Cardio-protective Signalling by Glyceryl Trinitrate and Cariporide in a Model of Donor Heart Preservation

Heart Lung and Circulation

Volumn 24, Issue 3, 2015, Pages 306-318

  Kwan, Jair C ^a,d,e   Gao, Ling ^a   Macdonald, Peter S ^a,b   Hicks, Mark ^a,b,c  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b ST VINCENT S HOSPITAL   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d HEART RESEARCH INSTITUTE   (Australia)

^e University of Sydney   (Australia)

Author keywords

Donor heart; Glyceryl trinitrate; Ischaemia reperfusion injury; Mitochondria; Pharmacological conditioning; Sodium hydrogen exchange inhibitor

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CARIPORIDE; CASPASE 3; CELSIOR; GLYCERYL TRINITRATE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE DONOR; PROTEIN BCL 2; PROTEIN KINASE B; STAT3 PROTEIN; CARDIOTONIC AGENT; GUANIDINE DERIVATIVE; MUSCLE PROTEIN; PRESERVATION SOLUTION; SULFONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CORRELATIONAL STUDY; DONOR HEART; ENZYME PHOSPHORYLATION; HEART FUNCTION; HEART PRESERVATION; HEART PROTECTION; HISTOLOGY; HOMEOSTASIS; IMMUNOBLOTTING; MALE; MITOCHONDRION; NONHUMAN; ORGAN DONOR; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; HEART MUSCLE; METABOLISM; ORGAN PRESERVATION; PROCEDURES; WISTAR RAT;

ANIMALS; CARDIOTONIC AGENTS; GUANIDINES; MALE; MAP KINASE SIGNALING SYSTEM; MUSCLE PROTEINS; MYOCARDIUM; NITROGLYCERIN; ORGAN PRESERVATION; ORGAN PRESERVATION SOLUTIONS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; SULFONES;

EID: 84923229032     PISSN: 14439506     EISSN: 14442892     Source Type: Journal    
DOI: 10.1016/j.hlc.2014.10.001     Document Type: Article

References (71)

