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Angiotensin (1–7) facilitates cardioprotection of ischemic preconditioning on ischemia–reperfusion-challenged rat heart

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Abstract

Ischemic preconditioning (IPC) is one of the most promising strategies used to protect the myocardium from ischemia–reperfusion injury. Ang (1–7) exhibits cardioprotective activity; however, its therapeutic potential on IPC-induced cardioprotection has not been reported in ischemia–reperfusion injury till date. Therefore, the first set of experiment was designed to evaluate the direct effect of Ang (1–7), in perfusion medium, on cardioprotective activity of IPC in rat heart challenged to ischemia–reperfusion injury. In addition, the acute and chronic effects of pretreated Ang (1–7) were investigated on cardioprotection of IPC in ischemia–reperfusion-challenged hearts in subsequent sets of experiments. The results showed that Ang (1–7) potentiated the IPC-induced increase in coronary flow and heart rate, decrease in lactate dehydrogenase and creatine kinase activity, ventricular fibrillation, and infarct size in ischemia–reperfusion-challenged animals in direct and chronic sets of experiments. Further, Ang (1–7) enhanced the IPC-induced attenuation in mitochondrial dysfunction, oxidative stress, and apoptosis in ischemia–reperfusion-challenged hearts in both sets of experiments. A-779, Mas receptor antagonist, abrogated potentiation effects of Ang (1–7) on IPC-induced cardioprotection in ischemia–reperfusion-challenged rats in the above set of experiments. These observations indicate that Ang (1–7)/Mas receptor activation could be a potential adjuvant to IPC during ischemia–reperfusion-induced cardiac injury.

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References

  1. Mathers CD, Loncar D (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3:e442

    Article  PubMed  PubMed Central  Google Scholar 

  2. Go AS, Mozaffarian D, Roger VL et al (2013) American Heart Association Statistics Committee and Stroke Statistics Subcommittee: Heart disease and stroke statistics—2013 update: a report from the American Heart Association. Circulation 127:e6–e245

    Article  PubMed  Google Scholar 

  3. Liu M, Zhang P, Chen M, et al (2012) Aging might increase myocardial ischemia/reperfusion–induced apoptosis in humans and rats. Age (Dordr) 34:621–632

    Article  Google Scholar 

  4. Marczak J, Nowicki R, Kulbacka J et al (2012) Is remote ischaemic preconditioning of benefit to patients undergoing cardiac surgery? Interact Cardiovasc Thorac Surg 14:634–639

    Article  PubMed  PubMed Central  Google Scholar 

  5. Han S, Huang W, Liu Y et al (2013) Does leukocyte–depleted blood cardioplegia reduce myocardial reperfusion injury in cardiac surgery? A systematic review and meta–analysis. Perfusion 28:474–483

    Article  CAS  PubMed  Google Scholar 

  6. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136

    Article  CAS  PubMed  Google Scholar 

  7. Yellon DM, Downey JM (2003) Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83:1113–1151

    Article  CAS  PubMed  Google Scholar 

  8. Sharma A, Singh M (2000) Possible mechanism of cardioprotective effect of angiotensin preconditioning in isolated rat heart. Eur J Pharmacol 406:85–92

    Article  CAS  PubMed  Google Scholar 

  9. Ferreira AJ, Santos RA, Almeida AP (2001) Angiotensin: cardioprotective effect in myocardial ischemia/reperfusion. Hypertension 38:665–668

    Article  CAS  PubMed  Google Scholar 

  10. Mehta PK, Griendling KK (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292:C82–C97

    Article  CAS  PubMed  Google Scholar 

  11. Nussberger J, Cugno M, Amstutz C et al (1998) Plasma bradykinin in angio-oedema. Lancet 351:1693–1697

    Article  CAS  PubMed  Google Scholar 

  12. Strauss MH, Hall AS (2006) Angiotensin receptor blockers may increase risk of myocardial infarction: unraveling the ARB-MI paradox. Circulation 114:838–854

    Article  PubMed  Google Scholar 

  13. Ferreira AJ, Santos RA (2005) Cardiovascular actions of angiotensin-(1–7). Braz J Med Biol Res 38:499–507

    Article  CAS  PubMed  Google Scholar 

  14. Lin L, Liu X, Xu J et al (2016) Mas receptor mediates cardioprotection of angiotensin-(1–7) against Angiotensin II-induced cardiomyocyte autophagy and cardiac remodelling through inhibition of oxidative stress. J Cell Mol Med 20:48–57

    Article  CAS  PubMed  Google Scholar 

  15. Westermeier F, Bustamante M, Pavez M et al (2015) Novel players in cardioprotection: Insulin like growth factor-1, angiotensin-(1–7) and angiotensin-(1–9). Pharmacol Res 101:41–55

    Article  CAS  PubMed  Google Scholar 

  16. Bolli R (2000) The late phase of preconditioning. Circ Res 87:972–983

    Article  CAS  PubMed  Google Scholar 

  17. Heusch G, Boengler K, Schulz R (2010) Inhibition of mitochondrial permeability transition pore opening: the Holy Grail of cardioprotection. Basic Res Cardiol 105:151–154

    Article  PubMed  Google Scholar 

  18. Bernardi P, Di Lisa F (2015) The mitochondrial permeability transition pore: molecular nature and role as a target in cardioprotection. J Mol Cell Cardiol 78C:100–106

