The mitochondria-targeted anti-oxidant MitoQ decreases ischemia-reperfusion injury in a murine syngeneic heart transplant model

Journal of Heart and Lung Transplantation

Volumn 34, Issue 11, 2015, Pages 1471-1480

  Dare, Anna J ^a   Logan, Angela ^a   Prime, Tracy A ^a   Rogatti, Sebastian ^a   Goddard, Martin ^b   Bolton, Eleanor M ^c   Bradley, J Andrew ^c   Pettigrew, Gavin J ^c   Murphy, Michael P ^a   Saeb Parsy, Kourosh ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b PAPWORTH HOSPITAL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

ischemia; mitochondria targeted anti oxidants; MitoQ; reperfusion; transplantation

Indexed keywords

ANTIOXIDANT; CARBONYL DERIVATIVE; CXCL1 CHEMOKINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOCHONDRIAL DNA; MITOQ; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; MITOQUINONE; ORGANOPHOSPHORUS COMPOUND; SCAVENGER; TRACE ELEMENT; UBIQUINONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CRYOPRESERVATION; CYTOKINE RELEASE; DNA DAMAGE; DOSE RESPONSE; DRUG EFFICACY; DRUG UPTAKE; FEMALE; HEART GRAFT; INNATE IMMUNITY; MALE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DISEASE MODEL; HEART MITOCHONDRION; HEART TRANSPLANTATION; METABOLISM; ORGAN PRESERVATION; OXIDATIVE STRESS; PATHOLOGY; PRIMARY GRAFT DYSFUNCTION; RAT; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; FEMALE; FREE RADICAL SCAVENGERS; HEART TRANSPLANTATION; MALE; MICE; MICE, INBRED C57BL; MICRONUTRIENTS; MITOCHONDRIA, HEART; ORGAN PRESERVATION; ORGANOPHOSPHORUS COMPOUNDS; OXIDATIVE STRESS; PRIMARY GRAFT DYSFUNCTION; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; UBIQUINONE;

EID: 84946487152     PISSN: 10532498     EISSN: 15573117     Source Type: Journal    
DOI: 10.1016/j.healun.2015.05.007     Document Type: Article

References (47)

