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Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 925167, 13 pages
http://dx.doi.org/10.1155/2015/925167
Review Article

The Cardioprotective Effects of Hydrogen Sulfide in Heart Diseases: From Molecular Mechanisms to Therapeutic Potential

1Department of Pharmacology, School of Pharmacy, Fudan University, Zhangheng Road 826, Pudong New District, Shanghai 201203, China
2Department of Physiology and Pathophysiology, Shanghai Medical College, Fudan University, Shanghai 200032, China
3Department of Pharmacology, National University of Singapore, Singapore 117597

Received 3 November 2014; Accepted 18 December 2014

Academic Editor: Steven S. An

Copyright © 2015 Yaqi Shen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Abe and H. Kimura, “The possible role of hydrogen sulfide as an endogenous neuromodulator,” The Journal of Neuroscience, vol. 16, no. 3, pp. 1066–1071, 1996. View at Google Scholar · View at Scopus
  2. R. Wang, “Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter?” The FASEB Journal, vol. 16, no. 13, pp. 1792–1798, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Wang, “Physiological implications of hydrogen sulfide: a whiff exploration that blossomed,” Physiological Reviews, vol. 92, no. 2, pp. 791–896, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Liu, X.-B. Bai, S. Shi, and Y.-X. Cao, “Hydrogen sulfide protects from intestinal ischaemia-reperfusion injury in rats,” Journal of Pharmacy and Pharmacology, vol. 61, no. 2, pp. 207–212, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Wagner, P. Asfar, E. Calzia, P. Radermacher, and C. Szabó, “Bench-to-bedside review: hydrogen sulfide—the third gaseous transmitter: applications for critical care,” Critical Care, vol. 13, no. 3, p. 213, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Shibuya, M. Tanaka, M. Yoshida et al., “3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain,” Antioxidants and Redox Signaling, vol. 11, no. 4, pp. 703–714, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Yang, L. Wu, B. Jiang et al., “H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase,” Science, vol. 322, no. 5901, pp. 587–590, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Yang, Z. Yang, M. Zhang et al., “Hydrogen sulfide protects against chemical hypoxia-induced cytotoxicity and inflammation in hacat cells through inhibition of ROS/NF-κB/COX-2 pathway,” PLoS ONE, vol. 6, no. 7, Article ID e21971, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Kaneko, Y. Kimura, H. Kimura, and I. Niki, “l-cysteine inhibits insulin release from the pancreatic α-cell: possible involvement of metabolic production of hydrogen sulfide, a novel gasotransmitter,” Diabetes, vol. 55, no. 5, pp. 1391–1397, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Patel, M. Vatish, J. Heptinstall, R. Wang, and R. J. Carson, “The endogenous production of hydrogen sulphide in intrauterine tissues,” Reproductive Biology and Endocrinology, vol. 7, article 10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. M. H. Stipanuk and P. W. Beck, “Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat,” Biochemical Journal, vol. 206, no. 2, pp. 267–277, 1982. View at Google Scholar · View at Scopus
  12. R. Hosoki, N. Matsuki, and H. Kimura, “The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide,” Biochemical and Biophysical Research Communications, vol. 237, no. 3, pp. 527–531, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. W. Yang, G. Yang, X. Jia, L. Wu, and R. Wang, “Activation of KATP channels by H2S in rat insulin-secreting cells and the underlying mechanisms,” The Journal of Physiology, vol. 569, no. 2, pp. 519–531, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Mikami, N. Shibuya, Y. Kimura, N. Nagahara, Y. Ogasawara, and H. Kimura, “Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide,” Biochemical Journal, vol. 439, no. 3, pp. 479–485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Mikami, N. Shibuya, Y. Kimura, N. Nagahara, M. Yamada, and H. Kimura, “Hydrogen sulfide protects the retina from light-induced degeneration by the modulation of Ca2+ influx,” The