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Original Article

Inhibition of NADPH oxidase by apocynin promotes myocardial antioxidant response and prevents isoproterenol-induced myocardial oxidative stress in rats

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Pages 772-786 | Received 08 Apr 2017, Accepted 31 Aug 2017, Published online: 03 Oct 2017

References

  • Schaper J, Speiser B. The extracellular matrix in the failing human heart. In: Cellular and molecular alterations in the failing human heart. New York: Springer; 1992:303–309.
  • Sanada S, Komuro I, Kitakaze M. Pathophysiology of myocardial reperfusion injury: preconditioning, postconditioning, and translational aspects of protective measures. Am J Physiol Heart Circ Physiol 2011;301:H1723–H1741.
  • Kones R. Oxygen therapy for acute myocardial infarction-then and now. A century of uncertainty. Am J Med 2011;124:1000–1005.
  • Neumar RW, Shuster M, Callaway CW, Gent LM, Atkins DL, Bhanji F, et al. Part 1: executive summary: 2015 American Heart Association guidelines update for cardiopulmonary resuscitation and emergency cardiovascular care. Part 1. Circulation 2015;132:S315–S367.
  • Hearse JD, Opie LH, Katzeff IE, Lubbe WF, Van der Werff TJ, Peisach M, Boulle G. Characterization of the ‘border zone’ in acute regional ischemia in the dog. Am J Cardiol 1977;40:716–726.
  • Fabiani R, Ceconi C, Curello S, Alfieri O, Visioli O. Myocardial damage during ischaemia and reperfusion. Eur Heart J 1993;14:25–30.
  • Hansen PR. Role of neutrophils in myocardial ischemia and reperfusion. Circulation 1995;91:1872–1885.
  • Xiang YK. Compartmentalization of beta-adrenergic signals in cardiomyocytes. Circ Res 2011;109:231–244. Epub 2011/07/09
  • Yates JC, Beamish RE, Dhalla NS. Ventricular dysfunction and necrosis produced by adrenochrome metabolite of epinephrine: relation to pathogenesis of catecholamine cardiomyopathy. Am Heart J 1981;102:210–221.
  • Cohen G, Heikkila RE. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 1974;249:2447–2452.
  • Singal PK, Kapur N, Dhillon KS, Beamish RE, Dhalla NS. Role of free radicals in catecholamine-induced cardiomyopathy. Can J Physiol Pharmacol 1982;60:1390–1397.
  • Engle SK, Jordan WH, Pritt ML, Chiang AY, Davis MA, Zimmermann JL, et al. Qualification of cardiac troponin I concentration in mouse serum using isoproterenol and implementation in pharmacology studies to accelerate drug development. Toxicol Pathol 2009;37:617–628.
  • George JC, Liner A, Hoit BD. Isoproterenol-induced myocardial injury: a systematic comparison of subcutaneous versus intraperitoneal delivery in a rat model. Echocardiography 2010;27:716–721.
  • Stolk J, Hiltermann TJ, Dijkman JH, Verhoeven AJ. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am J Respir Cell Mol Biol 1994;11:95–102.
  • Saad SY, Najjar TA, Noreddin AM, Al-Rikabi AC. Effects of gemcitabine on cisplatin-induced nephrotoxicity in rats: schedule-dependent study. Pharmacol Res 2001;43:193–198.
  • Simonyi A, Serfozo P, Lehmidi TM, Cui J, Gu Z, Lubahn DB, et al. The neuroprotective effects of apocynin. Front Biosci 2012;4:2183–2193.
  • Impellizzeri D, Mazzon E, Esposito E, Paterniti I, Bramanti P, Cuzzocrea S. Effect of Apocynin, an inhibitor of NADPH oxidase, in the inflammatory process induced by an experimental model of spinal cord injury. Free Radic Res 2011;45:221–236.
  • Li JM, Gall NP, Grieve DJ, Chen M, Shah AM. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertension 2002;40:477–484.
  • El-Sawalhi MM, Ahmed LA. Exploring the protective role of apocynin, a specific NADPH oxidase inhibitor, in cisplatin-induced cardiotoxicity in rats. Chem Biol Interact 2014;207:58–66.
