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Role of Hydrogen Sulfide in Ischemia-Reperfusion Injury

Dongdong Wu, Jun Wang, Hui Li and 3 more

Oxidative Medicine and Cellular Longevity · 2015 · Review

doi:10.1155/2015/186908

Abstract

Ischemia-reperfusion (I/R) injury is one of the major causes of high morbidity, disability, and mortality in the world. I/R injury remains a complicated and unresolved situation in clinical practice, especially in the field of solid organ transplantation. Hydrogen sulfide (H 2 S) is the third gaseous signaling molecule and plays a broad range of physiological and pathophysiological roles in mammals. H 2 S could protect against I/R injury in many organs and tissues, such as heart, liver, kidney, brain, intestine, stomach, hind-limb, lung, and retina. The goal of this review is to highlight recent findings regarding the role of H 2 S in I/R injury. In this review, we present the production and metabolism of H 2 S and further discuss the effect and mechanism of H 2 S in I/R injury.

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    Szczesny B., Módis K., Yanagi K., 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: Biology and Chemistry. 2014;41:120-130.

    Not in our library10.1016/j.niox.2014.04.008

  96. 96.

    Foster J. C., Powell C. R., Radzinski S. C., Matson J. B. S-aroylthiooximes: a facile route to hydrogen sulfide releasing compounds with structure-dependent release kinetics. Organic Letters. 2014;16(6):1558-1561.

    Not in our library10.1021/ol500385a

  97. 97.

    Kan J., Guo W., Huang C., Bao G., Zhu Y., Zhu Y. Z. S-propargyl-cysteine, a novel water-soluble modulator of endogenous hydrogen sulfide, promotes angiogenesis through activation of signal transducer and activator of transcription 3. Antioxidants & Redox Signaling. 2014;20(15):2303-2316.

    Not in our library10.1089/ars.2013.5449

  98. 98.

    Ma K., Liu Y., Zhu Q., et al. H2S donor, S-propargyl-cysteine, increases CSE in SGC-7901 and cancer-induced mice: evidence for a novel anti-cancer effect of endogenous H2S? PLoS ONE. 2011;6(6).

    Not in our library10.1371/journal.pone.0020525

  99. 99.

    Wang Q., Wang X.-L., Liu H.-R., Rose P., Zhu Y.-Z. Protective effects of cysteine analogues on acute myocardial ischemia: novel modulators of endogenous H2S production. Antioxidants and Redox Signaling. 2010;12(10):1155-1165.

    Not in our library10.1089/ars.2009.2947

  100. 100.

    Pan L.-L., Liu X.-H., Gong Q.-H., Zhu Y.-Z. S-propargyl-cysteine (SPRC) attenuated lipopolysaccharide-induced inflammatory response in H9c2 cells involved in a hydrogen sulfide-dependent mechanism. Amino Acids. 2011;41(1):205-215.

    Not in our library10.1007/s00726-011-0834-1

  101. 101.

    Kondo K., Bhushan S., King A. L., et al. H2S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation. 2013;127(10):1116-1127.

    Not in our library10.1161/circulationaha.112.000855

  102. 102.

    Liu F., Chen D.-D., Sun X., et al. Hydrogen sulfide improves wound healing via restoration of endothelial progenitor cell functions and activation of angiopoietin-1 in type 2 diabetes. Diabetes. 2014;63(5):1763-1778.

    Not in our library10.2337/db13-0483

  103. 103.

    Martelli A., Testai L., Citi V., et al. Arylthioamides as H2S donors: l-cysteine-activated releasing properties and vascular effects in vitro and in vivo. ACS Medicinal Chemistry Letters. 2013;4(10):904-908.

    Not in our library10.1021/ml400239a

  104. 104.

    Zhao Y., Wang H., Xian M. Cysteine-activated hydrogen sulfide (H2S) donors. Journal of the American Chemical Society. 2011;133(1):15-17.

    Not in our library10.1021/ja1085723

  105. 105.