    Article  Google Scholar 

  19. Zhao P, Li F, Gao W et al (2015) Angiotensin1-7 protects cardiomyocytes from hypoxia/reoxygenation-induced oxidative stress by preventing ROS-associated mitochondrial dysfunction and activating the Akt signaling pathway. Acta Histochem 117:803–810

    Article  CAS  PubMed  Google Scholar 

  20. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011) Guide for the care and use of laboratory animals, 8th edn. National Academies Press (US), Washington, DC

    Google Scholar 

  21. Ferreira AJ, Santos RA, Almeida AP (2001) Angiotensin-(1–7): cardioprotective effect in myocardial ischemia/reperfusion. Hypertension 38:665–668

    Article  CAS  PubMed  Google Scholar 

  22. Pawlik MW, Kwiecien S, Ptak-Belowska A et al (2016) The renin-angiotensin system and its vasoactive metabolite angiotensin-(1–7) in the mechanism of the healing of preexisting gastric ulcers. The involvement of Mas receptors, nitric oxide, prostaglandins and proinflammatory cytokines. J Physiol Pharmacol 67:75–91

    CAS  PubMed  Google Scholar 

  23. Goyal A, Semwal BC, Yadav HN (2016) Abrogated cardioprotective effect of ischemic preconditioning in ovariectomized rat heart. Hum Exp Toxicol 35:644–653

    Article  CAS  PubMed  Google Scholar 

  24. Pedersen PL, Greenawalt JW, Reynafarje B et al (1978) Preparation and characterization of mitochondria and submitochondrial particles of rat liver and liver-derived tissues. Methods Cell Biol 20:411–481

    Article  CAS  PubMed  Google Scholar 

  25. Lowry OH, Rosebrough NJ, Farr AL et al (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  26. Kamboj SS, Kumar V, Kamboj A et al (2008) Mitochondrial oxidative stress and dysfunction in rat brain induced by carbofuran exposure. Cell Mol Neurobiol 28:961–969

    Article  CAS  PubMed  Google Scholar 

  27. Huang SG (2002) Development of a high throughput screening assay for mitochondrial membrane potential in living cells. J Biomol Screen 7:383–389

    Article  CAS  PubMed  Google Scholar 

  28. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  29. Green LC, Wagner DA, Glogowski J et al (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131–138

    Article  CAS  PubMed  Google Scholar 

  30. Kakkar P, Das B, Viswanathan PN (1984) A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophys 21:130–132

    CAS  PubMed  Google Scholar 

  31. Beers JRF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  PubMed  Google Scholar 

  32. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  33. Liu D, **ao B, Han F et al (2912) Single-prolonged stress induces apoptosis in dorsal raphe nucleus in the ratmodel of posttraumatic stress disorder. BMC Psychiatry 12:211

    Article  Google Scholar 

  34. Davie AP, Mcmurray JJ (1999) Effect of angiotensin-(1–7) and bradykinin in patients with heart failure treated with an ACE inhibitor. Hypertension 34:457–460

    Article  CAS  PubMed  Google Scholar 

  35. Javadov SA, Clarke S, Das M et al (2003) Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol 549:513–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhao ZQ, Corvera JS, Halkos ME et al (2003) Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285:H579–H588

    Article  CAS  PubMed  Google Scholar 

  37. Moon JY, Tanimoto M, Gohda T, et al. (2011) Attenuating effect of angiotensin-(1–7) on angiotensin II-mediated NAD(P)H oxidase activation in type 2 diabetic nephropathy of KK-A(y)/Ta mice. Am J Physiol Renal Physiol 300:F1271–1282

    Article  CAS  PubMed  Google Scholar 

  38. Kim SM, Kim YG, Jeong KH et al (2012) Angiotensin II-induced mitochondrial Nox4 is a major endogenous source of oxidative stress in kidney tubular cells. PLoS One 7:e39739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Xu P, Santos RA, Bader M et al (2007) Alterations in gene expression in the testis of angiotensin-(1–7)-receptor Mas-deficient mice. Regul Pept 138:51–55

    Article  CAS  PubMed  Google Scholar 

  40. Cai SM, Yang RQ, Li Y et al (2016) Angiotensin-(1–7) improves liver fibrosis by regulating the NLRP3 inflammasome via redox balance modulation. Antioxid Redox Signal 24:795–812

    Article  CAS  PubMed  Google Scholar 

  41. Nautiyal M, Katakam PV, Busija DW et al (2012) Differences in oxidative stress status and expression of MKP-1 in dorsal medulla of transgenic rats with altered brain renin-angiotensin system. Am J Physiol Regul Integr Comp Physiol 303:R799–R806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

PP is thankful to GLA University, Mathura, Uttar Pradesh, India for the financial assistantship.

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Correspondence to Debapriya Garabadu.

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Pachauri, P., Garabadu, D., Goyal, A. et al. Angiotensin (1–7) facilitates cardioprotection of ischemic preconditioning on ischemia–reperfusion-challenged rat heart. Mol Cell Biochem 430, 99–113 (2017). https://doi.org/10.1007/s11010-017-2958-4

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  • DOI: https://doi.org/10.1007/s11010-017-2958-4

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