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Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Review

Mechanisms by which hydrogen sulfide attenuates muscle function following ischemia–reperfusion injury: effects on Akt signaling, mitochondrial function, and apoptosis

Authors: Michael D. Wetzel, Joseph C. Wenke

Published in: Journal of Translational Medicine | Issue 1/2019

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Abstract

Ischemia–reperfusion injury is caused by a period of ischemia followed by massive blood flow into a tissue that had experienced restricted blood flow. The severity of the injury is dependent on the time the tissue was restricted from blood flow, becoming more severe after longer ischemia times. This can lead to many complications such as tissue necrosis, cellular apoptosis, inflammation, metabolic and mitochondrial dysfunction, and even organ failure. One of the emerging therapies to combat ischemic reperfusion injury complications is hydrogen sulfide, which is a gasotransmitter that diffuses across cell membranes to exert effects on various signaling pathways regulating cell survival such as Akt, mitochondrial activity, and apoptosis. Although commonly thought of as a toxic gas, low concentrations of hydrogen sulfide have been shown to be beneficial in promoting tissue survival post-ischemia, and modulate a wide variety of cellular responses. This review will detail the mechanisms of hydrogen sulfide in affecting the Akt signaling pathway, mitochondrial function, and apoptosis, particularly in regards to ischemic reperfusion injury in muscle tissue. It will conclude with potential clinical applications of hydrogen sulfide, combinations with other therapies, and perspectives for future studies.
Literature
1.
2.
Cheng F, Zhang Q, Yan FF, Wan JF, Lin CS. Lutein protects against ischemia/reperfusion injury in rat skeletal muscle by modulating oxidative stress and inflammation. Immunopharmacol Immunotoxicol. 2015;37:329–34.PubMedCrossRef
3.
Gillani S, Cao J, Suzuki T, Hak DJ. The effect of ischemia reperfusion injury on skeletal muscle. Injury. 2012;43:670–5.PubMedCrossRef
4.
Chen XK, Rathbone CR, Walters TJ. Treatment of tourniquet-induced ischemia reperfusion injury with muscle progenitor cells. J Surg Res. 2011;170:e65–73.PubMedCrossRef
5.
Ejaz A, Laursen AC, Kappel A, Jakobsen T, Nielsen PT, Rasmussen S. Tourniquet induced ischemia and changes in metabolism during TKA: a randomized study using microdialysis. BMC Musculoskelet Disord. 2015;16:326.PubMedPubMedCentralCrossRef
6.
Li H, Wang Y, Wei C, Bai S, Zhao Y, Wu B, Wang R, Wu L, Xu C. Mediation of exogenous hydrogen sulfide in recovery of ischemic post-conditioning-induced cardioprotection via down-regulating oxidative stress and up-regulating PI3K/Akt/GSK-3β pathway in isolated aging rat hearts. Cell Biosci. 2015;5:11.PubMedPubMedCentralCrossRef
7.
Petrosillo G, Di Venosa N, Ruggiero FM, Pistolese M, D’Agostino D, Tiravanti E, Fiore T, Paradies G. Mitochondrial dysfunction associated with cardiac ischemia/reperfusion can be attenuated by oxygen tension control. Role of oxygen-free radicals and cardiolipin. Biochim Biophys Acta. 2005;1710:78–86.PubMedCrossRef
8.
Blaisdell FW. The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc Surg. 2002;10:620–30.PubMedCrossRef
9.
Charles AL, Guilbert AS, Guillot M, Talha S, Lejay A, Meyer A, Kindo M, Wolff V, Bouitbir J, Zoll J, Geny B. Muscles susceptibility to ischemia-reperfusion injuries depends on fiber type specific antioxidant level. Front Physiol. 2017;8:52.PubMedPubMedCentralCrossRef
10.
Garbaisz D, Turoczi Z, Aranyi P, Fulop A, Rosero O, Hermesz E, Ferencz A, Lotz G, Harsanyi L, Szijarto A. Attenuation of skeletal muscle and renal injury to the lower limb following ischemia-reperfusion using mPTP inhibitor NIM-811. PLoS ONE. 2014;9:e101067.PubMedPubMedCentralCrossRef
11.
Jawhar A, Ponelies N, Schild L. Effect of limited ischemia time on the amount and function of mitochondria within human skeletal muscle cells. Eur J Trauma Emerg Surg. 2016;42:767–73.PubMedCrossRef
12.
