Interaction of δ and κ opioid receptors with adenosine A1 receptors mediates cardioprotection by remote ischemic preconditioning

Journal of Molecular and Cellular Cardiology

Volumn 60, Issue 1, 2013, Pages 142-150

  Surendra, Harinee ^a,b,c   Diaz, Roberto J ^a,b   Harvey, Kordan ^a,b,c   Tropak, Michael ^b   Callahan, John ^b   Hinek, Alina ^a,b   Hossain, Taneya ^a,b   Redington, Andrew ^b   Wilson, Gregory J ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Adenosine receptors; Cardiomyocytes; Opioid receptors; Remote ischemic preconditioning

Indexed keywords

ADENOSINE A1 RECEPTOR; ADENOSINE A1 RECEPTOR ANTAGONIST; ADENOSINE A3 RECEPTOR; ADENOSINE A3 RECEPTOR ANTAGONIST; DELTA OPIATE RECEPTOR; HEMAGGLUTININ; KAPPA OPIATE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOCKING FACTOR; CELL ISOLATION; CELL LYSATE; CELL PROTECTION; CELL STRAIN HEK293; CONTROLLED STUDY; DIALYSATE LEVEL; HEART MUSCLE CELL; HEART PROTECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; ISCHEMIC PRECONDITIONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; REMOTE ISCHEMIC PRECONDITIONING; REPERFUSION INJURY;

ADENOSINE A1 RECEPTOR ANTAGONISTS; ANIMALS; HEK293 CELLS; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCYTES, CARDIAC; RABBITS; RECEPTOR, ADENOSINE A1; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, KAPPA;

HARNESS; ORYCTOLAGUS CUNICULUS;

EID: 84877835896     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.04.010     Document Type: Article

References (48)

