Enhanced preservation of pig cardiac allografts by combining erythropoietin with glyceryl trinitrate and zoniporide

American Journal of Transplantation

Volumn 13, Issue 7, 2013, Pages 1676-1687

  Watson, A J ^a,b   Gao, L ^a   Sun, L ^a   Tsun, J ^a   Doyle, A ^a   Faddy, S C ^b   Jabbour, A ^a,b   Orr, Y ^b   Dhital, K ^b   Hicks, M ^a,b   Jansz, P C ^b   Macdonald, P S ^a,b  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Cardiac allograft preservation; Celsior; erythropoietin; glyceryl trinitrate; heart transplantation; ischaemia reperfusion injury; zoniporide

Indexed keywords

EXTRACELLULAR BASED PRESERVATION SOLUTION; GLYCERYL TRINITRATE; PRESERVATION SOLUTION; RECOMBINANT ERYTHROPOIETIN; TROPONIN I; UNCLASSIFIED DRUG; ZONIPORIDE;

ANIMAL EXPERIMENT; ARTICLE; CARDIOPULMONARY BYPASS; CONTROLLED STUDY; DIASTOLE; DRUG EFFECT; HEART; HEART PRESERVATION; HEART TRANSPLANTATION; HEMODYNAMICS; NONHUMAN; ORGAN DONOR; ORTHOTOPIC HEART TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN SECRETION; SWINE; WEANING;

ANIMALS; DRUG COMBINATIONS; ERYTHROPOIETIN; GRAFT REJECTION; GUANIDINES; HEART TRANSPLANTATION; NITROGLYCERIN; ORGAN PRESERVATION; PYRAZOLES; SWINE; TRANSPLANTATION, HOMOLOGOUS; VASODILATOR AGENTS;

EID: 84879552298     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12249     Document Type: Article

References (47)

