Respiratory uncoupling by increased H+ or K+ flux is beneficial for heart mitochondrial turnover of reactive oxygen species but not for permeability transition

BMC Cell Biology

Volumn 14, Issue 1, 2013, Pages

  Morota, Saori ^a,b   Piel, Sarah ^a   Hansson, Magnus J ^a  

^a LUND UNIVERSITY   (Sweden)

^b TOKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Ischemic preconditioning; Mitochondrial permeability transition; Potassium channels; Reactive oxygen species; Respiratory uncoupling

Indexed keywords

CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; REACTIVE OXYGEN METABOLITE; VALINOMYCIN;

ANIMAL TISSUE; ARTICLE; CALCIUM RETENTION CAPACITY; CHEMICAL PARAMETERS; CONTROLLED STUDY; HEART MITOCHONDRION; HEART MUSCLE METABOLISM; HYPEROSMOLARITY; MALE; METABOLIC PARAMETERS; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; NONHUMAN; POTASSIUM CONDUCTANCE; POTASSIUM TRANSPORT; PROTON MOTIVE FORCE; PROTON TRANSPORT; RAT; RESPIRATION CONTROL; RESPIRATORY UNCOUPLING; SENSITIZATION; TURNOVER TIME;

RATTUS;

ANIMALS; CALCIUM; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CATIONS, MONOVALENT; CYCLOSPORINE; DIAZOXIDE; HYDROGEN PEROXIDE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL SWELLING; OSMOLAR CONCENTRATION; OXIDATIVE PHOSPHORYLATION; OXYGEN; PERMEABILITY; POTASSIUM; POTASSIUM CHANNELS; PROTON IONOPHORES; PROTONS; RATS; REACTIVE OXYGEN SPECIES; UNCOUPLING AGENTS; VALINOMYCIN;

EID: 84884323953     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-14-40     Document Type: Article

