Hydrogen sulfide prodrugs-a review

Acta Pharmaceutica Sinica B

Volumn 5, Issue 5, 2015, Pages 367-377

  Zheng, Yueqin ^a   Ji, Xingyue ^a   Ji, Kaili ^a   Wang, Binghe ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Controllable H2S prodrugs; Gasotransmitters; H2S prodrugs; H2S hybrid nonsteroidal anti inflammatory drugs; Hydrogen sulfide (H2S); Hydrolysis based H2S prodrugs

Indexed keywords

1,2 DITHIOLE 3 THIONE DERIVATIVE; ANTIINFLAMMATORY AGENT; ANTINEOPLASTIC AGENT; AP 39; ATB 337; ATB 429; BISULFITE; CARDIOVASCULAR AGENT; CATALASE; CYSTATHIONINE GAMMA LYASE; CYTOCHROME C OXIDASE; DIALLYL DISULFIDE; DIALLYL TRISULFIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GASTROINTESTINAL MUCOSA PROTECTIVE AGENT; GLUTATHIONE; GYY 4137; HYDROGEN SULFIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LAWESSON REAGENT; NBS 1120; PRODRUG; S ALLYLCYSTEINE; SG 1002; UNCLASSIFIED DRUG; VASCULOTROPIN;

ACUTE HEART INFARCTION; ACUTE LUNG INJURY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTERIAL OXYGEN TENSION; CARDIOVASCULAR MORTALITY; DRUG EFFICACY; DRUG HYDROLYSIS; DRUG POTENCY; DRUG SOLUBILITY; ENZYME ACTIVITY; ENZYME INHIBITION; HEART FAILURE; HEART PROTECTION; HUMAN; IC50; NONHUMAN; NUCLEOPHILICITY; OXIDATIVE STRESS; PEAK EXPIRATORY FLOW; PROTEIN EXPRESSION; REVIEW; STOMACH INJURY; UPREGULATION;

EID: 84947202526     PISSN: 22113835     EISSN: 22113843     Source Type: Journal    
DOI: 10.1016/j.apsb.2015.06.004     Document Type: Review

References (91)

1. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 1996, 16:1066-1071.
2. Vandiver MS, Snyder SH. Hydrogen sulfide: a gasotransmitter of clinical relevance. J Mol Med 2012, 90:255-263.
3. Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 2012, 92:791-896.
4. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 2007, 6:917-935.
5. 2S)-the third gas of interest for pharmacologists. Pharmacol Rep 2007, 59:4-24.
6. 2S induces a suspended animation-like state in mice. Science 2005, 308:518.
7. Li L, Moore PK. Putative biological roles of hydrogen sulfide in health and disease: a breath of not so fresh air?. Trends Pharmacol Sci 2008, 29:84-90.
8. Li T, Zhao B, Wang C, Wang H, Liu Z, Li W, 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 2008, 233:1081-1087.
9. Andruski B, McCafferty DM, Ignacy T, Millen B, McDougall JJ. Leukocyte trafficking and pain behavioral responses to a hydrogen sulfide donor in acute monoarthritis. Am J Physiol Regul Integr Comp Physiol 2008, 295:R814-R820.
10. Shrotriya S, Kundu JK, Na HK, Surh YJ. Diallyl trisulfide inhibits phorbol ester-induced tumor promotion, activation of AP-1, and expression of COX-2 in mouse skin by blocking JNK and Akt signaling. Cancer Res 2010, 70:1932-1940.
11. 2S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 2001, 20:6008-6016.
12. 2S on myogenic responses in rat cerebral arterioles. Circ J 2012, 76:1012-1019.
13. Buckler KJ. Effects of exogenous hydrogen sulphide on calcium signalling, background (TASK) K channel activity and mitochondrial function in chemoreceptor cells. Pflug Arch 2012, 463:743-754.
14. Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, et al. A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 2010, 48:931-935.
15. 2S) releasing agents: chemistry and biological applications. Chem Commun 2014, 50:11788-11805.
16. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee S, et al. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 2008, 117:2351-2360.
17. 2S)-releasing derivative of aspirin (ACS14). Neurochem Int 2012, 60:365-378.
18. 2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 2012, 13:499-507.
19. Giggenbach W. Optical spectra of highly alkaline sulfide solutions and the second dissociation constant of hydrogen sulfide. Inorg Chem 1971, 10:1333-1338.
20. 2S-rich gases. Mol Simul 2004, 30:631-648.
21. Hughes MN, Centelles MN, Moore KP. Making and working with hydrogen sulfide: the chemistry and generation of hydrogen sulfide in vitro and its measurement in vivo: a review. Free Radic Biol Med 2009, 47:1346-1353.
22. DeLeon ER, Stoy GF, Olson KR. Passive loss of hydrogen sulfide in biological experiments. Anal Biochem 2012, 421:203-207.
23. Peng B, Xian M. Hydrogen sulfide detection using nucleophilic substitution-cyclization-based fluorescent probes. Methods Enzymol 2015, 554:47-62.
24. Peng H, Cheng Y, Dai C, King AL, Predmore BL, Lefer DJ, et al. A fluorescent probe for fast and quantitative detection of hydrogen sulfide in blood. Angew Chem Int Ed 2011, 50:9672-9675.
25. Wang K, Peng H, Wang B. Recent advances in thiol and sulfide reactive probes. J Cell Biochem 2014, 115:1007-1022.
26. Lin VS, Chang CJ. Fluorescent probes for sensing and imaging biological hydrogen sulfide. Curr Opin Chem Biol 2012, 16:595-601.
27. Qian Y, Karpus J, Kabil O, Zhang S.Y, Zhu H.L, Banerjee R, et al. Selective fluorescent probes for live-cell monitoring of sulphide. Nat Commun 2011, 2:495.
28. Lippert AR, New EJ, Chang CJ Reaction-based fluorescent probes for selective imaging of hydrogen sulfide in living cells. J Am Chem Soc 2011, 133:10078-10080.
29. Miles EW, Kraus JP. Cystathionine beta-synthase: structure, function, regulation, and location of homocystinuria-causing mutations. J Biol Chem 2004, 279:29871-29874.
30. Goodwin LR, Francom D, Dieken FP, Taylor JD, Warenycia MW, Reiffenstein RJ, et al. Determination of sulfide in brain tissue by gas dialysis/ion chromatography: postmortem studies and two case reports. J Anal Toxicol 1989, 13:105-109.
31. Warenycia MW, Goodwin LR, Benishin CG, Reiffenstein RJ, Francom DM, Taylor JD, et al. Acute hydrogen sulfide poisoning. Demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels. Biochem Pharmacol 1989, 38:973-981.
32. Savage J.C, Gould D.H. Determination of sulfide in brain tissue and rumen fluid by ion-interaction reversed-phase high-performance liquid chromatography. J Chromatogr 1990, 526:540-545.
33. Stipanuk M.H, Beck P.W. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 1982, 206:267-277.
34. 2S biogenesis via alternative trans-sulfuration reactions. J Biol Chem 2009, 284:22457-22466.
35. 2S biogenesis by human cystathionine γ-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J Biol Chem 2009, 284:11601-11612.