1. Stehlik J, Edwards LB, Kucheryavaya AY, Benden C, Christie JD, Dipchand AI, et al. The registry of the international society for heart and lung transplantation: 29th Official adult heart transplant report 2012. J Heart Lung Transplant 2012; 31: 1052-1064.
2. Iyer A, Kumarasinghe G, Hicks M, Watson A, Gao L, Doyle A, et al. Primary graft failure after heart transplantation. J Transplant 2011; 2011: 175768.
3. Gao L, Hicks M, Macdonald PS., Improved preservation of the rat heart with celsior solution supplemented with cariporide plus glyceryl trinitrate. Am J Transplant 2005; 5: 1820-1826.
4. Hing AJ, Watson A, Hicks M, Gao L, Faddy SC, McMahon AC, et al. Combining cariporide with glyceryl trinitrate optimizes cardiac preservation during porcine heart transplantation. Am J Transplant 2009; 9: 2048-2056.
5. Mentzer RM Jr., Bartels C, Bolli R, Boyce S, Buckberg GD, Chaitman B, et al. Sodium-hydrogen exchange inhibition by cariporide to reduce the risk of ischemic cardiac events in patients undergoing coronary artery bypass grafting: Results of the EXPEDITION study. Ann Thorac Surg 2008; 85: 1261-1270.
6. Gao L, Tsun J, Sun L, Kwan J, Watson A, Macdonald PS, et al. Critical role of the STAT3 pathway in the cardioprotective efficacy of zoniporide in a model of myocardial preservation-the rat isolated working heart. Br J Pharmacol 2011; 162: 633-647.
7. Cai Z, Manalo DJ, Wei G, Rodriguez ER, Fox-Talbot K, Lu H, et al. Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation 2003; 108: 79-85.
8. Burger D, Lei M, Geoghegan-Morphet N, Lu X, Xenocostas A, Feng Q., Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase. Cardiovasc Res 2006; 72: 51-59.
9. Ohori K, Miura T, Tanno M, Miki T, Sato T, Ishikawa S, et al. Ser9 phosphorylation of mitochondrial GSK-3β is a primary mechanism of cardiomyocyte protection by erythropoietin against oxidant-induced apoptosis. Am J Physiol Heart Circ Physiol 2008; 295: H2079-2086.
10. Ammar HI, Saba S, Ammar RI, Elsayed LA, Ghaly WBA-A, Dhingra S., Erythropoietin protects against doxorubicin-induced heart failure. Am J Physiol Heart Circ Physiol 2011; 301: H2413-H2421.
11. Watson A, Gao L, Tsun J, Sun L, Jabbour A, Hicks M, et al. Extended myocardial preservation by polypharmaceutical supplementation of celsior. J Heart Lung Transplant 2013 (in press).
12. Ryan J, Wilson MK, Hicks M, Nicholson A, Kesteven SH, Junius F, et al. A brain dead donor model of porcine orthotopic cardiac transplantation for assessment of cardiac allograft preservation. Heart. Lung Circ 2000; 9: 78-81.
13. Ryan JB, Hicks M, Cropper JR, Garlick SR, Kesteven SH, Wilson MK, et al. The preload recruitable stroke work relationship as a measure of left ventricular contractile dysfunction in porcine cardiac allografts. Eur J Cardiothorac Surg 2002; 22: 738-745.
14. Lower RR, Shumway NE., Studies on orthotopic homotransplantation of the canine heart. Surg Forum 1960; 11: 18-19.
15. Glower DD, Spratt JA, Snow ND, Kabas JS, Davis JW, Olsen CO, et al. Linearity of the Frank-Starling relationship in the intact heart: The concept of preload recruitable stroke work. Circulation 1985; 71: 994-1009.
16. Calvillo L, Latini R, Kajstura J, Leri A, Anversa P, Ghezzi P, et al. Recombinant human erythropoietin protects the myocardium from ischemia-reperfusion injury and promotes beneficial remodeling. Proc Nat Acad Sci USA 2003; 100: 4802-4806.
17. Bullard AJ, Govewalla P, Yellon DM., Erythropoietin protects the myocardium against reperfusion injury in vitro and in vivo. Basic Res Cardiol 2005; 100: 397-403.
18. Lipšic E, van der Meer P, Henning RH, Suurmeijer AJ, Boddeus KM, van Veldhuisen DJ, et al. Timing of erythropoietin treatment for cardioprotection in ischemia/reperfusion. J Cardiovasc Pharmacol 2004; 44: 473-479.
19. Moon C, Krawczyk M, Ahn D, Ahmet I, Paik D, Lakatta EG, et al. Erythropoietin reduces myocardial infarction and left ventricular functional decline after coronary artery ligation in rats. Proc Nat Acad Sci USA 2003; 100: 11612-11617.
20. Nishihara M, Miura T, Miki T, Sakamoto J, Tanno M, Kobayashi H, et al. Erythropoietin affords additional cardioprotection to preconditioned hearts by enhanced phosphorylation of glycogen synthase kinase-3 beta. Am J Physiol Heart Circ Phys 2006; 291: H748-H755.
21. Parsa CJ, Matsumoto A, Kim J, Riel RU, Pascal LS, Walton GB, et al. A novel protective effect of erythropoietin in the infarcted heart. J Clin Invest 2003; 112: 999-1007.
22. Fisher JW., Erythropoietin: Physiology and pharmacology update. Exp Biol Med (Maywood) 2003; 228: 1-14.
23. Hausenloy DJ, Yellon DM., New directions for protecting the heart against ischaemia-reperfusion injury: Targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res 2004; 61: 448-460.
