Abstract
A growing body of evidence suggests that oxidative stress and nitrosative stress are the common denominators in many disorders, including cardiac ischemia and reperfusion (I/R) injury resulting from coronary vascular disease. In acute myocardial infarction, two distinct types of damage occur to the heart: ischemic injury and reperfusion injury. Both ischemia and reperfusion are individually important in the manifestation of I/R injury. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) are well recognized for playing dual roles as both beneficial and harmful reactive species. ROS generation from myriad sources may contribute to tissue infarction, but mitochondrial sources of ROS, particularly from cardiomyocytes, are considered the primary sites for ROS generation during I/R. During myocardial oxidative stress (excess ROS) the generation of ROS is enhanced and the antioxidant defense mechanisms are compromised. Excess ROS can cause a feed-forward effect on further ROS generation (ROS-induced-ROS release), which is also linked to mitochondrial Ca2+ overload. These factors lead to mitochondrial dysfunction manifested as mitochondrial permeability transition pore opening and mitochondrial outer membrane permeabilization with concomitant release of apoptotic factors, inhibition of oxidative phosphorylation, depletion of cellular ATP, and subsequent cell death by apoptosis and/or necrosis. This book chapter will present a broad overview on the most current state in the discussion of the role of ROS/RNS and redox signaling in cardiac I/R injury and on potential therapeutic approaches to mitigate infarction and no-reflow following an ischemic episode.
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References
Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J (2010) Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 106(7):1253–1264
Ahmad KA, Iskandar KB, Hirpara JL, Clement MV, Pervaiz S (2004) Hydrogen peroxide-mediated cytosolic acidification is a signal for mitochondrial translocation of Bax during drug-induced apoptosis of tumor cells. Cancer Res 64(21):7867–7878
Aldakkak M, Stowe DF, Chen Q, Lesnefsky EJ, Camara AK (2008a) Inhibited mitochondrial respiration by amobarbital during cardiac ischaemia improves redox state and reduces matrix Ca2+ overload and ROS release. Cardiovasc Res 77(2):406–415
Aldakkak M, Stowe DF, Heisner JS, Spence M, Camara AK (2008b) Enhanced Na+/H+ exchange during ischemia and reperfusion impairs mitochondrial bioenergetics and myocardial function. J Cardiovasc Pharmacol 52(3):236–244
Aldakkak M, Camara AK, Heisner JS, Yang M, Stowe DF (2012) Ranolazine reduces Ca2+ overload and oxidative stress and improves mitochondrial integrity to protect against ischemia reperfusion injury in isolated hearts. Pharmcol Res 64(4):381–392
Aldakkak M, Stowe DF, Dash RK, Camara AK (2013) Mitochondrial handling of excess Ca2+ is substrate-dependent with implications for reactive oxygen species generation. Free Radic Biol Med 56:193–203
Ambrosio G, Zweier JL, Duilio C, Kuppusamy P, Santoro G, Elia PP, Tritto I, Cirillo P, Condorelli M, Chiariello M (1993) Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem 268(25):18532–18541
An J, Varadarajan SG, Camara A, Chen Q, Novalija E, Gross GJ, Stowe DF (2001) Blocking Na+/H+ exchange reduces [Na+]i and [Ca2+]i load after ischemia and improves function in intact hearts. Am J Physiol Heart Circ Physiol 281(6):H2398–H2409
Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70(2):200–214
Andrienko TN, Picht E, Bers DM (2009) Mitochondrial free calcium regulation during sarcoplasmic reticulum calcium release in rat cardiac myocytes. J Mol Cell Cardiol 46(6):1027–1036
Antico Arciuch VG, Elguero ME, Poderoso JJ, Carreras MC (2012) Mitochondrial regulation of cell cycle and proliferation. Antioxid Redox Signal 16(10):1150–1180
Aon MA, Cortassa S, Marban E, O’Rourke B (2003) Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem 278(45):44735–44744
Aon MA, Cortassa S, Maack C, O’Rourke B (2007) Sequential opening of mitochondrial ion channels as a function of glutathione redox thiol status. J Biol Chem 282(30):21889–21900
Ardanaz N, Pagano PJ (2006) Hydrogen peroxide as a paracrine vascular mediator: regulation and signaling leading to dysfunction. Exp Biol Med (Maywood) 231(3):237–251
Armstrong JS (2007) Mitochondrial medicine: pharmacological targeting of mitochondria in disease. Br J Pharmacol 151(8):1154–1165
Ashraf M, Samra ZQ (1993) Subcellular distribution of xanthine oxidase during cardiac ischemia and reperfusion: an immunocytochemical study. J Submicrosc Cytol Pathol 25(2):193–201
Azoulay-Zohar H, Israelson A, Abu-Hamad S, Shoshan-Barmatz V (2004) In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem J 377(Pt 2):347–355
Azzu V, Parker N, Brand MD (2008) High membrane potential promotes alkenal-induced mitochondrial uncoupling and influences adenine nucleotide translocase conformation. Biochem J 413(2):323–332
Baines CP (2007) The mitochondrial permeability transition pore as a target of cardioprotective signaling. Am J Physiol Heart Circ Physiol 293(2):H903–H904
Baines CP (2010) The cardiac mitochondrion: nexus of stress. Annu Rev Physiol 72:61–80
Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P (2003) Protein kinase cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92(8):873–880
Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434(7033):658–662
Ballinger SW (2005) Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med 38(10):1278–1295
Baudry N, Laemmel E, Vicaut E (2008) In vivo reactive oxygen species production induced by ischemia in muscle arterioles of mice: involvement of xanthine oxidase and mitochondria. Am J Physiol Heart Circ Physiol 294(2):H821–H828
Bazil JN, Blomeyer CA, Pradhan RK, Camara AK, Dash RK (2013) Modeling the calcium sequestration system in isolated guinea pig cardiac mitochondria. J Bioenerg Biomembr (in press)
Beauloye C, Bertrand L, Horman S, Hue L (2011) AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc Res 90(2):224–233
Becker LB (2004) New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res 61(3):461–470 [review]
Becker LB, Vanden Hoek TL, Shao ZH, Li CQ, Schumacker PT (1999) Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am J Physiol Heart Circ Physiol 277(6 Pt 2):H2240–H2246
Beckman JS, Chen J, Ischiropoulos H, Crow JP (1994) Oxidative chemistry of peroxynitrite. Methods Enzymol 233:229–240
Beckman JS, Koppenol WH (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271(5 Pt 1):C1424–C1437
Bendall JK, Cave AC, Heymes C, Gall N, Shah AM (2002) Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 105(3):293–296
Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K (2002) Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med 346(8):557–563
Bernardi P, Krauskopf A, Basso E, Petronilli V, Blachly-Dyson E, Di Lisa F, Forte MA (2006) The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 273(10):2077–2099
Betaneli V, Petrov EP, Schwille P (2012) The role of lipids in VDAC oligomerization. Biophys J 102(3):523–531
Bhagatte Y, Lodwick D, Storey N (2012) Mitochondrial ROS production and subsequent ERK phosphorylation are necessary for temperature preconditioning of isolated ventricular myocytes. Cell Death Dis 3:e345
Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282(2):1183–1192
Blomeyer CA, Bazil JN, Stowe DF, Pradhan RK, Dash RK, Camara AK (2013) Dynamic buffering of mitochondrial Ca2+ during Ca2+ uptake and Na+-induced Ca2+ release. J Bioenerg Biomembr. E-pub ahead of print
Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R (2010) Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105(6):771–785
Bolli R, Dawn B (2009) The cornucopia of “pleiotropic” actions of statins: myogenesis as a new mechanism for statin-induced benefits? Circ Res 104(2):144–146
Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287(4):C817–C833 [review]
Brown GC, Borutaite V (2004) Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim Biophys Acta 1658(1–2):44–49
Buday A, Orsy P, Godo M, Mozes M, Kokeny G, Lacza Z, Koller A, Ungvari Z, Gross ML, Benyo Z, Hamar P (2010) Elevated systemic TGF-beta impairs aortic vasomotor function through activation of NADPH oxidase-driven superoxide production and leads to hypertension, myocardial remodeling, and increased plaque formation in apoE−/− mice. Am J Physiol Heart Circ Physiol 299(2):H386–H395
Burgering BM, Medema RH (2003) Decisions on life and death: FOXO forkhead transcription factors are in command when PKB/Akt is off duty. J Leukoc Biol 73(6):689–701
Burwell LS, Brookes PS (2008) Mitochondria as a target for the cardioprotective effects of nitric oxide in ischemia-reperfusion injury. Antioxid Redox Signal 10(3):579–599
Burwell LS, Nadtochiy SM, Tompkins AJ, Young S, Brookes PS (2006) Direct evidence for S-nitrosation of mitochondrial complex I. Biochem J 394(3):627–634
Burwell LS, Nadtochiy SM, Brookes PS (2009) Cardioprotection by metabolic shut-down and gradual wake-up. J Mol Cell Cardiol 46(6):804–810
Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29(3–4):222–230
Camara AK, An J, Chen Q, Novalija E, Varadarajan SG, Schelling P, Stowe DF (2003) Na+/H+ exchange inhibition with cardioplegia reduces cytosolic [Ca2+] and myocardial damage after cold ischemia. J Cardiovasc Pharmacol 41(5):686–698
Camara AK, Aldakkak M, Heisner JS, Rhodes SS, Riess ML, An J, Heinen A, Stowe DF (2007) ROS scavenging before 27 °C ischemia protects hearts and reduces mitochondrial ROS, Ca2+ overload, and changes in redox state. Am J Physiol Cell Physiol 292:C2021–C2031
Camara AK, Lesnefsky EJ, Stowe DF (2010) Potential therapeutic benefits of strategies directed to mitochondria. Antioxid Redox Signal 13(3):279–347
Camara AK, Aldakkak M, Bienengraeber M, Stowe DF (2011a) Cardioprotection by pre- and post-conditioning: implications for the role of mitochondria. Acta Anaesthesiologica Croatica 8(1):7–18
Camara AK, Aldakkak M, Stowe DF (2011b) Mitochondria as potential therapeutic targets in mitochondria-related diseases. In: Svensson OL (ed) Mitochondria structure, functions and dysfunctions. Nova Science, New York, pp 471–552
Camara AK, Bienengraeber M, Stowe DF (2011c) Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front Physiol 2(13):1–34
Carpi A, Menabo R, Kaludercic N, Pelicci P, Di Lisa F, Giorgio M (2009) The cardioprotective effects elicited by p66Shc ablation demonstrate the crucial role of mitochondrial ROS formation in ischemia/reperfusion injury. Biochim Biophys Acta 1787(7):774–780
Castiglione N, Rinaldo S, Giardina G, Stelitano V, Cutruzzola F (2012) Nitrite and nitrite reductases: from molecular mechanisms to significance in human health and disease. Antioxid Redox Signal 17(4):684–716
Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, Shah AM (2006) NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 8(5–6):691–728
Ceolotto G, Gallo A, Papparella I, Franco L, Murphy E, Iori E, Pagnin E, Fadini GP, Albiero M, Semplicini A, Avogaro A (2007) Rosiglitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPK-dependent mechanism. Arterioscler Thromb Vasc Biol 27(12):2627–2633
Chandra S, Romero MJ, Shatanawi A, Alkilany AM, Caldwell RB, Caldwell RW (2012) Oxidative species increase arginase activity in endothelial cells through the RhoA/Rho kinase pathway. Br J Pharmacol 165(2):506–519
Chen X, Niroomand F, Liu Z, Zankl A, Katus HA, Jahn L, Tiefenbacher CP (2006) Expression of nitric oxide related enzymes in coronary heart disease. Basic Res Cardiol 101(4):346–353
Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2008) Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol 294(2):C460–C466
Chen Q, Paillard M, Gomez L, Li H, Hu Y, Lesnefsky EJ (2012) Postconditioning modulates ischemia-damaged mitochondria during reperfusion. J Cardiovasc Pharmacol 59(1):101–108
Cheng Z, Volkers M, Din S, Avitabile D, Khan M, Gude N, Mohsin S, Bo T, Truffa S, Alvarez R, Mason M, Fischer KM, Konstandin MH, Zhang XK, Heller Brown J, Sussman MA (2011) Mitochondrial translocation of Nur77 mediates cardiomyocyte apoptosis. Eur Heart J 32(17):2179–2188
Chinta SJ, Kumar JM, Zhang H, Forman HJ, Andersen JK (2006) Up-regulation of gamma-glutamyl transpeptidase activity following glutathione depletion has a compensatory rather than an inhibitory effect on mitochondrial complex I activity: implications for Parkinson’s disease. Free Radic Biol Med 40(9):1557–1563
Cho S, Szeto HH, Kim E, Kim H, Tolhurst AT, Pinto JT (2007) A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J Biol Chem 282(7):4634–4642
Choi SY, Gonzalvez F, Jenkins GM, Slomianny C, Chretien D, Arnoult D, Petit PX, Frohman MA (2007) Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Differ 14(3):597–606
Choksi KB, Boylston WH, Rabek JP, Widger WR, Papaconstantinou J (2004) Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim Biophys Acta 1688(2):95–101
Churchill EN, Murriel CL, Chen CH, Mochly-Rosen D, Szweda LI (2005) Reperfusion-induced translocation of deltaPKC to cardiac mitochondria prevents pyruvate dehydrogenase reactivation. Circ Res 97(1):78–85
Churchill EN, Szweda LI (2005) Translocation of deltaPKC to mitochondria during cardiac reperfusion enhances superoxide anion production and induces loss in mitochondrial function. Arch Biochem Biophys 439(2):194–199
