To access this material please log in or register

Register Authorize

The phenomenon of preconditioning

Vatutin N. T., Kalinkina N. V., Kolesnikov V. S., Sheveliok A. N.

Keywords: ischemic preconditioning

DOI: 10.18087/rhj.2013.4.1810

The review presents data of current reports on mechanisms of ischemic preconditioning in normal and abnormal states (dyslipidemia, atherosclerosis, obesity, metabolic syndrome, DM, AH). The authors considered effects of exercise on myocardial protection against ischemic injury and pointed to agents possessing the property of ischemic preconditioning inducer.
  1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74 (5):1124–1136.
  2. Kremastinos DT. The phenomenon of preconditioning today. Hellenic J Cardiol. 2005;46 (1):1–4.
  3. Lange R, Ingwall J, Hale SL et al. Preservation of high-energy phosphates by verapamil in reperfused myocardium. Circulation. 1984;70 (4):734–741.
  4. Cohen MV, Liu GS, Downey JM. Preconditioning causes improved wall motion as well as smaller infarcts after transient coronary occlusion in rabbits. Circulation. 1991;84 (1):341–349.
  5. Wong GT, Ling Ling J, Irwin MG. Activation of central opioid receptors induces cardioprotection against ischemia-reperfusion injury. Anesth Analg. 2010;111 (1):24–28.
  6. Kloner R, Shook T, Przyklenk K et al. Previous angina alters in-hospital outcome in TIMI 4. A clinical correlate to preconditioning? Circulation. 1995;91 (1):37–45.
  7. Cokkinos DV, Pantos C. Myocardial protection in man – from research concept to clinical practice. Heart Fail Rev. 2007;12 (3-4):345–362.
  8. Ishihara M, Sato H, Tateishi H et al. Implications of prodromal angina pectoris in anterior wall acute myocardial infarction: acute angiographic findings and long-term prognosis. J Am Coll Cardiol. 1997;30 (4):970–975.
  9. Takahashi T, Hiasa Y, Ohara Y et al. Acute hyperglycaemia prevents the protective effect of pre-infarction angina on microvascular function after primary angioplasty for acute myocardial infarction. Heart. 2008;94 (11):1402–1406.
  10. Yang X, Cohen MV, Downey JM. Mechanism of cardioprotection by early ischemic preconditioning. Cardiovasc Drugs Ther. 2010;24 (3):225–234.
  11. Headrick JP, Lasley RD. Adenosine receptors and reperfusion injury of the heart. Handb Exp Pharmacol. 2009; (193):189–214.
  12. Kawada T, Akiyama T, Shimizu S et al. Detection of endogenous acetylcholine release during brief ischemia in the rabbit ventricle: a possible trigger for ischemic preconditioning. Life Sci. 2009;85 (15-16):597–601.
  13. Fan WJ, van Vuuren D, Genade S, Lochner A. Kinases and phosphatases in ischaemic preconditioning: a re-evaluation. Basic Res Cardiol. 2010;105 (4):495–511.
  14. Sadat U. Signaling pathways of cardioprotective ischemic preconditioning. Int J Surg. 2009;7 (6):490–498.
  15. Davidson SM, Hausenloy D, Duchen MR, Yellon DM. Signalling via the reperfusion injury signalling kinase (RISK) pathway links closure of the mitochondrial permeability transition pore to cardioprotection. Int J Biochem Cell Biol. 2006;38 (3):414–419.
  16. Cohen MV, Yang XM, Liu Y et al. Cardioprotective PKG-independent NO signaling at reperfusion. Am J Physiol Heart Circ Physiol. 2010;299 (6):H2028–2036.
  17. Talukder MA, Yang F, Shimokawa H, Zweier JL. eNOS is required for acute in vivo ischemic preconditioning of the heart: effects of ischemic duration and sex. Am J Physiol Heart Circ Physiol. 2010;299 (2):H437–445.
  18. Matsuzaki S, Szweda PA, Szweda LI, Humphries KM. Regulated production of free radicals by the mitochondrial electron transport chain: Cardiac ischemic preconditioning. Adv Drug Deliv Rev. 2009;61 (14):1324–1331.
  19. Lishmanov IuB, Maslov LN, Khaliulin IG et al. Role of heat shock proteins, aldose reductase, Bcl-2 protein and microRNA in the mechanism of delayed preconditioning of heart. Ross Fiziol Zh Im I M Sechenova. 2010;96 (5):472–488.
