Evidence that cardioprotection by postconditioning involves preservation of myocardial opioid content and selective opioid receptor activation

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 3, 2008, Pages

  Zatta, Amanda J ^a   Kin, Hajime ^a   Yoshishige, Darice ^b   Jiang, Rong ^a   Wang, Ningping ^a   Reeves, James G ^a   Mykytenko, James ^a   Guyton, Robert A ^a   Zhao, Zhi Qing ^a   Caffrey, James L ^b   Vinten Johansen, Jakob ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Myocardial enkephalins; Opioid receptor activation; Postconditioning; Reperfusion injury

Indexed keywords

17 METHYLNALOXONE; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLARGINYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENKEPHALIN; METENKEPHALIN; METENKEPHALIN[6 ARGININE 7 PHENYLALANINE]; METHYL IODIDE; NALOXONE; NALTRINDOLE; NORBINALTORPHIMINE; OPIATE; OPIATE RECEPTOR; PEPTIDE B; PROENKEPHALIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; HEART INFARCTION SIZE; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PRESERVATION; HEART PROTECTION; MALE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIOIMMUNOASSAY; RAT;

ANALGESICS, OPIOID; ANIMALS; ENDORPHINS; ENKEPHALINS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MYOCARDIAL INFARCTION; MYOCARDIUM; NALTREXONE; NOREPINEPHRINE; PEPTIDES; PROTEIN PRECURSORS; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; RECEPTORS, OPIOID, DELTA;

EID: 41549140030     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01279.2006     Document Type: Article

References (45)

