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 Sciences

Volumn 84, Issue 19-20, 2009, Pages 657-663

  Maslov, Leonid N ^a   Lishmanov, Yury B ^a   Oeltgen, Peter R ^b   Barzakh, Eva I ^a   Krylatov, Andrey V ^a   Govindaswami, Meera ^b   Brown, Stephen A ^c  

^a CARDIOLOGY RESEARCH INSTITUTE   (Russian Federation)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Catecholamine; Delta opioid; Deltorphin II; KATP channel; NOS; PKC; Tyrosine kinase

Indexed keywords

17 METHYLNALOXONE; 5 HYDROXYDECANOIC ACID; 7 BENZYLIDENENALTREXONE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CATECHOLAMINE; CHELERYTHRINE; DELTA 2 OPIATE RECEPTOR; DELTA OPIATE RECEPTOR; DELTORPHIN; DELTORPHIN 2; GENISTEIN; GLIBENCLAMIDE; GUANETHIDINE; HEXAMETHONIUM; LEUCINE ENKEPHALIN[2 DEXTRO ALANINE 6 ARGININE]; N(G) NITROARGININE METHYL ESTER; NALTREXONE; NALTRIBEN; NITRIC OXIDE SYNTHASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; 5-HYDROXYDECANOIC ACID; ANTIARRHYTHMIC AGENT; ANTIDIABETIC AGENT; BENZOPHENANTHRIDINE DERIVATIVE; CARDIOTONIC AGENT; DECANOIC ACID DERIVATIVE; DELTORPHIN II, ALA(2); DELTORPHIN II, ALA(2)-; HYDROXYACID; OLIGOPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIARRHYTHMIC ACTIVITY; ARRHYTHMOGENESIS; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; CORONARY REPERFUSION; ENZYME ACTIVATION; ENZYME INHIBITION; HEART ARRHYTHMIA; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MALE; NONHUMAN; RAT; REPERFUSION INJURY; ANIMAL; DRUG ANTAGONISM; HEART MUSCLE; METABOLISM; PATHOLOGY; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; ARRHYTHMIAS, CARDIAC; AUTONOMIC NERVOUS SYSTEM; BENZOPHENANTHRIDINES; CARDIOTONIC AGENTS; DECANOIC ACIDS; GLYBURIDE; HYDROXY ACIDS; HYPOGLYCEMIC AGENTS; KATP CHANNELS; MALE; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NITRIC OXIDE SYNTHASE; OLIGOPEPTIDES; PROTEIN KINASE C; RATS; RATS, WISTAR; RECEPTORS, OPIOID, DELTA;

EID: 65049087438     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2009.02.016     Document Type: Article

References (45)

