Hyperbaric oxygenation improves redox control and reduces mortality in the acute phase of myocardial infarction in a rat model

Oliveira,Mario S.; Tanaka,Leonardo  Y.; Antonio,Ednei  L.; Brandizzi,Laura  I.; Serra,Andrey  J.; Dos Santos,Leonardo; Krieger,José  E.; Laurindo,Francisco  R.M.; Tucci,Paulo  J.F.

doi:10.3892/mmr.2020.10968

Hyperbaric oxygenation improves redox control and reduces mortality in the acute phase of myocardial infarction in a rat model

Authors:
- Mario S. Oliveira
- Leonardo Y. Tanaka
- Ednei L. Antonio
- Laura I. Brandizzi
- Andrey J. Serra
- Leonardo Dos Santos
- José E. Krieger
- Francisco R.M. Laurindo
- Paulo J.F. Tucci
View Affiliations

Affiliations: Division of Cardiology, Federal University of São Paulo (UNIFESP), São Paulo 04039‑032, Brazil, Vascular Biology Laboratory, Heart Institute, University of São Paulo (USP), São Paulo 05403‑900, Brazil, Department of Physiological Sciences, Federal University of Espírito Santo (UFES), Vitória, Espírito Santo 29043‑215, Brazil, Laboratory of Genetics and Molecular Cardiology, Heart Institute, University of São Paulo (USP), São Paulo 05403‑900, Brazil
Published online on: January 29, 2020 https://doi.org/10.3892/mmr.2020.10968
Pages: 1431-1438
Copyright: © Oliveira et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Among the mechanisms of action of hyperbaric oxygenation (HBO), the chance of reducing injury by interfering with the mechanisms of redox homeostasis in the heart leads to the possibility of extending the period of viability of the myocardium at risk. This would benefit late interventions for reperfusion to the ischemic area. The objective of the present study was to investigate the changes in the redox system associated with HBO therapy maintained during the first hour after coronary occlusion in an acute myocardial infarction (MI) rat model. Surviving male rats (n=105) were randomly assigned to one of three groups: Sham (SH=26), myocardial infarction (MI=45) and infarction+hyperbaric therapy (HBO=34, 1 h at 2.5 atm). After 90 min of coronary occlusion, a sample of the heart was collected for western blot analysis of total protein levels of superoxide dismutase, catalase, peroxiredoxin and 3‑nitrotyrosine. Glutathione was measured by enzyme‑linked immunosorbent assay (ELISA). The detection of the superoxide radical anion was carried out by oxidation of dihydroethidium analyzed with confocal microscopy. The mortality rate of the MI group was significantly higher than that of the HBO group. No difference was noted in the myocardial infarction size. The oxidized/reduced glutathione ratio and peroxiredoxin were significantly higher in the SH and MI when compared to the HBO group. Superoxide dismutase enzymes and catalase were significantly higher in the HBO group compared to the MI and SH groups. 3‑Nitrotyrosine and the superoxide radical were significantly lower in the HBO group compared to these in the MI and SH groups. These data demonstrated that hyperbaric oxygenation therapy decreased mortality by improving redox control in the hearts of rats in the acute phase of myocardial infarction.

