Remote cardioprotection by transfer of coronary effluent from ischemic preconditioned rabbit heart preserves mitochondrial integrity and function via adenosine receptor activation

Cardiovascular Drugs and Therapy

Volumn 28, Issue 1, 2014, Pages 7-17

  Leung, Chung Ho ^a   Wang, Lixing ^a   Nielsen, Jan M ^b   Tropak, Michael B ^a   Fu, Yana Y ^a   Kato, Hideyuki ^a   Callahan, John ^a   Redington, Andrew N ^a   Caldarone, Christopher A ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Adenosine; Cardioprotection; Ischemia reperfusion injury; Ischemic preconditioning; Mitochondria; Remote ischemic preconditioning

Indexed keywords

ADENOSINE; ANIMALS; DISEASE MODELS, ANIMAL; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MITOCHONDRIA; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; RABBITS; REACTIVE OXYGEN SPECIES; RECEPTORS, PURINERGIC P1; THEOPHYLLINE;

EID: 84896761871     PISSN: 09203206     EISSN: 15737241     Source Type: Journal    
DOI: 10.1007/s10557-013-6489-2     Document Type: Article

References (49)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124-36. (Pubitemid 17174962)
2. Oxman T, Arad M, Klein R, Avazov N, Rabinowitz B. Limb ischemia preconditions the heart against reperfusion tachyarrhythmia. Am J Physiol. 1997;273(4 Pt 2):H1707-12.
3. Pell TJ, Baxter GF, Yellon DM, Drew GM. Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels. Am J Physiol. 1998;275(5 Pt 2):H1542-7.
4. Konstantinov IE, Li J, Cheung MM, Shimizu M, Stokoe J, Kharbanda RK, 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):1691-5. (Pubitemid 40885266)
5. Yang X, Cohen MV, Downey JM. Mechanism of cardioprotection by early ischemic preconditioning. Cardiovasc Drugs Ther. 2010;24(3):225-34.
6. Shimizu M, Tropak M, Diaz RJ, 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.
7. Wang L, Oka N, Tropak M, Callahan J, Lee J, Wilson G, et al. Remote ischemic preconditioning elaborates a transferable blood-borne effector that protects mitochondrial structure and function and preserves myocardial performance after neonatal cardioplegic arrest. J Thorac Cardiovasc Surg. 2008;136(2):335-42.
8. Dickson EW, Lorbar M, Porcaro WA, Fenton RA, Reinhardt CP, Gysembergh A, et al. Rabbit heart can be "preconditioned" via transfer of coronary effluent. Am J Physiol. 1999;277(6 Pt 2):H2451-7. (Pubitemid 30048169)
9. Serejo FC, Rodrigues Jr LF, da Silva Tavares KC, de Carvalho AC, Nascimento JH. Cardioprotective properties of humoral factors released from rat hearts subject to ischemic preconditioning. J Cardiovasc Pharmacol. 2007;49(4):214-20. (Pubitemid 46626013)
10. Breivik L, Helgeland E, Aarnes EK, Mrdalj J, Jonassen AK. Remote postconditioning by humoral factors in effluent from ischemic preconditioned rat hearts is mediated via PI3K/Akt-dependent cell-survival signaling at reperfusion. Basic Res Cardiol. 2010;106(1):135-45.
11. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ. Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol. 2008;294(2):C460-6. (Pubitemid 351276913)
12. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem. 2003;278(38):36027-31. (Pubitemid 37139922)
13. Borutaite V, Jekabsone A, Morkuniene R, Brown GC. Inhibition of mitochondrial permeability transition prevents mitochondrial dysfunction, cytochrome c release and apoptosis induced by heart ischemia. J Mol Cell Cardiol. 2003;35(4):357-66. (Pubitemid 36411697)
