Breathing nitric oxide plus hydrogen gas reduces ischemia-reperfusion injury and nitrotyrosine production in murine heart

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 4, 2013, Pages

  Shinbo, Toshihiro ^a   Kokubo, Kenichi ^a   Sato, Yuri ^a   Hagiri, Shintaro ^b   Hataishi, Ryuji ^b   Hirose, Minoru ^a   Kobayashi, Hirosuke ^a  

^a KITASATO UNIVERSITY   (Japan)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Antioxidants; Hydrogen gas; Ischemia; Nitric oxide; Reperfusion injury

Indexed keywords

3 NITROTYROSINE; HYDROGEN; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING; CONTROLLED STUDY; DOSE RESPONSE; ECHOCARDIOGRAPHY; EXPIRED AIR; HEART FUNCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FUNCTION; IMMUNOHISTOCHEMISTRY; INHALATION; ISCHEMIC PRECONDITIONING; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY;

ANTIOXIDANTS; HYDROGEN GAS; ISCHEMIA; NITRIC OXIDE; REPERFUSION INJURY;

ADMINISTRATION, INHALATION; ALDEHYDES; ANIMALS; ANTIOXIDANTS; CARDIOTONIC AGENTS; DEOXYGUANOSINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; GASES; HYDROGEN; IMMUNOHISTOCHEMISTRY; INHALATION; MALE; MICE; MICE, INBRED C57BL; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NEUTROPHIL INFILTRATION; NITRIC OXIDE; OXIDATIVE STRESS; RECEPTORS, CELL SURFACE; TIME FACTORS; TYROSINE; VENTRICULAR FUNCTION, LEFT;

EID: 84881641404     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00844.2012     Document Type: Article

References (31)