Journal of Biological Chemistry, vol. 286, no. 45, pp. 39379–39386, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Shibuya, Y. Mikami, Y. Kimura, N. Nagahara, and H. Kimura, “Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide,” The Journal of Biochemistry, vol. 146, no. 5, pp. 623–626, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Shibuya, M. Tanaka, M. Yoshida et al., “3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain,” Antioxidants and Redox Signaling, vol. 11, no. 4, pp. 703–714, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Li, P. Rose, and P. K. Moore, “Hydrogen sulfide and cell signaling,” Annual Review of Pharmacology and Toxicology, vol. 51, pp. 169–187, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Lavu, S. Bhushan, and D. J. Lefer, “Hydrogen sulfide-mediated cardioprotection: mechanisms and therapeutic potential,” Clinical Science, vol. 120, no. 6, pp. 219–229, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Shibuya, S. Koike, M. Tanaka et al., “A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells,” Nature Communications, vol. 4, article 1366, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Kimura, “Metabolic turnover of hydrogen sulfide,” Frontiers in Physiology, vol. 3, article 101, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Kimura, “Physiological role of hydrogen sulfide and polysulfide in the central nervous system,” Neurochemistry International, vol. 63, no. 5, pp. 492–497, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. T. C. Bartholomew, G. M. Powell, K. S. Dodgson, and C. G. Curtis, “Oxidation of sodium sulphide by rat liver, lungs and kidney,” Biochemical Pharmacology, vol. 29, no. 18, pp. 2431–2437, 1980. View at Publisher · View at Google Scholar · View at Scopus
  24. H.-L. Jiang, H.-C. Wu, Z.-L. Li, B. Geng, and C.-S. Tang, “Changes of the new gaseous transmitter H2S in patients with coronary heart disease,” Academic Journal of the First Medical College of PLA, vol. 25, no. 8, pp. 951–954, 2005. View at Google Scholar · View at Scopus
  25. D. J. Polhemus, J. W. Calvert, J. Butler, and D. J. Lefer, “The cardioprotective actions of hydrogen sulfide in acute myocardial infarction and heart failure,” Scientifica, vol. 2014, Article ID 768607, 8 pages, 2014. View at Publisher · View at Google Scholar
  26. Y. H. Liu, M. Lu, L. F. Hu, P. T. H. Wong, G. D. Webb, and J. S. Bian, “Hydrogen sulfide in the mammalian cardiovascular system,” Antioxidants & Redox Signaling, vol. 17, no. 1, pp. 141–185, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. N. S. Dhalla, A. B. Elmoselhi, T. Hata, and N. Makino, “Status of myocardial antioxidants in ischemia-reperfusion injury,” Cardiovascular Research, vol. 47, no. 3, pp. 446–456, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. H.-F. Luan, Z.-B. Zhao, Q.-H. Zhao, P. Zhu, M.-Y. Xiu, and Y. Ji, “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, vol. 45, no. 10, pp. 898–905, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. H. F. Jin, Y. Wang, X. B. Wang, Y. Sun, C. S. Tang, and J. B. Du, “Sulfur dioxide preconditioning increases antioxidative capacity in rat with myocardial ischemia reperfusion (I/R) injury,” Nitric Oxide: Biology and Chemistry, vol. 32, pp. 56–61, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. R. M. Osipov, M. P. Robich, J. Feng 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, vol. 54, no. 4, pp. 287–297, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. T. V. Shymans'ka, I. V. Hoshovs'ka, O. M. Semenikhina, and V. F. Sahach, “Effect of hydrogen sulfide on isolated rat heart reaction under volume load and ischemia-reperfusion,” Fiziolohichnyǐ Zhurnal, vol. 58, no. 6, pp. 57–66, 2012. View at Google Scholar · View at Scopus
