Skip to main content

Advertisement

SpringerLink
Log in

Opioids as Triggers of the Adaptive Phenomenon of Ischemic Preconditioning of the Heart

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Transient ischemia/reperfusion has been shown to evoke increases in enkephalin levels in myocardial tissue. Blockade of δ opioid receptors eliminates the cardioprotective effect of ischemic preconditioning both in vivo and in vitro. Inhibition of κ1 opioid receptors eliminates the cardioprotective effect of preconditioning only in vitro. Agonists of μ, δ1, δ2, and κ1 opioid receptors imitate the cardioprotective effect of preconditioning. These results indicate that endogenous opioid peptides are triggers of ischemic preconditioning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. T. V. Lasukova, T. Yu. Rebrova, and S. V. Tam, “Activation of μ opiate receptors as a factor in the regulation of the resistance of the heat to exposure to ischemia/reperfusion and oxidative stress,” Byull. Eksperim. Biol. Med., 130, No. 8, 163–167 (2000).

    Google Scholar 

  2. T. B. Lasukova, L. N. Maslov, Yu. B. Lishmanov, et al., “Effects of stimulation of μ opiate receptors on the contractility of isolated rat heart in conditions of normoxia and reperfusion,” Ros. Fiziol. Zh., 85, No. 5, 649–658 (2001).

    Google Scholar 

  3. T. B. Lasukova, L. N. Maslov, Yu. B. Lishmanov, and G. J. Gross, “The role of δ1 opiate in regulating the contractility of isolated rat hearts in conditions of normal oxygenation and ischemia/reperfusion,” Izv. Akad. Nauk Ser Biol., 31, No. 1, 92–99 (2004).

    Google Scholar 

  4. T. B. Lasukova, L. N. Maslov, A. A. Platonov, et al., “The cardioprotective effect of activation of κ1 opioid receptors and the role of cAMP in mediating it,” Byull. Eksperim. Biol. Med., 143, No. 1, 28–31 (2007).

    Google Scholar 

  5. T. B. Lasukova, L. N. Maslov, A. A. Platonov, et al., “The significance of κ1 opioid receptors and cAMP in regulating the resistance of isolated hearts to the actions of ischemia and reperfusion,” Izv. Akad. Nauk Ser Biol., 35, No. 5, 580–588 (2008).

    Google Scholar 

  6. T. B. Lasukova, L. N. Maslov, A. S. Gorbunov, and C. Yu. Tsi bu l’- nikov, “Intracellular mechanisms of the opioidergic regulation of myocardial functions in concentrations of normoxia and postischemic reperfusion,” Ros. Fiziol. Zh., 95, No. 4, 376–386 (2009).

    CAS  Google Scholar 

  7. Yu. B. Lishmanov, L. N. Maslov, S. V. Tam, and S. A. Bogomaz, “The opioid system and the resistance of the heart to damage on ischemia/reperfusion,” Ros. Fiziol. Zh., 86, No. 2, 164–173 (2000).

    CAS  Google Scholar 

  8. Yu. B. Lishmanov, L. N. Maslov, T. V. Lasukova, et al., “Activation of δ opioid receptors increases the resistance of isolated hearts to the actions of ischemia/reperfusion: the role of cAMP and intracellular calcium,” Izv. Ros. Akad. Nauk. Ser. Biol., 32, No. 1, 55–62 (2005).

    Google Scholar 

  9. L. N. Maslov, T. V. Lasukova, N. V. Solenkova, et al., “The role of KATP channels in mediating the cardioprotective actions of mu-opiate receptor agonists in acute ischemia and reperfusion of isolated hearts,” Eksper. Klin. Farmakol., 64, No. 5, 23–27 (2001).

    CAS  Google Scholar 

  10. L. N. Maslov, Yu. B. Lishmanov, J. Calo, and L. Ma, “Central effects of ORL1 receptor ligands,” Eksper. Klin. Farmakol., 66, No. 5, 59–68 (2003).

    CAS  Google Scholar 

  11. L. N. Maslov, A. A. Platonov, T. V. Lasukova, et al., “Activation of δ opioid receptors prevents the appearance of irreversible damage to cardiomyocytes and exacerbates myocardial contractile dysfunction in ischemia/reperfusion,” Pat. Fiziol. Eksper. Ter., No. 4, 13–17 (2006a).