Churchill EN, Mochly-Rosen D (2007) The roles of PKCdelta and epsilon isoenzymes in the regulation of myocardial ischaemia/reperfusion injury. Biochem Soc Trans 35(5):1040–1042
Clarke SJ, Khaliulin I, Das M, Parker JE, Heesom KJ, Halestrap AP (2008) 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 102(9):1082–1090
Cohen MV, Downey JM (2011) Ischemic postconditioning: from receptor to end-effector. Antioxid Redox Signal 14(5):821–831
Cohen MV, Yang XM, Downey JM (2007) The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation 115(14):1895–1903
Cohen MV, Yang XM, Downey JM (2008) Acidosis, oxygen, and interference with mitochondrial permeability transition pore formation in the early minutes of reperfusion are critical to postconditioning’s success. Basic Res Cardiol 103(5):464–471
Costa NJ, Dahm CC, Hurrell F, Taylor ER, Murphy MP (2003) Interactions of mitochondrial thiols with nitric oxide. Antioxid Redox Signal 5(3):291–305
Dahm CC, Moore K, Murphy MP (2006) Persistent S-nitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite: implications for the interaction of nitric oxide with mitochondria. J Biol Chem 281(15):10056–10065
Das S, Steenbergen C, Murphy E (2012) Does the voltage dependent anion channel modulate cardiac ischemia-reperfusion injury? Biochim Biophys Acta 1818(6):1451–1456
Dasgupta A, Zheng J, Bizzozero OA (2012) Protein carbonylation and aggregation precede neuronal apoptosis induced by partial glutathione depletion. ASN Neuro 4(3):161–174
de Jong JW, Schoemaker RG, de Jonge R, Bernocchi P, Keijzer E, Harrison R, Sharma HS, Ceconi C (2000) Enhanced expression and activity of xanthine oxidoreductase in the failing heart. J Mol Cell Cardiol 32(11):2083–2089
Di Lisa F, Blank PS, Colonna R, Gambassi G, Silverman HS, Stern MD, Hansford RG (1995) Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition. J Physiol 486(1):1–13
Di Lisa F, Kaludercic N, Carpi A, Menabo R, Giorgio M (2009) Mitochondrial pathways for ROS formation and myocardial injury: the relevance of p66(Shc) and monoamine oxidase. Basic Res Cardiol 104(2):131–139
Di Lisa F, Canton M, Carpi A, Kaludercic N, Menabo R, Menazza S, Semenzato M (2011) Mitochondrial injury and protection in ischemic pre- and postconditioning. Antioxid Redox Signal 14(5):881–891
Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI (2010) Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107(1):106–116
Doerries C, Grote K, Hilfiker-Kleiner D, Luchtefeld M, Schaefer A, Holland SM, Sorrentino S, Manes C, Schieffer B, Drexler H, Landmesser U (2007) Critical role of the NAD(P)H oxidase subunit p47phox for left ventricular remodeling/dysfunction and survival after myocardial infarction. Circ Res 100(6):894–903
Doughan AK, Harrison DG, Dikalov SI (2008) Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102(4):488–496
Downey JM, Miura T, Eddy LJ, Chambers DE, Mellert T, Hearse DJ, Yellon DM (1987) Xanthine oxidase is not a source of free radicals in the ischemic rabbit heart. J Mol Cell Cardiol 19(11):1053–1060
Downey JM, Davis AM, Cohen MV (2007) Signaling pathways in ischemic preconditioning. Heart Fail Rev 12(3–4):181–188
Duan Y, Gross RA, Sheu SS (2007) Ca2+−Dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J Physiol 585(Pt 3):741–758
Duncan JG, Ravi R, Stull LB, Murphy AM (2005) Chronic xanthine oxidase inhibition prevents myofibrillar protein oxidation and preserves cardiac function in a transgenic mouse model of cardiomyopathy. Am J Physiol Heart Circ Physiol 289(4):H1512–H1518
Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, Portero-Otin M, Pamplona R, Vidal-Puig AJ, Wang S, Roebuck SJ, Brand MD (2003) A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J 22(16):4103–4110
Favero TG, Zable AC, Abramson JJ (1995) Hydrogen peroxide stimulates the Ca2+ release channel from skeletal muscle sarcoplasmic reticulum. J Biol Chem 270(43):25557–25563
Flaherty JT, Pitt B, Gruber JW, Heuser RR, Rothbaum DA, Burwell LR, George BS, Kereiakes DJ, Deitchman D, Gustafson N et al (1994) Recombinant human superoxide dismutase (h-SOD) fails to improve recovery of ventricular function in patients undergoing coronary angioplasty for acute myocardial infarction. Circulation 89(5):1982–1991
Fulop N, Marchase RB, Chatham JC (2007) Role of protein O-linked N-acetyl-glucosamine in mediating cell function and survival in the cardiovascular system. Cardiovasc Res 73(2):288–297
Gadicherla AK, Stowe DF, Antholine WE, Yang M, Camara AK (2012) Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine. Biochim Biophys Acta 1817(3):419–429
Gertz M, Steegborn C (2010) The lifespan-regulator p66Shc in mitochondria: redox enzyme or redox sensor? Antioxid Redox Signal 13(9):1417–1428
Geula S, Ben-Hail D, Shoshan-Barmatz V (2012) Structure-based analysis of VDAC1: N-terminus location, translocation, channel gating and association with anti-apoptotic proteins. Biochem J 444(3):475–485
Gidday JM, Park TS, Shah AR, Gonzales ER (1998) Modulation of basal and postischemic leukocyte-endothelial adherence by nitric oxide. Stroke 29(7):1423–1429 discussion 1429–30
Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122(2):221–233
Gonzalez DR, Treuer AV, Castellanos J, Dulce RA, Hare JM (2010) Impaired S-nitrosylation of the ryanodine receptor caused by xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem 285(37):28938–28945
Gopalakrishna R, Jaken S (2000) Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28(9):1349–1361
Granville DJ, Tashakkor B, Takeuchi C, Gustafsson AB, Huang C, Sayen MR, Wentworth P Jr, Yeager M, Gottlieb RA (2004) Reduction of ischemia and reperfusion-induced myocardial damage by cytochrome P450 inhibitors. Proc Natl Acad Sci USA 101(5):1321–1326
Griendling KK, Sorescu D, Ushio-Fukai M (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86(5):494–501
Griffiths EJ, Halestrap AP (1995) Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 307(1):93–98
Griffiths EJ, Ocampo CJ, Savage JS, Stern MD, Silverman HS (2000) Protective effects of low and high doses of cyclosporin a against reoxygenation injury in isolated rat cardiomyocytes are associated with differential effects on mitochondrial calcium levels. Cell Calcium 27(2):87–95
Gross GJ, O’Rourke ST, Pelc LR, Warltier DC (1992) Myocardial and endothelial dysfunction after multiple, brief coronary occlusions: role of oxygen radicals. Am J Physiol 263(6 Pt 2):H1703–H1709
Group, T. H. A. C. A. S (2002) Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med 346(8):549–556