1. Hicks M., Hing A., Gao L., Ryan J., Macdonald P.S. Organ preservation. Methods Mol Biol. 2006, 333:331-373.
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. 10.1155/2011/175768.
3. Stehlik J., Edwards L.B., Kucheryavaya A.Y., Benden C., Christie J.D., Dipchand A.I., et al. The registry of the International Society for Heart and Lung Translantation: 29th Official Adult Heart Transplant Report. J Heart Lung Transplant. 2012, 31:1052-1064.
4. Demmy T.L., Biddle J.S., Bennett L.E., Walls J.T., Schmaltz R.A., Curtis J.J. Organ preservation solutions in heart transplantation - patterns of usage and related survival. Transplantation. 1997, 63:262-269.
5. Menasche P., Termignon J.L., Pradier F., Grousset C., Mouas C., Alberici G., et al. Experimental evaluation of Celsior, a new heart preservation solution. Eur J Cardiothorac Surg. 1994, 8:207-213.
6. Costanzo M.R., Dipchand A., Starling R., Anderson A., Chan M., Desai S., et al. ISHLT guidelines for the care of heart transplant recipients. J Heart Lung Transplant. 2010, 29:914-956.
7. Hausenloy D.J., Yellon D.M. Therapeutic potential of ischemic conditioning: an update. Nat Rev Cardiol. 2011, 8:619-629.
8. Pinsky D.J. The vascular biology of heart and lung preservation for transplantation. Thromb Haemost. 1995, 74:58-65.
9. + exchange inhibitor HOE 694. Ann Thorac Surg. 1996, 61:1400-1406.
10. Hicks M., Du Z.Y., Jansz P., Rainer S., Spratt P., Macdonald P.S. ATP - sensitive potassium channel activation mimics the protective effects of ischemic preconditioning in the isolated working rat heart after prolonged hypothermic storage. Clin Exp Pharmacol Physiol 1999, 26:20-25.
11. Du Z.Y., Hicks M., Jansz P., Rainer S., Spratt P., Macdonald P. The nitric oxide donor, diethylamine NONOate enhances preservation of the donor rat heart. J Heart Lung Transplant 1998, 17:1113-1120.
12. Gao L., Hicks M., Macdonald P.S. Improved preservation of the rat heart with celsior solution supplemented with cariporide plus glyceryl trinitrate. Am J Transplant 2005, 5:1820-1826.
13. Hing A.J., Watson A., Hicks M., Gao L., Faddy S.C., McMahon A.C., et al. Combining cariporide with glyceryl trinitrate optimizes cardiac preservation during porcine heart transplantation. Am J Transplant. 2009, 9:2048-2056.
14. Hausenloy D.J., Lecour S., Yellon D.M. Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: two sides of the same coin. Antioxid Redox Signal. 2011, 14:893-907.
15. Gao L., Tsun J., Sun L., Kwan J., Watson A., Macdonald P., et al. Critical role of the STAT3 pathway in the cardioprotective efficacy of zoniporide in a model of myocardial preservation - the isolated working rat heart. Brit J Pharmacol 2011, 162:633.
16. Watson A.J., Gao L., Sun L., Tsun J., Jabbour A., Ru Qiu M., et al. Enhanced preservation of the rat heart after prolonged hypothermic ischemia with erythropoietin-supplemented Celsior solution. J Heart Lung Transplant 2013, 32:633-640.
17. Oliveira C.J., Schindler F., Ventura A.M., Morais M.S., Arai R.J., Debbas V., et al. Nitric oxide and cGMP activate the Ras-MAP kinase pathway - stimulating protein tyrosine kinase phosphorylation in rabbit aortic endothelial cells. Free Radical Biol Med 2003, 35:381-396.
18. Haworth R.S., Dashnyam S., Avkiran M. Ras triggers acidosis - induced activation of the extracellular signal - related kinase pathway in cardiac myocytes. Biochem J 2006, 399:493-501.
19. Xuan Y.T., Guo Y., Zhu Y., Wang O.L., Rokosh G., Bolli R. Endothelial nitric oxide synthase plays an obligatory role in the late phase of ischemic preconditioning by activating the protein kinase Ce - p44/42 mitogen activated protein kinase - pSer-signal transducers and activators of transcription 1/3 pathway. Circulation 2007, 116:535-544.
20. + inhibition and ATP-sensitive potassium channel activation. J Heart Lung Transplant. 2003, 22:1245-1253.
21. Ganote C.E. Contraction band necrosis and irreversible myocardial injury. J Mol Cell Cardiol. 1983, 15:67-73.
22. Deng X., Ruvolo P., Carr B., May W.S. Survival function of ERK 1/2 as IL-3 - activated, staurosporine - resistant Bcl2 kinase. Proc Natl Acac Sci. (USA) 2000, 97:1578-1583.