1. Benowitz NL. Compounds affected cardiovascular system and kidney. Antihypertensive drugs. (Chapter 11). In: Katzung B (Ed) Basic and Clinical Pharmacology, Sixth edition. Prentice-Hall International Inc. 1995; Zvzrtau EE (Ed) Translation from English to Russian, Moscow, Petersburg. Binom, Nevskyi Dialect; Vol 1. pp 192-221, 1998
2. Bilfinger T.V., Vosswinkel J.A., Cadet P., Rialas C.M., Magazine H.I., and Stefano G.B. Direct assessment and diminished production of morphine stimulated NO by diabetic endothelium from saphenous vein. Acta Pharmacologica Sinica 23 2 (2002) 97-102
3. Bilinska M., Maczewski M., and Beresewicz A. Donors of nitric oxide mimic effects of ischaemic preconditioning on reperfusion induced arrhythmias in isolated rat heart. Molecular and Cellular Biochemistry 160-161 1 (1996) 265-271
4. Cadet P., Weeks B.S., Bilfinger T.V., Mantione K.J., Casares F., Stefano G.B., Rialas C.M., Fimiani C., Bilfinger T.V., Salzet M., and Stefano G.B. Endomorphin-1 and -2 inhibit human vascular sympathetic norepinephrine release: lack of interaction with mu 3 opiate receptor subtype. Acta Pharmacologica Sinica 19 5 (1998) 403-407
5. ATP channels. American Journal of Physiology Heart and Circulatory Physiology 285 3 (2003) H1032-H1039
6. Champion H.C., Bivalacqua T.J., Zadina J.E., Kastin A.J., Hyman A.L., and Kadowitz P.J. Role of nitric oxide in mediating vasodilator responses to opioid peptides in the rat. Clinical and Experimental Pharmacology and Physiology 29 3 (2002) 229-232
7. degli Uberti E.C., Ambrosio M.R., Vergnani L., Portaluppi F., Bondanelli M., Trasforini G., Margutti A., and Salvadori S. Stress-induced activation of sympathetic nervous system is attenuated by the δ-opioid receptor agonist deltorphin in healthy man. Journal of Clinical Endocrinology and Metabolism 77 6 (1993) 1490-1494
8. 2-adrenoceptor subtypes in preconditioning against myocardial dysfunction after ischemia and reperfusion. Journal of Cardiovascular Pharmacology 41 3 (2003) 396-405
9. Fryer R.M., Schultz J.E., Hsu A.K., and Gross G.J. Importance of PKC and tyrosine kinase in single or multiple cycles of preconditioning in rat hearts. American Journal of Physiology 276 4 (1999) H1229-H1235
10. Fryer R.M., Hsu A.K., Nagase H., and Gross G.J. Opioid-induced cardioprotection against myocardial infarction and arrhythmias: mitochondrial versus sarcolemmal ATP-sensitive potassium channels. Journal of Pharmacology and Experimental Therapeutics 294 2 (2000) 451-457
11. 1-opioid receptor-induced cardioprotection on a tyrosine kinase-dependent but not a Src-dependent pathway. Journal of Pharmacology and Experimental Therapeutics 299 2 (2001) 477-482
12. Giles T., Sander G., and Merz H. Quaternary opiate antagonists lowered blood pressure and inhibit leucine-enkephalin responses. European Journal of Pharmacology 95 3-4 (1983) 247-252
13. Govindaswami M., Sanchez J.A., Wedge J., Langston M.D., Bishop P.D., Bruce D.S., and Oeltgen P.R. Opioid-like hibernation factors provide protection to the ischemic myocardium. In: Heldmaier G., and Klingenspor M. (Eds). 11th International Hibernation Symposium, Jungholz, Austria, August 13-18, 2000 (2000), Springer Verlag 377-387
14. 2 adrenoceptors. Pain 83 1 (1999) 47-55
15. 1-opioid receptor agonists is mediated by iNOS. American Journal of Physiology Heart and Circulatory Physiology 289 5 (2005) H2251-H2257
16. Hajnal A., Nagy O., Litvai A., Papp J., Parratt J.R., and Vegh A. Nitric oxide involvement in the delayed antiarrhythmic effect of treadmill exercise in dogs. Life Sciences 77 16 (2005) 1960-1971
17. Hoehe M., and Duka T. Opiates increase plasma catecholamines in humans. Psychoneuroendocrinology 18 2 (1993) 141-148
18. ATP channels. Journal of Cardiovascular Electrophysiology 19 3 (2008) 309-315
19. Jiang X., Shi E., Nakajima Y., and Sato S. COX-2 mediates morphine-induced delayed cardioprotection via an iNOS-dependent mechanism. Life Sciences 78 22 (2006) 2543-2549
20. Jones S.P., Greer J.J., Kakkar A.K., Ware P.D., Turnage R.H., Hicks M., van Haperen R., de Crom R., Kawashima S., Yokoyama M., and Lefer D.J. Endothelial nitric oxide synthase overexpression attenuates myocardial reperfusion injury. American Journal of Physiology Heart and Circulatory Physiology 286 1 (2004) H276-H282
21. Kamei J., Saitoh A., Ohsawa M., Suzuki T., Misawa M., Nagase H., and Kasuya Y. Antinociceptive effects of the selective non-peptidic δ-opioid receptor agonist TAN-67 in diabetic mice. European Journal of Pharmacology 276 1-2 (1995) 131-135