  32. Y. Zhuo, P. F. Chen, A. Z. Zhang, H. Zhong, C. Q. Chen, and Y. Z. Zhu, “Cardioprotective effect of hydrogen sulfide in ischemic reperfusion experimental rats and its influence on expression of survivin gene,” Biological and Pharmaceutical Bulletin, vol. 32, no. 8, pp. 1406–1410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. W. Elrod, J. W. Calvert, J. Morrison 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, vol. 104, no. 39, pp. 15560–15565, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Olivetti, F. Quaini, R. Sala et al., “Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart,” Journal of Molecular and Cellular Cardiology, vol. 28, no. 9, pp. 2005–2016, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Anversa, W. Cheng, Y. Liu, A. Leri, G. Redaelli, and J. Kajstura, “Apoptosis and myocardial infarction,” Basic Research in Cardiology, vol. 93, no. 3, supplement, pp. 8–12, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Z. Zhu, J. W. Zhong, P. Ho et al., “Hydrogen sulfide and its possible roles in myocardial ischemia in experimental rats,” Journal of Applied Physiology, vol. 102, no. 1, pp. 261–268, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. Q. Wang, X.-L. Wang, H.-R. Liu, P. Rose, and Y.-Z. Zhu, “Protective effects of cysteine analogues on acute myocardial ischemia: novel modulators of endogenous H2S production,” Antioxidants & Redox Signaling, vol. 12, no. 10, pp. 1155–1165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Shen, Z. Shen, L. Miao et al., “MiRNA-30 family inhibition protects against cardiac ischemic injury by regulating cystathionine-gamma-lyase expression,” Antioxidants & Redox Signaling, 2014. View at Google Scholar
  39. N. Qipshidze, N. Metreveli, P. K. Mishra, D. Lominadze, and S. C. Tyagi, “Hydrogen sulfide mitigates cardiac remodeling during myocardial infarction via improvement of angiogenesis,” International Journal of Biological Sciences, vol. 8, no. 4, pp. 430–441, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. X. Xie, A. Sun, W. Zhu et al., “Transplantation of mesenchymal stem cells preconditioned with hydrogen sulfide enhances repair of myocardial infarction in rats,” The Tohoku Journal of Experimental Medicine, vol. 226, no. 1, pp. 29–36, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Pourkhalili, S. Hajizadeh, T. Tiraihi et al., “Ischemia and reperfusion-induced arrhythmias: role of hyperoxic preconditioning,” Journal of Cardiovascular Medicine, vol. 10, no. 8, pp. 635–642, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. Z. Zhang, H. Huang, P. Liu, C. Tang, and J. Wang, “Hydrogen sulfide contributes to cardioprotection during ischemia-reperfusion injury by opening KATP channels,” Canadian Journal of Physiology and Pharmacology, vol. 85, no. 12, pp. 1248–1253, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. J.-S. Bian, Q. C. Yong, T.-T. Pan et al., “Role of hydrogen sulfide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes,” The Journal of Pharmacology and Experimental Therapeutics, vol. 316, no. 2, pp. 670–678, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. W. Roell, T. Lewalter, P. Sasse et al., “Engraftment of connexin 43-expressing cells prevents post-infarct arrhythmia,” Nature, vol. 450, no. 7171, pp. 819–824, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. J. L. Huang, D. M. Wang, J. B. Zheng, X. S. Huang, and H. Jin, “Hydrogen sulfide attenuates cardiac hypertrophy and fibrosis induced by abdominal aortic coarctation in rats,” Molecular Medicine Reports, vol. 5, no. 4, pp. 923–928, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. Q. C. Yong, T.-T. Pan, L.-F. Hu, and J.-S. Bian, “Negative regulation of β-adrenergic function by hydrogen sulphide in the rat hearts,” Journal of Molecular and Cellular Cardiology, vol. 44, no. 4, pp. 701–710, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. G.-M. Qi, L.-X. Jia, Y.-L. Li, H.-H. Li, and J. Du, “Adiponectin suppresses angiotensin II-induced inflammation and cardiac fibrosis through activation of macrophage autophagy,” Endocrinology, vol. 155, no. 6, pp. 2254–2265, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Camelliti, T. K. Borg, and P. Kohl, “Structural and functional characterisation of cardiac fibroblasts,” Cardiovascular Research, vol. 65, no. 1, pp. 40–51, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. P. K. Mishra, N. Tyagi, U. Sen, S. Givvimani, and S. C. Tyagi, “H2S ameliorates oxidative and proteolytic stresses and protects the heart against adverse remodeling in chronic heart failure,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 298, no. 2, pp. H451–H456, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. G.