Generation of DNA-damaging reactive oxygen species via the autoxidation of hydrogen sulfide under physiologically relevant conditions: Chemistry relevant to both the genotoxic and cell signaling properties of H2S

Chemical Research in Toxicology

Volumn 25, Issue 8, 2012, Pages 1609-1615

  Hoffman, Marjorie ^a   Rajapakse, Anuruddha ^a   Shen, Xiulong ^a   Gates, Kent S ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; HYDROGEN SULFIDE; HYDROXYL RADICAL; PERSULFIDE; PLASMID DNA; REACTIVE OXYGEN METABOLITE; SINGLE STRANDED DNA; SULFATE; SULFIDE; SULFITE; SUPEROXIDE; THIOL; THIOSULFATE; TRACE METAL; UNCLASSIFIED DRUG;

ARTICLE; ASSAY; AUTOOXIDATION; DNA CLEAVAGE; DNA DAMAGE; DNA STRAND CLEAVAGE ASSAY; FENTON REACTION; GENOTOXICITY; INTRACELLULAR SIGNALING; MOLECULAR MECHANICS; OXIDATION;

DNA; DNA DAMAGE; FERROUS COMPOUNDS; HYDROGEN SULFIDE; HYDROXYL RADICAL; OXIDATION-REDUCTION; PLASMIDS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS; SUPEROXIDES;

EID: 84865208348     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300066z     Document Type: Article

References (97)

1. Beauchamp, R. O., Bus, J. C., Popp, J. A., Boreiko, C. J., and Andjelkovich, D. A. (1984) A critical review of the literature on hydrogen sulfide toxicity Crit. Rev. Toxicol. 13, 25-97 (Pubitemid 14069476)
2. Truong, D. H., Eghbal, M. A., Hindmarsh, W., Roth, S. H., and O'Brien, P. J. (2006) Molecular mechanisms of hydrogen sulfide toxicity Drug Metab. Rev. 38, 733-744 (Pubitemid 44903265)
3. Dorman, D. C., Moulin, F. J.-M., McManus, B. F., Mahle, K. C., James, A. L., and Struve, M. (2002) Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium Toxicol. Sci. 65, 18-25 (Pubitemid 34092686)
4. 2S cytotoxicity mechanism involves reactive oxygen species formation and mitochodrial depolarisation Toxicology 203, 69-76 (Pubitemid 39200939)
5. Smith, L., Kruszyna, H., and Smith, R. P. (1977) The effect of methemoglobin on the inhibition of cytochrome c oxidase by cyanide, sulfide, or azide Biochem. Pharmacol. 26, 2247-2250 (Pubitemid 8338300)
6. Li, L., Rose, P., and Moore, P. K. (2011) Hydrogen sulfide and cell signaling Annu. Rev. Pharmacol. Toxicol. 51, 169-187
7. Mustafa, A. K., Gadalla, M. M., and Snyder, S. H. (2009) Signaling by gasotransmitters Sci. Signal. 2, re2
8. Olson, K. R. (2009) Is hydrogen sulfide a circulating "gasotransmitter" in vertebrate blood? Biochim. Biophys. Acta 1787, 856-863
9. Mancardi, D., Penna, C., Merlino, A., Del Soldato, P., Wink, D. A., and Pagliaro, P. (2009) Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide Biochim. Biophys. Acta 1787, 864-872
10. Pryor, W. A., Houk, K. N., Foote, C. S., Fukuto, J. M., Ingarro, L. J., Squadrito, G. L., and Davies, K. J. A. (2006) Free radical biology and medicine: it's a gas, man! Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R491-R511
11. Gadalla, M. M. and Snyder, S. H. (2010) Hydrogen sulfide as a gasotransmitter J. Neurochem. 113, 14-26
12. Banerjee, R. and Kabil, O. (2010) Redox biochemistry of hydrogen sulfide J. Biol. Chem. 285, 21903-21907
13. Olson, K. R. (2011) The therapeutic potential of hydrogen sulfide: separating hype from hope Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R297-R312
14. Zhu, L., Ang, A. D., Zhang, H., Moore, P. K., and Bhatia, M. (2007) Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kB pathway J. Leukocyte Biol. 81, 1322-1332 (Pubitemid 46702052)
15. Papapetropoulos, A., Pyriochou, A., Altaany, Z., Yang, G., Marazioti, A., Zhou, Z., Jeschke, M. G., Branski, L. K., Herndon, D. N., Wang, R., and Szabó, C. (2009) Hydrogen sulfide is an endogenous stimulator of angiogenesis Proc. Natl. Acad. Sci. U.S.A. 106, 21972-21977