Corona BT, Rivera JC, Owens JG, Wenke JC, Rathbone CR. Volumetric muscle loss leads to permanent disability following extremity trauma. J Rehabil Res Dev. 2015;52:785–92.PubMedCrossRef
13.
Novelli GP, Adembri C, Gandini E, Orlandini SZ, Papucci L, Formigli L, Manneschi LI, Quattrone A, Pratesi C, Capaccioli S. Vitamin E protects human skeletal muscle from damage during surgical ischemia-reperfusion. Am J Surg. 1997;173:206–9.PubMedCrossRef
14.
Percival TJ, Rasmussen TE. Reperfusion strategies in the management of extremity vascular injury with ischaemia. Br J Surg. 2012;99(Suppl 1):66–74.PubMedCrossRef
15.
Barreto-Torres G, Parodi-Rullán R, Javadov S. The role of PPARα in metformin-induced attenuation of mitochondrial dysfunction in acute cardiac ischemia/reperfusion in rats. Int J Mol Sci. 2012;13:7694–709.PubMedPubMedCentralCrossRef
16.
Ozkan H, Ekinci S, Uysal B, Akyildiz F, Turkkan S, Ersen O, Koca K, Seven MM. Evaluation and comparison of the effect of hypothermia and ozone on ischemia-reperfusion injury of skeletal muscle in rats. J Surg Res. 2015;196:313–9.PubMedCrossRef
17.
Zhu YZ, Wang ZJ, Ho P, Loke YY, Zhu YC, Huang SH, Tan CS, Whiteman M, Lu J, Moore PK. Hydrogen sulfide and its possible roles in myocardial ischemia in experimental rats. J Appl Physiol. 1985;2007(102):261–8.
18.
Hunter JP, Hosgood SA, Patel M, Furness P, Sayers RD, Nicholson ML. Hydrogen sulfide reduces inflammation following abdominal aortic occlusion in rats. Ann Vasc Surg. 2015;29:353–60.PubMedCrossRef
19.
Hurtgen BJ, Ward CL, Garg K, Pollot BE, Goldman SM, McKinley TO, Wenke JC, Corona BT. Severe muscle trauma triggers heightened and prolonged local musculoskeletal inflammation and impairs adjacent tibia fracture healing. J Musculoskelet Neuronal Interact. 2016;16:122–34.PubMedPubMedCentral
20.
Bełtowski J. Hydrogen sulfide in pharmacology and medicine–an update. Pharmacol Rep. 2015;67:647–58.PubMedCrossRef
21.
Módis K, Panopoulos P, Coletta C, Papapetropoulos A, Szabo C. Hydrogen sulfide-mediated stimulation of mitochondrial electron transport involves inhibition of the mitochondrial phosphodiesterase 2A, elevation of cAMP and activation of protein kinase A. Biochem Pharmacol. 2013;86:1311–9.PubMedCrossRef
22.
Olson KR, DeLeon ER, Liu F. Controversies and conundrums in hydrogen sulfide biology. Nitric Oxide. 2014;41:11–26.PubMedCrossRef
23.
Veeranki S, Tyagi SC. Role of hydrogen sulfide in skeletal muscle biology and metabolism. Nitric Oxide. 2015;46:66–71.PubMedCrossRef
24.
Du JT, Li W, Yang JY, Tang CS, Li Q, Jin HF. Hydrogen sulfide is endogenously generated in rat skeletal muscle and exerts a protective effect against oxidative stress. Chin Med J (Engl). 2013;126:930–6.
25.
Carter RN, Morton NM. Cysteine and hydrogen sulphide in the regulation of metabolism: insights from genetics and pharmacology. J Pathol. 2016;238:321–32.PubMedCrossRef
26.
Polhemus DJ, Lefer DJ. Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease. Circ Res. 2014;114:730–7.PubMedPubMedCentralCrossRef
27.
Polhemus DJ, Calvert JW, Butler J, Lefer DJ. The cardioprotective actions of hydrogen sulfide in acute myocardial infarction and heart failure. Scientifica (Cairo). 2014;2014:768607.
28.
Vitvitsky V, Kabil O, Banerjee R. High turnover rates for hydrogen sulfide allow for rapid regulation of its tissue concentrations. Antioxid Redox Signal. 2012;17:22–31.PubMedPubMedCentralCrossRef
29.
Li N, Wang MJ, Jin S, Bai YD, Hou CL, Ma FF, Li XH, Zhu YC. The H2S donor NaHS changes the expression pattern of H2S-producing enzymes after myocardial infarction. Oxid Med Cell Longev. 2016;2016:6492469.PubMedPubMedCentral
30.