-R. Li, H.-Y. Sun, J.-B. Chen, Y. Zhou, H.-F. Tse, and C.-P. Lau, “Characterization of multiple ion channels in cultured human cardiac fibroblasts,” PLoS ONE, vol. 4, no. 10, Article ID e7307, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Sheng, W. Shim, H. Wei et al., “Hydrogen sulphide suppresses human atrial fibroblast proliferation and transformation to myofibroblasts,” Journal of Cellular and Molecular Medicine, vol. 17, no. 10, pp. 1345–1354, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. X. Wang, Q. Wang, W. Guo, and Y. Z. Zhu, “Hydrogen sulfide attenuates cardiac dysfunction in a rat model of heart failure: a mechanism through cardiac mitochondrial protection,” Bioscience Reports, vol. 31, no. 2, pp. 87–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. L.-L. Pan, X.-H. Liu, Y.-Q. Shen et al., “Inhibition of NADPH oxidase 4-related signaling by sodium hydrosulfide attenuates myocardial fibrotic response,” International Journal of Cardiology, vol. 168, no. 4, pp. 3770–3778, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Indolfi, E. di Lorenzo, C. Perrino et al., “Hydroxymethylglutaryl coenzyme a reductase inhibitor simvastatin prevents cardiac hypertrophy induced by pressure overload and inhibits p21ras activation,” Circulation, vol. 106, no. 16, pp. 2118–2124, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Lu, J. Xing, X. Zhang et al., “Exogenous hydrogen sulfide prevents cardiomyocyte apoptosis from cardiac hypertrophy induced by isoproterenol,” Molecular and Cellular Biochemistry, vol. 381, no. 1-2, pp. 41–50, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. C. K. Nicholson, J. P. Lambert, J. D. Molkentin, J. Sadoshima, and J. W. Calvert, “Thioredoxin 1 is essential for sodium sulfide-mediated cardioprotection in the setting of heart failure,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 4, pp. 744–751, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Yang, Z. Liu, Y. Wang, Z. Li, H. Yu, and Q. Wang, “Hydrogen sulfide endothelin-induced myocardial hypertrophy in rats and the mechanism involved,” Cell Biochemistry and Biophysics, vol. 70, no. 3, pp. 1683–1686, 2014. View at Publisher · View at Google Scholar
  58. J. Huang, D. Wang, J. Zheng, X. Huang, and H. Jin, “Hydrogen sulfide attenuates cardiac hypertrophy and fibrosis induced by abdominal aortic coarctation in rats,” Molecular Medicine Reports, vol. 5, no. 4, pp. 923–928, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Padiya, D. Chowdhury, R. Borkar, R. Srinivas, M. P. Bhadra, and S. K. Banerjee, “Garlic attenuates cardiac oxidative stress via activation of PI3K/AKT/Nrf2-Keap1 pathway in fructose-fed diabetic rat,” PLoS ONE, vol. 9, no. 5, Article ID e94228, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. J. W. Calvert, M. Elston, C. K. Nicholson et al., “Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice,” Circulation, vol. 122, no. 1, pp. 11–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Kondo, S. Bhushan, A. L. King et al., “H2S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase,” Circulation, vol. 127, no. 10, pp. 1116–1127, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Kondo, S. Bhushan, M. E. Condit, A. L. King, B. L. Predmore, and d. J. Lefer, “Hydrogen sulfide attenuates cardiac dysfunction following pressure overload induced hypertrophy and heart failure via augmentation of angiogenesis,” Circulation, vol. 124, no. 21, 2011. View at Google Scholar
  63. D. J. Polhemus, K. Kondo, S. Bhushan et al., “Hydrogen sulfide attenuates cardiac dysfunction after heart failure via induction of angiogenesis,” Circulation: Heart Failure, vol. 6, no. 5, pp. 1077–1086, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Givvimani, S. Kundu, N. Narayanan et al., “TIMP-2 mutant decreases MMP-2 activity and augments pressure overload induced LV dysfunction and heart failure,” Archives of Physiology and Biochemistry, vol. 119, no. 2, pp. 65–74, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Y. Zhang, X. H. Li, T. Zhang, J. Fu, and X. D. Cui, “Hydrogen sulfide upregulates heme oxygenase-1 expression in rats with volume overload-induced heart failure,” Biomedical Reports, vol. 1, no. 3, pp. 454–458, 2013. View at Google Scholar