Grover AK, Samson SE (1988) Effect of superoxide radical on Ca2+ pumps of coronary artery. Am J Physiol 255(3 Pt 1):C297–C303
Grum CM, Gallagher KP, Kirsh MM, Shlafer M (1989) Absence of detectable xanthine oxidase in human myocardium. J Mol Cell Cardiol 21(3):263–267
Gunter TE, Pfeiffer DR (1990) Mechanisms by which mitochondria transport calcium. Am J Physiol 258(5 Pt 1):C755–C786
Guo J, Gertsberg Z, Ozgen N, Steinberg SF (2009) p66Shc Links alpha1-adrenergic receptors to a reactive oxygen species-dependent AKT-FOXO3A phosphorylation pathway in cardiomyocytes. Circ Res 104(5):660–669
Guzik TJ, Sadowski J, Guzik B, Jopek A, Kapelak B, Przybylowski P, Wierzbicki K, Korbut R, Harrison DG, Channon KM (2006) Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler Thromb Vasc Biol 26(2):333–339
Guzy RD, Schumacker PT (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91(5):807–819 [review]
Ha T, Liu L, Kelley J, Kao R, Williams D, Li C (2011) Toll-like receptors: new players in myocardial ischemia/reperfusion injury. Antioxid Redox Signal 15(7):1875–1893
Halestrap AP (2009) Mitochondrial calcium in health and disease. Biochim Biophys Acta 1787(11):1289–1290
Halestrap AP, Pasdois P (2009) The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta 1787(11):1402–1415
Halestrap AP, Kerr PM, Javadov S, Woodfield KY (1998) Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart. Biochim Biophys Acta 1366(1–2):79–94
Halliwell B, Gutteridge JMC (1999) Free radical in biology and medicine, 3rd edn. Oxford University Press, New York, p 936
Handy DE, Loscalzo J (2012) Redox regulation of mitochondrial function. Antioxid Redox Signal 16(11):1323–1367
Hanley PJ, Daut J (2005) KATP channels and preconditioning: a re-examination of the role of mitochondrial KATP channels and an overview of alternative mechanisms. J Mol Cell Cardiol 39(1):17–50
Hanukoglu I, Rapoport R (1995) Routes and regulation of NADPH production in steroidogenic mitochondria. Endocr Res 21(1–2):231–241
Hausenloy DJ, Yellon DM (2007) Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection. Heart Fail Rev 12(3–4):217–234
Hausenloy DJ, Ong SB, Yellon DM (2009) The mitochondrial permeability transition pore as a target for preconditioning and postconditioning. Basic Res Cardiol 104(2):189–202
Haworth RA, Hunter DR (1979) The Ca2+−induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site. Arch Biochem Biophys 195(2):460–467
Heinen A, Aldakkak M, Stowe DF, Rhodes SS, Riess ML, Varadarajan SG, Camara AK (2007) Reverse electron flow-induced ROS production is attenuated by activation of mitochondrial Ca2+-sensitive K+ channels. Am J Physiol Heart Circ Physiol 293(3):H1400–H1407
Hirata N, Shim YH, Pravdic D, Lohr NL, Pratt PF Jr, Weihrauch D, Kersten JR, Warltier DC, Bosnjak ZJ, Bienengraeber M (2012) Isoflurane differentially modulates mitochondrial reactive oxygen species production via forward versus reverse electron transport flow: implications for preconditioning. Anesthesiology 115(3):531–540
Hirota Y, Kang D, Kanki T (2012) The physiological role of mitophagy: new insights into phosphorylation events. Int J Cell Biol 2012, 354914
Hortelano S, Alvarez AM, Bosca L (1999) Nitric oxide induces tyrosine nitration and release of cytochrome c preceding an increase of mitochondrial transmembrane potential in macrophages. FASEB J 13(15):2311–2317
Hoye AT, Davoren JE, Wipf P, Fink MP, Kagan VE (2008) Targeting mitochondria. Acc Chem Res 41(1):87–97
Hunter AL, Bai N, Laher I, Granville DJ (2005) Cytochrome p450 2C inhibition reduces post-ischemic vascular dysfunction. Vascul Pharmacol 43(4):213–219
Javadov S, Karmazyn M, Escobales N (2009) Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases. J Pharmacol Exp Ther 330(3):670–678
Jolly SR, Kane WJ, Bailie MB, Abrams GD, Lucchesi BR (1984) Canine myocardial reperfusion injury. Its reduction by the combined administration of superoxide dismutase and catalase. Circ Res 54(3):277–285
Jordan JE, Zhao ZQ, Vinten-Johansen J (1999) The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc Res 43(4):860–878
Judkins CP, Diep H, Broughton BR, Mast AE, Hooker EU, Miller AA, Selemidis S, Dusting GJ, Sobey CG, Drummond GR (2010) Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE−/− mice. Am J Physiol Heart Circ Physiol 298(1):H24–H32
Kaludercic N, Takimoto E, Nagayama T, Feng N, Lai EW, Bedja D, Chen K, Gabrielson KL, Blakely RD, Shih JC, Pacak K, Kass DA, Di Lisa F, Paolocci N (2010) Monoamine oxidase a-mediated enhanced catabolism of norepinephrine contributes to adverse remodeling and pump failure in hearts with pressure overload. Circ Res 106(1):193–202
Kaludercic N, Carpi A, Menabo R, Di Lisa F, Paolocci N (2011) Monoamine oxidases (MAO) in the pathogenesis of heart failure and ischemia/reperfusion injury. Biochim Biophys Acta 1813(7):1323–1332
Kanno T, Kobuchi H, Kajitani N, Utsumi T, Yano H, Horton AA, Yasuda T, Utsumi K (2002) Mevastatin, an inhibitor of HMG-CoA reductase, induces apoptosis, differentiation and Rap1 expression in HL-60 cells. Physiol Chem Phys Med NMR 34(1):1–15
Kanno T, Sato EE, Muranaka S, Fujita H, Fujiwara T, Utsumi T, Inoue M, Utsumi K (2004) Oxidative stress underlies the mechanism for Ca2+-induced permeability transition of mitochondria. Free Radic Res 38(1):27–35
Keinan N, Tyomkin D, Shoshan-Barmatz V (2010) Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol Cell Biol 30(24):5698–5709
Kevin LG, Camara AK, Riess ML, Novalija E, Stowe DF (2003) Ischemic preconditioning alters real-time measure of O2 radicals in intact hearts with ischemia and reperfusion. Am J Physiol Heart Circ Physiol 284(2):H566–H574
Khadour FH, Panas D, Ferdinandy P, Schulze C, Csont T, Lalu MM, Wildhirt SM, Schulz R (2002) Enhanced NO and superoxide generation in dysfunctional hearts from endotoxemic rats. Am J Physiol Heart Circ Physiol 283(3):H1108–H1115
Kibbey RG, Pongratz RL, Romanelli AJ, Wollheim CB, Cline GW, Shulman GI (2007) Mitochondrial GTP regulates glucose-stimulated insulin secretion. Cell Metab 5(4):253–264
Kim HD, Kim CH, Rah BJ, Chung HI, Shim TS (1994) Quantitative study on the relation between structural and functional properties of the hearts from three different mammals. Anat Rec 238(2):199–206
Kim JS, Jin Y, Lemasters JJ (2006) Reactive oxygen species, but not Ca2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 290(5):H2024–H2034
Kimura S, Zhang GX, Nishiyama A, Shokoji T, Yao L, Fan YY, Rahman M, Suzuki T, Maeta H, Abe Y (2005) Role of NAD(P)H oxidase- and mitochondria-derived reactive oxygen species in cardioprotection of ischemic reperfusion injury by angiotensin II. Hypertension 45(5):860–866