Xu Z, Prathapasinghe G, Wu N, Hwang SY, Siow YL. Ischemia-reperfusion reduces cystathionine-beta-synthase-mediated hydrogen sulfide generation in the kidney. Am J Physiol Renal Physiol. 2009;297:F27–35.PubMedCrossRef
31.
Islam KN, Polhemus DJ, Donnarumma E, Brewster LP, Lefer DJ. Hydrogen sulfide levels and nuclear factor-erythroid 2-related factor 2 (NRF2) activity are attenuated in the setting of critical limb ischemia (CLI). J Am Heart Assoc. 2015;4:e001986.PubMedPubMedCentralCrossRef
32.
Liu MH, Zhang Y, He J, Tan TP, Wu SJ, Guo DM, He H, Peng J, Tang ZH, Jiang ZS. Hydrogen sulfide protects H9c2 cardiac cells against doxorubicin-induced cytotoxicity through the PI3 K/Akt/FoxO3a pathway. Int J Mol Med. 2016;37:1661–8.PubMedCrossRef
33.
Zhou Y, Wang D, Gao X, Lew K, Richards AM, Wang P. mTORC2 phosphorylation of Akt1: a possible mechanism for hydrogen sulfide-induced cardioprotection. PLoS ONE. 2014;9:e99665.PubMedPubMedCentralCrossRef
34.
Zhao H, Lu S, Chai J, Zhang Y, Ma X, Chen J, Guan Q, Wan M, Liu Y. Hydrogen sulfide improves diabetic wound healing in ob/ob mice via attenuating inflammation. J Diabetes Complications. 2017;31:1363–9.PubMedCrossRef
35.
Jensen AR, Drucker NA, Khaneki S, Ferkowicz MJ, Markel TA. Hydrogen sulfide improves intestinal recovery following ischemia by endothelial nitric oxide-dependent mechanisms. Am J Physiol Gastrointest Liver Physiol. 2017;312:G450–6.PubMedPubMedCentralCrossRef
36.
Ercole F, Mansfeld FM, Kavallaris M, Whittaker MR, Quinn JF, Halls ML, Davis TP. Macromolecular hydrogen sulfide donors trigger spatiotemporally confined changes in cell signaling. Biomacromology. 2016;17:371–83.CrossRef
37.
Sun X, Wang W, Dai J, Jin S, Huang J, Guo C, Wang C, Pang L, Wang Y. A long-term and slow-releasing hydrogen sulfide donor protects against myocardial ischemia/reperfusion injury. Sci Rep. 2017;7:3541.PubMedPubMedCentralCrossRef
38.
Minamishima S, Bougaki M, Sips PY, Yu JD, Minamishima YA, Elrod JW, Lefer DJ, Bloch KD, Ichinose F. Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation. 2009;120:888–96.PubMedPubMedCentralCrossRef
39.
Xie H, Xu Q, Jia J, Ao G, Sun Y, Hu L, Alkayed NJ, Wang C, Cheng J. Hydrogen sulfide protects against myocardial ischemia and reperfusion injury by activating AMP-activated protein kinase to restore autophagic flux. Biochem Biophys Res Commun. 2015;458:632–8.PubMedCrossRef
40.
41.
Yong QC, Lee SW, Foo CS, Neo KL, Chen X, Bian JS. Endogenous hydrogen sulphide mediates the cardioprotection induced by ischemic postconditioning. Am J Physiol Heart Circ Physiol. 2008;295:H1330–40.PubMedCrossRef
42.
Wang D, Ma Y, Li Z, Kang K, Sun X, Pan S, Wang J, Pan H, Liu L, Liang D, Jiang H. The role of AKT1 and autophagy in the protective effect of hydrogen sulphide against hepatic ischemia/reperfusion injury in mice. Autophagy. 2012;8:954–62.PubMedPubMedCentralCrossRef
43.
Karwi QG, Whiteman M, Wood ME, Torregrossa R, Baxter GF. Pharmacological postconditioning against myocardial infarction with a slow-releasing hydrogen sulfide donor, GYY4137. Pharmacol Res. 2016;111:442–51.CrossRef
44.
45.
Cao HH, Chu JH, Kwan HY, Su T, Yu H, Cheng CY, Fu XQ, Guo H, Li T, Tse AK, et al. Inhibition of the STAT3 signaling pathway contributes to apigenin-mediated anti-metastatic effect in melanoma. Sci Rep. 2016;6:21731.PubMedPubMedCentralCrossRef
46.