1. Przyklenk K., Bauer B., Ovize M., Kloner R.A., Whittaker P. Regional ischemic 'preconditioning' protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 1993, 87(3):893-899.
2. Pell T.J., Baxter G.F., Yellon D.M., Drew G.M. Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels. Am J Physiol 1998, 275(5 Pt 2):H1542-H1547.
3. Takaoka A., Nakae I., Mitsunami K., Yabe T., Morikawa S., Inubushi T., et al. Renal ischemia/reperfusion remotely improves myocardial energy metabolism during myocardial ischemia via adenosine receptors in rabbits: effects of "remote preconditioning". J Am Coll Cardiol 1999, 33(2):556-564.
4. Shimizu M., Tropak M., Diaz R.J., Suto F., Surendra H., Kuzmin E., et al. Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci (Lond) 2009, 117(5):191-200.
5. Schmidt M.R., Smerup M., Konstantinov I.E., Shimizu M., Li J., Cheung M., et al. Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATP-dependent mechanism: first demonstration of remote ischemic perconditioning. Am J Physiol Heart Circ Physiol 2007, 292(4):H1883-H1890.
6. Kharbanda R.K., Mortensen U.M., White P.A., Kristiansen S.B., Schmidt M.R., Hoschtitzky J.A., et al. Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 2002, 106(23):2881-2883.
7. Gho B.C., Schoemaker R.G., van den Doel M.A., Duncker D.J., Verdouw P.D. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 1996, 94(9):2193-2200.
8. Liem D.A., Verdouw P.D., Ploeg H., Kazim S., Duncker D.J. Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol Heart Circ Physiol 2002, 283(1):H29-H37.
9. Wolfrum S., Schneider K., Heidbreder M., Nienstedt J., Dominiak P., Dendorfer A. Remote preconditioning protects the heart by activating myocardial PKCepsilon-isoform. Cardiovasc Res 2002, 55(3):583-589.
10. Marczak J., Nowicki R., Kulbacka J., Saczko J. Is remote ischaemic preconditioning of benefit to patients undergoing cardiac surgery?. Interact Cardiovasc Thorac Surg 2012, 14(5):634-639.
11. Botker H.E., Kharbanda R., Schmidt M.R., Bottcher M., Kaltoft A.K., Terkelsen C.J., et al. Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet 2010, 375(9716):727-734.
12. Hoole S.P., Heck P.M., Sharples L., Khan S.N., Duehmke R., Densem C.G., et al. Cardiac remote ischemic preconditioning in coronary stenting (CRISP stent) study: a prospective, randomized control trial. Circulation 2009, 119(6):820-827.
13. Rentoukas I., Giannopoulos G., Kaoukis A., Kossyvakis C., Raisakis K., Driva M., et al. Cardioprotective role of remote ischemic periconditioning in primary percutaneous coronary intervention: enhancement by opioid action. JACC Cardiovasc Interv 2010, 3(1):49-55.
14. Venugopal V., Laing C.M., Ludman A., Yellon D.M., Hausenloy D. Effect of remote ischemic preconditioning on acute kidney injury in nondiabetic patients undergoing coronary artery bypass graft surgery: a secondary analysis of 2 small randomized trials. Am J Kidney Dis 2010, 56(6):1043-1049.
15. Hausenloy D.J., Mwamure P.K., Venugopal V., Harris J., Barnard M., Grundy E., et al. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 2007, 370(9587):575-579.
16. Cheung M.M., Kharbanda R.K., Konstantinov I.E., Shimizu M., Frndova H., Li J., et al. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 2006, 47(11):2277-2282.
17. Steensrud T., Li J., Dai X., Manlhiot C., Kharbanda R.K., Tropak M., et al. Pretreatment with the nitric oxide donor SNAP or nerve transection blocks humoral preconditioning by remote limb ischemia or intra-arterial adenosine. Am J Physiol Heart Circ Physiol 2010, 299(5):H1598-H1603.
18. Konstantinov I.E., Li J., Cheung M.M., Shimizu M., Stokoe J., Kharbanda R.K., et al. Remote ischemic preconditioning of the recipient reduces myocardial ischemia-reperfusion injury of the denervated donor heart via a Katp channel-dependent mechanism. Transplantation 2005, 79(12):1691-1695.
19. Diaz R.J., Wilson G.J. Studying ischemic preconditioning in isolated cardiomyocyte models. Cardiovasc Res 2006, 70(2):286-296.
20. Yang X., Cohen M.V., Downey J.M. Mechanism of cardioprotection by early ischemic preconditioning. Cardiovasc Drugs Ther 2010, 24(3):225-234.
21. Yao L., Wong G.T., Xia Z., Irwin M.G. Interaction between spinal opioid and adenosine receptors in remote cardiac preconditioning: effect of intrathecal morphine. J Cardiothorac Vasc Anesth 2011, 25(3):444-448.
22. Peart J.N., Gross G.J. Adenosine and opioid receptor-mediated cardioprotection in the rat: evidence for cross-talk between receptors. Am J Physiol Heart Circ Physiol 2003, 285(1):H81-H89.
23. George S.R., O'Dowd B.F., Lee S.P. G-protein-coupled receptor oligomerization and its potential for drug discovery. Nat Rev Drug Discov 2002, 1(10):808-820.
24. Juhasz J.R., Hasbi A., Rashid A.J., So C.H., George S.R., O'Dowd B.F. Mu-opioid receptor heterooligomer formation with the dopamine D1 receptor as directly visualized in living cells. Eur J Pharmacol 2008, 581(3):235-243.