Kloner RA (2012) No-reflow phenomenon: maintaining vascular integrity. J Cardiovasc Pharmacol Ther 16(3–4):244–250
Kloner RA, Hale SL, Dai W, Gorman RC, Shuto T, Koomalsingh KJ, Gorman JH, Sloan RC, Frasier CR, Watson CA, Bostian PA, Kypson AP, Brown DA (2012) Reduction of ischemia/reperfusion injury with bendavia, a mitochondria-targeting cytoprotective peptide. J Am Heart Assoc 1(3):e001644
Kohda Y, Gemba M (2005) Cephaloridine induces translocation of protein kinase C delta into mitochondria and enhances mitochondrial generation of free radicals in the kidney cortex of rats causing renal dysfunction. J Pharmacol Sci 98(1):49–57
Kohr MJ, Sun J, Aponte A, Wang G, Gucek M, Murphy E, Steenbergen C (2011) Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ischemia/reperfusion injury with resin-assisted capture. Circ Res 108(4):418–426
Konishi H, Tanaka M, Takemura Y, Matsuzaki H, Ono Y, Kikkawa U, Nishizuka Y (1997) Activation of protein kinase C by tyrosine phosphorylation in response to H2O2. Proc Natl Acad Sci USA 94(21):11233–11237
Korge P, Yang L, Yang JH, Wang Y, Qu Z, Weiss JN (2011) Protective role of transient pore openings in calcium handling by cardiac mitochondria. J Biol Chem 286(40):34851–34857
Koszela-Piotrowska I, Matkovic K, Szewczyk A, Jarmuszkiewicz W (2009) A large-conductance calcium-activated potassium channel in potato (solanum tuberosum) tuber mitochondria. Biochem J 424(2):307–316
Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J (2010) NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci USA 107(35):15565–15570
Lam EW, Francis RE, Petkovic M (2006) FOXO transcription factors: key regulators of cell fate. Biochem Soc Trans 34(5):722–726
Lambert AJ, Brand MD (2004) Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem 279(38):39414–39420
Landmesser U, Spiekermann S, Dikalov S, Tatge H, Wilke R, Kohler C, Harrison DG, Hornig B, Drexler H (2002) Vascular oxidative stress and endothelial dysfunction in patients with chronic heart failure: role of xanthine-oxidase and extracellular superoxide dismutase. Circulation 106(24):3073–3078
Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111(8):1201–1209
Landmesser U, Spiekermann S, Preuss C, Sorrentino S, Fischer D, Manes C, Mueller M, Drexler H (2007) Angiotensin II induces endothelial xanthine oxidase activation: role for endothelial dysfunction in patients with coronary disease. Arterioscler Thromb Vasc Biol 27(4):943–948
Lassegue B, Clempus RE (2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285(2):R277–R297
Lebuffe G, Schumacker PT, Shao ZH, Anderson T, Iwase H, Vanden Hoek TL (2003) ROS and NO trigger early preconditioning: relationship to mitochondrial KATP channel. Am J Physiol Heart Circ Physiol 284(1):H299–H308
Lee J, Giordano S, Zhang J (2012) Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441(2):523–540
Lehninger AL, Vercesi A, Bababunmi EA (1978) Regulation of Ca2+ release from mitochondria by the oxidation-reduction state of pyridine nucleotides. Proc Natl Acad Sci USA 75(4):1690–1694
Lemasters JJ, Holmuhamedov E (2006) Voltage-dependent anion channel (VDAC) as mitochondrial governator–thinking outside the box. Biochim Biophys Acta 1762(2):181–190
Lenaz G, Baracca A, Barbero G, Bergamini C, Dalmonte ME, Del Sole M, Faccioli M, Falasca A, Fato R, Genova ML, Sgarbi G, Solaini G (2010) Mitochondrial respiratory chain super-complex I–III in physiology and pathology. Biochim Biophys Acta 1797(6–7):633–640
Lesnefsky EJ, Gudz TI, Migita CT, Ikeda-Saito M, Hassan MO, Turkaly PJ, Hoppel CL (2001) 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(1):117–128
Li Q, Sato EF, Zhu X, Inoue M (2009) A simultaneous release of SOD1 with cytochrome c regulates mitochondria-dependent apoptosis. Mol Cell Biochem 322(1–2):151–159
Lira VA, Benton CR, Yan Z, Bonen A (2010) PGC-1alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am J Physiol Endocrinol Metab 299(2):E145–E161
Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80(5):780–787
Liu YH, Carretero OA, Cingolani OH, Liao TD, Sun Y, Xu J, Li LY, Pagano PJ, Yang JJ, Yang XP (2005) Role of inducible nitric oxide synthase in cardiac function and remodeling in mice with heart failure due to myocardial infarction. Am J Physiol Heart Circ Physiol 289(6):H2616–H2623
Liu M, Liu H, Dudley SC Jr (2010) Reactive oxygen species originating from mitochondria regulate the cardiac sodium channel. Circ Res 107(8):967–974
Lustgarten MS, Bhattacharya A, Muller FL, Jang YC, Shimizu T, Shirasawa T, Richardson A, Van Remmen H (2012) Complex I generated, mitochondrial matrix-directed superoxide is released from the mitochondria through voltage dependent anion channels. Biochem Biophys Res Commun 422(3):515–521
Maciel EN, Vercesi AE, Castilho RF (2001) Oxidative stress in Ca2+-induced membrane permeability transition in brain mitochondria. J Neurochem 79(6):1237–1245
Martinez MC, Andriantsitohaina R (2009) Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid Redox Signal 11(3):669–702
Mattson MP, Kroemer G (2003) Mitochondria in cell death: novel targets for neuroprotection and cardioprotection. Trends Mol Med 9(5):196–205
McCommis KS, Baines CP (2012) The role of VDAC in cell death: friend or foe? Biochim Biophys Acta 1818(6):1444–1450
Mello CF, Sultana R, Piroddi M, Cai J, Pierce WM, Klein JB, Butterfield DA (2007) Acrolein induces selective protein carbonylation in synaptosomes. Neuroscience 147(3):674–679
Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G, Pawson T, Di Fiore PP, Lanfrancone L, Pelicci PG (1997) Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J 16(4):706–716
Miura T, Tanno M (2012) The mPTP and its regulatory proteins: final common targets of signalling pathways for protection against necrosis. Cardiovasc Res 94(2):181–189
Miura T, Downey JM, Hotta D, Iimura O (1988) Effect of superoxide dismutase plus catalase on myocardial infarct size in rabbits. Can J Cardiol 4(8):407–411
Morin D, Assaly R, Paradis S, Berdeaux A (2009) Inhibition of mitochondrial membrane permeability as a putative pharmacological target for cardioprotection. Curr Med Chem 16(33):4382–4398
Morris RG (2003) Cyclosporin therapeutic drug monitoring – an established service revisited. Clin Biochem Rev 24(2):33–46
Murdoch CE, Zhang M, Cave AC, Shah AM (2006) NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc Res 71(2):208–215
Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417(1):1–13
Murphy E, Steenbergen C (2008) Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 88(2):581–609
Murphy E, Steenbergen C (2011) What makes the mitochondria a killer? Can we condition them to be less destructive? Biochim Biophys Acta 1813(7):1302–1308