16. Calvert, J. W., Jha, S., Gundewar, S., Elrod, J. W., Ramachandran, A., Patillo, C. B., Kevil, C. G., and Lefer, D. J. (2009) Hydrogen sulfide mediates cardioprotection through Nrf2 signaling Circ. Res. 105, 365-374
17. Kawabata, A., Ishiki, T., Nagasawa, K., Yoshida, S., Maeda, Y., Takahashi, T., Sekiguchi, F., Wada, T., Ichida, S., and Nishikawa, H. (2007) Hydrogen sulfide as a novel nociceptive messenger Pain 132, 74-81 (Pubitemid 47494563)
18. 2S as a novel endogenous gaseous K-ATP channel opener EMBO J. 20, 6008-6016 (Pubitemid 33049276)
19. 2S generated by heart in rat and its effects on cardiac function Biochem. Biophys. Res. Commun. 313, 362-368 (Pubitemid 37543594)
20. 2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathione gamma-lyase Science 322, 587-590
21. Benavides, G. A., Squadrito, G. L., Mills, R. W., Patel, R. P., Darley-Usmar, V. M., Doeller, J. E., and Kraus, D. W. (2007) Hydrogen sulfide mediates vasoactivity of garlic Proc. Natl. Acad. Sci. U.S.A. 104, 17977-17982 (Pubitemid 350210806)
22. Mitra, K., Kim, W., Daniels, J. S., and Gates, K. S. (1997) Oxidative DNA cleavage by the antitumor antibiotic leinamycin and simple 1,2-dithiolan-3-one 1-oxides: Evidence for thiol-dependent conversion of molecular oxygen to DNA-cleaving oxygen radicals mediated by polysulfides J. Am. Chem. Soc. 119, 11691-11692 (Pubitemid 28006133)
23. Sivaramakrishnan, S. and Gates, K. S. (2008) Possible mechanisms underlying the antitumor activity of S-deoxyleinamycin Bioorg. Med. Chem. Lett. 18, 3076-3080 (Pubitemid 351689029)
24. Chatterji, T. and Gates, K. S. (1998) DNA cleavage by 7-methylbenzopentathiepin: a simple analog of the antitumor agent varacin Bioorg. Med. Chem. Lett. 8, 535-538 (Pubitemid 28092389)
25. Chatterji, T. and Gates, K. S. (2003) Reaction of thiols with 7-methylbenzopentathiepin Bioorg. Med. Chem. Lett. 13, 1349-1352 (Pubitemid 36351350)
26. Chatterji, T., Keerthi, K., and Gates, K. S. (2005) Generation of reactive oxygen species by a persulfide (BnSSH) Bioorg. Med. Chem. Lett. 15, 3921-3924 (Pubitemid 41095495)
27. Fiorucci, S., Orlandi, S., Mencarelli, A., Caliendo, G., Santagada, V., Distrutti, E., Santucci, L., Cirino, G., and Wallace, J. L. (2007) Enhanced activity of a hydrogen sulphide-releasing derivative of masalamine (ATB-429) in a mouse model of colitis Br. J. Pharmacol. 150, 996-1002 (Pubitemid 46625099)
28. Wallace, J. L., Caliendo, G., Santagada, V., Cirino, G., and Fiorucci, S. (2007) Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulfide-releasing diclofenac derivative in the rat Gastroenterology 132, 261-271 (Pubitemid 46108763)
29. Das, D. K. (2007) Hydrogen sulfide preconditioning by garlic when it starts to smell Am. J. Physiol. Heart Circ. Physiol. 293, H2629-H2630
30. Chuah, S. C., Moore, P. K., and Zhu, Y. Z. (2007) S-allylcysteine mediates cardioprotection in an acute myocardial infarction rat model via a hydrogen sulfide-mediated pathway Am. J. Physiol. Heart Circ. Physiol. 293, H2693-H2701
31. Lefer, D. J. (2007) A new gaseous signaling molecule emerges: cardioprotective role of hydrogen sulfide Proc. Natl. Acad. Sci. U.S.A. 104, 17907-17908 (Pubitemid 350210795)
32. Attene-Ramos, M. S., Wagner, E. D., Plewa, M. J., and Gaskins, H. R. (2006) Evidence that hydrogen sulfide is a genotoxic agent Mol. Cancer Res. 4, 9-14 (Pubitemid 43259885)
33. Attene-Ramos, M. S., Nava, G. M., Muellner, M. G., Wagner, E. D., Plewa, M. J., and Gaskins, H. R. (2010) DNA damage and toxicogenomic analysis of hydrogen sulfide in human intestinal epithelial FHs 74 Int cells Env. Mol. Mutagenesis 51, 304-314
34. Attene-Ramos, M. S., Wagner, E. D., Gaskins, H. R., and Plewa, M. J. (2007) Hydrogen sulfide induces direct radical-associated DNA damage Mol. Cancer Res. 5, 455-459 (Pubitemid 46903954)
