T, Suematsu M. Cystathionine γ-lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury. J Biol Chem 2010;285:26358-26368.
64. Kubo S, Doe I, Kurokawa Y, Kawabata A. Hydrogen sulfide causes relaxation in mouse bronchial smooth muscle. J Pharmacol Sci 2007;104:392-6.
65. Kiss L, Deitch EA and Szabo C. Hydrogen sulfide decreases adenosine triphosphate levels in aortic rings and leads to vasorelaxation via metabolic inhibition. Life Sci 2008;83:589-594.
66. Koenitzer JR, Isbell TS, Patel HD, et al. Hydrogen sulfide mediates vasoactivity in an O2-dependent manner. Am J Physiol Heart Circ Physiol 2007;292:H1953-60.
67. Kimura H. Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 2000;267: 129-33.
68. Yong QC, Pan TT, Hu LF, Bian JS. Negative regulation of betaadrenergic function by hydrogen sulphide in the rat hearts. J Mol Cell Cardiol 2008 44:701-10.
69. Bucci M, Papapetropoulos A, Vellecco V, et al. Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol 2010 30:1998-2004.
70. Coletta C, Papapetropoulos A, Erdelyi K, 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, Jun 5;109(23):9161-6.
71. Alioua A, Tanaka Y, Wallner M, et al. The large conductance, voltage-dependent, and calcium-sensitive K channel, Hslo, is a target of cGMP-dependent protein kinase phosphorylation in vivo. J Biol Chem 1998;273:32950-32956.
72. Han J, Kim N, Joo H, Kim E, Earm Y. ATP-sensitive K+ channel activation by nitric oxide and protein kinase G in rabbit ventricular myocytes. Am J Physiol Heart Circ Physiol 2002;283:H1545-H1554.
73. Ali MY, Ping CY, Mok YY, et al. Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol 2006;149:625-34.
74. Liu YH, Bian JS. Bicarbonate-dependent effect of hydrogen sulfide on vascular contractility in rat aortic rings. Am. J. Physiol. Cell Physiol 2010;299:C866-C872.
75. Whiteman M, Li L, Kostetski I, et al. Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulfide. Biochem Biophys Res Commun 2006;343:303-310.
76. d'Emmanuele di Villa Bianca R, Sorrentino R, Coletta C, et al. Hydrogen sulfide-induced dual vascular effect involves arachidonic acid cascade in rat mesenteric arterial bed. J Pharmacol Exp Ther 2011 337:59-64.
77. Zhao W, Ndisang JF, Wang R. Modulation of endogenous production of H2S in rat tissues. Can J Physiol Pharmacol 2003; 81:848-53.
78. Łowicka E, Bełtowski J. Hydrogen sulfide (H2S)-the third gas of interest for pharmacologists. Pharmacol Rep 2007;59:4-24.
79. Kubo S, Kurokawa Y, Doe I, Masuko T, Sekiguchi F, Kawabata A. Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 2007;241:92-7.
80. Bauer CC, Boyle JP, Porter KE, Peers C. Modulation of Ca(2+) signalling in human vascular endothelial cells by hydrogen sulfide. Atherosclerosis 2000;209:374-380.
81. Papapetropoulos A, Pyriochou A, Altaany Z, et al. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci USA 2009;106:21972-21977.
82. Cai WJ, Wang MJ, Moore PK, Jin HM, Yao T, Zhu YC. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res 2007;76:29-40.
83. Minamishima S, Bougaki M, Sips PY, et al. Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation 2009;120:888-896.
84. Yusof M, Kamada K, Kalogeris T, Gaskin FS, Korthuis RJ. Hydrogen sulfide triggers late-phase preconditioning in postischemic small intestine by an NO-and p38 MAPK-dependent mechanism. Am J Physiol Heart Circ Physiol 2009;296:H868-H876.
85. Kilbourn RG Nitric oxide overproduction in septic shock--methemoglobin concentrations and blockade with diaspirin crosslinked hemoglobin. Crit Care Med 1997;25:1446-7.
86. Rangel-Frausto MS, Pittet D, Costigan M, Hwang T, Davis CS, Wenzel RP. The natural history of the systemic inflammatory response syndrome (SIRS). A prospective study. JAMA 1995;273:117-123.
87. Lorigados CB, Soriano FG, Szabo C. Pathomechanisms of myocardial dysfunction in sepsis. Endocr Metab Immune Disord Drug Targets 2010;10:274-84.
88. Zhang H, Zhi L, Moore PK, Bhatia M. Role of hydrogen sulfide in cecal ligation and puncture-induced sepsis in the mouse. Am J Physiol Lung Cell Mol Physiol 2006;290:L1193-L1201.
89. Hui Y, Du J, Tang C, Bin G, Jiang H. Changes in arterial hydrogen sulfide (H2S) content during septic shock and endotoxin shock in rats. J Infect 2003;47:155-160.