View Figures

View References

1	Braunwald E and Kloner RA: Myocardial reperfusion: A double-edged sword? J Clin Invest. 76:1713–1719. 1985. View Article : Google Scholar : PubMed/NCBI
2	Bulluck H, Yellon DM and Hausenloy DJ: Reducing myocardial infarct size: Challenges and future opportunities. Heart. 102:341–348. 2016. View Article : Google Scholar : PubMed/NCBI
3	Facundo HT, Carreira RS, de Paula JG, Santos CC, Ferranti R, Laurindo FR and Kowaltowski AJ: Ischemic preconditioning requires increases in reactive oxygen release independent of mitochondrial K⁺ channel activity. Free Radic Biol Med. 40:469–479. 2006. View Article : Google Scholar : PubMed/NCBI
4	Granger DN and Kvietys PR: Reperfusion injury and reactive oxygen species: The evolution of a concept. Redox Biol. 6:524–551. 2015. View Article : Google Scholar : PubMed/NCBI
5	Zhang Y, Sano M, Shinmura K, Tamaki K, Katsumata Y, Matsuhashi T, Morizane S, Ito H, Hishiki T, Endo J, et al: 4-hydroxy-2-nonenal protects against cardiac ischemia-reperfusion injury via the Nrf2-dependent pathway. J Mol Cell Cardiol. 49:576–586. 2010. View Article : Google Scholar : PubMed/NCBI
6	Fröhlich GM, Meier P, White SK, Yellon DM and Hausenloy DJ: Myocardial reperfusion injury: Looking beyond primary PCI. Eur Heart J. 34:1714–1722. 2013. View Article : Google Scholar : PubMed/NCBI
7	Bennett MH, Lehm JP and Jepson N: Hyperbaric oxygen therapy for acute coronary syndrome. Cochrane Database Syst Rev. CD0048182015.PubMed/NCBI
8	Undersea and Hyperbaric Medical Society: Indications for hyperbaric oxygen therapy. https://www.uhms.org/resources/hbo-indications.htmlMarch 25–2019
9	Sterling DL, Thornton JD, Swafford A, Gottlieb SF, Bishop SP, Stanley AW and Downey JM: Hyperbaric oxygen limits infarct size in ischemic rabbit myocardium in vivo. Circulation. 88:1931–1936. 1993. View Article : Google Scholar : PubMed/NCBI
10	Tibbles PM and Edelsberg JS: Hyperbaric-oxygen therapy. N Engl J Med. 334:1642–1648. 1996. View Article : Google Scholar : PubMed/NCBI
11	Whalen RE and Saltzman HA: Hyperbaric oxygenation in the treatment of acute myocardial infarction. Prog Cardiovasc Dis. 10:575–583. 1968. View Article : Google Scholar : PubMed/NCBI
12	Poff AM, Kernagis D and D'Agostino DP: Hyperbaric Environment: Oxygen and Cellular damage versus protection. Compr Physiol. 7:213–234. 2016. View Article : Google Scholar : PubMed/NCBI
13	Cabigas BP, Su J, Hutchins W, Shi Y, Schaefer RB, Recinos RF, Nilakantan V, Kindwall E, Niezgoda JA and Baker JE: Hyperoxic and hyperbaric-induced cardioprotection: Role of nitric oxide synthase 3. Cardiovasc Res. 72:143–151. 2006. View Article : Google Scholar : PubMed/NCBI
14	Jones DP: Redefining oxidative stress. Antioxid Redox Signal. 8:1865–1879. 2006. View Article : Google Scholar : PubMed/NCBI
15	Kim CH, Choi H, Chun YS, Kim GT, Park JW and Kim MS: Hyperbaric oxygenation pretreatment induces catalase and reduces infarct size in ischemic rat myocardium. Pflugers Arch. 442:519–525. 2001. View Article : Google Scholar : PubMed/NCBI
16	Tavares AM, da Rosa Araujo AS, Llesuy S, Khaper N, Rohde LE, Clausell N and Belló-Klein A: Early loss of cardiac function in acute myocardial infarction is associated with redox imbalance. Exp Clin Cardiol. 17:263–267. 2012.PubMed/NCBI
17	Thom SR: Hyperbaric oxygen: Its mechanisms and efficacy. Plast Reconstr Surg. 127 (Suppl 1):131S–141S. 2011. View Article : Google Scholar : PubMed/NCBI
18	dos Santos L, Serra AJ, Antônio EL, Hull HF and Tucci PJ: Hyperbaric oxygenation applied immediately after coronary occlusion reduces myocardial necrosis and acute mortality in rats. Clin Exp Pharmacol Physiol. 36:594–598. 2009. View Article : Google Scholar : PubMed/NCBI
19	Guadalupe NBM, Castillo-Hernandez MDC, Kormanovski A, Lara-Padilla E, Pimentel-Montejano VH, Olaf GV, Lopez-Mayorga RM and Gustavo GB: Effect of hyperbaric oxygenation in total antioxidant system, nitric oxide and 3 nitrotyrosine levels in a rat model of acute myocardial infarct in the absence of reperfusion. Int J Pharmacol. 11:834–839. 2015. View Article : Google Scholar
