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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Oxidative Stress and Pathways of Molecular Hydrogen Effects in Medicine

Author(s): Jan Slezak*, Branislav Kura, Tyler W. LeBaron, Pawan K. Singal, Jozef Buday and Miroslav Barancik

Volume 27, Issue 5, 2021

Published on: 21 August, 2020

Page: [610 - 625] Pages: 16

DOI: 10.2174/1381612826666200821114016

Price: $65

Abstract

There are many situations of excessive production of reactive oxygen species (ROS) such as radiation, ischemia/reperfusion (I/R), and inflammation. ROS contribute to and arises from numerous cellular pathologies, diseases, and aging. ROS can cause direct deleterious effects by damaging proteins, lipids, and nucleic acids as well as exert detrimental effects on several cell signaling pathways. However, ROS are important in many cellular functions. The injurious effect of excessive ROS can hypothetically be mitigated by exogenous antioxidants, but clinically this intervention is often not favorable. In contrast, molecular hydrogen provides a variety of advantages for mitigating oxidative stress due to its unique physical and chemical properties. H2 may be superior to conventional antioxidants, since it can selectively reduce ●OH radicals while preserving important ROS that are otherwise used for normal cellular signaling. Additionally, H2 exerts many biological effects, including antioxidation, anti-inflammation, anti-apoptosis, and anti-shock. H2 accomplishes these effects by indirectly regulating signal transduction and gene expression, each of which involves multiple signaling pathways and crosstalk. The Keap1-Nrf2-ARE signaling pathway, which can be activated by H2, plays a critical role in regulating cellular redox balance, metabolism, and inducing adaptive responses against cellular stress. H2 also influences the crosstalk among the regulatory mechanisms of autophagy and apoptosis, which involve MAPKs, p53, Nrf2, NF-κB, p38 MAPK, mTOR, etc. The pleiotropic effects of molecular hydrogen on various proteins, molecules and signaling pathways can at least partly explain its almost universal pluripotent therapeutic potential.

Keywords: Oxidative stress, molecular hydrogen, Nrf2, inflammation, autophagy, MAPKs.

[1]
Grassi D, Desideri G, Ferri C. Flavonoids: antioxidants against atherosclerosis. Nutrients 2010; 2(8): 889-902.
[http://dx.doi.org/10.3390/nu2080889] [PMID: 22254061]
[2]
Zhang J, Wang X, Vikash V, et al. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev 2016; 2016; 2016: 4350965
[3]
Altemeier WA, Sinclair SE. Hyperoxia in the intensive care unit: why more is not always better. Curr Opin Crit Care 2007; 13(1): 73-8.
[http://dx.doi.org/10.1097/MCC.0b013e32801162cb] [PMID: 17198052]
[4]
Lee PJ, Choi AMK. Pathways of cell signaling in hyperoxia. Free Radic Biol Med 2003; 35(4): 341-50.
[http://dx.doi.org/10.1016/S0891-5849(03)00279-X] [PMID: 12899937]
[5]
Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 2010; 49(11): 1603-16.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.09.006] [PMID: 20840865]
[6]
Singal PK, Khaper N, Palace V, Kumar D. Cardiovascular Conundra Series Series Editor: The role of oxidative stress in the genesis of heart disease. Cardiovasc Res 1998; 40: 426-32. Available from: https://academic.oup.com/cardiovascres/article-abstract/40/3/426/274656
[7]
Ludke A, Sharma AK, Bagchi AK, Singal PK. Subcellular basis of vitamin C protection against doxorubicin-induced changes in rat cardiomyocytes. Mol Cell Biochem 2012; 360(1-2): 215-24.
[http://dx.doi.org/10.1007/s11010-011-1059-z] [PMID: 21938406]
[8]
Majzunova M, Dovinova I, Barancik M, Chan JYH. Redox signaling in pathophysiology of hypertension. J Biomed Sci 2013; 20(1): 69.
[http://dx.doi.org/10.1186/1423-0127-20-69] [PMID: 24047403]
[9]
Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010; 45(7-8): 466-72.
[http://dx.doi.org/10.1016/j.exger.2010.01.003] [PMID: 20064600]
[10]
Roberge S, Roussel J, Andersson DC, et al. TNF-α-mediated caspase-8 activation induces ROS production and TRPM2 activation in adult ventricular myocytes. Cardiovasc Res 2014; 103(1): 90-9.
[http://dx.doi.org/10.1093/cvr/cvu112] [PMID: 24802330]
[11]
Ilatovskaya DV, Pavlov TS, Levchenko V, Staruschenko A. ROS production as a common mechanism of ENaC regulation by EGF, insulin, and IGF-1. Am J Physiol Cell Physiol 2013; 304(1): C102-11.
[http://dx.doi.org/10.1152/ajpcell.00231.2012] [PMID: 23135700]
[12]
Clauzure M, Valdivieso AG, Massip Copiz MM, Schulman G, Teiber ML, Santa-Coloma TA. Disruption of interleukin-1β autocrine signaling rescues complex I activity and improves ROS levels in immortalized epithelial cells with impaired cystic fibrosis transmembrane conductance regulator (CFTR) function. PLoS One 2014; 9(6)e99257
[http://dx.doi.org/10.1371/journal.pone.0099257] [PMID: 24901709]
[13]
Large M, Reichert S, Hehlgans S, Fournier C, Rödel C, Rödel F. A non-linear detection of phospho-histone H2AX in EA.hy926 endothelial cells following low-dose X-irradiation is modulated by reactive oxygen species. Radiat Oncol 2014; 9(1): 80.
[http://dx.doi.org/10.1186/1748-717X-9-80] [PMID: 24655916]
[14]
Noda M, Fujita K, Lee C-H, Yoshioka T. The principle and the potential approach to ROS-dependent cytotoxicity by non-pharmaceutical therapies: optimal use of medical gases with antioxidant properties. Curr Pharm Des 2011; 17(22): 2253-63.
[http://dx.doi.org/10.2174/138161211797052600] [PMID: 21736540]
[15]
Kajimura M, Nakanishi T, Takenouchi T, et al. Gas biology: tiny molecules controlling metabolic systems. Respir Physiol Neurobiol 2012; 184(2): 139-48.
[http://dx.doi.org/10.1016/j.resp.2012.03.016] [PMID: 22516267]
[16]
Watanabe S, Fujita M, Ishihara M, et al. Protective effect of inhalation of hydrogen gas on radiation-induced dermatitis and skin injury in rats. J Radiat Res (Tokyo) 2014; 55(6): 1107-13.
[http://dx.doi.org/10.1093/jrr/rru067] [PMID: 25034733]
[17]
Herrera BS, Coimbra LS, da Silva AR, et al. The H2S-releasing naproxen derivative, ATB-346, inhibits alveolar bone loss and inflammation in rats with ligature-induced periodontitis. Med Gas Res 2015; 5(1): 4.