1. Argaud L, Gateau-Roesch O, Raisky O, Loufouat J, Robert D, Ovize M. Postconditioning inhibits mitochondrial permeability transition. Circulation 111: 194-197, 2005.
2. Barron BA, Gu H, Gaugl JF, Caffrey JL. Screening for opioids in dog heart. J Mol Cell Cardiol 24: 67-77, 1992.
3. Bopassa JC, Ferrera R, Gateau-Roesch O, Couture-Lepetit E, Ovize M. PI 3-kinase regulates the mitochondrial transition pore in controlled reperfusion and postconditioning. Cardiovasc Res 69: 178-185, 2006.
4. Chang WL, Lee SS, Su MJ. Attenuation of post-ischemia reperfusion injury by thaliporphine and morphine in rat hearts. J Biomed Sci 12: 611-619, 2005.
5. Chiari PC, Bienengraeber M, Pagel PS, Krolikowski JG, Kersten JR, Warltier DC. Isoflurane protects against myocardial infarction during early reperfusion by activation of phosphatidylinositol-3-kinase signal transduction: evidence for anesthetic-induced postconditioning in rabbits. Anesthesiology 102: 102-109, 2005.
6. Cohen MV, Baines CP, Downey JM. Ischemic preconditioning: from adenosine receptor to KATP channel. Ann Rev Physiol 62: 79-109, 2000.
7. Coles JA Jr, Sigg DC, Iaizzo PA. Role of kappa -opioid receptor activation in pharmacological preconditioning of swine. Am J Physiol Heart Circ Physiol 284: H2091-H2099, 2003.
8. Darling CE, Jiang R, Maynard M, Whittaker P, Vinten-Johansen J, Przyklenk K. Postconditioning via stuttering reperfusion limits myocardial infarct size in rabbit hearts: role of ERK1/2. Am J Physiol Heart Circ Physiol 289: H1618-H1626, 2005.
9. Forster K, Kuno A, Solenkova N, Felix SB, Krieg T. The δ-opioid receptor agonist DADLE at reperfusion protects the heart through activation of pro-survival kinases via EGF receptor transactivation. Am J Physiol Heart Circ Physiol 293: H1604-H1608, 2007.
10. Fryer RM, Wang Y, Hsu AK, Gross GJ. Essential activation of PKC-δ in opioid-initiated cardioprotection. Am J Physiol Heart Circ Physiol 280: H1346-H1353, 2001.
11. Gross ER, Gross GJ. Ligand triggers of classical preconditioning and postconditioning. Cardiovasc Res 70: 212-221, 2006.
12. Gross ER, Hsu AK, Gross GJ. Acute aspirin treatment abolishes, whereas acute ibuprofen treatment enhances morphine-induced cardioprotection: role of 12-lipoxygenase. J Pharmacol Exp Ther 310: 185-191, 2004.
13. Gross ER, Hsu AK, Gross GJ. Opioid-induced cardioprotection occurs via glycogen synthase kinase β inhibition during reperfusion in intact rat hearts. Circ Res 94: 960-966, 2004.
14. Gross ER, Peart JN, Hsu AK, Auchampach JA, Gross GJ. Extending the cardioprotective window using a novel δ-opioid agonist fentanyl isothiocyanate via the PI3-kinase pathway. Am J Physiol Heart Circ Physiol 288: H2744-H2749, 2005.
15. Gross GJ. Role of opioids in acute and delayed preconditioning. J Mol Cell Cardiol 35: 709-718, 2003.
16. Hausenloy DJ, Tsang A, Yellon DM. The reperfusion injury salvage kinase pathway: a common target for both ischemic preconditioning and postconditioning. Trends Cardiovasc Med 15: 69-75, 2005.
17. Head BP, Patel HH, Roth DM, Lai NC, Niesman IR, Farquhar MG, Insel PA. G-protein-coupled receptor signaling components localize in both sarcolemmal and intracellular caveolin-3-associated microdomains in adult cardiac myocytes. J Biol Chem 280: 31036-31044, 2005.
18. Karck M, Tanaka S, Bolling SF, Simon A, Su TP, Oeltgen PR, Haverich A. Myocardial protection by ischemic preconditioning and δ-opioid receptor activation in the isolated working rat heart. J Thorac Cardiovasc Surg 122: 986-992, 2001.
19. Kin H, Zatta AJ, Lofye MT, Amerson BS, Halkos ME, Kerendi F, Zhao ZQ, Guyton RA, Headrick JP, Vinten-Johansen J. Postconditioning reduces infarct size via adenosine receptor activation by endogenous adenosine. Cardiovasc Res 67: 124-133, 2005.
20. Kin H, Zhao ZQ, Sun HY, Wang NP, Corvera JS, Halkos ME, Kerendi F, Guyton RA, Vinten-Johansen J. Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 62: 74-85, 2004.
21. Li JG, Raffa RB, Cheung P, Tzeng TB, Liu-Chen LY. Apparent thermodynamic parameters of ligand binding to the cloned rat μ-opioid receptor. Eur J Pharmacol 354: 227-237, 1998.
22. Magnan J, Paterson S, Tavani A, Kosterlitz H. The binding spectrum of narcotic analgesic drugs with different agonist and antagonist properties. Naunyn Schmiedebergs Arch Pharmacol 319: 197-205, 1982.
23. Miki T, Cohen MV, Downey JM. Opioid receptor contributes to ischemic preconditioning through protein kinase C activation in rabbits. Mol Cell Biochem 186: 3-12, 1998.