Yuan S, Shen X, Kevil CG. Beyond a gasotransmitter: hydrogen sulfide and polysulfide in cardiovascular health and immune response. Antioxid Redox Signal. 2017;27(10):634–53.PubMedPubMedCentralCrossRef
47.
Borselli C, Storrie H, Benesch-Lee F, Shvartsman D, Cezar C, Lichtman JW, Vandenburgh HH, Mooney DJ. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc Natl Acad Sci USA. 2010;107:3287–92.PubMedCrossRef
48.
Langston JW, Toombs CF. Defining the minimally effective dose and schedule for parenteral hydrogen sulfide: long-term benefits in a rat model of hindlimb ischemia. Med Gas Res. 2015;5:5.PubMedPubMedCentralCrossRef
49.
Deasy BM, Feduska JM, Payne TR, Li Y, Ambrosio F, Huard J. Effect of VEGF on the regenerative capacity of muscle stem cells in dystrophic skeletal muscle. Mol Ther. 2009;17:1788–98.PubMedPubMedCentralCrossRef
50.
Shvartsman D, Storrie-White H, Lee K, Kearney C, Brudno Y, Ho N, Cezar C, McCann C, Anderson E, Koullias J, et al. Sustained delivery of VEGF maintains innervation and promotes reperfusion in ischemic skeletal muscles via NGF/GDNF signaling. Mol Ther. 2014;22:1243–53.PubMedPubMedCentralCrossRef
51.
Kang Z, Jiang W, Luan H, Zhao F, Zhang S. Cornin induces angiogenesis through PI3 K-Akt-eNOS-VEGF signaling pathway. Food Chem Toxicol. 2013;58:340–6.PubMedCrossRef
52.
Kroll J, Waltenberger J. VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun. 1998;252:743–6.PubMedCrossRef
53.
Jang H, Oh MY, Kim YJ, Choi IY, Yang HS, Ryu WS, Lee SH, Yoon BW. Hydrogen sulfide treatment induces angiogenesis after cerebral ischemia. J Neurosci Res. 2014;92:1520–8.PubMedCrossRef
54.
Wang MJ, Cai WJ, Li N, Ding YJ, Chen Y, Zhu YC. The hydrogen sulfide donor NaHS promotes angiogenesis in a rat model of hind limb ischemia. Antioxid Redox Signal. 2010;12:1065–77.PubMedCrossRef
55.
Kondo K, Bhushan S, King AL, Prabhu SD, Hamid T, Koenig S, Murohara T, Predmore BL, Gojon G, Wang R, et al. H2S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation. 2013;127:1116–27.PubMedPubMedCentralCrossRef
56.
King AL, Polhemus DJ, Bhushan S, Otsuka H, Kondo K, Nicholson CK, Bradley JM, Islam KN, Calvert JW, Tao YX, et al. Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent. Proc Natl Acad Sci USA. 2014;111:3182–7.PubMedCrossRef
57.
Hayashida R, Kondo K, Morita S, Unno K, Shintani S, Shimizu Y, Calvert JW, Shibata R, Murohara T. Diallyl trisulfide augments ischemia-induced angiogenesis via an endothelial nitric oxide synthase-dependent mechanism. Circ J. 2017;81:870–8.PubMedCrossRef
58.
Chattopadhyay A, Bandyopadhyay D. Vitamin E in the prevention of ischemic heart disease. Pharmacol Rep. 2006;58:179–87.PubMed
59.
Saleh NK, Saleh HA. Protective effects of vitamin E against myocardial ischemia/reperfusion injury in rats. Saudi Med J. 2010;31:142–7.PubMed
60.
61.
62.
Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev. 2010;90:1383–435.PubMedCrossRef
63.
Lesnefsky EJ, Hoppel CL. Oxidative phosphorylation and aging. Ageing Research Reviews. 2006;5:402–33.PubMedCrossRef
64.
Hernández JS, Barreto-Torres G, Kuznetsov AV, Khuchua Z, Javadov S. Crosstalk between AMPK activation and angiotensin II-induced hypertrophy in cardiomyocytes: the role of mitochondria. J Cell Mol Med. 2014;18:709–20.PubMedPubMedCentralCrossRef
65.
Korth U, Merkel G, Fernandez FF, Jandewerth O, Dogan G, Koch T, van Ackern K, Weichel O, Klein J. Tourniquet-induced changes of energy metabolism in human skeletal muscle monitored by microdialysis. Anesthesiology. 2000;93:1407–12.PubMedCrossRef
66.