[http://dx.doi.org/10.1186/s13618-015-0025-3] [PMID: 25755876]
[18]
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.
[http://dx.doi.org/10.1186/s13618-015-0027-1] [PMID: 25918638]
[19]
Duan FF, Guo Y, Li JW, Yuan K. Antifatigue effect of luteolin-6-c-neohesperidoside on oxidative stress injury induced by forced swimming of rats through modulation of Nrf2/ARE signaling pathways. Oxid Med Cell Longev 2017; 20173159358
[20]
Shanmugam G, Narasimhan M, Conley RL, et al. Chronic endurance exercise impairs cardiac structure and function in middle-aged mice with impaired Nrf2 signaling. Front Physiol 2017; 8(MAY): 268.
[http://dx.doi.org/10.3389/fphys.2017.00268] [PMID: 28515695]
[21]
Chung E, Joiner HE, Skelton T, Looten KD, Manczak M, Reddy PH. Maternal exercise upregulates mitochondrial gene expression and increases enzyme activity of fetal mouse hearts. Physiol Rep 2017; 5(5)e13184
[http://dx.doi.org/10.14814/phy2.13184] [PMID: 28292876]
[22]
Bischoff LJM, Kuijper IA, Schimming JP, et al. A systematic analysis of Nrf2 pathway activation dynamics during repeated xenobiotic exposure. Arch Toxicol 2019; 93(2): 435-51.
[http://dx.doi.org/10.1007/s00204-018-2353-2] [PMID: 30456486]
[23]
Hoetzenecker W, Echtenacher B, Guenova E, et al. ROS-induced ATF3 causes susceptibility to secondary infections during sepsis-associated immunosuppression. Nat Med 2011; 18(1): 128-34.
[http://dx.doi.org/10.1038/nm.2557] [PMID: 22179317]
[24]
Lubos E, Loscalzo J, Handy DE. Glutathione peroxidase-1 in health and disease: From molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2011; 15: 1957-97.
[25]
Handy DE, Loscalzo J. Responses to reductive stress in the cardiovascular system Free Radical Biology and Medicine In Elsevier Inc 2017; 114-24.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.12.006]
[26]
Mahadev K, Motoshima H, Wu X, et al. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol 2004; 24(5): 1844-54.
[http://dx.doi.org/10.1128/MCB.24.5.1844-1854.2004] [PMID: 14966267]
[27]
Csala M, Kardon T, Legeza B, et al. On the role of 4-hydroxynonenal in health and diseaseVol 1852, Biochimica et Biophysica Acta - Molecular Basis of Disease. Elsevier 2015; pp. 826-38.
[28]
Endo J, Sano M, Katayama T, et al. Metabolic remodeling induced by mitochondrial aldehyde stress stimulates tolerance to oxidative stress in the heart. Circ Res 2009; 105(11): 1118-27.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.206607] [PMID: 19815821]
[29]
Ahmad A, Sattar MZA, Rathore HA, et al. Antioxidant activity and free radical scavenging capacity of L-arginine and NaHS: A comparative in vitro study. Acta Pol Pharm 2015; 72(2): 245-52.
[PMID: 26642674]
[30]
Lemasters JJ, Qian T, He L, et al. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal 2002; 4(5): 769-81.
[http://dx.doi.org/10.1089/152308602760598918] [PMID: 12470504]
[31]
Zaoualí MA, Reiter RJ, Padrissa-Altés S, et al. Melatonin protects steatotic and nonsteatotic liver grafts against cold ischemia and reperfusion injury. J Pineal Res 2011; 50(2): 213-21.
[PMID: 21108657]
[32]
Abu-Amara M, Gurusamy KS, Hori S, Glantzounis G, Fuller B, Davidson BR. Pharmacological interventions versus no pharmacological intervention for ischaemia reperfusion injury in liver resection surgery performed under vascular control. Cochrane Database Syst Rev 2009; (4): CD007472
[http://dx.doi.org/10.1002/14651858.CD007472.pub2] [PMID: 19821421]
[33]
Álvarez-Ayuso L, Gómez-Heras SG, Jorge E, et al. Vitamin E action on oxidative state, endothelial function and morphology in long-term myocardial preservation. Histol Histopathol 2010; 25(5): 577-87.
[PMID: 20238296]
[34]
Miller ER III, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E. Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 2005; 142(1): 37-46. Available from: https://annals.org
[http://dx.doi.org/10.7326/0003-4819-142-1-200501040-00110] [PMID: 15537682]
[35]
LeBaron TW, Laher I, Kura B, Slezak J. Hydrogen gas: from clinical medicine to an emerging ergogenic molecule for sports athletes. Can J Physiol Pharmacol 2019; 97(9): 797-807.
[http://dx.doi.org/10.1139/cjpp-2019-0067] [PMID: 30970215]
[36]
Barancik M, Okruhlicova L, Fogarassyova M, Bartekova M, Slezak J. Mediastinal irradiation modulates myocardial and circulating matrix metalloproteinases. Exp Clin Cardiol 2013; 18: 37A-40.
[37]
Ohsawa I, Ishikawa M, Takahashi K, et al. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 2007; 13(6): 688-94.
[http://dx.doi.org/10.1038/nm1577] [PMID: 17486089]
[38]
Huang CS, Kawamura T, Toyoda Y, Nakao A. Recent advances in hydrogen research as a therapeutic medical gas. Free Radic Res 2010; 44(9): 971-82.
[http://dx.doi.org/10.3109/10715762.2010.500328] [PMID: 20815764]
[39]
Ohta S. Recent progress toward hydrogen medicine: potential of molecular hydrogen for preventive and therapeutic applications. Curr Pharm Des 2011; 17(22): 2241-52.
[http://dx.doi.org/10.2174/138161211797052664] [PMID: 21736547]
[40]
Dixon BJ, Tang J, Zhang JH. The evolution of molecular hydrogen: a noteworthy potential therapy with clinical significance. Med Gas Res 2013; 3(1): 10.
[http://dx.doi.org/10.1186/2045-9912-3-10] [PMID: 23680032]
[41]
Qiu P, Liu Y, Zhang J. Recent advances in studies of molecular hydrogen against sepsis. Int J Biol Sci 2019; 1261-75.
[http://dx.doi.org/10.7150/ijbs.30741]
[42]
LeBaron TW, Singh RB, Fatima G, et al. The effects of 24-week, high-concentration hydrogen-rich water on body composition, blood lipid profiles and inflammation biomarkers in men and women with metabolic syndrome: a randomized controlled trial. Diabetes Metab Syndr Obes 2020; 13: 889-96.
[http://dx.doi.org/10.2147/DMSO.S240122] [PMID: 32273740]
[43]
Pinsky DJ, Naka Y, Chowdhury NC, et al. The nitric oxide/cyclic GMP pathway in organ transplantation: critical role in successful lung preservation. Proc Natl Acad Sci USA 1994; 91(25): 12086-90.