    Giustarini D., Milzani A., Dalle-Donne I., Tsikas D., Rossi R. N-acetylcysteine ethyl ester (NACET): a novel lipophilic cell-permeable cysteine derivative with an unusual pharmacokinetic feature and remarkable antioxidant potential. Biochemical Pharmacology. 2012;84(11):1522-1533.

    Not in our library10.1016/j.bcp.2012.09.010

  106. 106.

    Martelli A., Testai L., Citi V., et al. Pharmacological characterization of the vascular effects of aryl isothiocyanates: is hydrogen sulfide the real player? Vascular Pharmacology. 2014;60(1):32-41.

    Not in our library10.1016/j.vph.2013.11.003

  107. 107.

    Ekundi-Valentim E., Santos K. T., Camargo E. A., et al. Differing effects of exogenous and endogenous hydrogen sulphide in carrageenan-induced knee joint synovitis in the rat: research paper. British Journal of Pharmacology. 2010;159(7):1463-1474.

    Not in our library10.1111/j.1476-5381.2010.00640.x

  108. 108.

    Medeiros J. V. R., Bezerra V. H., Gomes A. S., et al. Hydrogen sulfide prevents ethanol-induced gastric damage in mice: role of ATP-sensitive potassium channels and capsaicin-sensitive primary afferent neurons. Journal of Pharmacology and Experimental Therapeutics. 2009;330(3):764-770.

    Not in our library10.1124/jpet.109.152801

  109. 109.

    Zhou Z., Von Wantoch Rekowski M., Coletta C., et al. Thioglycine and l-thiovaline: biologically active H2S-donors. Bioorganic and Medicinal Chemistry. 2012;20(8):2675-2678.

    Not in our library10.1016/j.bmc.2012.02.028

  110. 110.

    Zhao Y., Bhushan S., Yang C., et al. Controllable hydrogen sulfide donors and their activity against myocardial ischemia-reperfusion injury. ACS Chemical Biology. 2013;8(6):1283-1290.

    Not in our library10.1021/cb400090d

  111. 111.

    Fukushima N., Ieda N., Sasakura K., et al. Synthesis of a photocontrollable hydrogen sulfide donor using ketoprofenate photocages. Chemical Communications. 2014;50(5):587-589.

    Not in our library10.1039/c3cc47421f

  112. 112.

    Citi V., Martelli A., Testai L., Marino A., Breschi M., Calderone V. Hydrogen sulfide releasing capacity of natural isothiocyanates: is it a reliable explanation for the multiple biological effects of Brassicaceae? Planta Medica. 2014;80(8-9):610-613.

    Not in our library10.1055/s-0034-1368591

  113. 113.

    Hasegawa U., van der Vlies A. J. Design and synthesis of polymeric hydrogen sulfide donors. Bioconjugate Chemistry. 2014;25(7):1290-1300.

    Not in our library10.1021/bc500150s

  114. 114.

    Marutani E., Kosugi S., Tokuda K., et al. A novel hydrogen sulfide-releasing N-methyl-D-aspartate receptor antagonist prevents ischemic neuronal death. The Journal of Biological Chemistry. 2012;287(38):32124-32135.

    Not in our library10.1074/jbc.m112.374124

  115. 115.

    Osborne N. N., Ji D., Majid A. S. A., Del Soldata P., Sparatore A. Glutamate oxidative injury to RGC-5 cells in culture is necrostatin sensitive and blunted by a hydrogen sulfide (H2S)-releasing derivative of aspirin (ACS14). Neurochemistry International. 2012;60(4):365-378.

    Not in our library10.1016/j.neuint.2012.01.015

  116. 116.

    Switzer C. H., Cheng R. Y.-S., Ridnour L. A., et al. Dithiolethiones inhibit NF-κB activity via covalent modification in human estrogen receptor-negative breast cancer. Cancer Research. 2012;72(9):2394-2404.

    Not in our library10.1158/0008-5472.can-11-3115

  117. 117.