67.
Javadov S, Karmazyn M. Mitochondrial permeability transition pore opening as an endpoint to initiate cell death and as a putative target for cardioprotection. Cell Physiol Biochem. 2007;20:1–22.PubMedCrossRef
68.
Tompkins AJ, Burwell LS, Digerness SB, Zaragoza C, Holman WL, Brookes PS. Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim Biophys Acta. 2006;1762:223–31.PubMedCrossRef
69.
Pipinos II, Swanson SA, Zhu Z, Nella AA, Weiss DJ, Gutti TL, McComb RD, Baxter BT, Lynch TG, Casale GP. Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage. Am J Physiol Regul Integr Comp Physiol. 2008;295:R290–6.PubMedPubMedCentralCrossRef
70.
Narne P, Pandey V, Phanithi PB. Interplay between mitochondrial metabolism and oxidative stress in ischemic stroke: an epigenetic connection. Mol Cell Neurosci. 2017;82:176–94.PubMedCrossRef
71.
Flagg TP, Enkvetchakul D, Koster JC, Nichols CG. Muscle KATP channels: recent insights to energy sensing and myoprotection. Physiol Rev. 2010;90:799–829.PubMedPubMedCentralCrossRef
72.
Li H, Zhang C, Sun W, Li L, Wu B, Bai S, Zhong X, Wang R, Wu L, Xu C. Exogenous hydrogen sulfide restores cardioprotection of ischemic post-conditioning via inhibition of mPTP opening in the aging cardiomyocytes. Cell Biosci. 2015;5:43.PubMedPubMedCentralCrossRef
73.
Liang W, Chen J, Mo L, Ke X, Zhang W, Zheng D, Pan W, Wu S, Feng J, Song M, Liao X. ATP-sensitive K+ channels contribute to the protective effects of exogenous hydrogen sulfide against high glucose-induced injury in H9c2 cardiac cells. Int J Mol Med. 2016;37:763–72.PubMedCrossRef
74.
Du Q, Wang C, Zhang N, Li G, Zhang M, Li L, Zhang Q, Zhang J. In vivo study of the effects of exogenous hydrogen sulfide on lung mitochondria in acute lung injury in rats. BMC Anesthesiol. 2014;14:117.PubMedPubMedCentralCrossRef
75.
Lu M, Zhao FF, Tang JJ, Su CJ, Fan Y, Ding JH, Bian JS, Hu G. The neuroprotection of hydrogen sulfide against MPTP-induced dopaminergic neuron degeneration involves uncoupling protein 2 rather than ATP-sensitive potassium channels. Antioxid Redox Signal. 2012;17:849–59.PubMedPubMedCentralCrossRef
76.
Kida K, Yamada M, Tokuda K, Marutani E, Kakinohana M, Kaneki M, Ichinose F. Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson’s disease. Antioxid Redox Signal. 2011;15:343–52.PubMedPubMedCentralCrossRef
77.
Inagaki N, Inazawa J, Seino S. cDNA sequence, gene structure, and chromosomal localization of the human ATP-sensitive potassium channel, uKATP-1, gene (KCNJ8). Genomics. 1995;30:102–4.PubMedCrossRef
78.
Inagaki N, Gonoi T, Clement JP, Namba N, Inazawa J, Gonzalez G, Aguilar-Bryan L, Seino S, Bryan J. Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science. 1995;270:1166–70.PubMedCrossRef
79.
Gade AR, Kang M, Akbarali HI. Hydrogen sulfide as an allosteric modulator of ATP-sensitive potassium channels in colonic inflammation. Mol Pharmacol. 2013;83:294–306.PubMedPubMedCentralCrossRef
80.
Zhang HT, Zhang T, Chai M, Sun JJ, Yu XY, Liu CZ, Huang CC. Effect of tobacco smoke on hydrogen sulfide-induced rat thoracic aorta relaxation. Braz J Med Biol Res. 2017;50:e5592.PubMedPubMedCentral
81.
Berdeaux R, Stewart R. cAMP signaling in skeletal muscle adaptation: hypertrophy, metabolism, and regeneration. Am J Physiol Endocrinol Metab. 2012;303:E1–17.PubMedPubMedCentralCrossRef
82.
Shaikh D, Zhou Q, Chen T, Ibe JC, Raj JU, Zhou G. cAMP-dependent protein kinase is essential for hypoxia-mediated epithelial-mesenchymal transition, migration, and invasion in lung cancer cells. Cell Signal. 2012;24:2396–406.PubMedCrossRef
83.