14. Lesnefsky EJ, Tandler B, Ye J, Slabe TJ, Turkaly J, Hoppel CL. Myocardial ischemia decreases oxidative phosphorylation through cytochrome oxidase in subsarcolemmal mitochondria. Am J Physiol. 1997;273(3 Pt 2):H1544-54.
15. Jiang X, Wang X. Cytochrome C-mediated apoptosis. Annu Rev Biochem. 2004;73:87-106. (Pubitemid 39050364)
16. Crestanello JA, Lingle DM, Kamelgard J, Millili J, Whitman GJ. Ischemic preconditioning decreases oxidative stress during reperfusion: a chemiluminescence study. J Surg Res. 1996;65(1):53-8. (Pubitemid 26339194)
17. Javadov SA, Clarke S, Das M, Griffiths EJ, Lim KH, Halestrap AP. Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol. 2003;549(Pt 2):513-24. (Pubitemid 36701762)
18. Lundberg KC, Szweda LI. Preconditioning prevents loss in mitochondrial function and release of cytochrome c during prolonged cardiac ischemia/reperfusion. Arch Biochem Biophys. 2006;453(1):130-4.
19. Liu GS, Thornton J, Van Winkle DM, Stanley AW, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation. 1991;84(1):350-6.
20. 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):556-64. (Pubitemid 29234221)
21. Goto M, Cohen MV, van Wylen DG, Downey JM. Attenuated purine production during subsequent ischemia in preconditioned rabbit myocardium is unrelated to the mechanism of protection. J Mol Cell Cardiol. 1996;28(3):447-54. (Pubitemid 26110487)
22. Chen Q, Camara AK, Stowe DF, Hoppel CL, Lesnefsky EJ. Modulation of electron transport protects cardiac mitochondria and decreases myocardial injury during ischemia and reperfusion. Am J Physiol Cell Physiol. 2007;292(1):C137-47. (Pubitemid 46115127)
23. Palmer JW, Tandler B, Hoppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem. 1977;252(23):8731-9. (Pubitemid 8243644)
24. Ricci JE, Gottlieb RA, Green DR. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol. 2003;160(1):65-75. (Pubitemid 36091717)
25. Lee AC, Zizi M, Colombini M. Beta-NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6. J Biol Chem. 1994;269(49):30974-80. (Pubitemid 24377586)
26. Mootha VK, Wei MC, Buttle KF, Scorrano L, Panoutsakopoulou V, Mannella CA, et al. A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J. 2001;20(4):661-71. (Pubitemid 32167631)
27. William JN. A method for the simultaneous quantitative estimation of cytochrome a, b, c1 and and c in mitochondrial. Arch Biochem Biophys. 1964;107:537-43.
28. Leung CH, Wang L, Fu YY, Yuen W, Caldarone CA. Transient mitochondrial permeability transition pore opening after neonatal cardioplegic arrest. J Thorac Cardiovasc Surg. 2011;141(4):975-82.
29. Dickson EW, Blehar DJ, Carraway RE, Heard SO, Steinberg G, Przyklenk K. Naloxone blocks transferred preconditioning in isolated rabbit hearts. J Mol Cell Cardiol. 2001;33(9):1751-6. (Pubitemid 32844232)
30. Schrader J, Haddy FJ, Gerlach E. Release of adenosine, inosine and hypoxanthine from the isolated guinea pig heart during hypoxia, flow-autoregulation and reactive hyperemia. Pflugers Arch. 1977;369(1):1-6. (Pubitemid 8095711)
31. Peart JN, Gross GJ. Adenosine and opioid receptor-mediated cardioprotection in the rat: evidence for cross-talk between receptors. Am J Physiol Heart Circ Physiol. 2003;285(1):H81-9. (Pubitemid 36736417)
32. Surendra H, Diaz RJ, Harvey K, Tropak M, Callahan J, Hinek A, et al. Interaction of delta and kappa opioid receptors with adenosine A1 receptorsmediates cardioprotection by remote ischemic preconditioning. J Mol Cell Cardiol. 2013;60:142-50.
33. Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res. 2004;61(3):372-85. (Pubitemid 38210145)
34. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS, et al. The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J. 2005;392(Pt 2):353-62. (Pubitemid 41796524)
35. Yang Z, Sun W, Hu K. Molecular mechanism underlying adenosine receptor-mediated mitochondrial targeting of protein kinase C. Biochim Biophys Acta. 2012;1823(4):950-8.
36. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, et al. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res. 2003;92(8):873-80. (Pubitemid 36542528)
37. Scorrano L, Petronilli V, Bernardi P. On the voltage dependence of the mitochondrial permeability transition pore. A critical appraisal. J Biol Chem. 1997;272(19):12295-9. (Pubitemid 27203313)
38. Dana A, Jonassen AK, Yamashita N, Yellon DM. Adenosine A(1) receptor activation induces delayed preconditioning in rats mediated by manganese superoxide dismutase. Circulation. 2000;101(24):2841-8. (Pubitemid 30396016)
39. Clarke SJ, Khaliulin I, Das M, Parker JE, Heesom KJ, Halestrap AP. Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ Res. 2008;102(9):1082-90. (Pubitemid 351667862)
40. Kerr PM, Suleiman MS, Halestrap AP. Reversal of permeability transition during recovery of hearts from ischemia and its enhancement by pyruvate. Am J Physiol. 1999;276(2 Pt 2):H496-502. (Pubitemid 29100617)
41. Kristiansen SB, Henning O, Kharbanda RK, Nielsen-Kudsk JE, Schmidt MR, Redington AN, et al. Remote preconditioning reduces ischemic injury in the explanted heart by a KATP channel-dependent mechanism. Am J Physiol Heart Circ Physiol. 2005;288(3):H1252-6. (Pubitemid 40270031)
42. Wang L, Cherednichenko G, Hernandez L, Halow J, Camacho SA, Figueredo V, et al. Preconditioning limits mitochondrial Ca(2+) during ischemia in rat hearts: role of K(ATP) channels. Am J Physiol Heart Circ Physiol. 2001;280(5):H2321-8.
43. Murata M, Akao M, O'Rourke B, Marban E. Mitochondrial ATP-sensitive potassium channels attenuate matrix Ca(2+) overload during simulated ischemia and reperfusion: possible mechanism of cardioprotection. Circ Res. 2001;89(10):891-8. (Pubitemid 34627894)
44. Fryer RM, Eells JT, Hsu AK, Henry MM, Gross GJ. Ischemic preconditioning in rats: role of mitochondrial K(ATP) channel in preservation of mitochondrial function. Am J Physiol Heart Circ Physiol. 2000;278(1):H305-12. (Pubitemid 30101886)
45. Koomen JM, Wilson CR, Guthrie P, Androlewicz MJ, Kobayashi R, Taegtmeyer H. Proteome analysis of isolated perfused organ effluent as a novel model for protein biomarker discovery. J Proteome Res. 2006;5(1):177-82. (Pubitemid 43100810)
46. Naydenova Z, Rose JB, Coe IR. Inosine and equilibrative nucleoside transporter 2 contribute to hypoxic preconditioning in the murine cardiomyocyte HL-1 cell line. Am J Physiol Heart Circ Physiol. 2008;294(6):H2687-92.
47. Jin X, Shepherd RK, Duling BR, Linden J. Inosine binds to A3 adenosine receptors and stimulates mast cell degranulation. J Clin Invest. 1997;100(11):2849-57. (Pubitemid 28007555)
48. Peart J, Matherne GP, Cerniway RJ, Headrick JP. Cardioprotection with adenosine metabolism inhibitors in ischemic-reperfused mouse heart. Cardiovasc Res. 2001;52(1):120-9. (Pubitemid 32835245)
49. Steensrud T, Li J, Dai X, Manlhiot C, Kharbanda RK, 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):H1598-603.