  • Wang K, Li L, Song Y, Ye X, Fu S, Jiang J, Li S. Improvement of pharmacokinetics behavior of apocynin by nitrone derivatization: comparative pharmacokinetics of nitrone-apocynin and its parent apocynin in rats. PLoS One 2013;8:e70189.
  • Fan R, Shan X, Qian H, Song C, Wu G, Chen Y, et al. Protective effect of apocynin in an established alcoholic steatohepatitis rat model. Immunopharmacol Immunotoxicol 2012;34:633–638.
  • Walker MJ, Curtis MJ, Hearse DJ, Campbell RW, Janse MJ, Yellon DM, et al. The Lambeth Conventions: guidelines for the study of arrhythmias in ischaemia infarction, and reperfusion. Cardiovasc Res 1988;22:447–455.
  • Lasnier E, Mario N, Boque MC, You SN, Vaubourdolle M. Evaluation of the clinical chemistry analyser Olympus AU400. Clin Chem Lab Med 2000;38:1043–1049.
  • Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978;86:271–278.
  • Disli OM, Sarihan E, Colak MC, Vardi N, Polat A, Yagmur J, et al. Effects of molsidomine against doxorubicin-induced cardiotoxicity in rats. Eur Surg Res Eur Chir Forschung Recherches Chir Eur 2013;51:79–90.
  • Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem 1988;34:497–500.
  • Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121–126.
  • Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 1968;25:192–205.
  • Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 2004;37:277–285.
  • Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38:1103–1111.
  • Fromaget C, el Aoumari AE, Gros D. Distribution pattern of connexin 43, a gap junctional protein, during the differentiation of mouse heart myocytes. Differentiation 1992;51:9–20.
  • Dhein S. Gap junction channels in the cardiovascular system: pharmacological and physiological modulation. Trends Pharmacol Sci 1998;19:229–241.
  • Mitasíková M, Lin H, Soukup T, Imanaga I, Tribulová N. Diabetes and thyroid hormones affect connexin-43 and PKC-[epsilon] expression in rat heart atria. Physiol Res 2009;58:211–217.
  • Elbe H, Vardi N, Esrefoglu M, Ates B, Yologlu S, Taskapan C. Amelioration of streptozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats. Hum Exp Toxicol 2015;34:100–113.
  • Rona G, Chappel CI, Balazs T, Gaudry R. An infarct-like myocardial lesion and other toxic manifestations produced by isoproterenol in the rat. Arch Pathol 1959;67:443–455.
  • Chappel CI, Rona G, Balazs T, Gaudry R. Comparison of cardiotoxic actions of certain sympathomimetic amines. Can J Biochem Physiol 1959;37:35–42.
  • Singal PK, Yates JC, Beamish RE, Dhalla NS. Influence of reducing agents on adrenochrome-induced changes in the heart. Arch Pathol Lab Med 1981;105:664–669.
  • Yeager JC, Whitehurst ME. Verapamil prevents isoproterenol-induced cardiac failure in the rat. Life Sci 1982;30:299–306.
  • Bloom S, Davis DL. Calcium as mediator of isoproterenol-induced myocardial necrosis. Am J Pathol 1972;69:459–470.
  • Bhagat B, Sullivan JM, Fischer VW, Nadel EM, Dhalla NS. cAMP activity and isoproterenol-induced myocardial injury in rats. Recent Adv Stud Card Struct Metab 1976;12:465–470.
  • Beswick RA, Dorrance AM, Leite R, Webb RC. NADH/NADPH oxidase and enhanced superoxide production in the mineralocorticoid hypertensive rat. Hypertension 2001;38:1107–1111.
  • Ghosh M, Wang HD, McNeill JR. Role of oxidative stress and nitric oxide in regulation of spontaneous tone in aorta of DOCA-salt hypertensive rats. Br J Pharmacol 2004;141:562–573.
  • Carotenuto F, Minieri M, Monego G, Fiaccavento R, Bertoni A, Sinigaglia F, et al. A diet supplemented with ALA-rich flaxseed prevents cardiomyocyte apoptosis by regulating caveolin-3 expression. Cardiovasc Res 2013;100:422–431.