Murray J, Taylor SW, Zhang B, Ghosh SS, Capaldi RA (2003) Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem 278(39):37223–37230
Murray AJ, Edwards LM, Clarke K (2007) Mitochondria and heart failure. Curr Opin Clin Nutr Metab Care 10(6):704–711
Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124–1136
Nadtochiy SM, Burwell LS, Brookes PS (2007) Cardioprotection and mitochondrial S-nitrosation: effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury. J Mol Cell Cardiol 42(4):812–825
Nakagami H, Takemoto M, Liao JK (2003) NADPH oxidase-derived superoxide anion mediates angiotensin II-induced cardiac hypertrophy. J Mol Cell Cardiol 35(7):851–859
Nathan C, Xie QW (1994) Regulation of biosynthesis of nitric oxide. J Biol Chem 269(19):13725–13728
Nediani C, Raimondi L, Borchi E, Cerbai E (2011) Nitric oxide/reactive oxygen species generation and nitroso/redox imbalance in heart failure: from molecular mechanisms to therapeutic implications. Antioxid Redox Signal 14(2):289–331
Nickenig G, Strehlow K, Baumer AT, Baudler S, Wassmann S, Sauer H, Bohm M (2000) Negative feedback regulation of reactive oxygen species on AT1 receptor gene expression. Br J Pharmacol 131(4):795–803
Nowak G, Bakajsova D, Samarel AM (2011) Protein kinase C-epsilon activation induces mitochondrial dysfunction and fragmentation in renal proximal tubules. Am J Physiol Renal Physiol 301(1):F197–F208
Ohnishi ST, Ohnishi T, Muranaka S, Fujita H, Kimura H, Uemura K, Yoshida K, Utsumi K (2005) A possible site of superoxide generation in the complex I segment of rat heart mitochondria. J Bioenerg Biomembr 37(1):1–15
Ostrander DB, Sparagna GC, Amoscato AA, McMillin JB, Dowhan W (2001) Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis. J Biol Chem 276(41):38061–38067
Otera H, Mihara K (2012) Mitochondrial dynamics: functional link with apoptosis. Int J Cell Biol. 2012, 821676
Outten CE, Culotta VC (2003) A novel NADH kinase is the mitochondrial source of NADPH in saccharomyces cerevisiae. EMBO J 22(9):2015–2024
Paillard M, Gomez L, Augeul L, Loufouat J, Lesnefsky EJ, Ovize M (2009) Postconditioning inhibits mPTP opening independent of oxidative phosphorylation and membrane potential. J Mol Cell Cardiol 46(6):902–909
Paradies G, Petrosillo G, Paradies V, Ruggiero FM (2009) Role of cardiolipin peroxidation and Ca2+ in mitochondrial dysfunction and disease. Cell Calcium 45(6):643–650
Pasdois P, Parker JE, Griffiths EJ, Halestrap AP (2011) The role of oxidized cytochrome c in regulating mitochondrial reactive oxygen species production and its perturbation in ischaemia. Biochem J 436(2):493–505
Penna C, Rastaldo R, Mancardi D, Raimondo S, Cappello S, Gattullo D, Losano G, Pagliaro P (2006) Post-conditioning induced cardioprotection requires signaling through a redox-sensitive mechanism, mitochondrial ATP-sensitive K+ channel and protein kinase C activation. Basic Res Cardiol 101(2):180–189
Penna C, Perrelli MG, Raimondo S, Tullio F, Merlino A, Moro F, Geuna S, Mancardi D, Pagliaro P (2009) Postconditioning induces an anti-apoptotic effect and preserves mitochondrial integrity in isolated rat hearts. Biochim Biophys Acta 1787(7):794–801
Penna C, Perrelli MG, Pagliaro P (2013) Mitochondrial pathways, permeability transition pore and redox signaling in cardioprotection: therapeutic implications. Antioxid Redox Signal 18(5):556–599
Pesaresi MG, Amori I, Giorgi C, Ferri A, Fiorenzo P, Gabanella F, Salvatore AM, Giorgio M, Pelicci PG, Pinton P, Carri MT, Cozzolino M (2011) Mitochondrial redox signalling by p66Shc mediates ALS-like disease through Rac1 inactivation. Hum Mol Genet 20(21):4196–4208
Petronilli V, Penzo D, Scorrano L, Bernardi P, Di Lisa F (2001) The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J Biol Chem 276(15):12030–12034
Petrosillo G, Ruggiero FM, Di Venosa N, Paradies G (2003) Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin. FASEB J 17(6):714–716
Petrosillo G, Ruggiero FM, Pistolese M, Paradies G (2004) Ca2+−Induced reactive oxygen species production promotes cytochrome c release from rat liver mitochondria via mitochondrial permeability transition (MPT)-dependent and MPT-independent mechanisms: role of cardiolipin. J Biol Chem 279(51):53103–53108
Piantadosi CA (2012) Regulation of mitochondrial processes by protein S-nitrosylation. Biochim Biophys Acta 1820(6):712–721
Piantadosi CA, Suliman HB (2012) Transcriptional control of mitochondrial biogenesis and its interface with inflammatory processes. Biochim Biophys Acta 1820(4):532–541
Pipinos II, Judge AR, Zhu Z, Selsby JT, Swanson SA, Johanning JM, Baxter BT, Lynch TG, Dodd SL (2006) Mitochondrial defects and oxidative damage in patients with peripheral arterial disease. Free Radic Biol Med 41(2):262–269
Pradhan RK, Beard DA, Dash RK (2010) A biophysically based mathematical model for the kinetics of mitochondrial Na+-Ca2+ antiporter. Biophys J 98(2):218–230
Pravdic DB, Sedlic F, Stadnicka A, Bosnjak Z (2008) Intracellular Ca2+ and pH modulation of in cardiomyocytes during postconditioning. Anesthesiology 109:A859
Pravdic D, Mio Y, Sedlic F, Pratt PF, Warltier DC, Bosnjak ZJ, Bienengraeber M (2010) Isoflurane protects cardiomyocytes and mitochondria by immediate and cytosol-independent action at reperfusion. Br J Pharmacol 160(2):220–232
Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, Vitturi DA, Patel RP, Hiley CR, Abakumova I, Requejo R, Chouchani ET, Hurd TR, Garvey JF, Taylor CT, Brookes PS, Smith RA, Murphy MP (2009) A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci USA 106(26):10764–10769
Puri N, Zhang F, Monu SR, Sodhi K, Bellner L, Lamon BD, Zhang Y, Abraham NG, Nasjletti A (2013) Antioxidants condition pleiotropic vascular responses to exogenous H2O2: role of modulation of vascular TP receptors and the heme oxygenase system. Antioxid Redox Signal 18(5):471–480
Raha S, McEachern GE, Myint AT, Robinson BH (2000) Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase. Free Radic Biol Med 29(2):170–180
Rapola JM, Virtamo J, Ripatti S, Huttunen JK, Albanes D, Taylor PR, Heinonen OP (1997) Randomised trial of alpha-tocopherol and beta-carotene supplements on incidence of major coronary events in men with previous myocardial infarction. Lancet 349(9067):1715–1720
Ricci JE, Gottlieb RA, Green DR (2003) Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160(1):65–75
Riess ML, Camara AK, Kevin LG, An J, Stowe DF (2004) Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 °C ischemia in intact hearts. Cardiovasc Res 61(3):580–590
Robin E, Guzy RD, Loor G, Iwase H, Waypa GB, Marks JD, Hoek TL, Schumacker PT (2007) Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion. J Biol Chem 282(26):19133–19143