Zhang Z, Apse K, Pang J, Stanton RC. High glucose inhibits glucose-6-phosphate dehydrogenase via cAMP in aortic endothelial cells. J Biol Chem. 2000;275:40042–7.PubMedCrossRef
84.
Beauchamp RO, Bus JS, Popp JA, Boreiko CJ, Andjelkovich DA. A critical review of the literature on hydrogen sulfide toxicity. Crit Rev Toxicol. 1984;13:25–97.PubMedCrossRef
85.
Blackstone E, Morrison M, Roth MB. H2S induces a suspended animation-like state in mice. Science. 2005;308:518.PubMedCrossRef
86.
Aslami H, Schultz MJ, Juffermans NP. Potential applications of hydrogen sulfide-induced suspended animation. Curr Med Chem. 2009;16:1295–303.PubMedCrossRef
87.
Aslami H, Juffermans NP. Induction of a hypometabolic state during critical illness—a new concept in the ICU? Neth J Med. 2010;68:190–8.PubMed
88.
Bos EM, Leuvenink HG, Snijder PM, Kloosterhuis NJ, Hillebrands JL, Leemans JC, Florquin S, van Goor H. Hydrogen sulfide-induced hypometabolism prevents renal ischemia/reperfusion injury. J Am Soc Nephrol. 2009;20:1901–5.PubMedPubMedCentralCrossRef
89.
Dugbartey GJ, Bouma HR, Saha MN, Lobb I, Henning RH, Sener A. A hibernation-like state for transplantable organs: is hydrogen sulfide therapy the future of organ preservation? Antioxid Redox Signal. 2017;28(16):1503–15.PubMedCrossRef
90.
Shi S, Li QS, Li H, Zhang L, Xu M, Cheng JL, Peng CH, Xu CQ, Tian Y. Anti-apoptotic action of hydrogen sulfide is associated with early JNK inhibition. Cell Biol Int. 2009;33:1095–101.PubMedCrossRef
91.
Guan Q, Zhang Y, Yu C, Liu Y, Gao L, Zhao J. Hydrogen sulfide protects against high-glucose-induced apoptosis in endothelial cells. J Cardiovasc Pharmacol. 2012;59:188–93.PubMedCrossRef
92.
Dai HB, Xu MM, Lv J, Ji XJ, Zhu SH, Ma RM, Miao XL, Duan ML. Mild hypothermia combined with hydrogen sulfide treatment during resuscitation reduces hippocampal neuron apoptosis Via NR2A, NR2B, and PI3K-Akt signaling in a rat model of cerebral ischemia-reperfusion injury. Mol Neurobiol. 2016;53:4865–73.PubMedCrossRef
93.
Ji K, Xue L, Cheng J, Bai Y. Preconditioning of H2S inhalation protects against cerebral ischemia/reperfusion injury by induction of HSP70 through PI3K/Akt/Nrf2 pathway. Brain Res Bull. 2016;121:68–74.PubMedCrossRef
94.
Biermann J, Lagrèze WA, Schallner N, Schwer CI, Goebel U. Inhalative preconditioning with hydrogen sulfide attenuated apoptosis after retinal ischemia/reperfusion injury. Mol Vis. 2011;17:1275–86.PubMedPubMedCentral
95.
Yao LL, Huang XW, Wang YG, Cao YX, Zhang CC, Zhu YC. Hydrogen sulfide protects cardiomyocytes from hypoxia/reoxygenation-induced apoptosis by preventing GSK-3beta-dependent opening of mPTP. Am J Physiol Heart Circ Physiol. 2010;298:H1310–9.PubMedCrossRef
96.
Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA. 2007;104:15560–5.PubMedCrossRef
97.
Jeschke MG, Finnerty CC, Herndon DN, Song J, Boehning D, Tompkins RG, Baker HV, Gauglitz GG. Severe injury is associated with insulin resistance, endoplasmic reticulum stress response, and unfolded protein response. Ann Surg. 2012;255:370–8.PubMedPubMedCentralCrossRef
98.
Yao X, Wigginton JG, Maass DL, Ma L, Carlson D, Wolf SE, Minei JP, Zang QS. Estrogen-provided cardiac protection following burn trauma is mediated through a reduction in mitochondria-derived DAMPs. Am J Physiol Heart Circ Physiol. 2014;306:H882–94.PubMedCrossRef
99.
