Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1762, Issue 2, 2006, Pages 223-231

  Tompkins, Andrew J ^a   Burwell, Lindsay S ^a   Digerness, Stanley B ^b   Zaragoza, Corinne ^b   Holman, William L ^b   Brookes, Paul S ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b Kentucky   (United States)

Author keywords

Complex I; Ischemia; Mitochondria; Nitric oxide; ROS

Indexed keywords

IODOBUTYLTRIPHENYLPHOSPHONIUM; PHOSPHONIUM DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); THIOL; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPATHOLOGY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME MODIFICATION; ENZYME SUBUNIT; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; ISOLATED HEART; MALE; MITOCHONDRIAL RESPIRATION; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; RAT; REPERFUSION INJURY;

ANIMALIA;

EID: 29344464774     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2005.10.001     Document Type: Review

References (53)

1. G. Ambrosio, J.L. Zweier, and J.T. Flaherty The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion J. Mol. Cell. Cardiol. 23 1991 1359 1374
2. J.L. Zweier, J.T. Flaherty, and M.L. Weisfeldt Direct measurement of free radical generation following reperfusion of ischemic myocardium Proc. Natl. Acad. Sci. U. S. A. 84 1987 1404 1407
3. R. Bolli, and E. Marban Molecular and cellular mechanisms of myocardial stunning Physiol. Rev. 79 1999 609 634
4. M.M. Lalu, W. Wang, and R. Schulz Peroxynitrite in myocardial ischemia-reperfusion injury Heart Fail. Rev. 7 2002 359 369
5. S.R. Powell, and A.J. Tortolani Recent advances in the role of reactive oxygen intermediates in ischemic injury: I. Evidence demonstrating presence of reactive oxygen intermediates; II. Role of metals in site-specific formation of radicals J. Surg. Res. 53 1992 417 429
6. E.J. Lesnefsky, S. Moghaddas, B. Tandler, J. Kerner, and C.L. Hoppel Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure J. Mol. Cell. Cardiol. 33 2001 1065 1089
7. T. Anmann, M. Eimre, A.V. Kuznetsov, T. Andrienko, T. Kaambre, P. Sikk, E. Seppet, T. Tiivel, M. Vendelin, E. Seppet, and V.A. Saks Calcium-induced contraction of sarcomeres changes the regulation of mitochondrial respiration in permeabilized cardiac cells FEBS J. 272 2005 3145 3161
8. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem. J. 341 1999 233 249
9. W. Rouslin Mitochondrial complexes I, II, III, IV, and V in myocardial ischemia and autolysis Am. J. Physiol. 244 1983 H743 H748
10. G. Paradies, G. Petrosillo, M. Pistolese, N. Di Venosa, A. Federici, and F.M. Ruggiero Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin Circ. Res. 94 2004 53 59
11. D.L. Hardy, J.B. Clark, V.M. Darley-Usmar, and D.R. Smith Reoxygenation of the hypoxic myocardium causes a mitochondrial complex I defect Biochem. Soc. Trans. 18 1990 549
12. D.L. Hardy, J.B. Clark, V.M. Darley-Usmar, D.R. Smith, and D. Stone Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (Complex I) activity in the hypoxic/reoxygenated rat heart Biochem. J. 274 1991 133 137
13. D.T. Lucas, and L.I. Szweda Declines in mitochondrial respiration during cardiac reperfusion: age-dependent inactivation of alpha-ketoglutarate dehydrogenase Proc. Natl. Acad. Sci. U. S. A. 96 1999 6689 6693
14. W. Rouslin, and R.W. Millard Mitochondrial inner membrane enzyme defects in porcine myocardial ischemia Am. J. Physiol. 240 1981 H308 H313
15. P.S. Brookes, S.B. Digerness, D.A. Parks, and V.M. Darley-Usmar Mitochondrial function in response to cardiac ischemia-reperfusion after oral treatment with quercetin Free Radical Biol. Med. 32 2002 1220 1228