35. Joyner-Matos, J., Predmore, B. L., Stein, J. R., Christiaan, L., and Julian, D. (2010) Hydrogen sulfide induces oxidative damage to RNA and DNA in a sulfide-tolerant marine invertebrate Physiol. Biochem. Zool. 83, 356-365
36. Baskar, R., Li, L., and Moore, P. K. (2007) Hydrogen sulfide-induces DNA damage and changes in apoptotic gene expression in human lung fibroblast cells FASEB J. 21, 247-255 (Pubitemid 46052563)
37. Gocke, E., King, M. T., Eckhardt, K., and Wild, D. (1981) Mutagenicity of cosmetics ingredients licensed by the European Communities Mutat. Res. 90, 91-109 (Pubitemid 11006974)
38. Luther, G. W. I., Findlay, A. J., MacDonald, D. J., Owings, S. M., and Hanson, T. E. (2011) Thermodynamics and kinetics of sulfide oxidation by oxygen: a look at inorganically controlled reactions and biologically mediated processes in the environment Front. Microbiol. 2, 1-9
39. Zhang, J.-A. and Millero, F. J. (1993) The products from the oxidation of H2S in seawater Geochim. Acta 57, 1705-1718
40. Perrin, D. D. and Armarego, W. L. F. (1997) Purification of Laboratory Chemicals, Butterworth Heinemann, Oxford, U.K.
41. Hughes, M. N., Centelles, M. N., and Moore, K. P. (2009) Making and working with hydrogen sulfide. The chemistry and generation of hydrogen sulfide in vitro and its measurement in vivo: a review Free Radical Biol. Med. 47, 1346-1353
42. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Lab Manual, Cold Spring Harbor Press, Cold Spring Harbor, NY.
43. Millero, F. J., Hubinger, S., Fernadez, M., and Garnett, S. (1987) Oxidation of H2S in seawater as a function of temperature, pH, and ionic strength Environ. Sci. Technol. 21, 439-443
44. Chen, K. Y. and Morris, J. C. (1972) Kinetics of oxidation of aqueous sulfide by O2 Environ. Sci. Technol. 6, 529-537
45. Misra, H. P. (1974) Generation of superoxide free radical during the autooxidation of thiols J. Biol. Chem. 249, 2151-2155
46. Albro, P. W., Corbett, J. T., and Schroeder, J. L. (1986) Generation of hydrogen peroxide by incidental metal ion-catalyzed autooxidation of glutathione J. Inorg. Biochem. 27, 191-203
47. Cullis, C. F. and Trimm, D. L. (1968) Homogeneous catalysis of the oxidation of thiols by metal ions Disc. Faraday Soc. 46, 144-149
48. Halliwell, B. and Gutteridge, J. M. C. (1990) Role of free radicals and catalytic metal ions in human disease: an overview Methods Enzymol. 186, 1-85 (Pubitemid 20279941)
49. Hintermann, G., Fischer, H. M., Crameri, R., and Hutter, R. (1981) Simple procedure for distinguishing CCC, OC, and L forms of plasmid DNA by agarose gel electrophoresis Plasmid 5, 371-373 (Pubitemid 11035706)
50. Jonson, P. H. and Grossman, L. I. (1977) Electrophoresis of DNA in agarose gels. Optimizing separations of conformational isomers of double and single-stranded DNAs Biochemistry 16, 4217-4224
51. Mirabelli, C. K., Huang, C. H., Fenwick, R. G., and Crooke, S. T. (1985) Quantitative measurement of single- and double-strand breakage of DNA in Escherichia coli by the antitumor antibiotics bleomycin and talisomycin Antimicrob. Agents Chemother. 27, 460-467 (Pubitemid 15097639)
52. Greenberg, M. M. (2007) Elucidating DNA damage and repair processes by independently generating reactive and metastable intermediates Org. Biomol. Chem. 5, 18-30 (Pubitemid 44927096)
53. Pogozelski, W. K. and Tullius, T. D. (1998) Oxidative strand scission of nucleic acids: routes initiated by hydrogen atom abstraction from the sugar moiety Chem. Rev. 98, 1089-1107 (Pubitemid 128632238)
54. Gates, K. S. (2007) Chemical Reactions of DNA Damage and Degradation, in Reviews of Reactive Intermediates (Platz, M. S., Moss, R. A., and Jones, M. J., Eds.) pp 333-378, John Wiley and Sons, Inc., Hoboken, NJ.