References (47)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986, 74:1124-1136. 10.1161/01.CIR.74.5.1124, 3769170.
2. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 2003, 83:1113-1151.
3. Griffiths EJ, Halestrap AP. Protection by Cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol 1993, 25:1461-1469. 10.1006/jmcc.1993.1162, 7512654.
4. Argaud L, Gateau-Roesch O, Muntean D, Chalabreysse L, Loufouat J, Robert D, Ovize M. Specific inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury. J Mol Cell Cardiol 2005, 38:367-374. 10.1016/j.yjmcc.2004.12.001, 15698843.
5. Shanmuganathan S, Hausenloy DJ, Duchen MR, Yellon DM. Mitochondrial permeability transition pore as a target for cardioprotection in the human heart. Am J Physiol Heart Circ Physiol 2005, 289:H237-H242. 10.1152/ajpheart.01192.2004, 15961375.
6. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008, 359:473-481. 10.1056/NEJMoa071142, 18669426.
7. Lim SY, Davidson SM, Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: the essential role of the mitochondrial permeability transition pore. Cardiovasc Res 2007, 75:530-535. 10.1016/j.cardiores.2007.04.022, 2080572, 17512507.
8. Halestrap AP, Clarke SJ, Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim Biophys Acta 2007, 1767:1007-1031. 10.1016/j.bbabio.2007.05.008, 2212780, 17631856.
9. Garlid KD, Halestrap AP. The mitochondrial K(ATP) channel-Fact or fiction?. J Mol Cell Cardiol 2012, 52:578-583. 10.1016/j.yjmcc.2011.12.011, 3617982, 22240339.
10. McLeod CJ, Aziz A, Hoyt RF, McCoy JP, Sack MN. Uncoupling proteins 2 and 3 function in concert to augment tolerance to cardiac ischemia. J Biol Chem 2005, 280:33470-33476. 10.1074/jbc.M505258200, 16079144.
11. Skulachev VP. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q Rev Biophys 1996, 29:169-202. 10.1017/S0033583500005795, 8870073.
12. Baines CP. The cardiac mitochondrion: nexus of stress. Annu Rev Physiol 2010, 72:61-80. 10.1146/annurev-physiol-021909-135929, 20148667.
13. Sedlic F, Sepac A, Pravdic D, Camara AK, Bienengraeber M, Brzezinska AK, Wakatsuki T, Bosnjak ZJ. Mitochondrial depolarization underlies delay in permeability transition by preconditioning with isoflurane: roles of ROS and Ca2+. Am J Physiol Cell Physiol 2010, 299:C506-515. 10.1152/ajpcell.00006.2010, 2928640, 20519447.
14. Brennan JP, Southworth R, Medina RA, Davidson SM, Duchen MR, Shattock MJ. Mitochondrial uncoupling, with low concentration FCCP, induces ROS-dependent cardioprotection independent of KATP channel activation. Cardiovasc Res 2006, 72:313-321. 10.1016/j.cardiores.2006.07.019, 16950237.
15. Ozcan C, Bienengraeber M, Dzeja PP, Terzic A. Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation. Am J Physiol Heart Circ Physiol 2002, 282:H531-539.
16. Vanden Hoek T, Becker LB, Shao ZH, Li CQ, Schumacker PT. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res 2000, 86:541-548. 10.1161/01.RES.86.5.541, 10720416.
17. Andrukhiv A, Costa AD, West IC, Garlid KD. Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol 2006, 291:H2067-2074. 10.1152/ajpheart.00272.2006, 16798828.
18. Costa AD, Quinlan CL, Andrukhiv A, West IC, Jaburek M, Garlid KD. The direct physiological effects of mitoK(ATP) opening on heart mitochondria. Am J Physiol Heart Circ Physiol 2006, 290:H406-415.
19. Costa AD, Jakob R, Costa CL, Andrukhiv K, West IC, Garlid KD. The mechanism by which the mitochondrial ATP-sensitive K + channel opening and H2O2 inhibit the mitochondrial permeability transition. J Biol Chem 2006, 281:20801-20808. 10.1074/jbc.M600959200, 16720572.
20. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD. Bioenergetic consequences of opening the ATP-sensitive K(+) channel of heart mitochondria. Am J Physiol Heart Circ Physiol 2001, 280:H649-657.
21. Hansson MJ, Morota S, Teilum M, Mattiasson G, Uchino H, Elmer E. Increased potassium conductance of brain mitochondria induces resistance to permeability transition by enhancing matrix volume. J Biol Chem 2010, 285:741-750. 10.1074/jbc.M109.017731, 2804223, 19880514.
22. Nohl H, Kozlov AV, Gille L, Staniek K. Cell respiration and formation of reactive oxygen species: facts and artefacts. Biochem Soc Trans 2003, 31:1308-1311. 10.1042/BST0311308, 14641050.
23. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 2005, 70:200-214.
24. Hansson MJ, Mansson R, Morota S, Uchino H, Kallur T, Sumi T, Ishii N, Shimazu M, Keep MF, Jegorov A, Elmer E. Calcium-induced generation of reactive oxygen species in brain mitochondria is mediated by permeability transition. Free Radic Biol Med 2008, 45:284-294. 10.1016/j.freeradbiomed.2008.04.021, 18466779.