  66. Y.-H. Liu, M. Lu, Z.-Z. Xie et al., “Hydrogen sulfide prevents heart failure development via inhibition of renin release from mast cells in isoproterenol-treated rats,” Antioxidants & Redox Signaling, vol. 20, no. 5, pp. 759–769, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Huang, J. Kan, X. Liu 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, vol. 8, no. 7, Article ID e69205, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. J. T. Kan, W. Guo, C. R. Huang, G. Z. Bao, Y. C. Zhu, and Y. Z. Zhu, “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, vol. 20, no. 15, pp. 2303–2316, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. O. Asghar, A. Al-Sunni, K. Khavandi et al., “Diabetic cardiomyopathy,” Clinical Science, vol. 116, no. 10, pp. 741–760, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Dutta, U. K. Biswas, R. Chakraborty, P. Banerjee, U. Raychaudhuri, and A. Kumar, “Evaluation of plasma H2S levels and H2S synthesis in streptozotocin induced Type-2 diabetes-an experimental study based on Swietenia macrophylla seeds,” Asian Pacific Journal of Tropical Biomedicine, vol. 4, supplement 1, pp. S483–S487, 2014. View at Publisher · View at Google Scholar
  71. S. K. Jain, R. Bull, J. L. Rains et al., “Low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocin-treated rats causes vascular inflammation?” Antioxidants & Redox Signaling, vol. 12, no. 11, pp. 1333–1337, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. W. Xu, W. Wu, J. Chen et al., “Exogenous hydrogen sulfide protects H9c2 cardiac cells against high glucose-induced injury by inhibiting the activities of the p38 MAPK and ERK1/2 pathways,” International Journal of Molecular Medicine, vol. 32, no. 4, pp. 917–925, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. W.-B. Wei, X. Hu, X.-D. Zhuang, L.-Z. Liao, and W.-D. Li, “GYY4137, a novel hydrogen sulfide-releasing molecule, likely protects against high glucose-induced cytotoxicity by activation of the AMPK/mTOR signal pathway in H9c2 cells,” Molecular and Cellular Biochemistry, vol. 389, no. 1-2, pp. 249–256, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. X. Zhou, G. An, and X. Lu, “Hydrogen sulfide attenuates the development of diabetic cardiomyopathy,” Clinical Science, vol. 128, no. 5, pp. 325–335, 2015. View at Publisher · View at Google Scholar
  75. B. F. Peake, C. K. Nicholson, J. P. Lambert et al., “Hydrogen sulfide preconditions the db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 304, no. 9, pp. H1215–H1224, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. W.-H. Sun, F. Liu, Y. Chen, and Y.-C. Zhu, “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, vol. 421, no. 2, pp. 164–169, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Szabõ, “Hydrogen sulphide and its therapeutic potential,” Nature Reviews Drug Discovery, vol. 6, no. 11, pp. 917–935, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. J. W. Calvert, W. A. Coetzee, and D. J. Lefer, “Novel insights into hydrogen sulfide-mediated cytoprotection,” Antioxidants & Redox Signaling, vol. 12, no. 10, pp. 1203–1217, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. T. T. Pan, K. L. Neo, L. F. Hu, Q. C. Yong, and J. S. Bian, “H2S preconditioning-induced PKC activation regulates intracellular calcium handling in rat cardiomyocytes,” The American Journal of Physiology—Cell Physiology, vol. 294, no. 1, pp. C169–C177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. M. K. Muellner, S. M. Schreier, H. Laggner et al., “Hydrogen sulfide destroys lipid hydroperoxides in oxidized LDL,” Biochemical Journal, vol. 420, no. 2, pp. 277–281, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. M. Marí, A. Morales, A. Colell, C. García-Ruiz, and J. C. Fernández-Checa, “Mitochondrial glutathione, a key survival antioxidant,” Antioxidants & Redox Signaling, vol. 11, no. 11, pp. 2685–2700, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. M. G. Alves, A. F. Soares, R. A. Carvalho, and