    Google Scholar 

  12. L. N. Maslov, Yu. B. Lishmanov, N. V. Solenkova, “Adaptation of the myocardium to ischemia. First phase of ischemic preconditioning,” Usp. Fiziol. Nauk., 37, No. 3, 25–41 (2006b).

    CAS  PubMed  Google Scholar 

  13. L. N. Maslov, E. I. Barzakh, A. V. Krylatov, et al., “The significance of opioid receptors in regulating the tolerance of the heart to the pathogenic actions of prolonged ischemia/reperfusion in vivo,” Ros. Fiziol. Zh., 95, No. 6, 563–572 (2009).

    CAS  Google Scholar 

  14. L. N. Maslov, N. V. Naryzhnaya, S. Yu. Tsibul’nikov, et al., “The role of opioid receptors and linked intracellular signal cascades in regulating the resistance of the heart to the actions of ischemia and reperfusion (Proc. Russ. Nat. Congr. of Cardiologists, Oct. 11–13, 2011, Moscow),” Kardiovask. Ter. Profi l., 10, No. 6, 200–201 (2011).

    Google Scholar 

  15. L. N. Maslov, P. J. Hedrik, R. Meshoulam, et al., “The role of receptor transactivation in the cardioprotective effects of preconditioning and postconditioning,” Ros. Fiziol. Zh., 98, No. 3, 305–317 (2012).

    CAS  Google Scholar 

  16. L. N. Maslov, L. Hanush, P.-J. Pei, et al., “Signal mechanism for the cardioprotective effects of opioids,” Eksper. Klin. Farmakol., 76, No. 3, 41–48 (2013).

    CAS  Google Scholar 

  17. A. A. Platonov, T. V. Lasukova, L. N. Maslov, et al., “Opioid receptor agonists prevent the appearance of irreversible damage to cardiomyocytes in ischemia/reperfusion of isolated hearts,” Eksper. Klin. Farmakol., 47, No. 6, 26–29 (2004).

    Google Scholar 

  18. E. V. Shlyakhto, E. M. Nifontov, and M. M. Galagudza, “Pre- and postconditioning as means for cardioprotection: pathophysiological and clinical aspects,” Zh. Serdech. Nedostat., 9, No. 1, 4–10 (2008).

    Google Scholar 

  19. K. A. Aitchison, G. F. Baxter, M. M. Awan, et al., “Opposing effects on infarction of delta and kappa opioid receptor activation in the isolated rat heart: implications for ischemic preconditioning,” Basic Res. Cardiol., 95, No. 1, 1–10 (2000).

    Article  CAS  PubMed  Google Scholar 

  20. A. Bilir, N. Erkasap, T. Koken, et al., “Effects of tramadol on myocardial ischemia/reperfusion injury,” Scand. Cardiovasc. J., 41, No. 4, 242–247 (2007).

    Article  CAS  PubMed  Google Scholar 

  21. Z. Cao, L. Liu, and D. M. Van Winkle, “Activation of δ and κ-opioid receptors by opioid peptides protects cardiomyocytes via KATP channels,” Am. J. Physiol. Heart Circ. Physiol., 285, No. 3, H1032–H1039 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. C. M. Cao, M. Chen, and T. M. Wong, “The KCa channel as a trigger for the cardioprotection induced by kappa-opioid receptor stimulation – its relationship with protein kinase C,” Br. J. Pharmacol., 145, No. 7, 984–991 (2005).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Z. Chen, T. Li, and B. Hang, “Morphine postconditioning protects against reperfusion injury in the isolated rat hearts,” J. Surg. Res., 145, No. 2, 287–294 (2008).

    Article  CAS  PubMed  Google Scholar 

  24. G. L. Chien and D. M. Van Winkle, “Naloxone blockade of myocardial ischemic preconditioning is stereoselective,” J. Mol. Cell Cardiol., 28, No. 9, 1895–1900 (1996).

    Article  CAS  PubMed  Google Scholar 

  25. B. N. Dhawan, F. Cesselin, R. Raghubir, et al., “International union of pharmacology. XII. Classification of opioid receptors,” Pharma col. Rev., 48, No. 4, 567–592 (1996).

    CAS  Google Scholar 

  26. P. S. Fischbach, T. D. Barrett, N. J. Reed, and B. R. Lucchesi, “SNC-80-induced preconditioning: selective activation of the mitochondrial adenosine triphosphate-gated potassium channel,” J. Cardiovasc. Pharmacol., 41, No. 5, 744–750 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. R. M. Fryer, A. K. Hsu, H. Nagase, and G. J. Gross, “Opioid-induced cardioprotection against myocardial infarction and arrhythmias: mitochondrial versus sarcolemmal ATP-sensitive potassium channels,” J. Pharmacol. Exp. Ther., 294, No. 2, 451–457 (2000).