    Isenberg J. S., Jia Y., Field L., et al. Modulation of angiogenesis by dithiolethione-modified NSAIDs and valproic acid. British Journal of Pharmacology. 2007;151(1):63-72.

    Not in our library10.1038/sj.bjp.0707198

  118. 118.

    Lee M., Tazzari V., Giustarini D., et al. Effects of hydrogen sulfide-releasing L-DOPA derivatives on glial activation: potential for treating Parkinson disease. Journal of Biological Chemistry. 2010;285(23):17318-17328.

    Not in our library10.1074/jbc.m110.115261

  119. 119.

    Tang X.-Q., Chen R.-Q., Dong L., et al. Role of paraoxonase-1 in the protection of hydrogen sulfide-donating sildenafil (ACS6) against homocysteine-induced neurotoxicity. Journal of Molecular Neuroscience. 2013;50(1):70-77.

    Not in our library10.1007/s12031-012-9862-x

  120. 120.

    Muzaffar S., Jeremy J. Y., Sparatore A., Del Soldato P., Angelini G. D., Shukla N. H2S-donating sildenafil (ACS6) inhibits superoxide formation and gp91 phox expression in arterial endothelial cells: Role of protein kinases A and G. British Journal of Pharmacology. 2008;155(7):984-994.

    Not in our library10.1038/bjp.2008.326

  121. 121.

    Huang Q., Sparatore A., Del Soldato P., Wu L., Desai K., Nagaraj R. Hydrogen sulfide releasing aspirin, ACS14, attenuates high glucose-induced increased methylglyoxal and oxidative stress in cultured vascular smooth muscle cells. PLoS ONE. 2014;9(6).

    Not in our library10.1371/journal.pone.0097315

  122. 122.

    Zhang H., Guo C., Zhang A., et al. Effect of S-aspirin, a novel hydrogen-sulfide-releasing aspirin (ACS14), on atherosclerosis in apoE-deficient mice. European Journal of Pharmacology. 2012;697(1–3):106-116.

    Not in our library10.1016/j.ejphar.2012.10.005

  123. 123.

    Pircher J., Fochler F., Czermak T., et al. Hydrogen sulfide-releasing aspirin derivative acs14 exerts strong antithrombotic effects in vitro and in vivo. Arteriosclerosis, Thrombosis, and Vascular Biology. 2012;32(12):2884-2891.

    Not in our library10.1161/atvbaha.112.300627

  124. 124.

    Rossoni G., Manfredi B., Tazzari V., et al. Activity of a new hydrogen sulfide-releasing aspirin (ACS14) on pathological cardiovascular alterations induced by glutathione depletion in rats. European Journal of Pharmacology. 2010;648(1–3):139-145.

    Not in our library10.1016/j.ejphar.2010.08.039

  125. 125.

    Giustarini D., Del Soldato P., Sparatore A., Rossi R. Modulation of thiol homeostasis induced by H2S-releasing aspirin. Free Radical Biology and Medicine. 2010;48(9):1263-1272.

    Not in our library10.1016/j.freeradbiomed.2010.02.014

  126. 126.

    Bass S. E., Sienkiewicz P., MacDonald C. J., et al. Novel dithiolethione-modified nonsteroidal anti-inflammatory drugs in human hepatoma HepG2 and colon LS180 cells. Clinical Cancer Research. 2009;15(6):1964-1972.

    Not in our library10.1158/1078-0432.ccr-08-1870

  127. 127.

    Frantzias J., Logan J. G., Mollat P., et al. Hydrogen sulphide-releasing diclofenac derivatives inhibit breast cancer-induced osteoclastogenesis in vitro and prevent osteolysis ex vivo. British Journal of Pharmacology. 2012;165(6):1914-1925.

    Not in our library10.1111/j.1476-5381.2011.01704.x

  128. 128.

    Bhatia M., Sidhapuriwala J. N., Sparatore A., Moore P. K. Treatment with H2S-releasing diclofenac protects mice against acute pancreatitis-associated lung injury. Shock. 2008;29(1):84-88.