20	Kuhn LA, Kline HJ, Wang M, Yamaki T and Jacobson JH II: Hemodynamic effects of hyperbaric oxygenation in experimental acute myocardial infarction. Circ Res. 16:499–509. 1965. View Article : Google Scholar : PubMed/NCBI
21	Mogelson S, Davidson J, Sobel BE and Roberts R: The effect of hyperbaric oxygen on infarct size in the conscious animal. Eur J Cardiol. 12:135–146. 1981.PubMed/NCBI
22	Thomas MP, Brown LA, Sponseller DR, Williamson SE, Diaz JA and Guyton DP: Myocardial infarct size reduction by the synergistic effect of hyperbaric oxygen and recombinant tissue plasminogen activator. Am Heart J. 120:791–800. 1990. View Article : Google Scholar : PubMed/NCBI
23	Yogaratnam JZ, Laden G, Guvendik L, Cowen M, Cale A and Griffin S: Hyperbaric oxygen preconditioning improves myocardial function, reduces length of intensive care stay, and limits complications post coronary artery bypass graft surgery. Cardiovasc Revasc Med. 11:8–19. 2010. View Article : Google Scholar : PubMed/NCBI
24	Shandling AH, Ellestad MH, Hart GB, Crump R, Marlow D, Van Natta B, Messenger JC, Strauss M and Stavitsky Y: Hyperbaric oxygen and thrombolysis in myocardial infarction: The ‘HOT MI’ pilot study. Am Heart J. 134:544–550. 1997. View Article : Google Scholar : PubMed/NCBI
25	Stavitsky Y, Shandling AH, Ellestad MH, Hart GB, Van Natta B, Messenger JC, Strauss M, Dekleva MN, Alexander JM, Mattice M and Clarke D: Hyperbaric oxygen and thrombolysis in myocardial infarction: The ‘HOT MI’ randomized multicenter study. Cardiology. 90:131–136. 1998. View Article : Google Scholar : PubMed/NCBI
26	Dekleva M, Neskovic A, Vlahovic A, Putnikovic B, Beleslin B and Ostojic M: Adjunctive effect of hyperbaric oxygen treatment after thrombolysis on left ventricular function in patients with acute myocardial infarction. Am Heart J. 148:E142004. View Article : Google Scholar : PubMed/NCBI
27	Vlahović A, Nesković AN, Dekleva M, Putniković B, Popović ZB, Otasević P and Ostojić M: Hyperbaric oxygen treatment does not affect left ventricular chamber stiffness after myocardial infarction treated with thrombolysis. Am Heart J. 148:e12004. View Article : Google Scholar : PubMed/NCBI
28	Zhdanov GG and Sokolov IM: Tissue hypoxia in acute myocardial infarction and possible approaches to its correction. Anesteziol Reanimatol. 51–53. 2001.(In Russian). PubMed/NCBI
29	Hedström E, Engblom H, Frogner F, Aström-Olsson K, Öhlin H, Jovinge S and Arheden H: Infarct evolution in man studied in patients with first-time coronary occlusion in comparison to different species-implications for assessment of myocardial salvage. J Cardiovasc Magn Reson. 11:382009. View Article : Google Scholar : PubMed/NCBI
30	Vetterlein F, Schrader C, Volkmann R, Neckel M, Ochs M, Schmidt G and Hellige G: Extent of damage in ischemic, nonreperfused, and reperfused myocardium of anesthetized rats. Am J Physiol Heart Circ Physiol. 285:H755–H765. 2003. View Article : Google Scholar : PubMed/NCBI
31	dos Santos L, Mello AF, Antonio EL and Tucci PJF: Determination of myocardial infarction size in rats by echocardiography and tetrazolium staining: Correlation, agreements, and simplifications. Braz J Med Biol Res. 41:199–201. 2008. View Article : Google Scholar : PubMed/NCBI
32	Kanashiro RM, Nozawa E, Murad N, Gerola LR, Moisés VA and Tucci PJ: Myocardial infarction scar plication in the rat: Cardiac mechanics in an animal model for surgical procedures. Ann Thorac Surg. 73:1507–1513. 2002. View Article : Google Scholar : PubMed/NCBI
33	de Melo BL, Vieira SS, Antônio EL, Dos Santos LF, Portes LA, Feliciano RS, de Oliveira HÁ, Silva JÁ Jr, de Carvalho PT, Tucci PJ and Serra AJ: Exercise training attenuates right ventricular remodeling in rats with pulmonary arterial stenosis. Front Physiol. 7:5412016. View Article : Google Scholar : PubMed/NCBI
34	Tanito M, Elliott MH, Kotake Y and Anderson RE: Protein modifications by 4-hydroxynonenal and 4-hydroxyhexenal in light-exposed rat retina. Invest Ophthalmol Vis Sci. 46:3859–3868. 2005. View Article : Google Scholar : PubMed/NCBI