36. 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, 11:703-714.
37. 2+ influx. J Biol Chem 2011, 286:39379-39386.
38. Milner JA. Mechanisms by which garlic and allyl sulfur compounds suppress carcinogen bioactivation. Garlic and carcinogenesis. Adv Exp Med Biol 2001, 492:69-81.
39. Rahman K. Historical perspective on garlic and cardiovascular disease. J Nutr 2001, 131:977s-979s.
40. Powolny AA, Singh SV. Multitargeted prevention and therapy of cancer by diallyl trisulfide and related Allium vegetable-derived organosulfur compounds. Cancer Lett 2008, 269:305-314.
41. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, et al. Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A 2007, 104:17977-17982.
42. Chuah SC, Moore PK, Zhu YZ. S-allylcysteine mediates cardioprotection in an acute myocardial infarction rat model via a hydrogen sulfide-mediated pathway. Am J Physiol Heart Circ Physiol 2007, 293:H2693-H2701.
43. Amagase H. Clarifying the real bioactive constituents of garlic. J Nutr 2006, 136:716s-725s.
44. Truong D, Hindmarsh W, OBrien PJ. The molecular mechanisms of diallyl disulfide and diallyl sulfide induced hepatocyte cytotoxicity. Chem Biol Interact 2009, 180:79-88.
45. Huang C, Kan J, Liu X, Ma F, Tran B.H, Zou Y, et al. Cardioprotective effects of a novel hydrogen sulfide agent-controlled release formulation of S-propargyl-cysteine on heart failure rats and molecular mechanisms. PLoS One 2013, 8:e69205.
46. 2S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation 2013, 127:1116-1127.
47. Ellis AJ, Giggenbach W. Hydrogen sulphide ionization and sulphur hydrolysis in high temperature solution. Geochim Cosmochim Acta 1971, 35:247-260.
48. Chen YH, Wu R, Geng B, Qi Y.F, Wang PP, Yao W.Z, et al. Endogenous hydrogen sulfide reduces airway inflammation and remodeling in a rat model of asthma. Cytokine 2009, 45:117-123.
49. Esechie A, Kiss L, Olah G, Horvath EM, Hawkins H, Szabo C, et al. Protective effect of hydrogen sulfide in a murine model of acute lung injury induced by combined burn and smoke inhalation. Clin Sci 2008, 115:91-97.
50. Zhi L, Ang A.D, Zhang H, Moore PK, Bhatia M. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-κB pathway. J Leukoc Biol 2007, 81:1322-1332.
51. Zhang H, Zhi L, Moochhala SM, Moore PK, Bhatia M. Endogenous hydrogen sulfide regulates leukocyte trafficking in cecal ligation and puncture-induced sepsis. J Leukoc Biol 2007, 82:894-905.
52. Zhang H, Hegde A, Ng SW, Adhikari S, Moochhala SM, Bhatia M. Hydrogen sulfide up-regulates substance P in polymicrobial sepsis-associated lung injury. J Immunol 2007, 179:4153-4160.
53. 2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science 2008, 322:587-590.
54. Ghasemi M, Dehpour AR, Moore KP, Mani AR. Role of endogenous hydrogen sulfide in neurogenic relaxation of rat corpus cavernosum. Biochem Pharmacol 2012, 83:1261-1268.
55. Tumir H, Bosnir J, Vedrina-Dragojevic I, Dragun Z, Tomic S, Puntaric D Preliminary investigation of metal and metalloid contamination of homeopathic products marketed in Croatia. Homeopathy 2010, 99:183-188.
56. 2S): a new antihypertensive drug?. Med Hypotheses 2009, 73:445-447.
57. Ozturk T, Ertas E, Mert O. Use of Lawesson[U+05F3]s reagent in organic syntheses. Chem Rev 2007, 107:5210-5278.
58. Li L, Rossoni G, Sparatore A, Lee LC, del Soldato P, Moore PK. Anti-inflammatory and gastrointestinal effects of a novel diclofenac derivative. Free Radic Biol Med 2007, 42:706-719.
59. Nicolau LA, Silva RO, Damasceno SR, Carvalho NS, Costa NR, Aragao KS, et al. The hydrogen sulfide donor, Lawesson[U+05F3]s reagent, prevents alendronate-induced gastric damage in rats. Braz J Med Biol Res 2013, 46:708-714.
60. Medeiros JV, Bezerra VH, Gomes AS, Barbosa AL, Lima-Junior RC, Soares PM, et al. Hydrogen sulfide prevents ethanol-induced gastric damage in mice: role of ATP-sensitive potassium channels and capsaicin-sensitive primary afferent neurons. J Pharmacol Exp Ther 2009, 330:764-770.
61. Wu Z, Peng H, Du Q, Lin W, Liu Y. GYY4137, a hydrogen sulfidereleasing molecule, inhibits the inflammatory response by suppressing the activation of nuclear factor κB and mitogenactivated protein kinases in Coxsackie virus B3infected rat cardiomyocytes. Mole Med Rep 2015, 11:1837-1844.
62. Lee ZW, Zhou J, Chen CS, Zhao Y, Tan CH, Li L, et al. The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLoS One 2011, 6:e21077.
63. Wallace JL. Hydrogen sulfide-releasing anti-inflammatory drugs. Trends Pharmacol Sci 2007, 28:501-505.
64. Rose P, Moore PK, Ming SH, Nam OC, Armstrong JS, Whiteman M. Hydrogen sulfide protects colon cancer cells from chemopreventative agent β-phenylethyl isothiocyanate induced apoptosis. World J Gastroenterol 2005, 11:3990-3997.