Cheng P, Wang F, Chen K, Shen M, Dai W, Xu L, Zhang Y, Wang C, Li J, Yang J, et al. Hydrogen sulfide ameliorates ischemia/reperfusion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators Inflamm. 2014;2014:935251.PubMedPubMedCentral
100.
Liesa M, Palacín M, Zorzano A. Mitochondrial dynamics in mammalian health and disease. Physiol Rev. 2009;89:799–845.PubMedCrossRef
101.
Zhang Q, Fu H, Zhang H, Xu F, Zou Z, Liu M, Wang Q, Miao M, Shi X. 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:e74422.PubMedPubMedCentralCrossRef
102.
Jha S, Calvert JW, Duranski MR, Ramachandran A, Lefer DJ. Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: role of antioxidant and antiapoptotic signaling. Am J Physiol Heart Circ Physiol. 2008;295:H801–6.PubMedPubMedCentralCrossRef
103.
Boroujeni MB, Khayat ZK, Anbari K, Niapour A, Gholami M, Gharravi AM. Coenzyme Q10 protects skeletal muscle from ischemia-reperfusion through the NF-kappa B pathway. Perfusion. 2017;32:372–7.PubMedCrossRef
104.
Irie H, Kato T, Ikebe K, Tsuchida T, Oniki Y, Takagi K. Antioxidant effect of MCI-186, a new Free-Radical scavenger, on ischemia-reperfusion injury in a rat hindlimb amputation model. J Surg Res. 2004;120:312–9.PubMedCrossRef
105.
Sivarajah A, Collino M, Yasin M, Benetti E, Gallicchio M, Mazzon E, Cuzzocrea S, Fantozzi R, Thiemermann C. Anti-apoptotic and anti-inflammatory effects of hydrogen sulfide in a rat model of regional myocardial I/R. Shock. 2009;31:267–74.PubMedCrossRef
106.
Wu Z, Peng H, Du Q, Lin W, Liu Y. GYY4137, a hydrogen sulfide-releasing molecule, inhibits the inflammatory response by suppressing the activation of nuclear factor-kappa B and mitogen-activated protein kinases in Coxsackie virus B3-infected rat cardiomyocytes. Mol Med Rep. 2015;11:1837–44.PubMedCrossRef
107.
Li C, Liu Y, Tang P, Liu P, Hou C, Zhang X, Chen L, Zhang L, Gu C. Hydrogen sulfide prevents OGD/R-induced apoptosis by suppressing the phosphorylation of p38 and secretion of IL-6 in PC12 cells. NeuroReport. 2016;27:230–4.PubMedCrossRef
108.
Henderson PW, Singh SP, Weinstein AL, Nagineni V, Rafii DC, Kadouch D, Krijgh DD, Spector JA. Therapeutic metabolic inhibition: hydrogen sulfide significantly mitigates skeletal muscle ischemia reperfusion injury in vitro and in vivo. Plast Reconstr Surg. 2010;126:1890–8.PubMedCrossRef
109.
Henderson PW, Jimenez N, Ruffino J, Sohn AM, Weinstein AL, Krijgh DD, Reiffel AJ, Spector JA. Therapeutic delivery of hydrogen sulfide for salvage of ischemic skeletal muscle after the onset of critical ischemia. J Vasc Surg. 2011;53:785–91.PubMedCrossRef
110.
Tripatara P, Patel NS, Collino M, Gallicchio M, Kieswich J, Castiglia S, Benetti E, Stewart KN, Brown PA, Yaqoob MM, et al. Generation of endogenous hydrogen sulfide by cystathionine gamma-lyase limits renal ischemia/reperfusion injury and dysfunction. Lab Invest. 2008;88:1038–48.PubMedCrossRef
111.
Tran TP, Tu H, Liu J, Muelleman RL, Li YL. Mitochondria-derived superoxide links to tourniquet-induced apoptosis in mouse skeletal muscle. PLoS ONE. 2012;7:e43410.PubMedPubMedCentralCrossRef
112.
Mansour Z, Charles AL, Bouitbir J, Pottecher J, Kindo M, Mazzucotelli JP, Zoll J, Geny B. Remote and local ischemic postconditioning further impaired skeletal muscle mitochondrial function after ischemia-reperfusion. J Vasc Surg. 2012;56(774–782):e771.
113.