35	Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD and Davidson BL: Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res. 82:1298–1305. 1998. View Article : Google Scholar : PubMed/NCBI
36	Leite PF, Danilovic A, Moriel P, Dantas K, Marklund S, Dantas AP and Laurindo FR: Sustained decrease in superoxide dismutase activity underlies constrictive remodeling after balloon injury in rabbits. Arterioscler Thromb Vasc Biol. 23:2197–2202. 2003. View Article : Google Scholar : PubMed/NCBI
37	Fernandes DC, Wosniak J Jr, Pescatore LA, Bertoline MA, Liberman M, Laurindo FR and Santos CX: Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems. Am J Physiol Cell Physiol. 292:C413–C422. 2007. View Article : Google Scholar : PubMed/NCBI
38	Lundberg JO, Weitzberg E and Gladwin MT: The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov. 7:156–167. 2008. View Article : Google Scholar : PubMed/NCBI
39	Omar SA, Webb AJ, Lundberg JO and Weitzberg E: Therapeutic effects of inorganic nitrate and nitrite in cardiovascular and metabolic diseases. J Intern Med. 279:315–336. 2016. View Article : Google Scholar : PubMed/NCBI
40	Godman CA, Joshi R, Giardina C, Perdrizet G and Hightower LE: Hyperbaric oxygen treatment induces antioxidant gene expression. Ann N Y Acad Sci. 1197:178–183. 2010. View Article : Google Scholar : PubMed/NCBI
41	Soyer OS, Salathé M and Bonhoeffer S: Signal transduction networks: Topology, response and biochemical processes. J Theor Biol. 238:416–425. 2006. View Article : Google Scholar : PubMed/NCBI
42	Ristow M and Schmeisser S: Extending life span by increasing oxidative stress. Free Radic Biol Med. 51:327–336. 2011. View Article : Google Scholar : PubMed/NCBI
43	Bocci V and Valacchi G: Nrf2 activation as target to implement therapeutic treatments. Front Chem. 3:42015. View Article : Google Scholar : PubMed/NCBI
44	Yin X, Wang X, Fan Z, Peng C, Ren Z, Huang L, Liu Z and Zhao K: Hyperbaric oxygen preconditioning attenuates myocardium ischemia-reperfusion injury through upregulation of heme oxygenase 1 expression: PI3K/Akt/Nrf2 pathway involved. J Cardiovasc Pharmacol Ther. 20:428–438. 2015. View Article : Google Scholar : PubMed/NCBI
45	Aquilano K, Rotilio G and Ciriolo MR: Proteasome activation and nNOS down-regulation in neuroblastoma cells expressing a Cu, Zn superoxide dismutase mutant involved in familial ALS. J Neurochem. 85:1324–1335. 2003. View Article : Google Scholar : PubMed/NCBI
46	Cao C, Leng Y, Liu X, Yi Y, Li P and Kufe D: Catalase is regulated by ubiquitination and proteosomal degradation. Role of the c-Abl and Arg tyrosine kinases. Biochemistry. 42:10348–10353. 2003. View Article : Google Scholar : PubMed/NCBI
47	Poole LB, Karplus PA and Claiborne A: Protein sulfenic acids in redox signaling. Annu Rev Pharmacol Toxicol. 44:325–347. 2004. View Article : Google Scholar : PubMed/NCBI
48	Buettner GR, Wagner BA and Rodgers VG: Quantitative redox biology: An approach to understand the role of reactive species in defining the cellular redox environment. Cell Biochem Biophys. 67:477–483. 2013. View Article : Google Scholar : PubMed/NCBI
49	Baek JY, Han SH, Sung SH, Lee HE, Kim YM, Noh YH, Bae SH, Rhee SG and Chang TS: Sulfiredoxin protein is critical for redox balance and survival of cells exposed to low steady-state levels of H2O2. J Biol Chem. 287:81–89. 2012. View Article : Google Scholar : PubMed/NCBI
50	Day AM, Brown JD, Taylor SR, Rand JD, Morgan BA and Veal EA: Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival. Mol Cell. 45:398–408. 2012. View Article : Google Scholar : PubMed/NCBI
51	Pacher P, Beckman JS and Liaudet L: Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 87:315–424. 2007. View Article : Google Scholar : PubMed/NCBI
52	Totzeck M, Hendgen-Cotta UB and Rassaf T: Nitrite-Nitric oxide signaling and cardioprotection. Adv Exp Med Biol. 982:335–346. 2017. View Article : Google Scholar : PubMed/NCBI