24. Miller L, Shaw JS, Whiting EM. The contribution of intrinsic activity to the action of opioids in vitro. Br J Pharmacol 87: 595-601, 1986.
25. Mykytenko J, Reeves JG, Kin H, Zatta AJ, Jiang R, Guyton RA, Vinten-Johansen J. Postconditioning reduces myocardial infarct size via mitochondrial KATP Channel activation during 24 hours of reperfusion (Abstract). J Mol Cell Cardiol 38: 830, 2005.
26. Okubo S, Tanabe Y, Takeda K, Kitayama M, Kanemitsu S, Kukreja RC, Takekoshi N. Ischemic preconditioning and morphine attenuate myocardial apoptosis and infarction after ischemia-reperfusion in rabbits: role of δ-opioid receptor. Am J Physiol Heart Circ Physiol 287: H1786-H1791, 2004.
27. Pagel PS, Krolikowski JG, Neff DA, Weihrauch D, Bienengraeber M, Kersten JR, Warltier DC. Inhibition of glycogen synthase kinase enhances isoflurane-induced protection against myocardial infarction during early reperfusion in vivo. Anesth Analg 102: 1348-1354, 2006.
28. Peart JN, Gross ER, Gross GJ. Effect of exogenous kappa-opioid receptor activation in rat model of myocardial infarction. J Cardiovasc Pharmacol 43: 410-415, 2004.
29. Peart J, Gross G. Exogenous activation of delta- and kappa-opioid receptors affords cardioprotection in isolated murine heart. Basic Res Cardiol 99: 29-37, 2004.
30. Penna C, Rastaldo R, Mancardi D, Raimondo S, Cappello S, Gattullo D, Losano G, Pagliaro P. Postconditioning induced cardioprotection requires signaling through a redoxsensitive mechanism, mitochondrial ATP sensitive K+ channel and protein kinase C activation. Basic Res Cardiol 101: 180-189, 2006.
31. Philipp S, Yang XM, Cui L, Davis AM, Downey JM, Cohen MV. Postconditioning protects rabbit hearts through a protein kinase C-adenosine A2b receptor cascade. Cardiovasc Res 70: 308-314, 2006.
32. Romano MA, McNish R, Seymour EM, Traynor JR, Bolling SF. Differential effects of opioid peptides on myocardial ischemic tolerance. J Surg Res 119: 46-50, 2004.
33. Schultz JE, Hsu AK, Gross GJ. Ischemic preconditioning in the intact rat heart is mediated by δ- but not μ- or κ-opioid receptors. Circulation 97: 1282-1289, 1998.
34. Schultz JJ, Hsu AK, Gross GJ. Ischemic preconditioning and morphine-induced cardioprotection involve the delta (δ)-opioid receptor in the intact rat heart. J Mol Cell Cardiol 29: 2187-2195, 1997.
35. Schultz JJ, Hsu AK, Gross GJ. Ischemic preconditioning is mediated by a peripheral opioid receptor mechanism in the intact rat heart. J Mol Cell Cardiol 29: 1355-1362, 1997.
36. Tillack D, Reubner C, Strasser RH, Weinbrenner C. Postconditioning the in vivo rat heart reduces myocardial injury through a PI3K- and mTOR-dependent pathway which involves the activation of GSK3beta (Abstract). J Mol Cell Cardiol 40: 971, 2006.
37. Tsang A, Hausenloy DJ, Mocanu MM, Yellon DM. Postconditioning: a form of "modified reperfusion" protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res 95: 230-232, 2004.
38. Vinten-Johansen J, Zhao ZQ, Jiang R, Zatta AJ. Myocardial protection in reperfusion with postconditioning. Expert Rev Cardiovasc Ther 3: 1035-1045, 2005.
39. Wang GY, Wu S, Pei JM, Yu XC, Wong TM. 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: H384-H391, 2001.
40. Weihrauch D, Krolikowski JG, Bienengraeber M, Kersten JR, Warltier DC, Pagel PS. Morphine enhances isoflurane-induced postconditioning against myocardial infarction: the role of phosphatidylinositol-3-kinase and opioid receptors in rabbits. Anesth Analg 101: 942-949, 2005.
41. Yang XM, Philipp S, Downey JM, Cohen MV. Postconditionings protection is not dependent on circulating blood factors or cells but involves adenosine receptors and requires PI3kinase and guanylyl cyclase activation. Basic Res Cardiol 100: 57-63, 2005.
42. Younes A, Pepe S, Barron BA, Spurgeon HA, Lakatta EG, Caffrey JL. Cardiac synthesis, processing, and coronary release of enkephalin-related peptides. Am J Physiol Heart Circ Physiol 279: H1989-H1998, 2000.
43. Younes A, Pepe S, Yoshishige D, Caffrey JL, Lakatta EG. Ischemic preconditioning increases the bioavailability of cardiac enkephalins. Am J Physiol Heart Circ Physiol 289: H1652-H1661, 2005.
44. Zatta AJ, Kin H, Lee G, Wang N, Jiang R, Lust R, Reeves JG, Mykytenko J, Guyton RA, Zhao ZQ, Vinten-Johansen J. Infarct-sparing effect of myocardial postconditioning is dependent on protein kinase C signalling. Cardiovasc Res 70: 315-324, 2006.
45. Zhou JJ, Bian JS, Pei JM, Wu S, Li HY, Wong TM. Role of protein kinase C-epsilon in the development of κ-opioid receptor tolerance to U50,488H in rat ventricular myocytes. Br J Pharmacol 135: 1675-1684, 2002.