  • Stanely Mainzen Prince PSM, Rajakumar S, Dhanasekar K. Protective effects of vanillic acid on electrocardiogram, lipid peroxidation, antioxidants, proinflammatory markers and histopathology in isoproterenol induced cardiotoxic rats. Eur J Pharmacol 2011;668:233–240.
  • Roy SJ, Mainzen Prince PS. Protective effects of sinapic acid on cardiac hypertrophy, dyslipidaemia and altered electrocardiogram in isoproterenol-induced myocardial infarcted rats. Eur J Pharmacol 2013;699:213–218.
  • Parlakpinar H, Ozer MK, Acet A. Effect of aminoguanidine on ischemia–reperfusion induced myocardial injury in rats. Mol Cell Biochem 2005;277:137–142.
  • Eşrefoğlu M, Gül M, Parlakpinar H, Acet A. Effects of melatonin and caffeic acid phenethyl ester on testicular injury induced by myocardial ischemia/reperfusion in rats. Fundam Clin Pharmacol 2005;19:365–372.
  • Hamilton CA, Brosnan MJ, McIntyre M, Graham D, Dominiczak AF. Superoxide excess in hypertension and aging: a common cause of endothelial dysfunction. Hypertension 2001;37:529–534.
  • Li B, Tian J, Sun Y, Xu TR, Chi RF, Zhang XL, et al. Activation of NADPH oxidase mediates increased endoplasmic reticulum stress and left ventricular remodeling after myocardial infarction in rabbits. Biochim Biophys Acta 2015;1852:805–815.
  • Meyer JW, Schmitt ME. A central role for the endothelial NADPH oxidase in atherosclerosis. FEBS Lett 2000;472:1–4.
  • Hu L, Zhang Y, Lim PS, Miao Y, Tan C, McKenzie KU, et al. Apocynin but not L-arginine prevents and reverses dexamethasone-induced hypertension in the rat. Am J Hypertens 2006;19:413–418.
  • Zhang Y, Chan MMK, Andrews MC, Mori TA, Croft KD, McKenzie KU, et al. Apocynin but not allopurinol prevents and reverses adrenocorticotropic hormone-induced hypertension in the rat. Am J Hypertens 2005;18:910–916.
  • Park YM, Park MY, Suh YL, Park JB. NAD(P)H oxidase inhibitor prevents blood pressure elevation and cardiovascular hypertrophy in aldosterone-infused rats. Biochem Biophys Res Commun 2004;313:812–817.
  • Privratsky JR, Wold LE, Sowers JR, Quinn MT, Ren J. AT1 blockade prevents glucose-induced cardiac dysfunction in ventricular myocytes: role of the AT1 receptor and NADPH oxidase. Hypertension 2003;42:206–212.
  • Altintas R, Polat A, Vardi N, Oguz F, Beytur A, Sagir M, et al. The protective effects of apocynin on kidney damage caused by renal ischemia/reperfusion. J Endourol. Endourological Society 2013;27:617–624.
  • Cagin YF, Parlakpinar H, Polat A, Vardi N, Atayan Y, Erdogan MA, et al. The protective effects of apocynin on ionizing radiation-induced intestinal damage in rats. Drug Dev Ind Pharm 2016;42:317–324.
  • Kilic T, Parlakpinar H, Taslidere E, Yildiz S, Polat A, Vardi N, et al. Protective and therapeutic effect of apocynin on bleomycin-induced lung fibrosis in rats. Inflammation 2015;38:1166–1180.
  • Thygesen K, Alpert JS, Jaffe AS, et al. Third universal definition of myocardial infarction. J Am Coll Cardiol 2012;60:1581–1598.
  • Potje SR, Troiano JA, Graton ME, Ximenes VF, Nakamune AC, Antoniali C. Hypotensive and vasorelaxant effect of Diapocynin in normotensive rats. Free Radic Biol Med 2017;106:148–157.
  • Zhang LL, Ding L, Zhang F, Gao R, Chen Q, Li YH, et al. Salusin-β in rostral ventrolateral medulla increases sympathetic outflow and blood pressure via superoxide anions in hypertensive rats. J Hypertens 2014;32:1059–1067; discussion 1067
  • Feuerstein GZ, Young PR. Apoptosis in cardiac diseases: stress- and mitogen-activated signaling pathways. Cardiovasc Res 2000;45:560–569.