    CAS  PubMed  Google Scholar 

  28. M. M. Galagudza, I. O. Blokhin, A. A. Shimonin, and K. A. Mischenko, “Reduction of myocardial ischemia/reperfusion injury with preand postconditioning: molecular mechanisms and therapeutic targets,” Cardiovasc. Hematol. Disord. Drug Targets, 8, No. 1, 47–65 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. E. R. Gross, A. K. Hsu, and G. J. Gross, “The JAK/STAT pathway is essential for opioid-induced cardioprotection: JAK2 as a mediator of STAT3, Akt, and GSK-313,” Am. J. Physiol. Heart Circ. Physiol., 291, No. 2, H827–H834 (2006).

    Article  CAS  PubMed  Google Scholar 

  30. E. R. Gross, A. K. Hsu, and G. J. Gross, “GSK3β inhibition and KATP, channel opening mediate acute opioid-induced cardioprotection at reperfusion,” Basic Res. Cardiol., 102, No. 4, 341–349 (2007).

    Article  CAS  PubMed  Google Scholar 

  31. E. R. Gross, A. K. Hsu, and G. J. Gross, “Acute methadone treatment reduces myocardial infarct size via the δ-opioid receptor in rats during reperfusion,” Anesth. Analg., 109, No. 5, 1395–1402 (2009).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. D. J. Hausenloy and D. M. Yellon, “Preconditioning and postconditioning: united at reperfusion,” Pharmacol. Ther., 116, No. 2, 173–191 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. M. H. Heijna, M. Padt, F. Hogenboom, et al., “Opioid receptor-mediated inhibition of dopamine and acetylcholine release from slices of rat nucleus accumbens, olfactory tubercle and frontal cortex,” Eur. J. Pharmacol., 181, No. 3, 267–278 (1990).

    Article  CAS  PubMed  Google Scholar 

  34. M. H. Huang, V. Nguyen, Y. Wu, et al., “Reducing ischaemia/reperfusion injury through δ-opioid-regulated intrinsic cardiac adrenergic cells: adrenopeptidergic co-signalling,” Cardiovasc. Res., 84, No. 3, 452–460 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. J. Huh, G. J. Gross, H. Nagase, and B. T. Liang, “Protection of cardiac myocytes via δ1-opioid receptors, protein kinase C and mitochondrial KATP channels,” Am. J. Physiol. Heart Circ. Physiol., 280, No. 1, H377–H383 (2001).

    CAS  PubMed  Google Scholar 

  36. Y. Ikeda, T. Miura, J. Sakamoto, et al., “Activation of ERK and suppression of calcineurin are interacting mechanisms of cardioprotection afforded by δ-opioid receptor activation,” Basic Res. Cardiol., 101, No. 5, 418–426 (2006).

    Article  CAS  PubMed  Google Scholar 

  37. M. Karck, S. Tanaka, S. F. Bolling, et al., “Myocardial protection by ischemic preconditioning and delta-opioid receptor activation in the isolated working rat heart,” J. Thorac. Cardiovasc. Surg., 122, No. 5, 986–992 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. W. Kazmierski, W. S. Wire, G. K. Lui, et al., “Design and synthesis of somatostatin analogues with topographical properties that lead to highly potent and specific μ opioid receptor antagonists with greatly reduced binding at somatostatin receptors,” J. Med. Chem., 31, No. 11, 2170–2177 (1988).

    Article  CAS  PubMed  Google Scholar 

  39. E. Kevelaitis, J. Peynet, C. Mouas, et al., “Opening of potassium channels: the common cardioprotective link between preconditioning and natural hibernation?” Circulation, 99, No. 23, 3079–3085 (1999).

    Article  CAS  PubMed  Google Scholar 

  40. H. S. Kim, J. E. Cho, K. C. Hwang, 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., 628, No. 1–3, 132–139 (2010).

    Article  CAS  PubMed  Google Scholar 

  41. I. Kisin, W. Markiewicz, and J. Birkhahn, “Effect of large doses of morphine on experimental myocardial ischemia in cats,” Isr. J. Med. Sci., 15, No. 7, 588–591 (1979).