  20. Wei H, Vander Heide RS. Ischemic preconditioning and heat shock activate Akt via a focal adhesion kinase-mediated pathway in Langendorff-perfused adult rat hearts. Am J Physiol Heart Circ Physiol. 2010;298 (1):H152–157.
  21. Kondo-Nakamura M, Shintani-Ishida K, Uemura K, Yoshida K. Brief exposure to carbon monoxide preconditions cardiomyogenic cells against apoptosis in ischemia-reperfusion. Biochem Biophys Res Commun. 2010;393 (3):449–454.
  22. Diaz RJ, Hinek A, Wilson GJ. Direct evidence of chloride ion efflux in ischaemic and pharmacological preconditioning of cultured cardiomyocytes. Cardiovasc Res. 2010;87 (3):545–551.
  23. Chevion M, Leibowitz S, Aye NN et al. Heart protection by ische­mic preconditioning: a novel pathway initiated by iron and mediated by ferritin. J Mol Cell Cardiol. 2008;45 (6):839–845.
  24. Li Z, Jin ZQ. Ischemic preconditioning enhances integrity of coronary endothelial tight junctions. Biochem Biophys Res Commun. 2012;425 (3):630–635.
  25. Przyklenk K, Kloner RA. Ischemic preconditioning: exploring the paradox. Prog Cardiovasc Dis. 1998;40 (6):517–547.
  26. Loubani M, Ghosh S, Galiñanes M. The aging human myocardium: tolerance to ischemia and responsiveness to ischemic preconditio­ning. J Thorac Cardiovasc Surg. 2003;126 (1):143–147.
  27. Fenton RA, Dickson EW, Meyer TE, Dobson JG Jr. Aging reduces the cardioprotective effect of ischemic preconditioning in the rat heart. J Mol Cell Cardiol. 2000;32 (7):1371–1375.
  28. Abete P, Cacciatore F, Testa G. Clinical application of ischemic preconditioning in the elderly. Dose Response. 2009;8 (1):34–40.
  29. Pepe S. Dysfunctional ischemic preconditioning mechanisms in aging. Cardiovasc Res. 2001;49 (1):11–14.
  30. Abete P, Cacciatore F, Testa G et al. Ischemic preconditioning in the aging heart: from bench to bedside. Ageing Res Rev. 2010;9 (2):153–162.
  31. Ishihara M, Inoue I, Kawagoe T et al. Diabetes mellitus prevents ischemic preconditioning in patients with a first acute anterior wall myocardial infarction. J Am Coll Cardiol. 2001;38 (4):1007–1011.
  32. Randall MD, Gardiner SM, Bennett T. Enhanced cardiac preconditioning in the isolated heart of the transgenic ( (mREN-2) 27) hypertensive rat. Cardiovasc Res. 1997;33 (2):400–409.
  33. Katakam PV, Jordan JE, Snipes JA et al. Myocardial preconditio­ning against ischemia-reperfusion injury is abolished in Zucker obese rats with insulin resistance. Am J Physiol Regul Integr Comp Physiol. 2007;292 (2):R920–926.
  34. Wan R, Camandola S, Mattson MP. Intermittent food deprivation improves cardiovascular and neuroendocrine responses to stress in rats. J Nutr. 2003;133 (6):1921–1929.
  35. Kim HS, Cho JE, Hwang KC et al. Diabetes mellitus mitigates cardioprotective effects of remifentanil preconditioning in ischemia-reperfused rat heart in association with anti-apoptotic pathways of survival. Eur J Pharmacol. 2010;628 (1-3):132–139.
  36. Sivaraman V, Hausenloy DJ, Wynne AM, Yellon DM. Preconditioning the diabetic human myocardium. J Cell Mol Med. 2010;14 (6B): 1740–1746.
  37. Pantos C, Mourouzis I, Cokkinos DV. Protection of the abnormal heart. Heart Fail Rev. 2007;12 (3-4):319–330.
  38. Старенькая И. Сахарный диабет и феномен закаливания тканей миокарда ишемией. Здоров’я України. 2004;96:41–42.
  39. Peart JN, Headrick JP. Clinical cardioprotection and the value of conditioning responses. Am J Physiol Heart Circ Physiol. 2009;296 (6):H1705–1720.
  40. Yadav HN, Singh M, Sharma PL. Modulation of the cardioprotective effect of ischemic preconditioning in hyperlipidaemic rat heart. Eur J Pharmacol. 2010;643 (1):78–83.
  41. Molecular biology of the cell, 3rd ed., by Alberts et al., Garland Publishing, New York, 1994. – 477.
  42. Thuc LC, Teshima Y, Takahashi N et al. Mitochondrial K (ATP) channels-derived reactive oxygen species activate pro-survival pathway in pravastatin-induced cardioprotection. Apoptosis. 2010;15 (6):669–678.