    Not in our library10.1097/shk.0b013e31806ec26

  129. 129.

    Tesei A., Brigliadori G., Carloni S., et al. Organosulfur derivatives of the HDAC inhibitor valproic acid sensitize human lung cancer cell lines to apoptosis and to cisplatin cytotoxicity. Journal of Cellular Physiology. 2012;227(10):3389-3396.

    Not in our library10.1002/jcp.24039

  130. 130.

    Perrino E., Uliva C., Lanzi C., Soldato P. D., Masini E., Sparatore A. New prostaglandin derivative for glaucoma treatment. Bioorganic and Medicinal Chemistry Letters. 2009;19(6):1639-1642.

    Not in our library10.1016/j.bmcl.2009.02.007

  131. 131.

    Predmore B. L., Lefer D. J., Gojon G. Hydrogen sulfide in biochemistry and medicine. Antioxidants & Redox Signaling. 2012;17(1):119-140.

    Not in our library10.1089/ars.2012.4612

  132. 132.

    Xie L., Hu L.-F., Teo X. Q., et al. Therapeutic effect of hydrogen sulfide-releasing L-Dopa derivative ACS84 on 6-OHDA-induced Parkinson's disease rat model. PLoS ONE. 2013;8(4).

    Not in our library10.1371/journal.pone.0060200

  133. 133.

    Szabõ C. Hydrogen sulphide and its therapeutic potential. Nature Reviews Drug Discovery. 2007;6(11):917-935.

    Not in our library10.1038/nrd2425

  134. 134.

    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(1):261-271.

    Not in our library10.1053/j.gastro.2006.11.042

  135. 135.

    Wallace J. L. Hydrogen sulfide-releasing anti-inflammatory drugs. Trends in Pharmacological Sciences. 2007;28(10):501-505.

    Not in our library10.1016/j.tips.2007.09.003

  136. 136.

    Wallace J. L., Caliendo G., Santagada V., Cirino G. Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346). British Journal of Pharmacology. 2010;159(6):1236-1246.

    Not in our library10.1111/j.1476-5381.2009.00611.x

  137. 137.

    Elsheikh W., Blackler R. W., Flannigan K. L., Wallace J. L. Enhanced chemopreventive effects of a hydrogen sulfide-releasing anti-inflammatory drug (ATB-346) in experimental colorectal cancer. Nitric Oxide. 2014;41:131-137.

    Not in our library10.1016/j.niox.2014.04.006

  138. 138.

    Fiorucci S., Orlandi S., Mencarelli A., et al. Enhanced activity of a hydrogen sulphide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. British Journal of Pharmacology. 2007;150(8):996-1002.

    Not in our library10.1038/sj.bjp.0707193

  139. 139.

    Distrutti E., Sediari L., Mencarelli A., et al. 5-Amino-2-hydroxybenzoic acid 4-(5-thioxo-5H-[1,2]dithiol-3yl)-phenyl ester (ATB-429), a hydrogen sulfide-releasing derivative of mesalamine, exerts antinociceptive effects in a model of postinflammatory hypersensitivity. Journal of Pharmacology and Experimental Therapeutics. 2006;319(1):447-458.

    Not in our library10.1124/jpet.106.106435

  140. 140.

    Chattopadhyay M., Kodela R., Nath N., Barsegian A., Boring D., Kashfi K. Hydrogen sulfide-releasing aspirin suppresses NF-κB signaling in estrogen receptor negative breast cancer cells in vitro and in vivo. Biochemical Pharmacology. 2012;83(6):723-732.

    Not in our library10.1016/j.bcp.2011.12.019

  141. 141.

    Wang X., Wang L., Sheng X., et al. Design, synthesis and biological evaluation of hydrogen sulfide releasing derivatives of 3-n-butylphthalide as potential antiplatelet and antithrombotic agents. Organic & Biomolecular Chemistry. 2014;12(31):5995-6004.

    Not in our library10.1039/c4ob00830h

  142. 142.