[http://dx.doi.org/10.1073/pnas.91.25.12086] [PMID: 7527550]
[44]
Nakao A, Kaczorowski DJ, Wang Y, et al. Amelioration of rat cardiac cold ischemia/reperfusion injury with inhaled hydrogen or carbon monoxide, or both. J Heart Lung Transplant 2010; 29(5): 544-53.
[http://dx.doi.org/10.1016/j.healun.2009.10.011] [PMID: 20036162]
[45]
Gharib B, Hanna S, Abdallahi OM, Lepidi H, Gardette B, De Reggi M. Anti-inflammatory properties of molecular hydrogen: investigation on parasite-induced liver inflammation. C R Acad Sci III 2001; 324(8): 719-24.
[http://dx.doi.org/10.1016/S0764-4469(01)01350-6] [PMID: 11510417]
[46]
Ramachandran A, Madesh M, Balasubramanian KA. Apoptosis in the intestinal epithelium: its relevance in normal and pathophysiological conditions. J Gastroenterol Hepatol 2000; 15(2): 109-20.
[http://dx.doi.org/10.1046/j.1440-1746.2000.02059.x] [PMID: 10735533]
[47]
Qian L, Cao F, Cui J, et al. Radioprotective effect of hydrogen in cultured cells and mice. Free Radic Res 2010; 44(3): 275-82.
[http://dx.doi.org/10.3109/10715760903468758] [PMID: 20166892]
[48]
Vijayalaxmi, Reiter RJ, Tan DX, Herman TS, Thomas CR Jr. Melatonin as a radioprotective agent: a review. Int J Radiat Oncol Biol Phys 2004; 59(3): 639-53.
[http://dx.doi.org/10.1016/j.ijrobp.2004.02.006] [PMID: 15183467]
[49]
Slezak J, Surovy J, Buday J, Kura B. Molecular hydrogen as a novel therapeutic tool in situations of increased production of free radicals. Clin Oncol (R Coll Radiol) 2017; 2: 1367.
[50]
Qin Z xue, Yu P, Qian D hui, et al. Hydrogen-rich saline prevents neointima formation after carotid balloon injury by suppressing ROS and the TNF-α/NF-κB pathway Atherosclerosis 2012; 220(2): 343-50.
[51]
Wang C, Li J, Liu Q, et al. Hydrogen-rich saline reduces oxidative stress and inflammation by inhibit of JNK and NF-κB activation in a rat model of amyloid-beta-induced Alzheimer’s disease. Neurosci Lett 2011; 491(2): 127-32.
[http://dx.doi.org/10.1016/j.neulet.2011.01.022] [PMID: 21238541]
[52]
Huang CS, Kawamura T, Peng X, et al. Hydrogen inhalation reduced epithelial apoptosis in ventilator-induced lung injury via a mechanism involving nuclear factor-kappa B activation. Biochem Biophys Res Commun 2011; 408(2): 253-8.
[http://dx.doi.org/10.1016/j.bbrc.2011.04.008] [PMID: 21473852]
[53]
Fan M, Xu X, He X, et al. Protective effects of hydrogen-rich saline against erectile dysfunction in a streptozotocin induced diabetic rat model. J Urol 2013; 190(1): 350-6.
[http://dx.doi.org/10.1016/j.juro.2012.12.001] [PMID: 23220246]
[54]
Chen Y, Jiang J, Miao H, Chen X, Sun X, Li Y. Hydrogen-rich saline attenuates vascular smooth muscle cell proliferation and neointimal hyperplasia by inhibiting reactive oxygen species production and inactivating the Ras-ERK1/2-MEK1/2 and Akt pathways. Int J Mol Med 2013; 31(3): 597-606.
[http://dx.doi.org/10.3892/ijmm.2013.1256] [PMID: 23340693]
[55]
Sun Q, Kang Z, Cai J, et al. Hydrogen-rich saline protects myocardium against ischemia/reperfusion injury in rats. Exp Biol Med (Maywood) 2009; 234(10): 1212-9.
[http://dx.doi.org/10.3181/0812-RM-349] [PMID: 19596825]
[56]
Ohta S. Molecular hydrogen as a novel antioxidant: Overview of the advantages of hydrogen for medical applicationsMethods in Enzymology. 1st ed. Elsevier Inc. In: 2015; 555: pp. 289-317.
[57]
Soltés L, Brezová V, Stankovská M, Kogan G, Gemeiner P. Degradation of high-molecular-weight hyaluronan by hydrogen peroxide in the presence of cupric ions. Carbohydr Res 2006; 341(5): 639-44.
[http://dx.doi.org/10.1016/j.carres.2006.01.014] [PMID: 16445893]
[58]
Kura B, Bagchi AK, Singal PK, et al. Molecular hydrogen: Potential in mitigating oxidative-stress-induced radiation injury. Can J Physiol Pharmacol 2019; 287-92.
[59]
LeBaron TW, Kura B, Kalocayova B, Tribulova N, Slezak J. A new approach for the prevention and treatment of cardiovascular disorders. Molecular hydrogen significantly reduces the effects of oxidative stress. Molecules 2019; 24(11)E2076
[http://dx.doi.org/10.3390/molecules24112076] [PMID: 31159153]
[60]
Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007; 87(1): 315-424.
[http://dx.doi.org/10.1152/physrev.00029.2006] [PMID: 17237348]
[61]
Cai WW, Zhang MH, Yu YS, Cai JH. Treatment with hydrogen molecule alleviates TNFα-induced cell injury in osteoblast. Mol Cell Biochem 2013; 373(1-2): 1-9.
[http://dx.doi.org/10.1007/s11010-012-1450-4] [PMID: 23212446]
[62]
Shinbo T, Kokubo K, Sato Y, et al. Breathing nitric oxide plus hydrogen gas reduces ischemia-reperfusion injury and nitrotyrosine production in murine heart. Am J Physiol Heart Circ Physiol 2013; 305(4): H542-50.
[http://dx.doi.org/10.1152/ajpheart.00844.2012] [PMID: 23771690]
[63]
Itoh T, Hamada N, Terazawa R, et al. Molecular hydrogen inhibits lipopolysaccharide/interferon γ-induced nitric oxide production through modulation of signal transduction in macrophages. Biochem Biophys Res Commun 2011; 411(1): 143-9.
[http://dx.doi.org/10.1016/j.bbrc.2011.06.116] [PMID: 21723254]
[64]
Zheng H, Yu YS. Chronic hydrogen-rich saline treatment attenuates vascular dysfunction in spontaneous hypertensive rats. Biochem Pharmacol 2012; 83(9): 1269-77.
[http://dx.doi.org/10.1016/j.bcp.2012.01.031] [PMID: 22342731]
[65]
Liang C, Liu X, Liu L, He D. Effect of hydrogen inhalation on p38 MAPK activation in rats with lipopolysaccharide- induced acute lung injury. Nan Fang Yi Ke Da Xue Xue Bao 2012; 32(8): 1211-3.