  43. Ebrahim Z, Yellon DM, Baxter GF. Ischemic preconditioning is lost in aging hypertensive rat heart: independent effects of aging and longstanding hypertension. Exp Gerontol. 2007;42 (8):807–814.
  44. Dai W, Simkhovich BZ, Kloner RA. Ischemic preconditioning maintains cardioprotection in aging normotensive and spontaneously hypertensive rats. Exp Gerontol. 2009;44 (5):344–349.
  45. Shah N, Redline S, Yaggi HK et al. Obstructive sleep apnea and acute myocardial infarction severity: ischemic preconditioning? Sleep Breath. 2013 May;17 (2):819–826.
  46. Domenech RJ. Preconditioning: a new concept about the benefit of exercise. Circulation. 2006;113 (1):e1–3.
  47. Végh A, Parratt JR. A common mechanism in the protective effects of preconditioning, cardiac pacing and physical exercise against ischemia and reperfusion-induced arrhythmias. Exp Clin Cardiol. 2005;10 (3):200–205.
  48. French JP, Hamilton KL, Quindry JC et al. Exercise-induced protection against myocardial apoptosis and necrosis: MnSOD, calcium-handling proteins, and calpain. FASEB J. 2008;22 (8):2862–2871.
  49. Parra VM, Macho P, Domenech RJ. Late cardiac preconditioning by exercise in dogs is mediated by mitochondrial potassium channels. J Cardiovasc Pharmacol. 2010;56 (3):268–274.
  50. Iliodromitis EK, Cokkinos P, Zoga A et al. Oral nicorandil recaptures the waned protection from preconditioning in vivo. Br J Pharmacol. 2003;138 (6):1101–1106.
  51. Mahaffey KW, Puma JA, Barbagelata NA et al. Adenosine as an adjunct to thrombolytic therapy for acute myocardial infarction: results of a multicenter, randomized, placebo-controlled trial: the Acute Myocardial Infarction STudy of ADenosine (AMISTAD) trial. J Am Coll Cardiol. 1999;34 (6):1711–1720.
  52. Smul TM, Redel A, Stumpner J et al. Time course of desflurane-induced preconditioning in rabbits. J Cardiothorac Vasc Anesth. 2010;24 (1):91–98.
  53. Lavi S, Lavi R. Conditioning of the heart: From pharmacological interventions to local and remote protection. Possible implications for clinical practice. Int J Cardiol. 2011;146 (3):311–318.
  54. Sadigh B, Quintana M, Sylvén C et al. The ischemic preconditio­ning effect of adenosine in patients with ischemic heart disease. Cardiovasc Ultrasound. 2009;7:52.
  55. Sadigh B, Shahgaldi K, Sylvén C et al. Preconditioning effects of adenosine in patients with severe coronary artery disease but preserved coronary flow reserve. Coron Artery Dis. 2009;20 (5):354–359.
  56. McCully JD, Uematsu M, Parker RA, Levitsky S. Adenosine-enhanced ischemic preconditioning provides enhanced cardioprotection in the aged heart. Ann Thorac Surg. 1998;66 (6):2037–2043.
  57. Ватутин Н. Т., Калинкина Н. В., Колесников В. С. Влияние фармакологического прекондиционирования на тяжесть ишемии миокарда у больных со стенокардией. Программа III съезда по медицине неотложных состояний «Острые неотложные состояния в практике врача: диагностика, лечение, профилактика». – 2012. – c. 11.
  58. Мойбенко А. А, Досенко В. Е. Эндогенные механизмы кардиопротекции как основа патогенетической терапии заболеваний сердца. – Киев. 2008. – c. 305–306.
  59. Ватутин Н. Т, Калинкина Н. В, Колесников В. С. Влияние адвокарда на вариабельность сердечного ритма у больных стенокардией напряжения. Приоритетные задачи современной кардиологии и пути их решения: материалы XI съезда кардиологов Юга России. – Ростов-на-Дону. 2012. – c. 22.
  60. Kim HS, Cho JE, Hong SW et al. Remifentanil protects myocardium through activation of anti-apoptotic pathways of survival in ischemia-reperfused rat heart. Physiol Res. 2010;59 (3):347–356.
  61. Xu ZD, Jin M, He WX et al. Remifentanil preconditioning lowers cardiac troponin I levels in patients undergoing off-pump coronary artery bypass graft surgery. Nan Fang Yi Ke Da Xue Xue Bao. 2009;29 (8):1554–1556.
  62. Frässdorf J, Huhn R, Niersmann C et al. Morphine induces preconditioning via activation of mitochondrial K (Ca) channels. Can J Anaesth. 2010;57 (8):767–73.