Ronson RS, Nakamura M, Vinten-Johansen J (1999) The cardiovascular effects and implications of peroxynitrite. Cardiovasc Res 44(1):47–59
Ross R (1999) Atherosclerosis – an inflammatory disease. N Engl J Med 340(2):115–126
Rostovtseva T (2011) Control of mitochondrial outer membrane permeability: VDAC regulation by dimeric tubulin and cytosolic protein. In: Svensson OL (ed) Mitochondria structure, functions and dysfunctions. Nova Science, New York, pp 607–633
Rostovtseva T, Colombini M (1997) VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophys J 72(5):1954–1962
Rush JD, Maskos Z, Koppenol WH (1990) Distinction between hydroxyl radical and ferryl species. Methods Enzymol 186:148–156
Saeed SA, Waqar MA, Zubairi AJ, Bhurgri H, Khan A, Gowani SA, Waqar SN, Choudhary MI, Jalil S, Zaidi AH, Ara I (2005) Myocardial ischaemia and reperfusion injury: reactive oxygen species and the role of neutrophil. J Coll Physicians Surg Pak 15(8):507–514
Sasaki N, Sato T, Ohler A, O’Rourke B, Marban E (2000) Activation of mitochondrial ATP-dependent potassium channels by nitric oxide. Circulation 101(4):439–445
Schimmer AD, Dalili S (2005) Targeting the IAP family of caspase inhibitors as an emerging therapeutic strategy. Hematology Am Soc Hematol Educ Program 215–219
Shao ZH, Chang WT, Chan KC, Wojcik KR, Hsu CW, Li CQ, Li J, Anderson T, Qin Y, Becker LB, Hamann KJ, Vanden Hoek TL (2007) Hypothermia-induced cardioprotection using extended ischemia and early reperfusion cooling. Am J Physiol Heart Circ Physiol 292(4):H1995–H2003
Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399(6735):483–487
Shoshan-Barmatz V, Ben-Hail D (2012) VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12(1):24–34
Shulga N, Pastorino JG (2006) Acyl coenzyme a-binding protein augments bid-induced mitochondrial damage and cell death by activating mu-calpain. J Biol Chem 281(41):30824–30833
Simpson PJ, Lucchesi BR (1987) Free radicals and myocardial ischemia and reperfusion injury. J Lab Clin Med 110(1):13–30
Skyschally A, van Caster P, Boengler K, Gres P, Musiolik J, Schilawa D, Schulz R, Heusch G (2009) Ischemic postconditioning in pigs: no causal role for RISK activation. Circ Res 104(1):15–18
Sotnikova R (1998) Investigation of the mechanisms underlying H2O2-evoked contraction in the isolated rat aorta. Gen Pharmacol 31(1):115–119
Stamler JS (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78(6):931–936
Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, Beal MF (2004) Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 24(36):7779–7788
Stowe DF, Camara AK (2009) Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 11(6):1373–1396
Stowe DF, Aldakkak M, Camara AKS, Riess ML, Heinen A, Varadarajan SG, Jiang MT (2006) Cardiac mitochondrial preconditioning by big Ca2+-sensitive K+ channel opening requires superoxide radical generation. Am J Physiol Heart Circ Physiol 290:H434–H440
Stowe DF, Gadicherla AK, Zhou Y, Aldakkak M, Cheng Q, Kwok WM, Jiang MT, Heisner JS, Yang M, Camara AK (2013) Protection against cardiac injury by small Ca2+-sensitive K+ channels identified in guinea pig cardiac inner mitochondrial membrane. Biochim Biophys Acta 1829(2):427–442
Sun J, Murphy E (2010) Protein S-nitrosylation and cardioprotection. Circ Res 106(2):285–296
Sun J, Steenbergen C, Murphy E (2006) S-nitrosylation: NO-related redox signaling to protect against oxidative stress. Antioxid Redox Signal 8(9–10):1693–1705
Szabo C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6(8):662–680
Szczepanek K, Chen Q, Larner AC, Lesnefsky EJ (2012a) Cytoprotection by the modulation of mitochondrial electron transport chain: the emerging role of mitochondrial STAT3. Mitochondrion 12(2):180–189
Szczepanek K, Lesnefsky EJ, Larner AC (2012b) Multi-tasking: nuclear transcription factors with novel roles in the mitochondria. Trends Cell Biol 22:429–437
Szeto HH (2006) Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J 8(2):E277–E283
Szeto HH (2008a) Development of mitochondria-targeted aromatic-cationic peptides for neurodegenerative diseases. Ann N Y Acad Sci 1147:112–121
Szeto HH (2008b) Mitochondria-targeted cytoprotective peptides for ischemia-reperfusion injury. Antioxid Redox Signal 10(3):601–619
Tahara EB, Barros MH, Oliveira GA, Netto LE, Kowaltowski AJ (2007) Dihydrolipoyl dehydrogenase as a source of reactive oxygen species inhibited by caloric restriction and involved in saccharomyces cerevisiae aging. FASEB J 21(1):274–283
Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B, Lazzarino G, Paolocci N, Gabrielson KL, Wang Y, Kass DA (2005) Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 115(5):1221–1231
Tang D, Kang R, Zeh HJ 3rd, Lotze MT (2011) High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal 14(7):1315–1335
Tanno M, Miura T (2008) Adenine nucleotide translocator, a mitochondrial carrier protein, and fate of cardiomyocytes after ischaemia/reperfusion. Cardiovasc Res 80(1):1–2
Ten VS, Starkov A (2012) Hypoxic-ischemic injury in the developing brain: the role of reactive oxygen species originating in mitochondria. Neurol Res Int 2012(542976):1–10
Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279(6):L1005–L1028
Theruvath TP, Snoddy MC, Zhong Z, Lemasters JJ (2008a) Mitochondrial permeability transition in liver ischemia and reperfusion: role of c-Jun N-terminal kinase 2. Transplantation 85(10):1500–1504
Theruvath TP, Zhong Z, Pediaditakis P, Ramshesh VK, Currin RT, Tikunov A, Holmuhamedov E, Lemasters JJ (2008b) Minocycline and N-methyl-4-isoleucine cyclosporin (NIM811) mitigate storage/reperfusion injury after rat liver transplantation through suppression of the mitochondrial permeability transition. Hepatology 47(1):236–246
Thompson-Gorman SL, Zweier JL (1990) Evaluation of the role of xanthine oxidase in myocardial reperfusion injury. J Biol Chem 265(12):6656–6663
Tsutsumi YM, Yokoyama T, Horikawa Y, Roth DM, Patel HH (2007) Reactive oxygen species trigger ischemic and pharmacological postconditioning: in vivo and in vitro characterization. Life Sci 81(15):1223–1227
Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552(2):335–344
Ujwal R, Cascio D, Colletier JP, Faham S, Zhang J, Toro L, Ping P, Abramson J (2008) The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci USA 105(46):17742–17747
Umar S, van der Laarse A (2010) Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart. Mol Cell Biochem 333(1–2):191–201
Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr (1998) Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA 95(16):9220–9225