[PMID: 22931625]
[66]
Xie K, Liu L, Yu Y, Wang G. Hydrogen gas presents a promising therapeutic strategy for sepsis Biomed Res Int 2014; 2014: 2014.807635
[http://dx.doi.org/10.1155/2014/807635]
[67]
Qiu X, Li H, Tang H, et al. Hydrogen inhalation ameliorates lipopolysaccharide-induced acute lung injury in mice. Int Immunopharmacol 2011; 11(12): 2130-7.
[http://dx.doi.org/10.1016/j.intimp.2011.09.007] [PMID: 22015602]
[68]
Ge L, Yang M, Yang N-N, Yin X-X, Song W-G. Molecular hydrogen: a preventive and therapeutic medical gas for various diseases. Oncotarget 2017; 8(60): 102653-73. Available from: www.impactjournals.com/oncotarget%0Awww.impactjournals.com/oncotarget/
[http://dx.doi.org/10.18632/oncotarget.21130] [PMID: 29254278]
[69]
Okamoto A, Kohama K, Aoyama-Ishikawa M, et al. Intraperitoneally administered, hydrogen-rich physiologic solution protects against postoperative ileus and is associated with reduced nitric oxide production. Surgery 2016; 160(3): 623-31.
[http://dx.doi.org/10.1016/j.surg.2016.05.026] [PMID: 27425040]
[70]
Qi LS, Yao L, Liu W, et al. Sirtuin type 1 mediates the retinal protective effect of hydrogen-rich saline against light-induced damage in rats. Invest Ophthalmol Vis Sci 2015; 56(13): 8268-79.
[http://dx.doi.org/10.1167/iovs.15-17034] [PMID: 26720481]
[71]
Fernández-Gajardo R, Matamala JM, Carrasco R, Gutiérrez R, Melo R, Rodrigo R. Novel therapeutic strategies for traumatic brain injury: acute antioxidant reinforcement. CNS Drugs 2014; 28(3): 229-48.
[http://dx.doi.org/10.1007/s40263-013-0138-y] [PMID: 24532027]
[72]
Nakao A, Toyoda Y, Sharma P, Evans M, Guthrie N. Effectiveness of hydrogen rich water on antioxidant status of subjects with potential metabolic syndrome-an open label pilot study. J Clin Biochem Nutr 2010; 46(2): 140-9.
[http://dx.doi.org/10.3164/jcbn.09-100] [PMID: 20216947]
[73]
Ohta S. Molecular hydrogen as a preventive and therapeutic medical gas: initiation, development and potential of hydrogen medicine. Pharmacol Ther 2014; 144(1): 1-11.
[http://dx.doi.org/10.1016/j.pharmthera.2014.04.006] [PMID: 24769081]
[74]
Slezák J, Kura B, Frimmel K, et al. Preventive and therapeutic application of molecular hydrogen in situations with excessive production of free radicals. Physiol Res 2016; 65(Suppl. 1): S11-28.
[http://dx.doi.org/10.33549/physiolres.933414] [PMID: 27643933]
[75]
Slezak J, Kura B, Babal P, et al. Potential markers and metabolic processes involved in the mechanism of radiation-induced heart injury. Can J Physiol Pharmacol 2017; 95(10): 1190-203.
[http://dx.doi.org/10.1139/cjpp-2017-0121] [PMID: 28750189]
[76]
Kura B, Babal P, Slezak J. Implication of microRNAs in the development and potential treatment of radiation-induced heart disease. Can J Physiol Pharmacol 2017; 95(10): 1236-44.
[http://dx.doi.org/10.1139/cjpp-2016-0741] [PMID: 28679064]
[77]
Hirayama M, Ito M, Minato T, Yoritaka A, LeBaron TW, Ohno K. Inhalation of hydrogen gas elevates urinary 8-hydroxy-2′-deoxyguanine in Parkinson’s disease. Med Gas Res 2019; 8(4): 144-9.
[PMID: 30713666]
[78]
Bellezza I, Giambanco I, Minelli A, Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochimica et Biophysica Acta - Molecular Cell Research. Elsevier B 2018; 1865: 721-33.
[79]
Yang L, Palliyaguru DL, Kensler TW. Frugal chemoprevention: targeting Nrf2 with foods rich in sulforaphane. Semin Oncol 2016; 43(1): 146-53.
[http://dx.doi.org/10.1053/j.seminoncol.2015.09.013] [PMID: 26970133]
[80]
Hahn ME, Timme-Laragy AR, Karchner SI, Stegeman JJ. Nrf2 and Nrf2-related proteins in development and developmental toxicity: Insights from studies in zebrafish (Danio rerio) Free Radical Biology and Medicine. Elsevier Inc. 2015; pp. 275-89.
[81]
Fuse Y, Kobayashi M. Conservation of the Keap1-Nrf2 system: An evolutionary journey through stressful space and time. Molecules 2017; 22(3): 436.
[http://dx.doi.org/10.3390/molecules22030436] [PMID: 28282941]
[82]
Rojo de la Vega M, Chapman E, Zhang DD. NRF2 and the Hallmarks of Cancer. Cancer Cell 2018; 34(1): 21-43.
[http://dx.doi.org/10.1016/j.ccell.2018.03.022] [PMID: 29731393]
[83]
McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD. Redox-regulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive Neh2 degron and the redox-insensitive Neh6 degron. J Biol Chem 2004; 279(30): 31556-67.
[http://dx.doi.org/10.1074/jbc.M403061200] [PMID: 15143058]
[84]
Villeneuve NF, Lau A, Zhang DD. Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid Redox Signal 2010; 13(11): 1699-712. Available from: www.liebertonline.com
[http://dx.doi.org/10.1089/ars.2010.3211] [PMID: 20486766]
[85]
Hayes JD, McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 2009; 34(4): 176-88.
[http://dx.doi.org/10.1016/j.tibs.2008.12.008] [PMID: 19321346]
[86]
Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011; 16(2): 123-40.
[http://dx.doi.org/10.1111/j.1365-2443.2010.01473.x] [PMID: 21251164]
[87]
Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007; 47(1): 89-116.
[http://dx.doi.org/10.1146/annurev.pharmtox.46.120604.141046] [PMID: 16968214]
[88]
Lee J-M, Johnson JA. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 2004; 37(2): 139-43.
[PMID: 15469687]
[89]
Jung KA, Kwak MK. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010; 15(10): 7266-91.
[http://dx.doi.org/10.3390/molecules15107266] [PMID: 20966874]
[90]
Kim KC, Kang KA, Zhang R, et al. Up-regulation of Nrf2-mediated heme oxygenase-1 expression by eckol, a phlorotannin compound, through activation of Erk and PI3K/Akt. Int J Biochem Cell Biol 2010; 42(2): 297-305.