    CAS  PubMed  Google Scholar 

  42. J. R. Kistner, E. D. Miller, C. L. Lake, and W. T. Ross, “Indices of myocardial oxygenation during coronary-artery revascularization in man with morphine versus halothane anesthesia,” Anesthesiology, 50, No. 4, 324–330 (1979).

    Article  CAS  PubMed  Google Scholar 

  43. H. Kita, T. Miura, A. Tsuchida, et al., “Suppression of reperfusion arrhythmias by preconditioning is inhibited by an ATP-sensitive potassium channel blocker, 5-hydroxydecanoate, but not by protein kinase C blockers in the rat,” J. Cardiovasc. Pharmacol., 32, No. 5, 791–797 (1998).

    Article  CAS  PubMed  Google Scholar 

  44. K. Kuzume, R. A. Wolff, K. Amakawa, et al., “Sustained exogenous administration of Met5-enkephalin protects against infarction in vivo,” Am. J. Physiol. Heart Circ. Physiol., 285, No. 6, H2463–H2470 (2003).

    Article  CAS  PubMed  Google Scholar 

  45. R. A. Lahti, M. M. Mickelson, J. M. McCall, and P. F. Von Voigtlander, “[3H]U-69593 a highly selective ligand for the opioid κ receptor,” Eur. J. Pharmacol., 109, No. 2, 281–284 (1985).

    Article  CAS  PubMed  Google Scholar 

  46. A. Y. Lee and T. M. Wong, “Naloxone reduces release of creatine kinase in the isolated ischemic rat heart,” Proc. Soc. Exp. Biol. Med., 179, No. 2, 219–221 (1985).

    Article  CAS  PubMed  Google Scholar 

  47. B. T. Liang and G. J. Gross, “Direct preconditioning of cardiac myocytes via opioid receptors and KATP channels,” Circ. Res., 84, No. 12, 1396–1400 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Y. Lu, C. Dong, J. Yu, and L. Li, “Role of central and peripheral opioid receptors in the cardioprotection of intravenous morphine preconditioning,” Isr. J. Med. Sci., 180, No. 4, 881–885 (2011).

    Article  CAS  Google Scholar 

  49. W. Markiewicz, J. P. M. Finberg, and C. Lichtig, “Morphine increases myocardial infarct size in rats,” Anesth. Analg., 61, No. 10, 843–846 (1982).

    Article  CAS  PubMed  Google Scholar 

  50. L. N. Maslov, Y. B. Lishmanov, P. R. Oeltgen, et al., “Activation of peripheral δ2-opioid receptors increases cardiac tolerance to ischemia/reperfusion injury. Involvement of protein kinase C, NO-synthase, KATP channels and the autonomic nervous system,” Life Sci., 84, No. 19–20, 657–663 (2009).

    Article  CAS  PubMed  Google Scholar 

  51. L. N. Maslov, Y. B. Lishmanov, P. R. Oeltgen, et al., “Comparative analysis of the cardioprotective properties of opioid receptor agonists in a rat model of myocardial infarction,” Acad. Emerg. Med., 17, No. 11, 1239–1246 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  52. B. C. McPherson and Z. Yao, “Morphine mimics preconditioning via free radical signals and mitochondrial KATP channels in myocytes,” Circulation, 103, No. 2, 290–295 (2001a).

    Article  CAS  PubMed  Google Scholar 

  53. B. C. McPherson and Z. Yao, “Signal transduction of opioid-induced cardioprotection in ischemia/reperfusion,” Anesthesiology, 94, No. 6, 1982–1088 (2001b).

    Article  Google Scholar 

  54. T. Miki, M. V. Cohen, and J. M. Downey, “Opioid receptor contributes to ischemic preconditioning through protein kinase C activation in rabbits,” Mol. Cell. Biochem., 186, No. 1–2, 3–12 (1998).

    Article  CAS  PubMed  Google Scholar 

  55. C. E. Murry, R. B. Jennings, and K. A. Reimer, “Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium,” Circulation, 74, No. 5, 1124–1136 (1986).

    Article  CAS  PubMed  Google Scholar 

  56. F. N. Obame, C. Plin-Mercier, R. Assaly, et al., “Cardioprotective effect of morphine and a blocker of glycogen synthase kinase 3β, SB216763 [3-(2,4-dichlorophenyl)-4 (1-methyl-1H-indo1-3-yl)-1Hpyrrole-2,5-dione], via inhibition of the mitochondrial permeability transition pore,” J. Pharmacol. Exp. Ther., 326, No. 1, 252–258 (2008).