90. Li L, Bhatia M, Zhu YZ et al. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J 2005;19:1196-1198.
91. Collin M, Anuar FB, Murch O, Bhatia M, Moore PK, Thiemermann C. Inhibition of endogenous hydrogen sulfide formation reduces the organ injury caused by endotoxemia. Br J Pharmacol 2005;146:498-505.
92. Li L, Whiteman M, Moore PK. Dexamethasone inhibits lipopolysaccharide-induced hydrogen sulphide biosynthesis in intact cells and in an animal model of endotoxic shock. J Cell Mol Med 2009 13:2684-92.
93. Chen D, Pan H, Li C, Lan X, Liu B, Yang G. Effects of hydrogen sulfide on a rat model of sepsis-associated encephalopathy. J Huazhong Univ Sci Technolog Med Sci 2011;31:632-6.
94. Bhatia M, Sidhapuriwala J, Moochhala SM, Moore PK. Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat. Br. J. Pharmacol 2005;145:141-144.
95. Bhatia M, Sidhapuriwala JN, Ng SW, Tamizhselvi R, Moochhala SM. Proinflammatory effects of hydrogen sulphide on substance P in cerulein-induced acute pancreatitis. J Cell Mol Med 2008;12:580-590.
96. Zhang J, Sio SW, Moochhala S, Bhatia M. Role of hydrogen sulfide in severe burn injury-induced inflammation in mice. Mol Med 2010;16:417-424.
97. Whiteman M, Haigh R, Tarr JM, Gooding KM, Shore AC, Winyard PG. Detection of hydrogen sulfide in plasma and knee-joint synovial fluid from rheumatoid arthritis patients: relation to clinical and laboratory measures of inflammation. Ann NY Acad Sci 2010;1203:146-150.
98. Shi W, Cui N, Wu Z, et al. Lipopolysaccharides up-regulate Kir6.1/SUR2B channel expression and enhance vascular KATP channel activity via NF-NNB-dependent signaling. J Biol Chem 2010;285:3021-3029.
99. Landry DW, Oliver JA. The ATP-sensitive K+ channel mediates hypotension in endotoxemia and hypoxic lactic acidosis in dog. J Clin Invest 1992;89:2071-4.
100. Sorrentino R, Bianca R, Lippolis L, Sorrentino L, Autore G, Pinto A. Involvement of ATP-sensitive potassium channels in a model of a delayed vascular hyporeactivity induced by lipopolysaccharide in rats. Br J Pharmacol 1999;127:1447-53.
101. Vanelli G, Hussain SNA, Aguggini G. Glibenclamide, a blocker of ATP-sensitive potassium channels, reverses endotoxin-induced hypotension in pig. Exp Physiol 1995;80:167-70.
102. Kane GC, Lam CF, O'Cochlain F, et al. Gene knockout of the KCNJ8-encoded Kir6.1 K(ATP) channel imparts fatal susceptibility to endotoxemia FASEB J 2006;20:2271-80.
103. Trevisani M, Patacchini R, Nicoletti P et al. Hydrogen sulfide causes vanilloid receptor 1-mediated neurogenic inflammation in the airways. Br J Pharmacol 2005;145:1123-1131.
104. di Villa Bianca R, Coletta C, Mitidieri E, et al. Hydrogen sulphide induces mouse paw oedema through activation of phospholipase A2. Br J Pharmacol 2010;161:1835-42.
105. Ang SF, Moochhala SM, Bhatia M. Hydrogen sulfidde promotes transient receptor potential vanilloid 1-mediated neurogenic inflammation in polymicrobial sepsis. Crit Care Med 2010;38:619-628.
106. Muellner MK, Schreier SM, Laggner H et al. Hydrogen sulfide destroys lipid hydroperoxides in oxidized LDL. Biochem J 2009;420:277-281.
107. Szabó G, Veres G, Radovits T, et al. Cardioprotective effects of hydrogen sulfide. Nitric Oxide 2011;25:201-10.
108. Tyagi N, Moshal KS, Sen U, et al. H2S protects against methionine-induced oxidative stress in brain endothelial cells. Antioxid. Redox Signal 2009;11:25-33.
109. Wagner F, Wagner K, Weber S, et al. Inflammatory effects of hypothermia and inhaled H2S during resuscitated, hyperdynamic murine septic shock. Shock 2011;35:396-402.
110. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 2006;20:2118-2120.
111. Spiller F, Orrico MI, Nascimento DC, et al. Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. Am J Respir Crit Care Med 2010;182:360-8.
112. 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 2009;47:103-113.
113. Miller TW, Wang EA, Gould S, et al. Hydrogen sulfide is an endogenous potentiator of T cell activation. J Biol Chem 2012;287: 4211-21.
114. Shatalin K, Shatalina E, Mironov A, Nudler E. H2S: a universal defense against antibiotics in bacteria. Science 2011;334:986-90.
115. 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 2008 117:2351-60.
116. Konno R, Ikeda M, Yamaguchi K, Ueda Y, Niwa A. Nephrotoxicity of d-propargylglycine in mice. Arch Toxicol 2000;7:473-479.