[http://dx.doi.org/10.1016/j.biocel.2009.11.009] [PMID: 19931411]
[91]
Kaspar JW, Niture SK, Jaiswal AK. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009; 47(9): 1304-9.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.07.035] [PMID: 19666107]
[92]
Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 2003; 43(1): 233-60.
[http://dx.doi.org/10.1146/annurev.pharmtox.43.100901.140229] [PMID: 12359864]
[93]
Jain AK, Jaiswal AK. GSK-3β acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 2007; 282(22): 16502-10.
[http://dx.doi.org/10.1074/jbc.M611336200] [PMID: 17403689]
[94]
Kansanen E, Kuosmanen SM, Leinonen H, Levonen AL. The Keap1-Nrf2 pathway: Mechanisms of activation and dysregulation in cancer. Redox Biol 2013; 1(1): 45-9.
[http://dx.doi.org/10.1016/j.redox.2012.10.001] [PMID: 24024136]
[95]
Strom J, Xu B, Tian X, Chen QM. Nrf2 protects mitochondrial decay by oxidative stress. FASEB J 2016; 30(1): 66-80.
[http://dx.doi.org/10.1096/fj.14-268904] [PMID: 26340923]
[96]
Bellezza I, Tucci A, Galli F, et al. Inhibition of NF-κB nuclear translocation via HO-1 activation underlies α-tocopheryl succinate toxicity. J Nutr Biochem 2012; 23(12): 1583-91.
[http://dx.doi.org/10.1016/j.jnutbio.2011.10.012] [PMID: 22444871]
[97]
Bellezza I, Grottelli S, Mierla AL, et al. Neuroinflammation and endoplasmic reticulum stress are coregulated by cyclo(His-Pro) to prevent LPS neurotoxicity. Int J Biochem Cell Biol 2014; 51(1): 159-69.
[http://dx.doi.org/10.1016/j.biocel.2014.03.023] [PMID: 24699213]
[98]
Jakobs P, Serbulea V, Leitinger N, Eckers A, Haendeler J. Nuclear factor (erythroid-derived 2)-like 2 and thioredoxin-1 in atherosclerosis and ischemia/reperfusion injury in the heart. Antioxid Redox Signal 2017; 26(12): 630-44.
[http://dx.doi.org/10.1089/ars.2016.6795] [PMID: 27923281]
[99]
Piantadosi CA, Carraway MS, Babiker A, Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 2008; 103(11): 1232-40.
[http://dx.doi.org/10.1161/01.RES.0000338597.71702.ad] [PMID: 18845810]
[100]
Brewer AC, Murray TVA, Arno M, et al. Nox4 regulates Nrf2 and glutathione redox in cardiomyocytes in vivo. Free Radic Biol Med 2011; 51(1): 205-15.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.022] [PMID: 21554947]
[101]
Cuadrado A, Rojo AI, Wells G, et al. Therapeutic targeting of the NRF2 and KEAP1 partnership in chronic diseases. Nat Rev Drug Discov 2019; 18(4): 295-317.
[http://dx.doi.org/10.1038/s41573-018-0008-x] [PMID: 30610225]
[102]
Robledinos-Antón N, Fernández-Ginés R, Manda G, Cuadrado A. Activators and inhibitors of NRF2: A review of their potential for clinical development. Oxid Med Cell Longev 2019; 20199372182
[http://dx.doi.org/10.1155/2019/9372182] [PMID: 31396308]
[103]
Cominacini L, Mozzini C, Garbin U, et al. Endoplasmic reticulum stress and Nrf2 signaling in cardiovascular diseases Free Radic Biol Med 2015; 88(Pt B): 233-42.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.05.027]
[104]
Sandberg M, Patil J, D’Angelo B, Weber SG, Mallard C. NRF2-regulation in brain health and disease: Implication of cerebral inflammation. Neuropharmacology Elsevier Ltd 2014; 79: 298-306.
[105]
Wong MHL, Bryan HK, Copple IM, et al. Design and synthesis of irreversible analogues of bardoxolone methyl for the identification of pharmacologically relevant targets and interaction sites. J Med Chem 2016; 59(6): 2396-409.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01292] [PMID: 26908173]
[106]
Kansanen E, Bonacci G, Schopfer FJ, et al. Electrophilic nitro-fatty acids activate NRF2 by a KEAP1 cysteine 151-independent mechanism. J Biol Chem 2011; 286(16): 14019-27.
[http://dx.doi.org/10.1074/jbc.M110.190710] [PMID: 21357422]
[107]
Fourquet S, Guerois R, Biard D, Toledano MB. Activation of NRF2 by nitrosative agents and H2O2 involves KEAP1 disulfide formation. J Biol Chem 2010; 285(11): 8463-71.
[http://dx.doi.org/10.1074/jbc.M109.051714] [PMID: 20061377]
[108]
Kim JE, You DJ, Lee C, Ahn C, Seong JY, Hwang JI. Suppression of NF-kappaB signaling by KEAP1 regulation of IKKbeta activity through autophagic degradation and inhibition of phosphorylation. Cell Signal 2010; 22(11): 1645-54.
[http://dx.doi.org/10.1016/j.cellsig.2010.06.004] [PMID: 20600852]
[109]
Hara F, Tatebe J, Watanabe I, Yamazaki J, Ikeda T, Morita T. Molecular hydrogen alleviates cellular senescence in endothelial cells. Circ J 2016; 80(9): 2037-46.
[http://dx.doi.org/10.1253/circj.CJ-16-0227] [PMID: 27477846]
[110]
Kawamura T, Wakabayashi N, Shigemura N, et al. Hydrogen gas reduces hyperoxic lung injury via the Nrf2 pathway in vivo. Am J Physiol Lung Cell Mol Physiol 2013; 304(10): L646-56. Available from: www.ajplung.org
[http://dx.doi.org/10.1152/ajplung.00164.2012] [PMID: 23475767]
[111]
Kura B, Bagchi AK, Singal PK, et al. Molecular hydrogen: potential in mitigating oxidative-stress-induced radiation injury. Can J Physiol Pharmacol 2019; 97(4): 287-92.
[http://dx.doi.org/10.1139/cjpp-2018-0604] [PMID: 30543459]
[112]
Kajiyama S, Hasegawa G, Asano M, et al. Supplementation of hydrogen-rich water improves lipid and glucose metabolism in patients with type 2 diabetes or impaired glucose tolerance. Nutr Res 2008; 28(3): 137-43.
[http://dx.doi.org/10.1016/j.nutres.2008.01.008] [PMID: 19083400]
[113]
Xie K, Yu Y, Pei Y, et al. Protective effects of hydrogen gas on murine polymicrobial sepsis via reducing oxidative stress and HMGB1 release. Shock 2010; 34(1): 90-7.
[http://dx.doi.org/10.1097/SHK.0b013e3181cdc4ae] [PMID: 19997046]
[114]
Chen H, Xie K, Han H, et al. Molecular hydrogen protects mice against polymicrobial sepsis by ameliorating endothelial dysfunction via an Nrf2/HO-1 signaling pathway. Int Immunopharmacol 2015; 28(1): 643-54.