55. Gates, K. S. (2009) An overview of chemical processes that damage cellular DNA: spontaneous hydrolysis, alkylation, and reactions with radicals Chem. Res. Toxicol. 22, 1747-1760
56. O'Brien, D. J. and Birkner, F. B. (1977) Kinetics of oxygenation of reduced sulfur species in aqueous solution Environ. Sci. Technol. 11, 1114-1120 (Pubitemid 8223706)
57. Kleinjan, W. E., de Keizer, A., and Janssen, A. J. H. (2005) Kinetics of chemical oxidation of polysulfide anions in aqueous solution Water Res. 39, 4093-4100 (Pubitemid 41427013)
58. Zhang, J.-Z. and Millero, F. J. (1993) The products from the oxidation of H2S in seawater Geochim. Cosmochim. Acta 57, 1705-1718
59. Fridovich, I. (1972) Superoxide radical and superoxide dismutase Acc. Chem. Res. 5, 321-326
60. 2 Oxidoreductase activity of Cu,Zn superoxide dismutase Arch. Biochem. Biophys. 334, 50-58 (Pubitemid 26329800)
61. Vineyard, B. D. (1967) The versatility and mechanism of the n-butylamine-catalyzed reaction of thiols with sulfur J. Org. Chem. 32, 3833-3836
62. Hildebrandt, T. M. and Grieshaber, M. K. (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria FEBS J. 275, 3352-3361 (Pubitemid 351813547)
63. Mitsuhashi, H., Yamashita, S., Ikeuchi, H., Kuroiwa, T., Keneko, Y., Hiromura, K., Ueki, K., and Nojima, Y. (2005) Oxidative stress-dependent conversion of huydrogen sulfide to sulfite by activated neutrophils Shock 24, 529-534
64. Durand, M. and Weinstein, P. (2007) Thiosulfate in human urine following minor exposure to hydrogen sulfide: implications for forensic analysis of poisoning Forensic Toxicol. 25, 92-95
65. Lagoutte, E., Mimoun, S., Andriamihaja, M., Cheumontet, C., Blachier, F., and Bouillaud, F. (2010) Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes Biochim. Biophys. Acta 1797, 1500-1511
66. Avrahami, M. and Golding, R. M. (1968) The oxidation of sulphide ion at very low concentrations in aqueous solutions J. Chem. Soc. A 647-651
67. Jameton, R. A., Muller, J. G., and Burrows, C. J. (2002) Oxidative DNA damage from sulfite autoxidation catalyzed by manganese(III) Comptes Rendus 5, 461-466 (Pubitemid 36395811)
68. Hayatsu, H. and Miller, R. C. J. (1972) The cleavage of DNA by the oxygen-dependent reaction of disulfite Biochem. Biophys. Res. Commun. 46, 120-124
69. Muller, J. G., Hickerson, R. P., Perez, R. J., and Burrows, C. J. (1997) DNA damage from sulfite autoxidation catalyzed by a nickel(II) peptide J. Am. Chem. Soc. 119, 1501-1506 (Pubitemid 27145492)
70. Meister, A. and Anderson, M. E. (1983) Glutathione Annu. Rev. Biochem. 52, 711-760 (Pubitemid 13030692)
71. Soboll, S., Grundel, S., Harris, J., Kolb-Bachofen, V., Ketterer, B., and Sies, H. (1995) The content of glutathione and glutathione S-transferases and the glutathione peroxidase activity in rat liver nuclei determined by a non-aqueous technique of cell fractionation Biochem. J. 311, 889-894
72. Hwang, C., Sinskey, A. J., and Lodish, H. F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum Science 257, 1496-1502
73. Bode, V. C. (1967) Single-strand scissions induced in circular and linear lambda DNA by the presence of dithiothreitol and other reducing agents J. Mol. Biol. 26, 125-129
74. Rosenkrantz, H. S. and Rosenkrantz, S. (1971) Degradation of DNA by cysteine Arch. Biochem. Biophys. 146, 483-487
75. Bowers, J. W., Fuller, M. J. A., and Packer, J. E. (1966) Autoxidation of aqueous sulfide solutions Chem. Ind. (London) 65-66
76. Reid, T. M. and Loeb, L. A. (1992) Mutagenic specificity of oxygen radicals produced by human leukemia cells Cancer Res. 52, 1082-1086
77. LaButti, J. N., Chowdhury, G., Reilly, T. J., and Gates, K. S. (2007) Redox regulation of protein tyrosine phosphatase 1B by peroxymonophosphate J. Am. Chem. Soc. 129, 5320-5321 (Pubitemid 46697594)