1. J. Stehlik, L.B. Edwards, A.Y. Kucheryavaya, and et al. The Registry of the International Society for Heart and Lung Transplantation: twenty-seventh official adult heart transplant report - 2010 J Heart Lung Transplant 29 2010 1089 1103
2. J.E. Stahl, J.E. Kreke, F.A. Malek, A.J. Schaefer, and J. Vacanti Consequences of cold-ischemia time on primary nonfunction and patient and graft survival in liver transplantation: a meta-analysis PloS One 3 2008 e2468
3. C.L. Kuntz, D. Hadjiliadis, V.N. Ahya, and et al. Risk factors for early primary graft dysfunction after lung transplantation: a registry study Clin Transplant 23 2009 819 830
4. A. Iyer, G. Kumarasinghe, M. Hicks, and et al. Primary graft failure after heart transplantation J Transplant 2011 2011 175768
5. S.F. Marasco, D.S. Esmore, J. Negri, and et al. Early institution of mechanical support improves outcomes in primary cardiac allograft failure J Heart Lung Transplant 24 2005 2037 2042
6. J.W. Kupiec-Weglinski Tolerance induction Curr Opin Organ Transplant 13 2008 331 332
7. D. Mikhalski, K.M. Wissing, L. Ghisdal, and et al. Cold ischemia is a major determinant of acute rejection and renal graft survival in the modern era of immunosuppression Transplantation 85 7 Suppl 2008 S3 S9
8. G. Ambrosio, and I. Tritto Reperfusion injury: experimental evidence and clinical implications Am Heart J 138 1999 S69 S75
9. J.F. Turrens, M. Beconi, J. Barilla, U.B. Chavez, and J.M. McCord Mitochondrial generation of oxygen radicals during reoxygenation of ischemic tissues Free Radic Res Commun 12-13 1991 681 689
10. A.L. Bulteau, K.C. Lundberg, K.M. Humphries, and et al. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion J Biol Chem 276 2001 30057 30063
11. P. Bernardi, A. Krauskopf, E. Basso, and et al. The mitochondrial permeability transition from in vitro artifact to disease target FEBS J 273 2006 2077 2099
12. A.P. Halestrap, S.J. Clarke, and S.A. Javadov Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection Cardiovasc Res 61 2004 372 385
13. R. Zhou, A.S. Yazdi, P. Menu, and J. Tschopp A role for mitochondria in NLRP3 inflammasome activation Nature 469 2011 221 225
14. M. Kawaguchi, M. Takahashi, T. Hata, and et al. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury Circulation 123 2011 594 604
15. R.A.J. Smith, and M.P. Murphy Animal and human studies with the mitochondria-targeted antioxidant MitoQ Ann N Y Acad Sci 1201 2010 96 103
16. R.A.J. Smith, R.C. Hartley, H.M. Cocheme, and M.P. Murphy Mitochondrial pharmacology Trends Pharmacol Sci 33 2012 341 352
17. R.A.J. Smith, R.C. Hartley, and M.P. Murphy Mitochondria-targeted small molecule therapeutics and probes Antioxid Redox Signal 15 2011 3021 3038
18. G.F. Kelso, C.M. Porteous, C.V. Coulter, and et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties J Biol Chem 276 2001 4588 4596
19. M.F. Ross, G.F. Kelso, F.H. Blaikie, and et al. Lipophilic triphenylphosphonium cations as tools in mitochondrial bioenergetics and free radical biology Biochemistry (Mosc) 70 2005 222 230
20. V.J. Adlam, J.C. Harrison, C.M. Porteous, and et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury FASEB J 19 2005 1088 1095
21. P. Mukhopadhyay, B. Horvath, Z. Zsengeller, and et al. Mitochondrial reactive oxygen species generation triggers inflammatory response and tissue injury associated with hepatic ischemia-reperfusion: therapeutic potential of mitochondrially targeted antioxidants Free Radic Biol Med 53 2012 1123 1138
22. T. Mitchell, D. Rotaru, H. Saba, R.A. Smith, M.P. Murphy, and L.A. MacMillan-Crow The mitochondria-targeted antioxidant mitoquinone protects against cold storage injury of renal tubular cells and rat kidneys J Pharmacol Exp Ther 336 2011 682 692
23. B.J. Snow, F.L. Rolfe, M.M. Lockhart, and et al. A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease Mov Disord 25 2010 1670 1674
24. E.J. Gane, F. Weilert, D.W. Orr, and et al. The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients Liver Int 30 2010 1019 1026
25. R.J. Corry, H.J. Winn, and P.S. Russell Heart transplantation in congenic strains of mice Transplant Proc 5 1973 733 735
26. M. Tanaka, R.D. Terry, G.K. Mokhtari, and et al. Suppression of graft coronary artery disease by a brief treatment with a selective epsilonPKC activator and a deltaPKC inhibitor in murine cardiac allografts Circulation 110 11 Suppl 1 2004 Ii194-9
27. M.F. Ross, T.A. Prime, I. Abakumova, and et al. Rapid and extensive uptake and activation of hydrophobic triphenylphosphonium cations within cells Biochem J 411 2008 633 645
28. H.M. Cocheme, A. Logan, T.A. Prime, and et al. Using the mitochondria-targeted ratiometric mass spectrometry probe MitoB to measure H202 in living Drosophila Nat Protoc 7 2012 946 958
29. H.M. Cocheme, C. Quin, S.J. McQuaker, and et al. Measurement of H202 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix Cell Metab 13 2011 340 350
30. J.H. Santos, J.N. Meyer, B.S. Mandavilli, and B. Van Houten Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells Methods Mol Biol 314 2006 183 199
31. C.C. Winterbourn, and I.H. Buss Protein carbonyl measurement by enzyme-linked immunosorbent assay Methods Enzymol 300 1999 106 111
32. C.M. Porteous, A. Logan, C. Evans, and et al. Rapid uptake of lipophilic triphenylphosphonium cations by mitochondria in vivo following intravenous injection: implications for mitochondria-specific therapies and probes Biochim Biophys Acta 1800 2010 1009 1017
33. C.M. Porteous, D.K. Menon, F.I. Aigbirhio, R.A.J. Smith, and M.P. Murphy P-glycoprotein (Mdr1a/1b) and breast cancer resistance protein (Bcrp) decrease the uptake of hydrophobic alkyl triphenylphosphonium cations by the brain Bioch Biophys Acta 1830 2013 3458 3465
34. D. Graham, N.N. Huynh, C.A. Hamilton, and et al. Mitochondria-targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy Hypertension 54 2009 322 328
35. W.G. Land The role of postischemic reperfusion injury and other nonantigen-dependent inflammatory pathways in transplantation Transplantation 79 2005 505 514
36. A.V. Kuznetsov, S. Schneeberger, R. Seiler, and et al. Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion Am J Physiol Heart Circ Physiol 286 2004 H1633 H1641
37. R. Sucher, P. Gehwolf, T. Kaier, and et al. Intracellular signaling pathways control mitochondrial events associated with the development of ischemia/reperfusion-associated damage Transplant Int 22 2009 922 930
38. A.V. Kuznetsov, S. Schneeberger, O. Renz, and et al. Functional heterogeneity of mitochondria after cardiac cold ischemia and reperfusion revealed by confocal imaging Transplantation 77 2004 754 756
39. J. Huang, K. Nakamura, Y. Ito, and et al. Bcl-xL gene transfer inhibits Bax translocation and prolongs cardiac cold preservation time in rats Circulation 112 2005 76 83
40. M. Tanaka, G.K. Mokhtari, R.D. Terry, and et al. Prolonged cold ischemia in rat cardiac allografts promotes ischemia-reperfusion injury and the development of graft coronary artery disease in a linear fashion J Heart Lung Transplant 24 2005 1906 1914
41. A.P. West, G.S. Shadel, and S. Ghosh Mitochondria in innate immune responses Nat Rev Immunol 11 2011 389 402
42. I. Moreno, R. Vicente, F. Ramos, J.L. Vicente, and M. Barbera Determination of interleukin-6 in lung transplantation: association with primary graft dysfunction Transplant Proc 39 2007 2425 2426
43. X. Zhao, O. Boenisch, M. Yeung, and et al. Critical role of proinflammatory cytokine IL-6 in allograft rejection and tolerance Am J Transplant 12 2012 90 101
44. Q. Zhang, M. Raoof, Y. Chen, and et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury Nature 464 2010 104 107
45. K. Ishikawa, N. Toyama-Sorimachi, K. Nakada, and et al. The innate immune system in host mice targets cells with allogenic mitochondrial DNA J Exp Med 207 2010 2297 2305
46. W. Land The potential impact of the reperfusion injury on acute and chronic rejection events following organ transplantation Transplant Proc 26 1994 3169 3171
47. P.J. Evans, J.M. Tredger, J.B. Dunne, and B. Halliwell Catalytic metal ions and the loss of reduced glutathione from University of Wisconsin preservation solution Transplantation 62 1996 1046 1049