24. Cai Z, Semenza GL., Phosphatidylinositol-3-kinase signaling is required for erythropoietin-mediated acute protection against myocardial ischemia/reperfusion injury. Circulation 2004; 109: 2050-2053.
25. Hirata A, Minamino T, Asanuma H, Sanada S, Fujita M, Tsukamoto O, et al. Erythropoietin just before reperfusion reduces both lethal arrhythmias and infarct size via the phosphatidylinositol-3 kinase-dependent pathway in canine hearts. Cardiovasc Drugs Ther 2005; 19: 33-40.
26. Shan X, Xu X, Cao B, Wang Y, Guo L, Zhu Q, et al. Transcription factor GATA-4 is involved in erythropoietin-induced cardioprotection against myocardial ischemia/reperfusion injury. Int J Cardiol 2008; 134: 384-392.
27. Piuhola J, Kerkelä R, Keenan J, Hampton M, Richards A, Pemberton C., Direct cardiac actions of erythropoietin (EPO): Effects on cardiac contractility, BNP secretion and ischaemia/reperfusion injury. Clin Sci 2008; 114: 293-304.
28. van der Meer P, Lipšic E, Henning RH, de Boer RA, Suurmeijer AJ, van Veldhuisen DJ, et al. Erythropoietin improves left ventricular function and coronary flow in an experimental model of ischemia-reperfusion injury. Eur J Heart Fail 2004; 6: 853-859.
29. Lu MJ, Chen YS, Huang HS, Ma MC., Erythropoietin alleviates post-ischemic injury of rat hearts by attenuating nitrosative stress. Life Sci 2012; 90: 776-784.
30. Lecour S., Activation of the protective Survivor Activating Factor Enhancement (SAFE) pathway against reperfusion injury: Does it go beyond the RISK pathway ? J Mol Cell Cardiol 2009; 47: 32-40.
31. Boengler K, Hilfiker-Kleiner D, Drexler H, Heusch G, Schulz R., The myocardial JAK/STAT pathway: From protection to failure. Pharmacol Ther 2008; 120: 172-185.
32. Heusch G, Musiolik J, Gedik N, Skyschally A., Mitochondrial STAT3 activation and cardioprotection by ischemic postconditioning in pigs with regional myocardial ischemia/reperfusion. Circ Res 2011; 109: 1302-1308.
33. Pinsky DJ, Oz MC, Koga S, Taha Z, Broekman MJ, Marcus AJ, et al. Cardiac preservation is enhanced in a heterotopic rat transplant model by supplementing the nitric oxide pathway. J Clin Invest 1994; 93: 2291-2297.
34. Huk I, Nanobashvili J, Neumayer C, Punz A, Mueller M, Afkhampour K, et al. L-arginine treatment alters the kinetics of nitric oxide and superoxide release and reduces ischemia/reperfusion injury in skeletal muscle. Circulation 1997; 96: 667-675.
35. Hallstrom S, Franz M, Gasser H, Vodrazka M, Semsroth S, Losert UM, et al. S-nitroso human serum albumin reduces ischaemia/reperfusion injury in the pig heart after unprotected warm ischaemia. Cardiovasc Res 2008; 77: 506-514.
36. Podesser BK, Hallström S., Nitric oxide homeostasis as a target for drug additives to cardioplegia. Br J Pharmacol 2007; 151: 930-940.
37. Gielis JF, Lin JY, Wingler K, Van Schil PE, Schmidt HH, Moens AL., Pathogenetic role of eNOS uncoupling in cardiopulmonary disorders. Free Radic Biol Med 2011; 50: 765-776.
38. Csont T, Szilvássy Z, Fülöp F, Nedeianu S, Páli T, Tosaki Á, et al. Direct myocardial anti-ischaemic effect of GTN in both nitrate-tolerant and nontolerant rats: A cyclic GMP-independent activation of KATP. Br J Pharmacol 1999; 128: 1427-1434.
39. Semsroth S, Fellner B, Trescher K, Bernecker OY, Kalinowski L, Gasser H, et al. S-nitroso human serum albumin attenuates ischemia/reperfusion injury after cardioplegic arrest in isolated rabbit hearts. J Heart Lung Transplant 2005; 24: 2226-2234.
40. Karmazyn M., The role of the myocardial sodium-hydrogen exchanger in mediating ischemic and reperfusion injury. From amiloride to cariporide. Ann NY Acad Sci 1999; 874: 326-334.
41. + exchange. Am J Physiol Heart Circ Physiol 1988; 255: H608-H615.
42. 2+ exchange. Circ Res 1989; 65: 1045-1056.
43. Scholz W, Albus U, Counillon L, Gögelein H, Lang HJ, Linz W, et al. Protective effects of HOE642, a selective sodium-hydrogen exchange subtype 1 inhibitor, on cardiac ischaemia and reperfusion. Cardiovasc Res 1995; 29: 260-268.
44. Cropper JR, Hicks M, Ryan JB, Macdonald PS., Cardioprotection by cariporide after prolonged hypothermic storage of the isolated working rat heart. J Heart Lung Transplant 2003; 22: 929-936.
45. Ryan JB, Hicks M, Cropper JR, Garlick SR, Kesteven SH, Wilson MK, et al. Cariporide (HOE-642) improves cardiac allograft preservation in a porcine model of orthotopic heart transplantation. Transplantation 2003; 75: 625-631.
46. Knight DR, Smith AH, Flynn DM, MacAndrew JT, Ellery SS, Kong JX, et al. A novel sodium-hydrogen exchanger isoform-1 inhibitor, zoniporide, reduces ischemic myocardial injury in vitro and in vivo. J Pharmacol Exp Therap 2001; 297: 254-259.
47. Clements-Jewery H, Sutherland FJ, Allen MC, Tracey WR, Avkiran M., Cardioprotective efficacy of zoniporide, a potent and selective inhibitor of Na+ /H+ exchanger isoform 1, in an experimental model of cardiopulmonary bypass. Br J Pharmacol 2004; 142: 57-66.