78. LaButti, J. N. and Gates, K. S. (2009)) Biologically relevant properties of peroxymonophosphate (=O3POOH) Bioorg. Med. Chem. Lett. 19, 218-221
79. 2-mediated inactivation of protein tyrosine phosphatases J. Am. Chem. Soc. 132, 15803-15805
80. Tanner, J. J., Parson, Z. D., Cummings, A. H., Zhou, H., and Gates, K. S. (2011) Redox Regulation of Protein Tyrosine Phosphatases: Structural and Chemical Aspects Antioxid. Redox Signal. 15, 77-97
81. 2, a necessary evil for cell signaling Science 312, 1882-1883 (Pubitemid 43993698)
82. Paulson, C. E. and Carroll, K. S. (2010) Orchestrating redox signaling networks through regulatory cysteine switches ACS Chem. Biol. 5, 47-62
83. Dickinson, B. C. and Chang, C. J. (2011) Chemistry and biology of reactive oxygen species in signaling and stress responses Nat. Chem. Biol. 7, 504-511
84. Kimura, Y. and Kimura, H. (2004) Hydrogen sulfide protects neurons from oxidative stress FASEB J. 18, 1165-1167 (Pubitemid 39561558)
85. Kim, W. and Gates, K. S. (1997) Evidence for thiol-dependent production of oxygen radicals by 4-methyl-5-pyrazinyl-3H-1,2-dithiole-3-thione (oltipraz) and 3H-1,2-dithiole-3-thione: Possible relevance to the anticarcinogenic properties of 1,2-dithiole-3-thiones Chem. Res. Toxicol. 10, 296-301 (Pubitemid 27137140)
86. Chen, C., Pung, D., Leong, V., Hebbar, V., Shen, G., Nair, S., Li, W., and Kong, T. (2004) Induction of detoxifying enzymes by garlic organosulfur compounds through transcription factor Nrf2: effect of chemical structure and stress signals Free Radical Biol. Med. 37, 1578-1590 (Pubitemid 39349804)
87. Münchberg, U., Anwar, A., Mecklenberg, S., and Jacob, C. (2007) Polysulfides as biologically active ingredients of garlic Org. Biomol. Chem. 5, 1505-1518 (Pubitemid 46959417)
88. Munday, R., Munday, J. S., and Munday, C. M. (2003) Comparative effects of mono-, di-, tri-, and tetrasulfides derived from plants of the Allium family: redox cycling in vitro and hemolytic activity and phase 2 enzyme induction in vivo Free Radical Biol. Med. 34, 1200-1211 (Pubitemid 36423369)
89. Munday, R. and Munday, C. M. (2004) Induction of phase II enzymes by aliphatic sulfides derived fromo garlic and onions: an overview Methods Enzymol. 382, 449-456 (Pubitemid 38240804)
90. Holland, R., Navamal, M., Velayutham, M., Zweier, J. L., Kensler, T. W., and Fishbein, J. C. (2009) Hydrogen peroxide is a second messenger in phase 2 enzyme induction by cancer chemopreventive dithiolethiones Chem. Res. Toxicol. 22, 1427-1434
91. 2S signals through protein S-sulfhydration Sci. Signal. 2, 1-8
92. Krishnan, N., Fu, C., Pappin, D. J., and Tonks, N. K. (2011) Hydrogen Sulfide-Induced Sulfhydration of the Phosphatase PTP1B and Its Role in the Endoplasmic Reticulum Stress Response Sci. Signal. 4, ra86
93. Toohey, J. I. (2011) Sulfur signaling: Is the agent sulfide or sulfane? Anal. Biochem. 413, 1-7
94. Toohey, J. I. (1989) Sulfane sulfur in biological systems: a possible regulatory role Biochem. J. 264, 625-632 (Pubitemid 20023429)
95. Thomas, D. D., Ridnour, L. A., Isenberg, J. S., Flores-Santana, W., Switzer, C. H., Donzelli, S., Hussain, P., Vecoli, C., Paolocci, N., Ambs, S., Colton, C. A., Harris, C. C., Roberts, D. D., and Wink, D. A. (2008) The chemical biology of nitric oxide: implications in cellular signaling Free Radical Biol. Med. 45, 18-31
96. Ferrer-Suelta, G. and Radi, R. (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals ACS Chem. Biol. 4, 161-177
97. Hertzberg, R. P. and Dervan, P. B. (1984) Cleavage of DNA with methidiumpropyl-EDTA-Iron(II): Reaction conditions and product analyses Biochemistry 23, 3934-3945