    Martelli A., Testai L., Marino A., Breschi M. C., da Settimo F., Calderone V. Hydrogen sulphide: biopharmacological roles in the cardiovascular system and pharmaceutical perspectives. Current Medicinal Chemistry. 2012;19(20):3325-3336.

    Not in our library10.2174/092986712801215928

  143. 143.

    Chattopadhyay M., Kodela R., Olson K. R., 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. Biochemical and Biophysical Research Communications. 2012;419(3):523-528.

    Not in our library10.1016/j.bbrc.2012.02.051

  144. 144.

    Lee M., Mcgeer E., Kodela R., Kashfi K., Mcgeer P. L. NOSH-aspirin (NBS-1120), a novel nitric oxide and hydrogen sulfide releasing hybrid, attenuates neuroinflammation induced by microglial and astrocytic activation: a new candidate for treatment of neurodegenerative disorders. Glia. 2013;61(10):1724-1734.

    Not in our library10.1002/glia.22553

  145. 145.

    Kodela R., Chattopadhyay M., Kashfi K. Synthesis and biological activity of NOSH-naproxen (AVT-219) and NOSH-sulindac (AVT-18A) as potent anti-inflammatory agents with chemotherapeutic potential. MedChemComm. 2013;4(11):1472-1481.

    Not in our library10.1039/c3md00185g

  146. 146.

    Rossoni G., Sparatore A., Tazzari V., Manfredi B., Soldato P. D., Berti F. The hydrogen sulphide-releasing derivative of diclofenac protects against ischaemia-reperfusion injury in the isolated rabbit heart. British Journal of Pharmacology. 2008;153(1):100-109.

    Not in our library10.1038/sj.bjp.0707540

  147. 147.

    Bucci M., Vellecco V., Cantalupo A., et al. Hydrogen sulfide accounts for the peripheral vascular effects of zofenopril independently of ACE inhibition. Cardiovascular Research. 2014;102(1):138-147.

    Not in our library10.1093/cvr/cvu026

  148. 148.

    Issa K., Kimmoun A., Collin S., et al. Compared effects of inhibition and exogenous administration of hydrogen sulphide in ischaemia-reperfusion injury. Critical Care. 2013;17, article R129.

    Not in our library10.1186/cc12808

  149. 149.

    Sivarajah A., Collino M., Yasin M., et al. Anti-apoptotic and anti-inflammatory effects of hydrogen sulfide in a rat model of regional myocardial l/R. Shock. 2009;31(3):267-274.

    Not in our library10.1097/shk.0b013e318180ff89

  150. 150.

    Alves M. G., Soares A. F., Carvalho R. A., Oliveira P. J. Sodium hydrosulfide improves the protective potential of the cardioplegic histidine buffer solution. European Journal of Pharmacology. 2011;654(1):60-67.

    Not in our library10.1016/j.ejphar.2010.12.010

  151. 151.

    Ji Y., Pang Q.-F., Xu G., Wang L., Wang J.-K., Zeng Y.-M. Exogenous hydrogen sulfide postconditioning protects isolated rat hearts against ischemia-reperfusion injury. European Journal of Pharmacology. 2008;587(1–3):1-7.

    Not in our library10.1016/j.ejphar.2008.03.044

  152. 152.

    Sun W.-H., Liu F., Chen Y., Zhu Y.-C. Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochemical and Biophysical Research Communications. 2012;421(2):164-169.

    Not in our library10.1016/j.bbrc.2012.03.121

  153. 153.

    Luan H.-F., Zhao Z.-B., Zhao Q.-H., Zhu P., Xiu M.-Y., Ji Y. Hydrogen sulfide postconditioning protects isolated rat hearts against ischemia and reperfusion injury mediated by the JAK2/STAT3 survival pathway. Brazilian Journal of Medical and Biological Research. 2012;45(10):898-905.

    Not in our library10.1590/s0100-879x2012007500090

  154. 154.