Vasquez-Vivar J, Kalyanaraman B, Martasek P (2003) The role of tetrahydrobiopterin in superoxide generation from eNOS: enzymology and physiological implications. Free Radic Biol Med 37(2):121–127
Vieira HL, Belzacq AS, Haouzi D, Bernassola F, Cohen I, Jacotot E, Ferri KF, El Hamel C, Bartle LM, Melino G, Brenner C, Goldmacher V, Kroemer G (2001) The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20(32):4305–4316
Virdis A, Duranti E, Taddei S (2011) Oxidative stress and vascular damage in hypertension: role of angiotensin II. Int J Hypertens 2011, 916310
Waldmeier PC, Feldtrauer JJ, Qian T, Lemasters JJ (2002) Inhibition of the mitochondrial permeability transition by the nonimmunosuppressive cyclosporin derivative NIM811. Mol Pharmacol 62(1):22–29
Wang X, Perez E, Liu R, Yan LJ, Mallet RT, Yang SH (2007) Pyruvate protects mitochondria from oxidative stress in human neuroblastoma SK-N-SH cells. Brain Res 1132(1):1–9
Weidenbach R, Schulz R, Gres P, Behrends M, Post H, Heusch G (2000) Enhanced reduction of myocardial infarct size by combined ACE inhibition and AT(1)-receptor antagonism. Br J Pharmacol 131(1):138–144
Weiss JN, Korge P, Honda HM, Ping P (2003) Role of the mitochondrial permeability transition in myocardial disease [review]. Circ Res 93(4):292–301
Wenzel P, Mollnau H, Oelze M, Schulz E, Wickramanayake JM, Muller J, Schuhmacher S, Hortmann M, Baldus S, Gori T, Brandes RP, Munzel T, Daiber A (2008a) First evidence for a crosstalk between mitochondrial and NADPH oxidase-derived reactive oxygen species in nitroglycerin-triggered vascular dysfunction. Antioxid Redox Signal 10(8):1435–1447
Wenzel P, Schuhmacher S, Kienhofer J, Muller J, Hortmann M, Oelze M, Schulz E, Treiber N, Kawamoto T, Scharffetter-Kochanek K, Munzel T, Burkle A, Bachschmid MM, Daiber A (2008b) Manganese superoxide dismutase and aldehyde dehydrogenase deficiency increase mitochondrial oxidative stress and aggravate age-dependent vascular dysfunction. Cardiovasc Res 80(2):280–289
Widlansky ME, Gutterman DD (2011) Regulation of endothelial function by mitochondrial reactive oxygen species. Antioxid Redox Signal 15(6):1517–1530
Wilcox CS, Pearlman A (2008) Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 60(4):418–469
Wojtovich AP, Nadtochiy SM, Brookes PS, Nehrke K (2011) Ischemic preconditioning: the role of mitochondria and aging. Exp Gerontol 47(1):1–7
Wojtovich AP, Smith CO, Haynes CM, Nehrke KW, Brookes PS (2013) Physiological consequences of complex II inhibition for aging, disease, and the mKATP channel. Biochimica et Biophysica Acta 1827(5):598–611
Wolin MS, Ahmad M, Gupte SA (2005) Oxidant and redox signaling in vascular oxygen sensing mechanisms: basic concepts, current controversies, and potential importance of cytosolic NADPH. Am J Physiol Lung Cell Mol Physiol 289(2):L159–L173 [review]
Xia Y, Zweier JL (1995) Substrate control of free radical generation from xanthine oxidase in the postischemic heart. J Biol Chem 270(32):18797–18803
Yamamoto E, Kataoka K, Yamashita T, Tokutomi Y, Dong YF, Matsuba S, Ogawa H, Kim-Mitsuyama S (2007) Role of xanthine oxidoreductase in the reversal of diastolic heart failure by candesartan in the salt-sensitive hypertensive rat. Hypertension 50(4):657–662
Yan LJ, Sohal RS (1998) Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc Natl Acad Sci USA 95(22):12896–12901
Yang M, Camara AK, Wakim BT, Zhou Y, Gadicherla AK, Kwok WM, Stowe DF (2012a) Tyrosine nitration of voltage-dependent anion channels in cardiac ischemia-reperfusion: reduction by peroxynitrite scavenging. Biochim Biophys Acta 1817(11):2049–2059
Yang M, Stowe DF, Heisner JS, Aldakkak M, Camara AK (2012b) Resveratrol or 32°C hypothermia applied after cardiac ischemia reduces mitochondrial translocation of p66shc. FASEB J 104:052,678
Yellon DM, Hausenloy DJ (2005) Realizing the clinical potential of ischemic preconditioning and postconditioning. Nat Clin Pract Cardiovasc Med 2(11):568–575
Yu E, Mercer J, Bennett M (2012) Mitochondria in vascular disease. Cardiovasc Res 95(2):173–182
Zaccagnini G, Martelli F, Fasanaro P, Magenta A, Gaetano C, Di Carlo A, Biglioli P, Giorgio M, Martin-Padura I, Pelicci PG, Capogrossi MC (2004) p66ShcA Modulates tissue response to hindlimb ischemia. Circulation 109(23):2917–2923
Zhang C, Xu X, Potter BJ, Wang W, Kuo L, Michael L, Bagby GJ, Chilian WM (2006) TNF-alpha contributes to endothelial dysfunction in ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol 26(3):475–480
Zhang G, Zhang F, Muh R, Yi F, Chalupsky K, Cai H, Li PL (2007) Autocrine/paracrine pattern of superoxide production through NAD(P)H oxidase in coronary arterial myocytes. Am J Physiol Heart Circ Physiol 292(1):H483–H495
Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, Anilkumar N, Yu B, Dong X, Walker SJ, Brandes RP, Shah AM (2010) NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci USA 107(42):18121–18126
Zhdanov AV, Ward MW, Taylor CT, Souslova EA, Chudakov DM, Prehn JH, Papkovsky DB (2010) Extracellular calcium depletion transiently elevates oxygen consumption in neurosecretory PC12 cells through activation of mitochondrial Na+/Ca2+ exchange. Biochim Biophys Acta 1797(9):1627–1637
Zinkevich NS, Gutterman DD (2011) ROS-induced ROS release in vascular biology: redox-redox signaling. Am J Physiol Heart Circ Physiol 301(3):H647–H653
Zoccarato F, Cavallini L, Bortolami S, Alexandre A (2007) Succinate modulation of H2O2 release at NADH:ubiquinone oxidoreductase (complex I) in brain mitochondria. Biochem J 406(1):125–129
Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ (2000) Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192(7):1001–1014
Zuurbier CJ, Smeele KM, Eerbeek O (2009) Mitochondrial hexokinase and cardioprotection of the intact heart. J Bioenerg Biomembr 41(2):181–185
Zweier JL, Fertmann J, Wei G (2001) Nitric oxide and peroxynitrite in postischemic myocardium. Antioxid Redox Signal 3(1):11–22
Acknowledgments
The authors wish to thank Mohammed Aldakkak MD and Christoph Blomeyer MD for reading and critiquing the manuscript. The writing of this chapter was supported in part by grants from the National Institutes of Health (HL095122-Camara AKS/Dash RK; HL089514, HL098490-Stowe DF; P01GM066730-Bosnjak ZB; and the Veterans Administration (Merit Review 8204-05P-Stowe DF).
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Camara, A.K.S., Stowe, D.F. (2014). Reactive Oxygen Species (ROS) and Cardiac Ischemia and Reperfusion Injury. In: Laher, I. (eds) Systems Biology of Free Radicals and Antioxidants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30018-9_75
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