  63. Li R, Wong GT, Wong TM et al. Intrathecal morphine preconditioning induces cardioprotection via activation of delta, kappa, and mu opioid receptors in rats. Anesth Analg. 2009;108 (1):23–29.
  64. Lu XH, Ran K, Xu JM, Chang YT. Preconditioning of morphine protects rabbit myocardium from ischemia-reperfusion injury. Zhejiang Da Xue Xue Bao Yi Xue Ban. 2009;38 (4):399–403.
  65. Маслов Л. Н, Барзах Е. И, Крылатов А. В и др. Опиоидный пептид дельторфин II имитирует кардиопротекторный эффект ишемического прекондиционирования: роль d2‑опиоидных рецепторов, протеинкиназы С, КАТФ-каналов. Бюллетень экспериментальной биологии и медицины. 2010;5:524.
  66. Sun HT, Xue FS, Liu KP et al. Effect of remifentanil preconditio­ning on myocardial ischemia-reperfusion injury. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2009;31 (5):612–615.
  67. Hu ZY, Liu J. Mechanism of cardiac preconditioning with volatile anesthetics. Anaesth Intensive Care. 2009;37 (4):532–538.
  68. Sepac A, Sedlic F, Si-Tayeb K et al. Isoflurane preconditioning eli­cits competent endogenous mechanisms of protection from oxidative stress in cardiomyocytes derived from human embryonic stem cells. Anesthesiology. 2010;113 (4):906–916.
  69. Zadorozhnyĭ MV, Iavorovskiĭ AG, Ziuliaeva TP et al. [Method of pharmacological myocardial preconditioning with halogen-containing anesthetics in cardiosurgical patients]. Anesteziol Reanimatol. 2008; (5):4–8.
  70. Cohen MV, Yang XM, Liu GS et al. Acetylcholine, bradykinin, opioids and phenylephrine, but not adenosine, trigger preconditioning by generating free radicals and opening mitochondrial KATP channels. Circ Res. 2001;89 (3):273–278.
  71. Zaugg M, Lucchinetti E, Uecker M et al. Anaesthetics and cardiac preconditioning. Part I. Signalling and cytoprotective mechanisms. Br J Anaesth. 2003;91 (4):551–565.
  72. Horinaka S, Yabe A, Yagi H et al. Effects of nicorandil on cardiovascular events in patients with coronary artery disease in the Japanese Coronary Artery Disease (JCAD) study. Circ J. 2010;74 (3):503–509.
  73. Rezkalla SH, Kloner RA. Preconditioning in humans. Heart Fail Rev. 2007;12 (3-4):201–206.
  74. Бадриддинова Л. Ю., Юргель Н. В., Павлова Л. И. и др. Эффективность и безопасность никорандила у больных стабильной стенокардией. Фарматека. 2009;8:65–68.
  75. Barua A, Standen NB, Galiñanes M. Modulation of the nitric oxide metabolism overcomes the unresponsiveness of the diabetic human myocardium to protection against ischemic injury. J Surg Res. 2011;171 (2):452–456.
  76. Lai VK, Galiñanes M. Protection of human myocardium by bone marrow cells: role of long-term administration of the mitochondrial K (ATP) channel opener nicorandil. J Surg Res. 2011;171 (1):66–70.
  77. Wisel S, Khan M, Kuppusamy ML et al. Pharmacological preconditioning of mesenchymal stem cells with trimetazidine (1-[2,3,4‑trimethoxybenzyl] piperazine) protects hypoxic cells against oxidative stress and enhances recovery of myocardial function in infarcted heart through Bcl-2 expression. J Pharmacol Exp Ther. 2009;329 (2):543–550.
  78. Schwartz LM, Reimer KA, Crago MS, Jennings RB. Pharmacological preconditioning with diazoxide slows energy metabolism during sustained ischemia. Exp Clin Cardiol. 2007;12 (3):139–147.
  79. Abdallah Y, Wolf C, Meuter K et al. Preconditioning with diazo­xide prevents reoxygenation-induced rigor-type hypercontracture. J Mol Cell Cardiol. 2010;48 (1):270–276.
  80. Yang J, Jiang H, Yang J et al. Valsartan preconditioning protects against myocardial ischemia-reperfusion injury through TLR4 / NF-kappaB signaling pathway. Mol Cell Biochem. 2009;330 (1-2):39–46.
  81. Meyer K, Schipke JD, Klocke RC et al. Inotropic, vasodilating and preconditioning actions of levosimendan in the heart. Thorac Cardiovasc Surg. 2008;56 (7):379–385.
Vatutin N. T., Kalinkina N. V., Kolesnikov V. S. et al. The phenomenon of preconditioning. Russian Heart Journal. 2013;12(4):199-206

To access this material please log in or register

Register Authorize
Ru En