    Bliksøen M., Kaljusto M.-L., Vaage J., Stensløkken K.-O. Effects of hydrogen sulphide on ischaemia-reperfusion injury and ischaemic preconditioning in the isolated, perfused rat heart. European Journal of Cardio-thoracic Surgery. 2008;34(2):344-349.

    Not in our library10.1016/j.ejcts.2008.03.017

  155. 155.

    Elsey D. J., Fowkes R. C., Baxter G. F. L-cysteine stimulates hydrogen sulfide synthesis in myocardium associated with attenuation of ischemia-reperfusion injury. Journal of Cardiovascular Pharmacology and Therapeutics. 2010;15(1):53-59.

    Not in our library10.1177/1074248409357743

  156. 156.

    Gao Y., Yao X., Zhang Y., et al. The protective role of hydrogen sulfide in myocardial ischemia-reperfusion-induced injury in diabetic rats. International Journal of Cardiology. 2011;152(2):177-183.

    Not in our library10.1016/j.ijcard.2010.07.012

  157. 157.

    Bian J. S., Qian C. Y., Pan T. T., et al. Role of hydrogen sulfide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes. Journal of Pharmacology and Experimental Therapeutics. 2006;316(2):670-678.

    Not in our library10.1124/jpet.105.092023

  158. 158.

    Hu Y., Chen X., Pan T.-T., et al. Cardioprotection induced by hydrogen sulfide preconditioning involves activation of ERK and PI3K/Akt pathways. Pflugers Archiv European Journal of Physiology. 2008;455(4):607-616.

    Not in our library10.1007/s00424-007-0321-4

  159. 159.

    Hu L.-F., Pan T.-T., Neo K. L., Yong Q. C., Bian J.-S. Cyclooxygenase-2 mediates the delayed cardioprotection induced by hydrogen sulfide preconditioning in isolated rat cardiomyocytes. Pflugers Archiv European Journal of Physiology. 2008;455(6):971-978.

    Not in our library10.1007/s00424-007-0346-8

  160. 160.

    Sodha N. R., Clements R. T., Feng J., et al. Hydrogen sulfide therapy attenuates the inflammatory response in a porcine model of myocardial ischemia/reperfusion injury. Journal of Thoracic and Cardiovascular Surgery. 2009;138(4):977-984.

    Not in our library10.1016/j.jtcvs.2008.08.074

  161. 161.

    Sodha N. R., Clements R. T., Feng J., et al. The effects of therapeutic sulfide on myocardial apoptosis in response to ischemia-reperfusion injury. European Journal of Cardio-Thoracic Surgery. 2008;33(5):906-913.

    Not in our library10.1016/j.ejcts.2008.01.047

  162. 162.

    Johansen D., Ytrehus K., Baxter G. F. Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury. Evidence for a role of KATP channels. Basic Research in Cardiology. 2006;101(1):53-60.

    Not in our library10.1007/s00395-005-0569-9

  163. 163.

    Ganster F., Burban M., de la Bourdonnaye M., et al. Effects of hydrogen sulfide on hemodynamics, inflammatory response and oxidative stress during resuscitated hemorrhagic shock in rats. Critical Care. 2010;14(5, article R165).

    Not in our library10.1186/cc9257

  164. 164.

    Yao L. L., Huang X. W., Wang Y. G., Cao Y. X., Zhang C. C., Zhu Y. C. Hydrogen sulfide protects cardiomyocytes from hypoxia/reoxygenation-induced apoptosis by preventing GSK-3β-dependent opening of mPTP. The American Journal of Physiology—Heart and Circulatory Physiology. 2010;298(5):H1310-H1319.

    Not in our library10.1152/ajpheart.00339.2009

  165. 165.

    Peake B. F., Nicholson C. K., Lambert J. P., et al. Hydrogen sulfide preconditions the db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner. American Journal of Physiology—Heart and Circulatory Physiology. 2013;304(9):H1215-H1224.

    Not in our library10.1152/ajpheart.00796.2012

  166. 166.