[http://dx.doi.org/10.1016/j.intimp.2015.07.034] [PMID: 26253656]
[115]
Zálešák M, Kura B, Graban J, Farkašová V, Slezák J, Ravingerová T. Molecular hydrogen potentiates beneficial anti-infarct effect of hypoxic postconditioning in isolated rat hearts: a novel cardioprotective intervention. Can J Physiol Pharmacol 2017; 95(8): 888-93.
[http://dx.doi.org/10.1139/cjpp-2016-0693] [PMID: 28350967]
[116]
Bellezza I, Grottelli S, Gatticchi L, Mierla AL, Minelli A. α-Tocopheryl succinate pre-treatment attenuates quinone toxicity in prostate cancer PC3 cells. Gene 2014; 539(1): 1-7.
[http://dx.doi.org/10.1016/j.gene.2014.02.009] [PMID: 24530478]
[117]
Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25(6): 280-8.
[http://dx.doi.org/10.1016/j.it.2004.03.008] [PMID: 15145317]
[118]
Li W, Khor TO, Xu C, et al. Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem Pharmacol 2008; 76(11): 1485-9.
[http://dx.doi.org/10.1016/j.bcp.2008.07.017] [PMID: 18694732]
[119]
Zhang J, Wu Q, Song S, et al. Effect of hydrogen-rich water on acute peritonitis of rat models. Int Immunopharmacol 2014; 21(1): 94-101.
[http://dx.doi.org/10.1016/j.intimp.2014.04.011] [PMID: 24793096]
[120]
Xie K, Yu Y, Huang Y, et al. Molecular hydrogen ameliorates lipopolysaccharide-induced acute lung injury in mice through reducing inflammation and apoptosis. Shock 2012; 37(5): 548-55.
[http://dx.doi.org/10.1097/SHK.0b013e31824ddc81] [PMID: 22508291]
[121]
Tanaka Y, Shigemura N, Kawamura T, et al. Profiling molecular changes induced by hydrogen treatment of lung allografts prior to procurement. Biochem Biophys Res Commun 2012; 425(4): 873-9.
[http://dx.doi.org/10.1016/j.bbrc.2012.08.005] [PMID: 22902635]
[122]
Jung M, Schaefer A, Steiner I, et al. Robust microRNA stability in degraded RNA preparations from human tissue and cell samples. Clin Chem 2010; 56(6): 998-1006.
[http://dx.doi.org/10.1373/clinchem.2009.141580] [PMID: 20378769]
[123]
Wei R, Zhang R, Xie Y, Shen L, Chen F. Hydrogen suppresses hypoxia/reoxygenation-induced cell death in hippocampal neurons through reducing oxidative stress. Cell Physiol Biochem 2015; 36(2): 585-98.
[http://dx.doi.org/10.1159/000430122] [PMID: 25997722]
[124]
Kura B, Kalocayova B, LeBaron TW, et al. Regulation of microRNAs by molecular hydrogen contributes to the prevention of radiation-induced damage in the rat myocardium. Mol Cell Biochem 2019; 457(1-2): 61-72.
[http://dx.doi.org/10.1007/s11010-019-03512-z]
[125]
Kura B, Yin C, Frimmel K, et al. Changes of microRNA-1, -15b and -21 levels in irradiated rat hearts after treatment with potentially radioprotective drugs. Physiol Res 2016; 65(Suppl. 1): S129-37.
[http://dx.doi.org/10.33549/physiolres.933399] [PMID: 27643935]
[126]
Liu G-D, Zhang H, Wang L, Han Q, Zhou S-F, Liu P. 2013; Molecular hydrogen regulates the expression of miR-9, miR-21 and miR-199 in LPS-activated retinal microglia cells.Int J Ophthalmol 2013; 6(3): 280-5. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3693006&tool=pmcentrez&rendertype=abstract.
[PMID: 23826519]
[127]
Itoh T, Fujita Y, Ito M, et al. Molecular hydrogen suppresses FcepsilonRI-mediated signal transduction and prevents degranulation of mast cells. Biochem Biophys Res Commun 2009; 389(4): 651-6.
[http://dx.doi.org/10.1016/j.bbrc.2009.09.047] [PMID: 19766097]
[128]
Gvozdjáková A, Kucharská J, Kura B, et al. A new insight into the molecular hydrogen effect on coenzyme Q and mitochondrial function of rats. Can J Physiol Pharmacol 2020; 98(1): 29-34.
[http://dx.doi.org/10.1139/cjpp-2019-0281] [PMID: 31536712]
[129]
Matsumoto A, Yamafuji M, Tachibana T, Nakabeppu Y, Noda M, Nakaya H. Oral ‘hydrogen water’ induces neuroprotective ghrelin secretion in mice. Sci Rep 2013; 3: 3273.
[http://dx.doi.org/10.1038/srep03273] [PMID: 24253616]
[130]
Martins AD, Sá R, Monteiro MP, et al. Ghrelin acts as energy status sensor of male reproduction by modulating Sertoli cells glycolytic metabolism and mitochondrial bioenergetics. Mol Cell Endocrinol 2016; 434: 199-209.
[http://dx.doi.org/10.1016/j.mce.2016.07.008] [PMID: 27392494]
[131]
Iio A, Ito M, Itoh T, et al. Molecular hydrogen attenuates fatty acid uptake and lipid accumulation through downregulating CD36 expression in HepG2 cells. Med Gas Res 2013; 3(1): 6.
[http://dx.doi.org/10.1186/2045-9912-3-6] [PMID: 23448206]
[132]
Sobue S, Inoue C, Hori F, Qiao S, Murate T, Ichihara M. Molecular hydrogen modulates gene expression via histone modification and induces the mitochondrial unfolded protein response. Biochem Biophys Res Commun 2017; 493(1): 318-24.
[http://dx.doi.org/10.1016/j.bbrc.2017.09.024] [PMID: 28890349]
[133]
Ichihara M, Sobue S, Ito M, Ito M, Hirayama M, Ohno K. Beneficial biological effects and the underlying mechanisms of molecular hydrogen - comprehensive review of 321 original articles. Med Gas Res 2015; 5(1): 12.
[http://dx.doi.org/10.1186/s13618-015-0035-1] [PMID: 26483953]
[134]
Tao B, Liu L, Wang N, Wang W, Jiang J, Zhang J. Effects of hydrogen-rich saline on aquaporin 1, 5 in septic rat lungs. J Surg Res 2016; 202(2): 291-8.
[http://dx.doi.org/10.1016/j.jss.2016.01.009] [PMID: 27229103]
[135]
Mao YF, Zheng XF, Cai JM, et al. Hydrogen-rich saline reduces lung injury induced by intestinal ischemia/reperfusion in rats. Biochem Biophys Res Commun 2009; 381(4): 602-5.