Aslami H, Pulskens WP, Kuipers MT, Bos AP, van Kuilenburg AB, Wanders RJ, Roelofsen J, Roelofs JJ, Kerindongo RP, Beurskens CJ, et al. Hydrogen sulfide donor NaHS reduces organ injury in a rat model of pneumococcal pneumosepsis, associated with improved bio-energetic status. PLoS ONE. 2013;8:e63497.PubMedPubMedCentralCrossRef
114.
Kang B, Hong J, Xiao J, Zhu X, Ni X, Zhang Y, He B, Wang Z. Involvement of miR-1 in the protective effect of hydrogen sulfide against cardiomyocyte apoptosis induced by ischemia/reperfusion. Mol Biol Rep. 2014;41:6845–53.PubMedCrossRef
115.
Toldo S, Das A, Mezzaroma E, Chau VQ, Marchetti C, Durrant D, Samidurai A, Van Tassell BW, Yin C, Ockaili RA, et al. Induction of microRNA-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice. Circ Cardiovasc Genet. 2014;7:311–20.PubMedPubMedCentralCrossRef
116.
Chen Z, Zhang Z, Zhang D, Li H, Sun Z. Hydrogen sulfide protects against TNF-α induced neuronal cell apoptosis through miR-485-5p/TRADD signaling. Biochem Biophys Res Commun. 2016;478:1304–9.PubMedCrossRef
117.
Zhou X, An G, Chen J. Hydrogen sulfide improves left ventricular function in smoking rats via regulation of apoptosis and autophagy. Apoptosis. 2014;19:998–1005.PubMedCrossRef
118.
Guo C, Liang F, Shah Masood W, Yan X. Hydrogen sulfide protected gastric epithelial cell from ischemia/reperfusion injury by Keap1 s-sulfhydration, MAPK dependent anti-apoptosis and NF-κB dependent anti-inflammation pathway. Eur J Pharmacol. 2014;725:70–8.PubMedCrossRef
119.
Kuo WW, Wang WJ, Tsai CY, Way CL, Hsu HH, Chen LM. Diallyl trisufide (DATS) suppresses high glucose-induced cardiomyocyte apoptosis by inhibiting JNK/NFκB signaling via attenuating ROS generation. Int J Cardiol. 2013;168:270–80.PubMedCrossRef
120.
Cheng Z, Garikipati VN, Nickoloff E, Wang C, Polhemus DJ, Zhou J, Benedict C, Khan M, Verma SK, Rabinowitz JE, et al. Restoration of hydrogen sulfide production in diabetic mice improves reparative function of bone marrow cells. Circulation. 2016;134:1467–83.PubMedPubMedCentralCrossRef
121.
Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, Darley-Usmar VM, Doeller JE, Kraus DW. Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci USA. 2007;104:17977–82.PubMedCrossRef
122.
Hancock HM, Stannard A, Burkhardt GE, Williams K, Dixon P, Cowart J, Spencer J, Rasmussen TE. Hemorrhagic shock worsens neuromuscular recovery in a porcine model of hind limb vascular injury and ischemia-reperfusion. J Vasc Surg. 2011;53:1052–62 (discussion 1062).PubMedCrossRef
123.
Villamaria CY, Fries CA, Spencer JR, Roth M, Davis MR. Hydrogen sulfide mitigates reperfusion injury in a porcine model of vascularized composite autotransplantation. Ann Plast Surg. 2014;72:594–8.PubMedCrossRef
124.
Wilson HM, Welikson RE, Luo J, Kean TJ, Cao B, Dennis JE, Allen MD. Can cytoprotective cobalt protoporphyrin protect skeletal muscle and muscle-derived stem cells from ischemic injury? Clin Orthop Relat Res. 2015;473:2908–19.PubMedPubMedCentralCrossRef
125.
Knapp J, Heinzmann A, Schneider A, Padosch SA, Böttiger BW, Teschendorf P, Popp E. Hypothermia and neuroprotection by sulfide after cardiac arrest and cardiopulmonary resuscitation. Resuscitation. 2011;82:1076–80.PubMedCrossRef
126.
Dai HB, Ji X, Zhu SH, Hu YM, Zhang LD, Miao XL, Ma RM, Duan ML, Li WY. Hydrogen sulphide and mild hypothermia activate the CREB signaling pathway and prevent ischemia-reperfusion injury. BMC Anesthesiol. 2015;15:119.PubMedPubMedCentralCrossRef
Metadata
Title
Mechanisms by which hydrogen sulfide attenuates muscle function following ischemia–reperfusion injury: effects on Akt signaling, mitochondrial function, and apoptosis
Authors
Michael D. Wetzel
Joseph C. Wenke
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-018-1753-7

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