    Yao X., Tan G., He C., et al. Hydrogen sulfide protects cardiomyocytes from myocardial ischemia-reperfusion injury by enhancing phosphorylation of apoptosis repressor with caspase recruitment domain. The Tohoku Journal of Experimental Medicine. 2012;226(4):275-285.

    Not in our library10.1620/tjem.226.275

  167. 167.

    Elrod J. W., Calvert J. W., Morrison J., et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(39):15560-15565.

    Not in our library10.1073/pnas.0705891104

  168. 168.

    Toldo S., Das A., Mezzaroma E., et al. Induction of microRNA-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice. Circulation: Cardiovascular Genetics. 2014;7(3):311-320.

    Not in our library10.1161/circgenetics.113.000381

  169. 169.

    Calvert J. W., Jha S., Gundewar S., et al. Hydrogen sulfide mediates cardioprotection through nrf2 signaling. Circulation Research. 2009;105(4):365-374.

    Not in our library10.1161/circresaha.109.199919

  170. 170.

    Zhang W.-J., Shi Z.-X., Wang B.-B., Cui Y.-J., Guo J.-Z., Li B. Allitridum mimics effect of ischemic preconditioning by activation of protein kinase C. Acta Pharmacologica Sinica. 2001;22(2):132-136.

    Not in our library

  171. 171.

    Zhou Y., Wang D., Gao X., Lew K., Richards A. M., Wang P. mTORC2 phosphorylation of Akt1: a possible mechanism for hydrogen sulfide-induced cardioprotection. PLoS ONE. 2014;9(6).

    Not in our library10.1371/journal.pone.0099665

  172. 172.

    Sivarajah A., McDonald M. C., Thiemermann C. The production of hydrogen sulfide limits myocardial ischemia and reperfusion injury and contributes to the cardioprotective effects of preconditioning with endotoxin, but not ischemia in the rat. Shock. 2006;26(2):154-161.

    Not in our library10.1097/01.shk.0000225722.56681.64

  173. 173.

    Kang B., Hong J., Xiao J., et al. Involvement of miR-1 in the protective effect of hydrogen sulfide against cardiomyocyte apoptosis induced by ischemia/reperfusion. Molecular Biology Reports. 2014;41(10):6845-6853.

    Not in our library10.1007/s11033-014-3570-2

  174. 174.

    Minamishima S., Bougaki M., Sips P. Y., 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(10):888-896.

    Not in our library10.1161/circulationaha.108.833491

  175. 175.

    Zhuo Y., Chen P.-F., Zhang A.-Z., Zhong H., Chen C.-Q., Zhu Y.-Z. Cardioprotective effect of hydrogen sulfide in ischemic reperfusion experimental rats and its influence on expression of survivin gene. Biological and Pharmaceutical Bulletin. 2009;32(8):1406-1410.

    Not in our library10.1248/bpb.32.1406

  176. 176.

    Osipov R. M., Robich M. P., Feng J., et al. Effect of hydrogen sulfide in a porcine model of myocardial ischemia-reperfusion: comparison of different administration regimens and characterization of the cellular mechanisms of protection. Journal of Cardiovascular Pharmacology. 2009;54(4):287-297.

    Not in our library10.1097/fjc.0b013e3181b2b72b

  177. 177.

    Chen Y., Liu Z., Xie X. Hydrogen sulphide attenuates renal and cardiac injury after total hepatic ischemia and reperfusion. Journal of Surgical Research. 2010;164(2):e305-e313.

    Not in our library10.1016/j.jss.2010.08.010

  178. 178.

    Shaik I. H., George J. M., Thekkumkara T. J., Mehvar R. Protective effects of diallyl sulfide, a garlic constituent, on the warm hepatic ischemia-reperfusion injury in a rat model. Pharmaceutical Research. 2008;25(10):2231-2242.

    Not in our library10.1007/s11095-008-9601-8

  179. 179.

    Jha S., Calvert J. W., Duranski M. R., Ramachandran A., Lefer D. J. Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: role of antioxidant and antiapoptotic signaling. American Journal of Physiology—Heart and Circulatory Physiology. 2008;295(2):H801-H806.