16. E.J. Lesnefsky, B. Tandler, J. Ye, T.J. Slabe, J. Turkaly, and C.L. Hoppel Myocardial ischemia decreases oxidative phosphorylation through cytochrome oxidase in subsarcolemmal mitochondria Am. J. Physiol. 273 1997 H1544 H1554
17. E.J. Lesnefsky, T.I. Gudz, C.T. Migita, M. Ikeda-Saito, M.O. Hassan, P.J. Turkaly, and C.L. Hoppel Ischemic injury to mitochondrial electron transport in the aging heart: damage to the iron-sulfur protein subunit of electron transport complex III Arch. Biochem. Biophys. 385 2001 117 128
18. W. Rouslin, and R.W. Millard Canine myocardial ischemia: defect in mitochondrial electron transfer complex I J. Mol. Cell. Cardiol. 12 1980 639 645
19. A.C. Nulton-Persson, and L.I. Szweda Modulation of mitochondrial function by hydrogen peroxide J. Biol. Chem. 276 2001 23357 23361
20. W.C. Stanley, G.D. Lopaschuk, J.L. Hall, and J.G. McCormack Regulation of myocardial carbohydrate metabolism under normal and ischemic conditions Cardiovasc. Res. 33 1997 243 257
21. H. Taegtmeyer Energy substrate metabolism as target for pharmacotherapy in ischemic and reperfused heart muscle Heart Metab. 1 1998 5 9
22. Y. Liu, G. Fiskum, and D. Schubert Generation of reactive oxygen species by the mitochondrial electron transport chain J. Neurochem. 80 2002 780 787
23. A.P. Kudin, N.Y.-B. Bimpong-Buta, S. Vielhaber, C.E. Elger, and W.S. Kunz Characterization of superoxide-producing sites in isolated brain mitochondria J. Biol. Chem. 279 2004 4127 4135
24. J. St-Pierre, J.A. Buckingham, S.J. Roebuck, and M.D. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784 44790
25. A. Jekabsone, L. Ivanoviene, G.C. Brown, and V. Borutaite Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release J. Mol. Cell. Cardiol. 35 2003 803 809
26. A. Orsi, B. Beltran, E. Clementi, K. Hallen, M. Feelisch, and S. Moncada Continuous exposure to high concentrations of nitric oxide leads to persistent inhibition of oxygen consumption by J774 cells as well as extraction of oxygen by the extracellular medium Biochem. J. 346 2000 407 412
27. F. Schopfer, N. Riobo, M.C. Carreras, B. Alvarez, R. Radi, A. Boveris, E. Cadenas, and J.J. Poderoso Oxidation of ubiquinol by peroxynitrite: implications for protection of mitochondria against nitrosative damage Biochem. J. 349 2000 35 42
28. N.A. Riobo, E. Clementi, M. Melani, A. Boveris, E. Cadenas, S. Moncada, and J.J. Poderoso Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation Biochem. J. 359 2001 139 145
29. G.C. Brown, and V. Borutaite Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols Biochim. Biophys. Acta 1658 2004 44 49
30. A. Cassina, and R. Radi Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport Arch. Biochem. Biophys. 328 1996 309 316
31. E. Clementi, G.C. Brown, M. Feelisch, and S. Moncada Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione Proc. Natl. Acad. Sci. U. S. A. 95 1998 7631 7636
32. F.R. Gadelha, L. Thomson, M.M. Fagian, A.D. Costa, R. Radi, and A.E. Vercesi Ca2+-independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiol cross-linking and lipid peroxidation Arch. Biochem. Biophys. 345 1997 243 250
33. A.A. Starkov, B.M. Polster, and G. Fiskum Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax J. Neurochem. 83 2002 220 228
34. S.B. Digerness, P.S. Brookes, S.P. Goldberg, C.R. Katholi, and W.L. Holman Modulation of mitochondrial adenosine triphosphate-sensitive potassium channels and sodium-hydrogen exchange provide additive protection from severe ischemia-reperfusion injury J. Thorac. Cardiovasc. Surg. 125 2003 863 871