P. J. Oliveira, “Sodium hydrosulfide improves the protective potential of the cardioplegic histidine buffer solution,” European Journal of Pharmacology, vol. 654, no. 1, pp. 60–67, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. M. A. Aon, S. Cortassa, F. G. Akar, and B. O'Rourke, “Mitochondrial criticality: a new concept at the turning point of life or death,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1762, no. 2, pp. 232–240, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. E. N. Churchill and D. Mochly-Rosen, “The roles of PKCδ and ε isoenzymes in the regulation of myocardial ischaemia/reperfusion injury,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1040–1042, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. E. Murphy and C. Steenbergen, “Preconditioning: the mitochondrial connection,” Annual Review of Physiology, vol. 69, pp. 51–67, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. X. Zhou and X. Lu, “Hydrogen sulfide inhibits high-glucose-induced apoptosis in neonatal rat cardiomyocytes,” Experimental Biology and Medicine, vol. 238, no. 4, pp. 370–374, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. N. R. Sodha, R. T. Clements, J. Feng et al., “The effects of therapeutic sulfide on myocardial apoptosis in response to ischemia-reperfusion injury,” European Journal of Cardio-Thoracic Surgery, vol. 33, no. 5, pp. 906–913, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. L.-L. Yao, X.-W. Huang, Y.-G. Wang, Y.-X. Cao, C.-C. Zhang, and Y.-C. Zhu, “Hydrogen sulfide protects cardiomyocytes from hypoxia/reoxygenation-induced apoptosis by preventing GSK-3β-dependent opening of mPTP,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 298, no. 5, pp. H1310–H1319, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. B. J. Pomerantz, L. L. Reznikov, A. H. Harken, and C. A. Dinarello, “Inhibition of caspase 1 reduces human myocardial ischemic dysfunction via inhibition of IL-18 and IL-1 beta,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 5, pp. 2871–2876, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. H. A. Hennein, H. Ebba, J. L. Rodriguez et al., “Relationship of the proinflammatory cytokines to myocardial ischemia and dysfunction after uncomplicated coronary revascularization,” Journal of Thoracic and Cardiovascular Surgery, vol. 108, no. 4, pp. 626–635, 1994. View at Google Scholar · View at Scopus
  91. C. A. Dinarello, “Proinflammatory cytokines,” Chest, vol. 118, no. 2, pp. 503–508, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Whiteman and P. G. Winyard, “Hydrogen sulfide and inflammation: the good, the bad, the ugly and the promising,” Expert Review of Clinical Pharmacology, vol. 4, no. 1, pp. 13–32, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. N. R. Sodha, R. T. Clements, J. Feng et al., “Hydrogen sulfide therapy attenuates the inflammatory response in a porcine model of myocardial ischemia/reperfusion injury,” The Journal of Thoracic and Cardiovascular Surgery, vol. 138, no. 4, pp. 977–984, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. R. C. O. Zanardo, V. Brancaleone, E. Distrutti, S. Fiorucci, G. Cirino, and J. L. Wallace, “Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation,” The FASEB Journal, vol. 20, no. 12, pp. 2118–2120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. L.-L. Pan, X.-H. Liu, Q.-H. Gong, and Y.-Z. Zhu, “S-Propargyl-cysteine (SPRC) attenuated lipopolysaccharide-induced inflammatory response in H9c2 cells involved in a hydrogen sulfide-dependent mechanism,” Amino Acids, vol. 41, no. 1, pp. 205–215, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Szabó and A. Papapetropoulos, “Hydrogen sulphide and angiogenesis: mechanisms and applications,” British Journal of Pharmacology, vol. 164, no. 3, pp. 853–865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Papapetropoulos, A. Pyriochou, Z. Altaany et al., “Hydrogen sulfide is an endogenous stimulator of angiogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 51, pp. 21972–21977, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Givvimani, C. Munjal, R. Gargoum et al., “Hydrogen sulfide mitigates transition from compensatory hypertrophy to heart failure,” Journal of Applied Physiology, vol. 110, no. 4, pp. 1093–1100, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. W. M. Zhao, J. Zhang, Y. J. Lu, and R. Wang, “The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener,” The EMBO Journal, vol. 20, no. 21, pp. 6008–6016, 2001. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Kai, T. Tanaka, H. Daijo et al., “Hydrogen sulfide inhibits hypoxia-but not anoxia-induced hypoxia-inducible factor 1 activation in a von hippel-lindau-and mitochondria-dependent manner,” Antioxidants and Redox Signaling, vol. 16, no. 3, pp. 203–216, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. B. B. Tao, S. Y. Liu, C. C. Zhang et al., “VEGFR2 functions as an H2S-targeting receptor protein kinase with its novel Cys1045–Cys1024 disulfide bond serving as a specific molecular switch for hydrogen sulfide actions in vascular endothelial cells,” Antioxidants & Redox Signaling, vol. 19, no. 5, pp. 448–464, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. D. M. Bers, “Calcium cycling and signaling in cardiac myocytes,” Annual Review of Physiology, vol. 70, pp. 23–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. G. H. Tang, L. Y. Wu, and R. Wang, “Interaction of hydrogen sulfide with ion channels,” Clinical and Experimental Pharmacology and Physiology, vol. 37, no. 7, pp. 753–763, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. G. Sun, Y. X. Cao, W. W. Wang, S. F. Ma, T. Yao, and Y. C. Zhu, “Hydrogen sulphide is an inhibitor of L-type calcium channels and mechanical contraction in rat cardiomyocytes,” Cardiovascular Research, vol. 79, no. 4, pp. 632–641, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. R. Y. Zhang, Y. Sun, H. J. Tsai, C. S. Tang, H. F. Jin, and J. B. Du, “Hydrogen sulfide inhibits L-type calcium currents depending upon the protein sulfhydryl state in rat cardiomyocytes,” PLoS ONE, vol. 7, no. 5, Article ID e37073, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. G. Vassort, K. Talavera, and J. L. Alvarez, “Role of T-type Ca2+ channels in the heart,” Cell Calcium, vol. 40, no. 2, pp. 205–220, 2006. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Elies, J. L. Scragg, S. Huang et al., “Hydrogen sulfide inhibits Cav3.2 T-type Ca2+ channels,” The FASEB Journal, vol. 28, no. 12, pp. 5376–5387, 2014. View at Publisher · View at Google Scholar
  108. G. Tang, L. Wu, W. Liang, and R. Wang, “Direct stimulation of KATP channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells,” Molecular Pharmacology, vol. 68, no. 6, pp. 1757–1764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. S. W. Lee, Y. Cheng, P. K. Moore, and J. S. Bian, “Hydrogen sulphide regulates intracellular pH in vascular smooth muscle cells,” Biochemical and Biophysical Research Communications, vol. 358, no. 4, pp. 1142–1147, 2007. View at Google Scholar
  110. D. Johansen, K. Ytrehus, and G. F. Baxter, “Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury—evidence for a role of KATP channels,” Basic Research in Cardiology, vol. 101, no. 1, pp. 53–60, 2006. View at Publisher · View at Google Scholar · View at Scopus
  111. Z. Zhang, H. Huang, P. Liu, C. Tang, and J. Wang, “Hydrogen sulfide contributes to cardioprotection during ischemia-reperfusion injury by opening KATP channels,” Canadian Journal of Physiology and Pharmacology, vol. 85, no. 12, pp. 1248–1253, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. P. R. Strege, C. E. Bernard, R. E. Kraichely et al., “Hydrogen sulfide is a partially redox-independent activator of the human jejunum Na+ channel, NAv1.5,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 300, no. 6, pp. G1105–G1114, 2011. View at Publisher · View at Google Scholar · View at Scopus
  113. L. Malekova, O. Krizanova, and K. Ondrias, “H2S and HS- donor NaHS inhibits intracellular chloride channels,” General Physiology and Biophysics, vol. 28, no. 2, pp. 190–194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. A. L. King, D. J. Polhemus, S. Bhushan et al., “Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 8, pp. 3182–3187, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. M. Whiteman, L. Li, I. Kostetski et al., “Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide,” Biochemical and Biophysical Research Communications, vol. 343, no. 1, pp. 303–310, 2006. View at Publisher · View at Google Scholar · View at Scopus