23. 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.
24. Navas J.P., Anderson W., Marsh J.D. Hypothermia increases calcium content of hypoxic myocytes. Am J Physiol. 1990, 259:H333-H339.
25. Kondratiev T.V., Wold R.M., Aasum E., Tveita T. Myocardial mechanical dysfunction and calcium overload following rewarming from experimental hypothermia in vivo. Cryobiology. 2008, 56:15-21.
26. Ruiz-Meana M., García-Dorado D. Pathophysiology of ischemia-reperfusion injury: new therapeutic options for acute myocardial infarction. Rev Esp Cardiol. 2009, 62:199-209.
27. Gori T., Daiber A., Di Stolfo G., Sicuro S., Dragoni S., Lisi M., et al. Nitroglycerine causes mitochondrial reactive oxygen species production: in vitro mechanistic insights. Can J Cardiol. 2007, 23:990-992.
28. Hausenloy D., Wynne A., Duchen M., Yellon D. Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation. 2004, 109:1714-1717.
29. + channels play a role in cardioprotection by Na+-H+ exchange inhibition against ischemia/reperfusion injury. J Am Coll Cardiol. 2001, 37:957-963.
30. Ruiz-Meana M., Garcia-Dorado D., Pina P., Inserte J., Agullo L., Soler-Soler J. Cariporide preserves mitochondrial proton gradient and delays ATP depletion in cardiomyocytes during ischemic conditions. Am J Physiol Heart Circ Physiol. 2003, 285:H999-H1006.
31. Garciarena C.D., Caldiz C.I., Correa M.V. Na+/H+ exchanger-1 inhibitors decrease myocardial superoxide production via direct mitochondrial action. J Appl Physiol. 2008, 105:1706-1713.
32. Teshima Y., Akao M., Jones S.P., Marban E. Cariporide (HOE642), a selective Na+-H+ exchange inhibitor, inhibits the mitochondrial death pathway. Circulation. 2003, 108:2275-2281.
33. Javadov S., Choi A., Rajapurohitam V., Zeidan A., Basnakian A.G., Karmazyn M. NHE-1 inhibition-induced cardioprotection against ischaemia/reperfusion is associated with attenuation of the mitochondrial permeability transition. Cardiovasc Res. 2008, 77:416-424.
34. Hausenloy D.J., Yellon D.M. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis. 2009, 204:334-341.
35. Lacerda L., Somers S., Opie L.H., Lecour S. Ischaemic postconditioning protects against reperfusion injury via the SAFE pathway. Cardiovasc Res. 2009, 84:201-208.
36. Yellon D.M., Hausenloy D.J. Myocardial reperfusion injury. N Engl J Med. 2007, 357:1121-1135.
37. Darling C.E., 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. 2005, 289:H1618-H1626.
38. Ito N., Bartunek J., Spitzer K.W., Lorell B.H. Effects of the nitric oxide donor sodium nitroprusside on intracellular pH and contraction in hypertrophied myocytes. Circulation. 1997, 95:2303-2311.
39. Strömer H., de Groot M.C., Horn M., Faul C., Leupold A., Morgan J.P., et al. Na(+)/H(+) exchange inhibition with HOE642 improves postischemic recovery due to attenuation of Ca(2+) overload and prolonged acidosis on reperfusion. Circulation. 2000, 101:2749-2755.
40. Cohen M.V., Yang X.M., Downey J.M. The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation. 2007, 115:1895-1903.
41. Penna C., Perrelli M.G., Tullio F., Angotti C., Pagliaro P. Acidic infusion in early reperfusion affects the activity of antioxidant enzymes in postischemic isolated rat heart. J Surg Res. 2013, 183:111-118.
42. Yang X., Liu Y., Yang X.-M., Hu F., Cui L., Swingle M.R., et al. Cardioprotection by mild hypothermia during ischemia involves preservation of ERK activity. Basic Res Cardiol. 2011, 106:421-430.
43. Chan E.Y.W., Stang S.L., Bottorff D.A., Stone J.C. Hypothermic stress leads to activation of Ras-Erk signaling. J Clin Invest. 1999, 103:1337-1344.
44. Ballif B.A., Blenis J. Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ. 2001, 12:397-408.
45. Hausenloy D.J., Moncanu M.M., Yellon D.M. Cross-talk between the survival kinases during early reperfusion: its contribution to ischemic preconditioning. Cardiovasc Res 2004, 63:305-312.
46. Das A., Salloum F.N., Durrant D., Ockaili R., Kukreja R.C. Rapamycin protects against myocardial ischemia-reperfusion injury through JAK2-STAT3 signaling pathway. J Mol Cell Cardiol. 2012, 53:858-869.