    Not in our library10.1152/ajpheart.00377.2008

  180. 180.

    Bos E. M., Snijder P. M., Jekel H., et al. Beneficial effects of gaseous hydrogen sulfide in hepatic ischemia/reperfusion injury. Transplant International. 2012;25(8):897-908.

    Not in our library10.1111/j.1432-2277.2012.01514.x

  181. 181.

    Cheng P., Wang F., Chen K., et al. Hydrogen sulfide ameliorates ischemia/reperfusion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators of Inflammation. 2014;2014:16.

    Not in our library10.1155/2014/935251

  182. 182.

    Zhang Q., Fu H., Zhang H., et al. Hydrogen sulfide preconditioning protects rat liver against ischemia/reperfusion injury by activating Akt-GSK-3β signaling and inhibiting mitochondrial permeability transition. PLoS ONE. 2013;8(9).

    Not in our library10.1371/journal.pone.0074422

  183. 183.

    Bos E. M., Leuvenink H. G. D., Snijder P. M., et al. Hydrogen sulfide-induced hypometabolism prevents renal ischemia/reperfusion injury. Journal of the American Society of Nephrology. 2009;20(9):1901-1905.

    Not in our library10.1681/asn.2008121269

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    Hunter J. P., Hosgood S. A., Patel M., Rose R., Read K., Nicholson M. L. Effects of hydrogen sulphide in an experimental model of renal ischaemia-reperfusion injury. British Journal of Surgery. 2012;99(12):1665-1671.

    Not in our library10.1002/bjs.8956

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    Hosgood S. A., Nicholson M. L. Hydrogen sulphide ameliorates ischaemia-reperfusion injury in an experimental model of non-heart-beating donor kidney transplantation. British Journal of Surgery. 2010;97(2):202-209.

    Not in our library10.1002/bjs.6856

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    Tripatara P., Patel N. S. A., Brancaleone V., et al. Characterisation of cystathionine gamma-lyase/hydrogen sulphide pathway in ischaemia/reperfusion injury of the mouse kidney: an in vivo study. European Journal of Pharmacology. 2009;606(1–3):205-209.

    Not in our library10.1016/j.ejphar.2009.01.041

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    Tripatara P., Patel N. S. A., Collino M., et al. Generation of endogenous hydrogen sulfide by cystathionine γ-lyase limits renal ischemia/reperfusion injury and dysfunction. Laboratory Investigation. 2008;88(10):1038-1048.

    Not in our library10.1038/labinvest.2008.73

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    Lobb I., Zhu J., Liu W., Haig A., Lan Z., Sener A. Hydrogen sulfide treatment ameliorates long-term renal dysfunction resulting from prolonged warm renal ischemia-reperfusion injury. Canadian Urological Association Journal. 2014;8(5-6):E413-E418.

    Not in our library10.5489/cuaj.1694

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    Zhu J. X. G., Kalbfleisch M., Yang Y. X., et al. Detrimental effects of prolonged warm renal ischaemia-reperfusion injury are abrogated by supplemental hydrogen sulphide: an analysis using real-time intravital microscopy and polymerase chain reaction. BJU International. 2012;110(11):E1218-E1227.

    Not in our library10.1111/j.1464-410x.2012.11555.x

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    Simon F., Scheuerle A., Gröger M., et al. Effects of intravenous sulfide during porcine aortic occlusion-induced kidney ischemia/reperfusion injury. Shock. 2011;35(2):156-163.

    Not in our library10.1097/shk.0b013e3181f0dc91

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    Xu Z., Prathapasinghe G., Wu N., Hwang S. Y., Siow Y. L., Karmin O. Ischemia-reperfusion reduces cystathionine-β-synthase-mediated hydrogen sulfide generation in the kidney. The American Journal of Physiology—Renal Physiology. 2009;297(1):F27-F35.

    Not in our library10.1152/ajprenal.00096.2009

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