35. J.E. Davies, S.B. Digerness, S.P. Goldberg, C.R. Killingsworth, C.R. Katholi, P.S. Brookes, and W.L. Holman Intra-myocyte ion homeostasis during ischemia-reperfusion injury: effects of pharmacologic preconditioning and controlled reperfusion Ann. Thorac. Surg. 76 2003 1252 1258
36. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
37. P.S. Brookes, J.M. Land, J.B. Clark, and S.J. Heales Peroxynitrite and brain mitochondria: evidence for increased proton leak J. Neurochem. 70 1998 2195 2202
38. T.K. Lin, G. Hughes, A. Muratovska, F.H. Blaikie, P.S. Brookes, V. Darley-Usmar, R.A. Smith, and M.P. Murphy Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach J. Biol. Chem. 277 2002 17048 17056
39. P.S. Brookes, A. Pinner, A. Ramachandran, L. Coward, S. Barnes, H. Kim, and V.M. Darley-Usmar High throughput two-dimensional blue-native electrophoresis: a tool for functional proteomics of mitochondria and signaling complexes Proteomics 2 2002 969 977
40. B.A. van Montfort, B. Canas, R. Duurkens, J. Godovac-Zimmermann, and G.T. Robillard Improved in-gel approaches to generate peptide maps of integral membrane proteins with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry J. Mass. Spectrom. 37 2002 322 330
41. C.S. Powell, and R.M. Jackson Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: modulation of enzyme activities by MnSOD Am. J. Physiol. 285 2003 L189 L198
42. U. Andersson, B. Leighton, M.E. Young, E. Blomstrand, and E.A. Newsholme Inactivation of aconitase and oxoglutarate dehydrogenase in skeletal muscle in-vitro by superoxide anions and/or nitric oxide Biochem. Biophys. Res. Commun. 249 1998 512 516
43. K.M. Humphries, and L.I. Szweda Selective inactivation of alpha-ketoglutarate dehydrogenase and pyruvate dehydrogenase: reaction of lipoic acid with 4-hydroxy-2-nonenal Biochemistry 37 1998 15835 15841
44. J. Murray, S.W. Taylor, B. Zhang, S.S. Ghosh, and R.A. Capaldi Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry J. Biol. Chem. 278 2003 37223 37230
45. B. Alvarez, and R. Radi Peroxynitrite reactivity with amino acids and proteins Amino Acids 25 2003 295 311
46. L.A. Sazanov, S.Y. Peak-Chew, I.M. Fearnley, and J.E. Walker Resolution of the membrane domain of bovine complex I into subcomplexes: implications for the structural organization of the enzyme Biochemistry 39 2000 7229 7235
47. P.S. Brookes, Y. Yoon, J.L. Robotham, M.W. Anders, and S.S. Sheu Calcium, ATP, and ROS: a mitochondrial love-hate triangle Am. J. Physiol. 287 2004 C817 C833
48. V.J. Adlam, J.C. Harrison, C.M. Porteous, A.M. James, R.A. Smith, M.P. Murphy, and I.A. Sammut Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury FASEB J. 19 2005 1088 1095
49. K. Zhao, G.M. Zhao, D. Wu, Y. Soong, A.V. Birk, P.W. Schiller, and H.H. Szeto Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury J. Biol. Chem. 279 2004 34682 34690
50. M.A. Aon, S. Cortassa, E. Marban, and B. O'Rourke Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes J. Biol. Chem. 278 2003 44735 44744
51. J. Minners, L. Lacerda, J. McCarthy, J.J. Meiring, D.M. Yellon, and M.N. Sack Ischemic and pharmacological preconditioning in Girardi cells and C2C12 myotubes induce mitochondrial uncoupling Circ. Res. 89 2001 787 792
52. D.A. Berkich, G. Salama, and K.F. LaNoue Mitochondrial membrane potentials in ischemic hearts Arch. Biochem. Biophys. 420 2003 279 286
53. J.S. Armstrong, M. Whiteman, H. Yang, and D.P. Jones The redox regulation of intermediary metabolism by a superoxide-aconitase rheostat BioEssays 26 2004 894 900