22. Kawahara K., Takase M., and Yamauchi Y. Increased vulnerability to ischemia/reperfusion-induced ventricular tachyarrhythmias by pre-ischemic inhibition of nitric oxide synthase in isolated rat hearts. Cardiovascular Pathology 12 1 (2003) 49-56
23. Kobara M., Tatsumi T., Takeda M., Mano A., Yamanaka S., Shiraishi J., Keira N., Matoba S., Asayama J., and Nakagawa M. The dual effects of nitric oxide synthase inhibitors on ischemia-reperfusion injury in rat hearts. Basic Research in Cardiology 98 5 (2003) 319-328
24. Krieg T., Qin Q., Philipp S., Alexeyev M.F., Cohen M.V., and Downey J.M. Acetylcholine and bradykinin trigger preconditioning in the heart through a pathway that includes Akt and NOS. American Journal of Physiology Heart and Circulatory Physiology 287 6 (2004) H2606-H2611
25. Lishmanov Y.B., Uskina E.V., Krylatov A.V., Kondratiev B.Y., Ugdyzhekova D.S., and Maslov L.N. A modulated effect of endogenous opioids on antiarrhythmic effect of hypoxic adaptation. Russian Journal of Physiology 84 4 (1998) 363-372
26. Maslov L.N., and Lishmanov Y.B. Role of central and peripheral mu- and delta-opiate receptors in mechanisms of the antiarrhythmic action of enkephalins. Bulletin of Experimental Biology and Medicine 112 2 (1991) 1066-1068
27. Maslov L.N., and Lishmanov Y.B. The anti-arrhythmic effect of d-Ala2,Leu5,Arg6-enkephalin and its possible mechanism. International Journal of Cardiology 40 2 (1993) 89-94
28. + channels. Life Science 73 7 (2003) 947-952
29. 2]deltorphin II in mice: evidence for delta receptor subtypes. Journal of Pharmacology and Experimental Therapeutics 258 2 (1991) 583-587
30. Patel H.H., Hsu A.K., and Gross G.J. COX-2 and iNOS in opioid-induced delayed cardioprotection in the intact rat. Life Sciences 75 2 (2004) 129-140
31. Rimoy G.H., Wright D.M., Bhaskar N.K., and Rubin P.C. The cardiovascular and central nervous system effects in the human of U-62066E. A selective opioid receptor agonist. European Journal of Clinical Pharmacology 46 3 (1994) 203-207
32. Russell D.C., Lawrie J.S., Riemersma R.A., and Oliver M.F. Mechanisms of phase 1a and 1b early ventricular arrhythmias during acute myocardial ischemia in the dog. American Journal of Cardiology 53 2 (1984) 307-312
33. Saini V., Carr D.B., Hagestad E.L., Lown B., and Verrier R.L. Antifibrillatory action of the narcotic agonist fentanyl. American Heart Journal 115 3 (1988) 598-605
34. Sander G.E., Lowe R.F., Given M.B., and Giles T.D. Interactions between circulating peptides and the central nervous system in hemodynamic regulation. American Journal of Cardiology 64 6 (1989) 44C-50C
35. Schultz J.E., Hsu A.K., and Gross G.J. Morphine mimics the cardioprotective effect of ischemic preconditioning via a glibenclamide-sensitive mechanism in the rat heart. Circulation Research 78 6 (1996) 1100-1104
36. Schultz J.E., Yao Z., Cavero I., and Gross G.J. Glibenclamide induced blockade of ischemic preconditioning is time dependent in intact rat heart. American Journal of Physiology 272 6 (1997) H2607-H2615
37. 1- but not μ- or κ-opioid receptors. Circulation 97 13 (1998) 1282-1289
38. ATP channels. American Journal of Physiology 274 3 Pt 2 (1998) H909-H914
39. Sharp B.R., Jones S.P., Rimmer D.M., and Lefer D.J. Differential response to myocardial reperfusion injury in eNOS-deficient mice. American Journal of Physiology Heart and Circulatory Physiology 282 6 (2002) H2422-H2426
40. Sigg D.C., Coles J.A., Oeltgen P.R., and Iaizzo P.A. Role of δ-opioid receptor agonists on infarct size reduction in swine. American Journal of Physiology. Heart and Circulatory Physiology 282 6 (2002) H1953-H1960
41. 1 opioid receptor antagonist in the mouse spinal cord. Life Sciences 52 8 (1993) 769-775
42. Szabo B., Hedler L., Ensinger H., and Starke K. Opioid peptides decrease noradrenaline release and blood pressure in the rabbit at peripheral receptors. Naunyn-Schmiedeberg's Archives of Pharmacology 332 1 (1986) 50-56
43. 1A receptors. British Journal of Pharmacology 139 8 (2003) 1498-1504
44. Vegh A., and Parratt J.R. Noradrenaline, infused locally, reduces arrhythmia severity during coronary artery occlusion in anaesthetised dogs. Cardiovascular Research 55 1 (2002) 53-63
45. Watson M.J., Holt J.D., O'Neill S.J., Wei K., Pendergast W., Gross G.J., Gengo P.J., and Chang K.J. ARD-353 [4-((2R,5S)-4-(R)-(4-diethylcarbamoylphenyl)(3-hydroxyphenyl) methyl)-2,5-dimethyl-piperazin-1-ylmethyl)benzoic acid], a novel nonpeptide delta receptor agonist, reduces myocardial infarct size without central effects. Journal of Pharmacology and Experimental Therapeutics 316 1 (2006) 423-430