  • Cagin YF, Erdogan MA, Sahin N, Parlakpinar H, Atayan Y, Polat A, et al. Protective effects of apocynin on cisplatin-induced hepatotoxicity in rats. Arch Med Res 2015;46:517–526.
  • Ozbek O, Altintas R, Polat A, Vardi N, Parlakpinar H, Sagir M, et al. The protective effect of apocynin on testicular ischemia-reperfusion injury. J Urol 2015;193:1417–1422.
  • Simplicio JA, do Vale GT, Gonzaga NA, Leite LN, Hipólito UV, Pereira CA, et al. Reactive oxygen species derived from NAD(P)H oxidase play a role on ethanol-induced hypertension and endothelial dysfunction in rat resistance arteries. J Physiol Biochem 2017;73:5–16.
  • Lapperre TS, Jimenez LA, Antonicelli F, et al. Apocynin increases glutathione synthesis and activates AP-1 in alveolar epithelial cells. FEBS Lett 1999;443:235–239.
  • Heumüller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schröder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 2008;51:211–217.
  • Cruz-Álvarez S, Santana-Martínez R, Avila-Chávez E, Barrera-Oviedo D, Hernández-Pando R, Pedraza-Chaverri J, Maldonado PD. Apocynin protects against neurological damage induced by quinolinic acid by an increase in glutathione synthesis and Nrf2 levels. Neuroscience 2017;350:65–74.
  • Ekici K, Temelli O, Parlakpinar H, Samdanci E, Polat A, Beytur A, et al. Beneficial effects of aminoguanidine on radiotherapy‐induced kidney and testis injury. Andrologia 2016;48:683–692.
  • Goldspink DF, Burniston JG, Ellison GM, Clark WA, Tan LB. Catecholamine-induced apoptosis and necrosis in cardiac and skeletal myocytes of the rat in vivo: the same or separate death pathways? Exp Physiol 2004;89:407–416.
  • Kanno S, Saffitz JE. The role of myocardial gap junctions in electrical conduction and arrhythmogenesis. Cardiovasc Pathol 2001;10:169–177.
  • Zhuo XZ, Wu Y, Ni YJ, Liu JH, Gong M, Wang XH, et al. Isoproterenol instigates cardiomyocyte apoptosis and heart failure via AMPK inactivation-mediated endoplasmic reticulum stress. Apoptosis 2013;18:800–810.
  • Duan WR, Garner DS, Williams SD, Funckes-Shippy CL, Spath IS, Blomme EA. Comparison of immunohistochemistry for activated caspase-3 and cleaved cytokeratin 18 with the TUNEL method for quantification of apoptosis in histological sections of PC-3 subcutaneous xenografts. J Pathol 2003;199:221–228.
  • Egashira K, Nishii K, Nakamura K, Kumai M, Morimoto S, Shibata Y. Conduction abnormality in Gap junction protein connexin45-deficient embryonic stem cell-derived cardiac myocytes. Anat Rec A Discov Mol Cell Evol Biol 2004;280:973–979.
  • Vinten-Johansen J. Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovasc Res 2004;61:481–497.
  • Huang QY, Li XF, Liu SP. Connexin43 and angiotensin II alterations in hearts of rats having undergone an acute exposure to alcohol. Am J Forensic Med Pathol 2013;34:68–71.
  • Steffens S, Montecucco F, Mach F. The inflammatory response as a target to reduce myocardial ischaemia and reperfusion injury. Thromb Haemost 2009;102:240–247.
  • De Zwart LL, Meerman JH, Commandeur JN, Vermeulen NP. Biomarkers of free radical damage applications in experimental animals and in humans. Free Radic Biol Med 1999;26:202–226.
  • Knight JA, Pieper RK, McClellan L. Specificity of the thiobarbituric acid reaction: its use in studies of lipid peroxidation. Clin Chem 1988;34:2433–2438.
  • Draper HH, Squires EJ, Mahmoodi H, Wu J, Agarwal S, Hadley M. A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 1993;15:353–363.
  • Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 1990;186:421–431.
  • Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 1990;9:515–540.
  • Bird RP, Hung SS, Hadley M, Draper HH. Determination of malonaldehyde in biological materials by high-pressure liquid chromatography. Anal Biochem 1983;128:240–244.

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