[http://dx.doi.org/10.1016/j.bbrc.2009.02.105] [PMID: 19249288]
[136]
Chen X-L, Zhang Q, Zhao R, Medford RM, Chen X. Superoxide, H2O2, and iron are required for TNF-alpha-induced MCP-1 gene expression in endothelial cells: role of Rac1 and NADPH oxidase Am J Physiol Hear Circ Physiol 2004; 286: 1001-7. Available from: www.ajpheart.org
[137]
Matei N, Camara R, Zhang JH. Emerging mechanisms and novel applications of hydrogen gas therapy. Med Gas Res 2018; 8(3): 98-102.
[http://dx.doi.org/10.4103/2045-9912.239959] [PMID: 30319764]
[138]
Hong Y, Shao A, Wang J, et al. Neuroprotective effect of hydrogen-rich saline against neurologic damage and apoptosis in early brain injury following subarachnoid hemorrhage: possible role of the Akt/GSK3β signaling pathway. PLoS One 2014; 9(4)e96212
[http://dx.doi.org/10.1371/journal.pone.0096212] [PMID: 24763696]
[139]
Chen K, Wang N, Diao Y, et al. Hydrogen-rich saline attenuates brain injury induced by cardiopulmonary bypass and inhibits microvascular endothelial cell apoptosis via the PI3K/Akt/GSK3β signaling pathway in rats. Cell Physiol Biochem 2017; 43(4): 1634-47.
[http://dx.doi.org/10.1159/000484024] [PMID: 29040978]
[140]
Yu H, Zhang H, Zhao W, et al. Gypenoside protects against myocardial ischemia-reperfusion injury by inhibiting cardiomyocytes apoptosis via inhibition of chop pathway and activation of pi3k/akt pathway in vivo and in vitro. Cell Physiol Biochem 2016; 39(1): 123-36.
[http://dx.doi.org/10.1159/000445611] [PMID: 27322831]
[141]
Endo H, Nito C, Kamada H, Yu F, Chan PH. Akt/GSK3β survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 2006; 37(8): 2140-6.
[http://dx.doi.org/10.1161/01.STR.0000229888.55078.72] [PMID: 16794215]
[142]
Teng L, Meng Q, Lu J, et al. Liquiritin modulates ERK and AKT/GSK 3β dependent pathways to protect against glutamate induced cell damage in differentiated PC12 cells. Mol Med Rep 2014; 10(2): 818-24.
[http://dx.doi.org/10.3892/mmr.2014.2289] [PMID: 24888902]
[143]
Tang Z, Hu B, Zang F, Wang J, Zhang X, Chen H. Nrf2 drives oxidative stress-induced autophagy in nucleus pulposus cells via a Keap1/Nrf2/p62 feedback loop to protect intervertebral disc from degeneration. Cell Death Dis 2019; 10(7): 510.
[http://dx.doi.org/10.1038/s41419-019-1701-3] [PMID: 31263165]
[144]
Pearson G, Robinson F, Beers Gibson T, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001; 22(2): 153-83. Available from:https://academic.oup.com/edrv/article-abstract/22/2/153/2423864
[PMID: 11294822]
[145]
Junttila MR, Li S-P, Westermarck J. Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J 2008; 22(4): 954-65.
[http://dx.doi.org/10.1096/fj.06-7859rev] [PMID: 18039929]
[146]
Pimienta G, Pascual J. Canonical and alternative MAPK signaling. Cell Cycle 2007; 6(21): 2628-32.
[http://dx.doi.org/10.4161/cc.6.21.4930] [PMID: 17957138]
[147]
Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001; 81(2): 807-69. Available from:http://physrev.physiology.org
[http://dx.doi.org/10.1152/physrev.2001.81.2.807] [PMID: 11274345]
[148]
Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 2001; 410(6824): 37-40. Available from:www.nature.com
[http://dx.doi.org/10.1038/35065000] [PMID: 11242034]
[149]
Tirumurugaan KG, Jude JA, Kang BN, Panettieri RA, Walseth TF, Kannan MS. TNF-alpha induced CD38 expression in human airway smooth muscle cells: role of MAP kinases and transcription factors NF-kappaB and AP-1. Am J Physiol Lung Cell Mol Physiol 2007; 292(6): L1385-95. Available from: www.ajplung.org
[http://dx.doi.org/10.1152/ajplung.00472.2006] [PMID: 17322278]
[150]
Mannning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298(5600): 1912-34.
[151]
Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 2011; 75(1): 50-83.
[http://dx.doi.org/10.1128/MMBR.00031-10] [PMID: 21372320]
[152]
Son Y, Cheong Y-K, Kim N-H, Chung H-T, Kang DG, Pae H-O. Mitogen-activated protein kinases and reactive oxygen species: How can ROS activate MAPK pathways? J Signal Transduct 2011; 2011792639
[http://dx.doi.org/10.1155/2011/792639] [PMID: 21637379]
[153]
Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 2000; 279: 1005-28.
[154]
Ping Z, Zhang LF, Cui YJ, et al. The protective effects of salidroside from exhaustive exercise-induced heart injury by enhancing the PGC-1 - NRF1/NRF2 pathway and mitochondrial respiratory function in rats. Oxid Med Cell Longev 2015.876825
[155]
Camera DM, Smiles WJ, Hawley JA. Exercise-induced skeletal muscle signaling pathways and human athletic performance. Free Radic Biol Med 2016; 98: 131-43.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.02.007] [PMID: 26876650]
[156]
Xu X-F, Zhang J. Saturated hydrogen saline attenuates endotoxin-induced acute liver dysfunction in rats. Physiol Res 2013; 62(4): 395-403. Available from: www.biomed.cas.cz/physiolres
[http://dx.doi.org/10.33549/physiolres.932515] [PMID: 23961899]
[157]
Shi Q, Chen C, Deng WH, et al. Hydrogen-rich saline attenuates acute hepatic injury in acute necrotizing pancreatitis by inhibiting inflammation and apoptosis, involving JNK and p38 mitogen-activated protein kinase-dependent Reactive Oxygen Species. Pancreas 2016; 45(10): 1424-31.
[http://dx.doi.org/10.1097/MPA.0000000000000678] [PMID: 27518466]
[158]
Han B, Zhou H, Jia G, et al. MAPKs and Hsc70 are critical to the protective effect of molecular hydrogen during the early phase of acute pancreatitis. FEBS J 2016; 283(4): 738-56.
[http://dx.doi.org/10.1111/febs.13629] [PMID: 26683671]
[159]
Obata T, Brown GE, Yaffe MB, Luce JM, Yaffe MB, Fink MP. MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit Care Med 2000; 28(4)(Suppl.): N67-77. Available from: http://journals.lww.com/ccmjournal
[http://dx.doi.org/10.1097/00003246-200004001-00008] [PMID: 10807318]
[160]
Crilly MJ, Tryon LD, Erlich AT, Hood DA. The role of Nrf2 in skeletal muscle contractile and mitochondrial function. J Appl Physiol 2016; 121(3): 730-40. Available from: http://www.jappl.org
[http://dx.doi.org/10.1152/japplphysiol.00042.2016] [PMID: 27471236]
[161]
Pavel M, Rubinsztein DC. Mammalian autophagy and the plasma membrane. FEBS J 2017; 284(5): 672-9.