    Article  CAS  PubMed  Google Scholar 

  57. J. N. Peart, H. H. Patel, and G. J. Gross, “Delta-opioid receptor activation mimics ischemic preconditioning in the canine heart,” J. Cardiovasc. Pharmacol., 42, No. 1, 78–81 (2003).

    Article  CAS  PubMed  Google Scholar 

  58. J. N. Peart, E. R. Gross, and G. J. Gross, “Effect of exogenous kappa-opioid receptor activation in rat model of myocardial infarction,” J. Cardiovasc. Pharmacol., 43, No. 3, 410–415 (2004).

    Article  CAS  PubMed  Google Scholar 

  59. J. N. Peart and G. J. Gross, “Exogenous activation of δ- and κ-opioid receptors affords cardioprotection in isolated murine heart,” Basic Res. Cardiol., 99, No. 1, 29–37 (2004).

    Article  CAS  PubMed  Google Scholar 

  60. B. P. Roques, G. Gacel, V. Dauge, et al., “Novel approaches in the development of new analgesics,” Neurophysiol. Clin., 20, No. 5, 369–387 (1990).

    Article  CAS  PubMed  Google Scholar 

  61. R. B. Rotherman, V. Bykov, B. G. Xue, et al., “Interaction of opioid peptides and other drugs with multiple kappa receptors in rat and human brain. Evidence for species differences,” Peptides, 13, No. 5, 977–987 (1992).

    Article  Google Scholar 

  62. C. W. Schindler, Z. Graczyk, J. P. Gilman, et al., “Effects of kappa-opioid agonists alone and in combination with cocaine on heart rate and blood pressure in conscious squirrel monkeys,” Eur. J. Pharmacol., 576, No. 1–3, 107–113 (2007).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. J. E. Schultz, E. Rose, Z. Yao, and G. J. Gross, “Evidence for involvement of opioid receptors in ischemic preconditioning in rat hearts,” Am. J. Physiol., 268, No. 5, Part 2, H2157–H2161 (1995).

  64. J. E. Schultz, A. K. Hsu, and G. J. Gross, “Morphine mimics the cardioprotective effect of ischemic preconditioning via a glibenclamide-sensitive mechanism in the rat heart,” Circ. Res., 78, No. 6, 1100–1104 (1996).

    Article  CAS  PubMed  Google Scholar 

  65. J. J. Schultz, A. K. Hsu, and G. J. Gross, “Ischemic preconditioning is mediated by a peripheral opioid receptor mechanism in the intact rat heart,” J. Mol. Cell. Cardiol., 29, No. 5, 1355–1362 (1997).

    Article  CAS  PubMed  Google Scholar 

  66. J. E. Schultz, A. K. Hsu, and G. J. Gross, “Ischemic preconditioning in the intact rat heart is mediated by δ1- but not μ- or κ-opioid receptors,” Circulation, 97, No. 13, 1282–1289 (1998).

    Article  CAS  PubMed  Google Scholar 

  67. J. J. Schultz, A. K. Hsu, H. Nagase, and G. J. Gross, “TAN-67, a δ1-opioid receptor agonist, reduces infarct size via activation of Gi/o proteins and KATP channels,” Am. J. Physiol., 274, No. 3, Part 2, H909–H914 (1998b).

  68. E. M. Seymour, S. Y. Wu, M. A. Kovach, et al., “HL-1 myocytes exhibit PKC and KATP channel-dependent delta opioid preconditioning,” J. Surg. Res., 114, No. 2, 187–194 (2003).

    Article  CAS  PubMed  Google Scholar 

  69. D. C. Sigg, J. A. Coles, P. R. Oeltgen, and P. A. Iaizzo, “Role of δ-opioid receptor agonists on infarct size reduction in swine,” Am. J. Physiol. Heart Circ. Physiol., 282, No. 6, H1953–H1960 (2002).

    Article  CAS  PubMed  Google Scholar 

  70. Y. Takasaki, R. A. Wolff, G. L. Chien, and D. M. Van Winkle, “Met5-enkephalin protects isolated adult rabbit cardiomyocytes via δ-opioid receptors,” Am. J. Physiol., 277, No. 6, Part 2, H2442–H2450 (1999).