65. Cai W.J, Wang M.J, Ju L.H, Wang C, Zhu Y.C. Hydrogen sulfide induces human colon cancer cell proliferation: role of Akt, ERK and p21. Cell Biol Int 2010, 34:565-572.
66. Park CM, Zhao Y, Zhu Z, Pacheco A, Peng B, devarie-Baez NO, et al. Synthesis and evaluation of phosphorodithioate-based hydrogen sulfide donors. Mol Biosyst 2013, 9:2430-2434.
67. 2S donors: l-cysteine-activated releasing properties and vascular effects in vitro and in vivo. ACS Med Chem Lett 2013, 4:904-908.
68. 2S) releasing agents: chemistry and biological applications. Chem Commun 2014, 50:11788-11805.
69. 2S-releasing drugs as pharmaceuticals. J Med Chem 2010, 53:6275-6286.
70. Schnitzer TJ, Burmester GR, Mysler E, Hochberg MC, Doherty M, Ehrsam E, et al. Comparison of lumiracoxib with naproxen and ibuprofen in the therapeutic arthritis research and gastrointestinal event trial (TARGET), reduction in ulcer complications: randomised controlled trial. Lancet 2004, 364:665-674.
71. Singh G, Fort JG, Goldstein JL, Levy RA, Hanrahan PS, Bello AE, et al. Celecoxib versus naproxen and diclofenac in osteoarthritis patients: SUCCESS-I study. Am J Med 2006, 119:255-266.
72. Kurahara K, Matsumoto T, Iida M, Honda K, Yao T, Fujishima M. Clinical and endoscopic features of nonsteroidal anti-inflammatory drug-induced colonic ulcerations. Am J Gastroenterol 2001, 96:473-480.
73. Sparatore A, Santus G, Giustarini D, Rossi R, Del Soldato P. Therapeutic potential of new hydrogen sulfide-releasing hybrids. Expert Rev Clin Pharmacol 2011, 4:109-121.
74. Chan MV, Wallace JL. Hydrogen sulfide-based therapeutics and gastrointestinal diseases: translating physiology to treatments. Am J Physiol Gastrointest Liver Physiol 2013, 305:G467-G473.
75. Wallace J.L, Caliendo G, Santagada V, Cirino G, Fiorucci S. Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulfide-releasing diclofenac derivative in the rat. Gastroenterology 2007, 132:261-271.
76. Fiorucci S, Orlandi S, Mencarelli A, Caliendo G, Santagada V, Distrutti E, Santucci L, Cirino G, Wallace J.L. Enhanced activity of a hydrogen sulphide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. Br J Pharmacol 2007, 150:996-1002.
77. Chattopadhyay M, Kodela R, Nath N, Dastagirzada YM, velazquez-Martinez CA, Boring D, et al. Hydrogen sulfide-releasing NSAIDs inhibit the growth of human cancer cells: a general property and evidence of a tissue type-independent effect. Biochem Pharmacol 2012, 83:715-722.
78. Chattopadhyay M, Kodela R, Olson KR, Kashfi K. NOSH-aspirin (NBS-1120), a novel nitric oxide- and hydrogen sulfide-releasing hybrid is a potent inhibitor of colon cancer cell growth in vitro and in a xenograft mouse model. Biochem Biophys Res Commun 2012, 419:523-528.
79. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci U S A 2007, 104:15560-15565.
80. Szabo C, Papapetropoulos A. Hydrogen sulphide and angiogenesis: mechanisms and applications. Br J Pharmacol 2011, 164:853-865.
81. Suzuki K, Olah G, Modis K, Coletta C, Kulp G, Gero D, et al. Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci U S A 2011, 108:13829-13834.
82. Sun WH, Liu F, Chen Y, Zhu YC. Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochem Biophys Res Commun 2012, 421:164-169.
83. Szczesny B, Modis K, Yanagi K, Coletta C, Le Trionnaire S, Perry A, et al. AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide 2014, 41:120-130.
84. Le Trionnaire S, Perry A, Szczesny B, Szabo C, Winyard PG, Whatmore JL, et al. The synthesis and functional evaluation of a mitochondria-targeted hydrogen sulfide donor, (10-oxo-10-(4-(3-thioxo-3H-1,2-dithiol-5-yl)phenoxy)decyl)triphenylphosphonium bromide (AP39). Med Chem Commun 2014, 5:728-736.
85. 2S) donors. J Am Chem Soc 2011, 133:15-17.
86. Zhao Y, Bhushan S, Yang C, Otsuka H, Stein JD, Pacheco A, et al. Controllable hydrogen sulfide donors and their activity against myocardial ischemia-reperfusion injury. ACS Chem Biol 2013, 8:1283-1290.
87. Roger T, Raynaud F, Bouillaud F, Ransy C, Simonet S, Crespo C, et al. New biologically active hydrogen sulfide donors. Chembiochem 2013, 14:2268-2271.
88. Devarie-Baez NO, Bagdon P.E., Peng B, Zhao Y, Park C.M., Xian M. Light-induced hydrogen sulfide release from "caged" gem-dithiols. Org Lett 2013, 15:2786-2789.
89. Fukushima N, Ieda N, Sasakura K, Nagano T, Hanaoka K, Suzuki T, et al. Synthesis of a photocontrollable hydrogen sulfide donor using ketoprofenate photocages. Chem Commun 2014, 50:587-589.
90. 2S-donors. Bioorg Med Chem 2012, 20:2675-2678.
91. Pan J, Devarie-Baez NO, Xian M. Facile amide formation via S-nitrosothioacids. Org Lett 2011, 13:1092-1094.