[http://dx.doi.org/10.1111/febs.13931] [PMID: 27758042]
[162]
Zachari M, Ganley IG. The mammalian ULK1 complex and autophagy initiation. Essays Biochem 2017; 61(6): 585-96.
[http://dx.doi.org/10.1042/EBC20170021] [PMID: 29233870]
[163]
Mathew R, Khor S, Hackett SR, Rabinowitz JD, Perlman DH, White E. Functional role of autophagy-mediated proteome remodeling in cell survival signaling and innate immunity. Mol Cell 2014; 55(6): 916-30.
[http://dx.doi.org/10.1016/j.molcel.2014.07.019] [PMID: 25175026]
[164]
Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8(9): 741-52.
[http://dx.doi.org/10.1038/nrm2239] [PMID: 17717517]
[165]
Cadwell K. Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis. Nat Rev Immunol 2016; 16(11): 661-75.
[http://dx.doi.org/10.1038/nri.2016.100] [PMID: 27694913]
[166]
Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469(7330): 323-35.
[http://dx.doi.org/10.1038/nature09782] [PMID: 21248839]
[167]
Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013; 13(10): 722-37.
[http://dx.doi.org/10.1038/nri3532] [PMID: 24064518]
[168]
Wang H, Huo X, Chen H, et al. Hydrogen-Rich Saline Activated Autophagy via HIF-1 α Pathways in Neuropathic Pain Model Biomed Res Int 2018; 20184670834
[169]
Jiao J, Demontis F. Skeletal muscle autophagy and its role in sarcopenia and organismal aging. Current Opinion Pharmacol 2017, Elsevier Ltd 2017; 34: 1-6.
[http://dx.doi.org//10.1016/j.coph.2017.03.009]
[170]
Bjørkøy G, Lamark T, Johansen T. p62/SQSTM1: a missing link between protein aggregates and the autophagy machinery. Autophagy 2006; 2(2): 138-9.
[http://dx.doi.org/10.4161/auto.2.2.2405] [PMID: 16874037]
[171]
Kapuy O, Papp D, Vellai T, Bánhegyi G, Korcsmáros T. Systems-level feedbacks of NRF2 controlling autophagy upon oxidative stress response. Antioxidants 2018; 7(3): 39.
[http://dx.doi.org/10.3390/antiox7030039] [PMID: 29510589]
[172]
Wang Y, Zhang J, Huang ZH, et al. Isodeoxyelephantopin induces protective autophagy in lung cancer cells via Nrf2-p62-keap1 feedback loop. Cell Death Dis 2017; 8(6)e2876
[http://dx.doi.org/10.1038/cddis.2017.265] [PMID: 28617433]
[173]
García-Prat L, Martínez-Vicente M, Perdiguero E, et al. Autophagy maintains stemness by preventing senescence. Nature 2016; 529(7584): 37-42.
[http://dx.doi.org/10.1038/nature16187] [PMID: 26738589]
[174]
Dimozi A, Mavrogonatou E, Sklirou A, Kletsas D. Oxidative stress inhibits the proliferation, induces premature senescence and promotes a catabolic phenotype in human nucleus pulposus intervertebral disc cells. Eur Cell Mater 2015; 30: 89-102.
[http://dx.doi.org/10.22203/eCM.v030a07] [PMID: 26337541]
[175]
Bai X, Liu S, Yuan L, et al. Hydrogen-rich saline mediates neuroprotection through the regulation of endoplasmic reticulum stress and autophagy under hypoxia-ischemia neonatal brain injury in mice. Brain Res 2016; 1646: 410-7.
[http://dx.doi.org/10.1016/j.brainres.2016.06.020] [PMID: 27317636]
[176]
Pan Z, Zhao Y, Yu H, Liu D, Xu H. Effect of hydrogen-rich saline on cardiomyocyte autophagy during myocardial ischemia-reperfusion in aged rats. Zhonghua Yi Xue Za Zhi 2015; 95(25): 2022-6.
[PMID: 26710815]
[177]
Chen J, Zhang H, Hu J, et al. Hydrogen-rich saline alleviates kidney fibrosis following AKI and retains klotho expression. Front Pharmacol 2017; 8: 499.
[http://dx.doi.org/10.3389/fphar.2017.00499] [PMID: 28848432]
[178]
Zhang Y, Liu Y, et al. Effects of hydrogen-rich saline on rats with acute carbon monoxide poisoning. J Emerg Med 2013; 44(1): 107-15.
[http://dx.doi.org/10.1016/j.jemermed.2012.01.065] [PMID: 22897968]
[179]
Wang W, Tian L, Li Y, et al. Saturated hydrogen saline attenuates endotoxin-induced lung dysfunction. J Surg Res 2015; 198(1): 41-9.
[http://dx.doi.org/10.1016/j.jss.2015.04.055] [PMID: 26004495]
[180]
Guo SX, Fang Q, You CG, et al. Effects of hydrogen-rich saline on early acute kidney injury in severely burned rats by suppressing oxidative stress induced apoptosis and inflammation. J Transl Med 2015; 13(1): 183.
[http://dx.doi.org/10.1186/s12967-015-0548-3] [PMID: 26047940]
[181]
Du H, Sheng M, Wu L, et al. Hydrogen-rich saline attenuates acute kidney injury after liver transplantation via activating p53-mediated autophagy. Transplantation 2016; 100(3): 563-70.
[http://dx.doi.org/10.1097/TP.0000000000001052] [PMID: 26714124]
[182]
Kawamura T, Huang CS, Tochigi N, et al. Inhaled hydrogen gas therapy for prevention of lung transplant-induced ischemia reperfusion injury in rats. Transplantation 2010; 90(12): 1344-51.
[http://dx.doi.org/10.1097/TP.0b013e3181fe1357] [PMID: 21048533]
[183]
Tait SWG, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11(9): 621-32.
[http://dx.doi.org/10.1038/nrm2952] [PMID: 20683470]
[184]
Jiang H, Yu P, Qian DH, et al. Hydrogen-rich medium suppresses the generation of reactive oxygen species, elevates the Bcl-2/Bax ratio and inhibits advanced glycation end product-induced apoptosis. Int J Mol Med 2013; 31(6): 1381-7.
[http://dx.doi.org/10.3892/ijmm.2013.1334] [PMID: 23563626]
[185]
Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I. Bistability in apoptosis: roles of bax, bcl-2, and mitochondrial permeability transition pores. Biophys J 2006; 90(5): 1546-59.
[http://dx.doi.org/10.1529/biophysj.105.068122] [PMID: 16339882]

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