  71. F. Tomai, F. Crea, A. Gaspardone, et al., “Effects of naloxone on myocardial ischemic preconditioning in humans,” J. Am. Coll. Cardiol., 33, No. 7, 1863–1869 (1999).

    Article  CAS  PubMed  Google Scholar 

  72. A. Tsuchida, T. Miura, M. Tanno, et al., “Time window for the contribution of the δ-opioid receptor to cardioprotection by ischemic preconditioning in the rat heart,” Cardiovasc. Drugs Ther., 12, No. 4, 365–373 (1998).

    Article  CAS  PubMed  Google Scholar 

  73. A. Valtchanova-Matchouganska and J. A. Ojewole, “Involvement of opioid delta (δ)- and kappa (κ)-receptors in ischemic preconditioning in a rat model of myocardial infarction,” Methods Find. Exp. Clin. Pharmacol., 24, No. 3, 139–144 (2002).

    Article  CAS  PubMed  Google Scholar 

  74. R. Wagner, P. Piler, H. Bedanova, et al., “Myocardial injury is decreased by late remote ischaemic preconditioning and aggravated by tramadol in patients undergoing cardiac surgery: a randomised controlled trial,” Interact. Cardiovasc. Thorac. Surg., 11, No. 6, 759–762 (2010).

    Article  Google Scholar 

  75. G. Y. Wang, S. Wu, J. M. Pei, et al., “Κ- but not δ-opioid receptors mediate effects of ischemic preconditioning on both infarct and arrhythmia in rats,” Am. J. Physiol. Heart Circ. Physiol., 280, No. 1, H384–H391 (2001).

    CAS  PubMed  Google Scholar 

  76. T. L. Wang, Y. H. Huang, and H. Chang, “Somatostatin analogue mimics acute ischemic preconditioning in a rat model of myocardial infarction,” J. Cardiovasc. Pharmacol., 5, No. 4, 327–332 (2005).

    Article  Google Scholar 

  77. M. J. Watson, J. D. Holt, S. J. O’Neill, et al., “ARD-353 [4-(2R,5S)-4-(R)-(4-diethylcarbamoylphenyl) (3-hydroxyphenyl)methyl)-2,5-dimethylpiperazin-1-ylmethyl)benzoic acid], a novel nonpeptide delta receptor agonist, reduces myocardial infarct size without central effects,” J. Pharmacol. Exp. Ther., 316, No. 1, 423–430 (2006).

    Article  CAS  PubMed  Google Scholar 

  78. G. T. Wong, Z. Huang, S. Ji, and M. G. Irwin, “Remifentanil reduces the release of biochemical markers of myocardial damage after coronary artery bypass surgery: a randomized trial,” J. Cardiothorac. Vasc. Anesth., 24, No. 5, 790–796 (2010).

    Article  CAS  PubMed  Google Scholar 

  79. S. Wu, H. Y. Li, and T. M. Wong, “Cardioprotection of preconditioning by metabolic inhibition in the rat ventricular myocyte. Involvement of κ-opioid receptor,” Circ. Res., 84, No. 12, 1388–1395 (1999).

    Article  CAS  PubMed  Google Scholar 

  80. S. Wu, M. C. Wong, M. Chen, et al., “Role of opioid receptors in cardioprotection of cold-restraint stress and morphine,” J. Biomed. Sci., 11, No. 6, 726–731 (2004).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Institute of Cardiology, Siberian Branch, Russian Academy of Medical Sciences, Tomsk, Russia

    L. N. Maslov, N. V. Naryzhnaya, Yu. K. Podoksenov, A. S. Gorbunov & S. Yu. Tsibul’nikov

  2. Tomsk National Research Polytechnic University, Tomsk, Russia

    L. N. Maslov, N. V. Naryzhnaya & S. Yu. Tsibul’nikov

  3. Republican Scientific-Applied Cardiology Center, Minsk, Belarus

    A. G. Mrochek

Authors
  1. L. N. Maslov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. V. Naryzhnaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu. K. Podoksenov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. G. Mrochek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. S. Gorbunov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Yu. Tsibul’nikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. N. Maslov.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 100, No. 9, pp. 993–1007, September, 2014.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maslov, L.N., Naryzhnaya, N.V., Podoksenov, Y.K. et al. Opioids as Triggers of the Adaptive Phenomenon of Ischemic Preconditioning of the Heart. Neurosci Behav Physi 46, 319–327 (2016). https://doi.org/10.1007/s11055-016-0236-7

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-016-0236-7

Keywords

Search

Navigation