25. Levac B.A., O'Dowd B.F., George S.R. Oligomerization of opioid receptors: generation of novel signaling units. Curr Opin Pharmacol 2002, 2(1):76-81.
26. Wang D., Sun X., Bohn L.M., Sadee W. Opioid receptor homo- and heterodimerization in living cells by quantitative bioluminescence resonance energy transfer. Mol Pharmacol 2005, 67(6):2173-2184.
27. Diaz R.J., Armstrong S.C., Batthish M., Backx P.H., Ganote C.E., Wilson G.J. Enhanced cell volume regulation: a key protective mechanism of ischemic preconditioning in rabbit ventricular myocytes. J Mol Cell Cardiol 2003, 35(1):45-58.
28. Diaz R.J., Losito V.A., Mao G.D., Ford M.K., Backx P.H., Wilson G.J. Chloride channel inhibition blocks the protection of ischemic preconditioning and hypo-osmotic stress in rabbit ventricular myocardium. Circ Res 1999, 84(7):763-775.
29. Jordan B.A., Devi L.A. G-protein-coupled receptor heterodimerization modulates receptor function. Nature 1999, 399(6737):697-700.
30. Jordan B.A., Trapaidze N., Gomes I., Nivarthi R., Devi L.A. Oligomerization of opioid receptors with beta 2-adrenergic receptors: a role in trafficking and mitogen-activated protein kinase activation. Proc Natl Acad Sci U S A 2001, 98(1):343-348.
31. Halimi G., Devaux C., Clot-Faybesse O., Sampol J., Legof L., Rochat H., et al. Modulation of adenosine concentration by opioid receptor agonists in rat striatum. Eur J Pharmacol 2000, 398(2):217-224.
32. Schultz J.E., Rose E., Yao Z., Gross G.J. Evidence for involvement of opioid receptors in ischemic preconditioning in rat hearts. Am J Physiol 1995, 268(5 Pt 2):H2157-H2161.
33. Miki T., Cohen M.V., Downey J.M. Opioid receptor contributes to ischemic preconditioning through protein kinase C activation in rabbits. Mol Cell Biochem 1998, 186(1-2):3-12.
34. Takasaki Y., Wolff R.A., Chien G.L., van Winkle D.M. Met5-enkephalin protects isolated adult rabbit cardiomyocytes via delta-opioid receptors. Am J Physiol 1999, 277(6 Pt 2):H2442-H2450.
35. Cao Z., Liu L., Van Winkle D.M. Activation of delta- and kappa-opioid receptors by opioid peptides protects cardiomyocytes via KATP channels. Am J Physiol Heart Circ Physiol 2003, 285(3):H1032-H1039.
36. Dickson E.W., Tubbs R.J., Porcaro W.A., Lee W.J., Blehar D.J., Carraway R.E., et al. Myocardial preconditioning factors evoke mesenteric ischemic tolerance via opioid receptors and K(ATP) channels. Am J Physiol Heart Circ Physiol 2002, 283(1):H22-H28.
37. Weinbrenner C., Schulze F., Sarvary L., Strasser R.H. Remote preconditioning by infrarenal aortic occlusion is operative via delta1-opioid receptors and free radicals in vivo in the rat heart. Cardiovasc Res 2004, 61(3):591-599.
38. Zhang S.Z., Wang N.F., Xu J., Gao Q., Lin G.H., Bruce I.C., et al. Kappa-opioid receptors mediate cardioprotection by remote preconditioning. Anesthesiology 2006, 105(3):550-556.
39. Cvejic S., Devi L.A. Dimerization of the delta opioid receptor: implication for a role in receptor internalization. J Biol Chem 1997, 272(43):26959-26964.
40. Gines S., Hillion J., Torvinen M., Le Crom S., Casado V., Canela E.I., et al. Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexes. Proc Natl Acad Sci U S A 2000, 97(15):8606-8611.
41. Milligan G., Bouvier M. Methods to monitor the quaternary structure of G protein-coupled receptors. FEBS J 2005, 272(12):2914-2925.
42. Lleres D., Swift S., Lamond A.I. Detecting protein-protein interactions in vivo with FRET using multiphoton fluorescence lifetime imaging microscopy (FLIM). Curr Protoc Cytom 2007, 12:1-19. (Chapter 12: Unit12.10).
43. Lasley R.D. Adenosine receptors and membrane microdomains. Biochim Biophys Acta 2011, 1808(5):1284-1289.
44. Lasley R.D., Narayan P., Uittenbogaard A., Smart E.J. Activated cardiac adenosine A(1) receptors translocate out of caveolae. J Biol Chem 2000, 275(6):4417-4421.
45. Manintveld O.C., te Lintel Hekkert M., Keijzer E., Verdouw P.D., Duncker D.J. Intravenous adenosine protects the myocardium primarily by activation of a neurogenic pathway. Br J Pharmacol 2005, 145(6):703-711.
46. Singh D., Chopra K. Evidence of the role of angiotensin AT(1) receptors in remote renal preconditioning of myocardium. Methods Find Exp Clin Pharmacol 2004, 26(2):117-122.
47. Hajrasouliha A.R., Tavakoli S., Ghasemi M., Jabehdar-Maralani P., Sadeghipour H., Ebrahimi F., et al. Endogenous cannabinoids contribute to remote ischemic preconditioning via cannabinoid CB2 receptors in the rat heart. Eur J Pharmacol 2008, 579(1-3):246-252.
48. Ling Ling J., Wong G.T., Yao L., Xia Z., Irwin M.G. Remote pharmacological post-conditioning by intrathecal morphine: cardiac protection from spinal opioid receptor activation. Acta Anaesthesiol Scand 2010, 54(9):1097-1104.