47. Green D.R., Evan G.I. A matter of life and death. Cancer Cell. 2002, 1:19-30.
48. Allan L.A., Morrice N., Brady S., Magee G., Pathak S., Clarke P.R. Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK. Nature Cell Biol 2003, 5:647-654.
49. Wortzel I., Seger R. The ERK cascade: Distinct functions within various subcellular organelles. Genes Cancer. 2011, 2:195-209.
50. Harris M.H., Thompson C.B. The role of Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ. 2000, 7:1182-1191.
51. Tamura Y., Simizu S., Osada H. The phosphorylation status and anti-apoptotic activity of Bcl2 are regulated by ERK and protein phosphatase 2A on the mitochondria. FEBS Lett. 2004, 569:249-255.
52. Kang R., Zeh H.J., Lotze M., Tang D. The beclin 1 network regulates autophagy and apoptosis. Cell Death Diff. 2011, 18:571-580.
53. Gottlieb R.A., Finley K.D., Mentzer R.M. Cardioprotection requires taking out the trash. Basic Res Cardiol. 2009, 104:169-180.
54. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., et al. Bcl-2 antiapoptotic proteins inhibit beclin 1 - dependent autophagy. Cell. 2005, 122:927-939.
55. Tang D., Kang R., Livesey K.M., Cheh C.W., Farkas A., Loughran P., et al. Endogenous HMGB1 regulates autophagy. J Cell Biol. 2010, 190:881-892.
56. Chen C.H., Wang W.J., Kuo J.C., Tsai H.C., Lin J.R., Chang Z.F., et al. Bidirectional signals transduced by DAPK-ERK interaction promote the apoptotic effect of DAPK. EMBO J. 2005, 24:294-304.
57. Andres A.M., Hernandez G., Lee P., Huang C., Ratliff E.P., Sin J., et al. Mitophagy is Required for Acute Cardioprotection by Simvastatin. Antioxid Redox Signal. 2013, 10.1089/ars.2013.5416.
58. Kirsch D.G., Doseff A., Chau B.N., Lim D.S., de Souza-Pinto N.C., Hansford R., et al. Caspase-3 - dependent cleavage of Bcl2 promotes release of cytochrome C. J Biol Chem. 1999, 274:21155-21161.
59. Carreira R.S., Lee P., Gottlieb R.A. Mitochondrial therapeutics for cardioprotection. Curr Pharm Des. 2011, 17:2017-2035.
60. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005, 434:658-662.
61. Rasola A., Sciacovelli M., Chiara F., Pantic B., Brusilow W.S., Bernardi P. Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc Natl Acad Sci. (USA) 2010, 107:726-731.
62. Wegrzyn J., Potla R., Chwae Y.J., Sepuri N.B., Zhang Q., Koeck T., et al. Function of mitochondrial STAT3 in cellular respiration. Science. 2009, 323:793-797.
63. Boengler K., Hilfiker-Kleiner D., Heusch G., Schulz R. Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol. 2010, 105:771-785.
64. Szczepanek K., Lesnefsky E.J., Larner A.C. Multi-tasking: nuclear transcription factors with novel roles in the mitochondria. Trends Cell Biol 2012, 22:429-437.
65. Alvarez B.V., Villa-Abrille M.C. Mitochondrial NHE1: a newly identified target to prevent heart disease. Front Physiol. 2013 Jun 28, 4:152. 10.3389/fphys.2013.00152.
66. Venugopal V., Ludman A., Yellon D.M., Hausenloy D.J. "Conditioning" the heart during surgery. Eur J Cardiothorac Surg. 2009, 35:977-987.
67. Iliodromitis E.K., Downey J.M., Heusch G., Kremastinos D.T. What is the optimal postconditioning algorithm?. J Cardiovasc Pharmacol Ther. 2009, 14:269-273.
68. Bon D., Chatauret N., Giraud S., Thuillier R., Favreau F., Hauet T. New strategies to optimize kidney recovery and preservation in transplantation. Nat Rev Nephrol. 2012, 8:339-347.
69. Watson A.J., Gao L., Sun L., Tsun J., Doyle A., Faddy S.C., et al. Enhanced preservation of pig cardiac allografts by combining erythropoietin with glyceryl trinitrate and zoniporide. Am J Transplant. 2013, 13:1676-1687.
70. Kumarasinghe G., Iyer A., Watson A., Mark Hicks, Ling Gao, Aoife Doyle, et al. Clinical experience supplementing celsior preservation solution with prosurvival kinase agents glyceryl trinitrate and erythropoietin demonstrates excellent myocardial recovery post transplantation. Transplantation. 2013, 96(suppl 10S):S259-S260.
71. Iyer A., Gao L., Doyle A., Rao P., Jayewardene D., Wan B., et al. Increasing the tolerance of DCD hearts to warm ischemia by pharmacological postconditioning. Am J Transplant. 2014, 14:1744-1752.