25. Holmuhamedov EL, Wang L, Terzic A. ATP-sensitive K + channel openers prevent Ca2+ overload in rat cardiac mitochondria. J Physiol 1999, 519(Pt 2):347-360. 2269505, 10457054.
26. Chalmers S, Nicholls DG. The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J Biol Chem 2003, 278:19062-19070. 10.1074/jbc.M212661200, 12660243.
27. Hunter DR, Haworth RA. The Ca2+-induced membrane transition in mitochondria. I. The protective mechanisms. Arch Biochem Biophys 1979, 195:453-459. 10.1016/0003-9861(79)90371-0, 383019.
28. Bernardi P. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 1992, 267:8834-8839.
29. Halestrap AP. The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim Biophys Acta 1989, 973:355-382. 10.1016/S0005-2728(89)80378-0, 2647140.
30. Devin A, Espie P, Guerin B, Rigoulet M. Energetics of swelling in isolated hepatocytes: a comprehensive study. Mol Cell Biochem 1998, 184:107-121. 10.1023/A:1006847214074, 9746316.
31. Nicholls DG, Lindberg O. Inhibited respiration and ATPase activity of rat liver mitochondria under conditions of matrix condensation. FEBS Lett 1972, 25:61-64. 10.1016/0014-5793(72)80454-X, 11946721.
32. Kossekova G, Atanasov B, Bolli R, Azzi A. Ionic-strength-dependence of the oxidation of native and pyridoxal 5′-phosphate-modified cytochromes c by cytochrome c oxidase. Biochem J 1989, 262:591-596. 1133309, 2553004.
33. Gogvadze V, Robertson JD, Enoksson M, Zhivotovsky B, Orrenius S. Mitochondrial cytochrome c release may occur by volume-dependent mechanisms not involving permeability transition. Biochem J 2004, 378:213-217. 10.1042/BJ20031193, 1223940, 14629197.
34. Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 1973, 134:707-716. 1177867, 4749271.
35. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997, 416:15-18. 10.1016/S0014-5793(97)01159-9, 9369223.
36. Toime LJ, Brand MD. Uncoupling protein-3 lowers reactive oxygen species production in isolated mitochondria. Free Radic Biol Med 2010, 49:606-611. 10.1016/j.freeradbiomed.2010.05.010, 2903626, 20493945.
37. 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, 102:1082-1090. 10.1161/CIRCRESAHA.107.167072, 2629616, 18356542.
38. Brown GC, Borutaite V. There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 2012, 12:1-4. 10.1016/j.mito.2011.02.001, 21303703.
39. Berndt C, Lillig CH, Holmgren A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am J Physiol Heart Circ Physiol 2007, 292:H1227-1236.
40. Sibbing D, Pfeufer A, Perisic T, Mannes AM, Fritz-Wolf K, Unwin S, Sinner MF, Gieger C, Gloeckner CJ, Wichmann HE, et al. Mutations in the mitochondrial thioredoxin reductase gene TXNRD2 cause dilated cardiomyopathy. Eur Heart J 2011, 32:1121-1133. 10.1093/eurheartj/ehq507, 21247928.
41. Horstkotte J, Perisic T, Schneider M, Lange P, Schroeder M, Kiermayer C, Hinkel R, Ziegler T, Mandal PK, David R, et al. Mitochondrial thioredoxin reductase is essential for early postischemic myocardial protection. Circulation 2011, 124:2892-2902. 10.1161/CIRCULATIONAHA.111.059253, 22144571.
42. Nagy N, Malik G, Tosaki A, Ho YS, Maulik N, Das DK. Overexpression of glutaredoxin-2 reduces myocardial cell death by preventing both apoptosis and necrosis. J Mol Cell Cardiol 2008, 44:252-260. 10.1016/j.yjmcc.2007.08.021, 18076901.
43. Nicholls DG, Budd SL. Mitochondria and neuronal survival. Physiol Rev 2000, 80:315-360.
44. Wojtovich AP, Brookes PS. The endogenous mitochondrial complex II inhibitor malonate regulates mitochondrial ATP-sensitive potassium channels: implications for ischemic preconditioning. Biochim Biophys Acta 2008, 1777:882-889. 10.1016/j.bbabio.2008.03.025, 2507763, 18433712.
45. Morota S, Hansson MJ, Ishii N, Kudo Y, Elmer E, Uchino H. Spinal cord mitochondria display lower calcium retention capacity compared with brain mitochondria without inherent differences in sensitivity to cyclophilin D inhibition. J Neurochem 2007, 103:2066-2076. 10.1111/j.1471-4159.2007.04912.x, 17868326.
46. Morota S, Manolopoulos T, Eyjolfsson A, Kimblad PO, Wierup P, Metzsch C, Blomquist S, Hansson MJ. Functional and pharmacological characteristics of permeability transition in isolated human heart mitochondria. PLoS One 2013, 8:e67747. 10.1371/journal.pone.0067747, 3695980, 23840770.
47. Hickey AJ, Renshaw GM, Speers-Roesch B, Richards JG, Wang Y, Farrell AP, Brauner CJ. A radical approach to beating hypoxia: depressed free radical release from heart fibres of the hypoxia-tolerant epaulette shark (Hemiscyllum ocellatum). J Comp Physiol B 2012, 182:91-100. 10.1007/s00360-011-0599-6, 21748398.