1. American Institute of Aeronautics and Astronautics. Guide to Safety of Hydrogen, and Hydrogen Systems. Virginia, 2005.
2. Brown GC, Borutaite V. Nitric oxide and mitochondrial respiration in the heart. Cardiovasc Res 75: 283-290, 2007.
3. Brüne B, Lapetina EG. Activation of a cytosolic ADP-ribosyltransferase by nitric oxide-generating agents. J Biol Chem 264: 8455-8458, 1989.
4. Buchholz BM, Masutani K, Kawamura T, Peng X, Toyoda Y, Billiar TR, Bauer AJ, Nakao A. Hydrogen-enriched preservation protects the isogeneic intestinal graft and amends recipient gastric function during transplantation. Transplantation 92: 985-992, 2011.
5. Calabrese V, Cornelius C, Rizzarelli E, Owen JB, Dinkova-Kostova AT, Butterfield DA. Nitric oxide in cell survival: a janus molecule. Antioxid Redox Signal 11: 2717-2739, 2009.
6. Fox-Robichaud A, Payne D, Hasan SU, Ostrovsky L, Fairhead T, Reinhardt P, Kubes P. Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J Clin Invest 101: 2497-2505, 1998.
7. Fukuda K, Asoh S, Ishikawa M, Yamamoto Y, Ohsawa I, Ohta S. Inhalation of hydrogen gas suppresses hepatic injury caused by ischemia/ reperfusion through reducing oxidative stress. Biochem Biophys Res Commun 361: 670-674, 2007.
8. Guery B, Neviere R, Viget N, Foucher C, Fialdes P, Wattel F, Beaucaire G. Inhaled NO preadministration modulates local and remote ischemia-reperfusion organ injury in a rat model. J Appl Physiol 87: 47-53, 1999.
9. Hataishi R, Rodrigues AC, Neilan TG, Morgan JG, Buys E, Shiva S, Tambouret R, Jassal DS, Raher MJ, Furutani E, Ichinose F, Gladwin MT, Rosenzweig A, Zapol WM, Picard MH, Bloch KD, Scherrer-Crosbie M. Inhaled nitric oxide decreases infarction size and improves left ventricular function in a murine model of myocardial ischemiareperfusion injury. Am J Physiol Heart Circ Physiol 291: H379-H384, 2006.
10. Hayashida K, Sano M, Ohsawa I, Shinmura K, Tamaki K, Kimura K, Endo J, Katayama T, Kawamura A, Kohsaka S, Makino S, Ohta S, Ogawa S, Fukuda K. Inhalation of hydrogen gas reduces infarct size in the rat model of myocardial ischemia-reperfusion injury. Biochem Biophys Res Commun 373: 30-35, 2008.
11. Kajiya M, Sato K, Silva MJ, Ouhara K, Do PM, Shanmugam KT, Kawai T. Hydrogen from intestinal bacteria is protective for Concanavalin A-induced hepatitis. Biochem Biophys Res Commun 386: 316-321, 2009.
12. Kinobe R, Ji Y, Nakatsu K. Peroxynitrite-mediated inactivation of heme oxygenases. BMC Pharmacol 4: 26, 2004.
13. Liu X, Huang Y, Pokreisz P, Vermeersch P, Marsboom G, Swinnen M, Verbeken E, Santos J, Pellens M, Gillijns H, Van de Werf F, Bloch KD, Janssens S. Nitric oxide inhalation improves microvascular flow and decreases infarction size after myocardial ischemia and reperfusion. J Am Coll Cardiol 50: 808-817, 2007.
14. Maybauer DM, Maybauer MO, Szabó C, Cox RA, Westphal M, Kiss L, Horvath EM, Traber LD, Hawkins HK, Salzman AL, Southan GJ, Herndon DN, Traber DL. The peroxynitrite catalyst WW-85 improves pulmonary function in ovine septic shock. Shock 35: 148-155, 2011.
15. McMahon TJ, Doctor A. Extrapulmonary effects of inhaled nitric oxide: role of reversible S-nitrosylation of erythrocytic hemoglobin. Proc Am Thorac Soc 3: 153-160, 2006.
16. Merkus D, Visser M, Houweling B, Zhou Z, Nelson J, Duncker DJ. Phosphodiesterase 5 inhibition-induced coronary vasodilation is reduced after myocardial infarction. Am J Physiol Heart Circ Physiol 304: H1370-H1381, 2013.
17. Moncada S, Higgs EA. Nitric oxide and the vascular endothelium. Handb Exp Pharmacol: 213-254, 2006.
18. 1 is required for the cardioprotective effects of inhaled nitric oxide. Am J Physiol Heart Circ Physiol 300: H1477-H1483, 2011.
19. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13: 688-694, 2007.
20. Radi R. Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci USA 101: 4003-4008, 2004.
21. Rumessen JJ. Hydrogen and methane breath tests for evaluation of resistant carbohydrates. Eur J Clin Nutr 46, Suppl 2: S77-S90, 1992.
22. Salloum FN, Das A, Samidurai A, Hoke NN, Chau VQ, Ockaili RA, Stasch JP, Kukreja RC. Cinaciguat, a novel activator of soluble guanylate cyclase, protects against ischemia/reperfusion injury: role of hydrogen sulfide. Am J Physiol Heart Circ Physiol 302: H1347-H1354, 2012.
23. Satija A, Hu FB. Cardiovascular benefits of dietary fiber. Curr Atheroscler Rep 14: 505-514, 2012.
24. Sies H. Strategies of antioxidant defense. Eur J Biochem 215: 213-219, 1993.
25. Snyder SH. Janus faces of nitric oxide. Nature 364: 577, 1993.
26. Suematsu M, Suganuma K, Kashiwagi S. Mechanistic probing of gaseous signal transduction in microcirculation. Antioxid Redox Signal 5: 485-492, 2003.
27. Szabó C, Mabley JG, Moeller SM, Shimanovich R, Pacher P, Virag L, Soriano FG, Van Duzer JH, Williams W, Salzman AL, Groves JT. Part I: pathogenetic role of peroxynitrite in the development of diabetes and diabetic vascular complications: studies with FP15, a novel potent peroxynitrite decomposition catalyst. Mol Med 8: 571-580, 2002.
28. Tanaka Y, Shigemura N, Kawamura T, Noda K, Isse K, Stolz DB, Billiar TR, Toyoda Y, Bermudez CA, Lyons-Weiler J, Nakao A. Profiling molecular changes induced by hydrogen treatment of lung allografts prior to procurement. Biochem Biophys Res Commun 425: 873-879, 2012.
29. Wood KC, Gladwin MT. The hydrogen highway to reperfusion therapy. Nat Med 13: 673-674, 2007.
30. ATP channels and permeability transition pores of mitochondria in dogs. Cardiovasc Drugs Ther 26: 217-226, 2012.
31. Zhu J, Rebecchi MJ, Wang Q, Glass PS, Brink PR, Liu L. Chronic Tempol treatment restores pharmacological preconditioning in the senescent rat heart. Am J Physiol Heart Circ Physiol 304: H649-H659, 2013.