  116. B. L. Predmore, K. Kondo, S. Bhushan et al., “The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 302, no. 11, pp. H2410–H2418, 2012. View at Publisher · View at Google Scholar · View at Scopus
  117. E. Łowicka and J. Bełtowski, “Hydrogen sulfide (H2S)—the third gas of interest for pharmacologists,” Pharmacological Reports, vol. 59, no. 1, pp. 4–24, 2007. View at Google Scholar · View at Scopus
  118. J. Fiedler, S. Batkai, and T. Thum, “MicroRNA-based therapy in cardiology,” Herz, vol. 39, no. 2, pp. 194–200, 2014. View at Publisher · View at Google Scholar · View at Scopus
  119. J. Shen, T. Xing, H. Yuan et al., “Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions,” PLoS ONE, vol. 8, no. 10, Article ID e77047, 2013. View at Publisher · View at Google Scholar · View at Scopus
  120. X. Huang, Y. Gao, J. Qin, and S. Lu, “The role of miR-34a in the hepatoprotective effect of hydrogen sulfide on ischemia/reperfusion injury in young and old rats,” PLoS ONE, vol. 9, no. 11, Article ID e113305, 2014. View at Publisher · View at Google Scholar
  121. J. Liu, D.-D. Hao, J.-S. Zhang, and Y.-C. Zhu, “Hydrogen sulphide inhibits cardiomyocyte hypertrophy by up-regulating miR-133a,” Biochemical and Biophysical Research Communications, vol. 413, no. 2, pp. 342–347, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Toldo, A. Das, E. Mezzaroma et al., “Induction of microRNA-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice,” Circulation: Cardiovascular Genetics, vol. 7, no. 3, pp. 311–320, 2014. View at Publisher · View at Google Scholar
  123. Y. Kimura and H. Kimura, “Hydrogen sulfide protects neurons from oxidative stress,” The FASEB Journal, vol. 18, no. 10, pp. 1165–1167, 2004. View at Publisher · View at Google Scholar · View at Scopus
  124. G. Caliendo, G. Cirino, V. Santagada, and J. L. Wallace, “Synthesis and biological effects of hydrogen sulfide (H2S): development of H2S-releasing drugs as pharmaceuticals,” Journal of Medicinal Chemistry, vol. 53, no. 17, pp. 6275–6286, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. Y. Zhao, S. Bhushan, C. Yang et al., “Controllable hydrogen sulfide donors and their activity against myocardial ischemia-reperfusion injury,” ACS Chemical Biology, vol. 8, no. 6, pp. 1283–1290, 2013. View at Publisher · View at Google Scholar · View at Scopus
  126. B. L. Predmore, K. Kondo, S. Bhushan et al., “The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 302, no. 11, pp. H2410–H2418, 2012. View at Publisher · View at Google Scholar · View at Scopus
  127. C.-Y. Tsai, C.-C. Wang, T.-Y. Lai et al., “Antioxidant effects of diallyl trisulfide on high glucose-induced apoptosis are mediated by the PI3K/Akt-dependent activation of Nrf2 in cardiomyocytes,” International Journal of Cardiology, vol. 168, no. 2, pp. 1286–1297, 2013. View at Publisher · View at Google Scholar · View at Scopus
  128. Y. P. Lei, C. T. Liu, L. Y. Sheen, H. W. Chen, and C. K. Lii, “Diallyl disulfide and diallyl trisulfide protect endothelial nitric oxide synthase against damage by oxidized low-density lipoprotein,” Molecular Nutrition and Food Research, vol. 54, supplement 1, pp. S42–S52, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. C. C. Shin, P. K. Moore, and Y. Z. Zhu, “S-allylcysteine mediates cardioprotection in an acute myocardial infarction rat model via a hydrogen sulfide-mediated pathway,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 293, no. 5, pp. H2693–H2701, 2007. View at Publisher · View at Google Scholar · View at Scopus
  130. Q. Wang, H.-R. Liu, Q. Mu, P. Rose, and Y. Z. Zhu, “S-propargyl-cysteine protects both adult rat hearts and neonatal cardiomyocytes from ischemia/hypoxia injury: the contribution of the hydrogen sulfide-mediated pathway,” Journal of Cardiovascular Pharmacology, vol. 54, no. 2, pp. 139–146, 2009. View at Publisher · View at Google Scholar · View at Scopus