Cytoprotection by the modulation of mitochondrial electron transport chain: The emerging role of mitochondrial STAT3

Mitochondrion

Volumn 12, Issue 2, 2012, Pages 180-189

  Szczepanek, Karol ^a,b   Chen, Qun ^b   Larner, Andrew C ^a   Lesnefsky, Edward J ^a,b,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Electron transport chain; Ischemia; Oxidative phosphorylation; Reactive oxygen species; Reperfusion; Stat 3

Indexed keywords

CYTOCHROME C; GLUTATHIONE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; STAT3 PROTEIN; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

CELL DAMAGE; CELL PROTECTION; CELL RESPIRATION; ENZYME ACTIVITY; GENE; GENE DELETION; GENE SILENCING; HEART INJURY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCER AND ACTIVATOR OF TRANSCRIPTION 3 GENE;

ANIMALS; CYTOPROTECTION; DOWN-REGULATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; HUMANS; MITOCHONDRIAL PROTEINS; REACTIVE OXYGEN SPECIES; STAT3 TRANSCRIPTION FACTOR;

EID: 84858007745     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.08.011     Document Type: Review

References (141)

1. Adams J.M., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998, 281:1322-1326.
2. Ahn B.H., Kim H.S., Song S., Lee I.H., Liu J., Vassilopoulos A., Deng C.X., Finkel T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:14447-14452.
3. 2+ overload and ROS release. Cardiovasc. Res. 2008, 77:406-415.
4. Ambrosio G., Zweier J.L., Duilio C., Kuppusamy P., Santoro G., Elia P.P., Tritto I., Cirillo P., Condorelli M., Chiariello M. 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. 1993, 268:18532-18541.
5. Antunes F., Cadenas E. The mechanism of cytochrome C oxidase inhibition by nitric oxide. Front. Biosci. 2007, 12:975-985.
6. Becker L.B. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc. Res. 2004, 61:461-470.
7. Becker L.B., vanden Hoek T.L., Shao Z.H., Li C.Q., Schumacker P.T. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am. J. Physiol. 1999, 277:H2240-H2246.
8. Beer S.M., Taylor E.R., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., Murphy M.P. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant DEFENSE. J. Biol. Chem. 2004, 279:47939-47951.
9. Belikova N.A., Vladimirov Y.A., Osipov A.N., Kapralov A.A., Tyurin V.A., Potapovich M.V., Basova L.V., Peterson J., Kurnikov I.V., Kagan V.E. Peroxidase activity and structural transitions of cytochrome c bound to cardiolipin-containing membranes. Biochemistry 2006, 45:4998-5009.
10. Boengler K., Konietzka I., Buechert A., Heinen Y., Garcia-Dorado D., Heusch G., Schulz R. Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochondrial levels of connexin 43. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H1764-H1769.
11. Boengler K., Buechert A., Heinen Y., Roeskes C., Hilfiker-Kleiner D., Heusch G., Schulz R. Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ. Res. 2008, 102:131-135.
12. Boengler K., Hilfiker-Kleiner D., Drexler H., Heusch G., Schulz R. The myocardial JAK/STAT pathway: from protection to failure. Pharmacol. Ther. 2008, 120:172-185.
13. Boengler K., Hilfiker-Kleiner D., Heusch G., Schulz R. Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res. Cardiol. 2010, 105:771-785.
14. Bolli R., McCay P.B. Use of spin traps in intact animals undergoing myocardial ischemia/reperfusion: a new approach to assessing the role of oxygen radicals in myocardial "stunning". Free Radic. Res. Commun. 1990, 9:169-180.
15. Borutaite V., Brown G.C. Mitochondria in apoptosis of ischemic heart. FEBS Lett. 2003, 541:1-5.
16. Borutaite V., Budriunaite A., Morkuniene R., Brown G.C. Release of mitochondrial cytochrome c and activation of cytosolic caspases induced by myocardial ischaemia. Biochim. Biophys. Acta 2001, 1537:101-109.
17. Borutaite V., Jekabsone A., Morkuniene R., Brown G.C. Inhibition of mitochondrial permeability transition prevents mitochondrial dysfunction, cytochrome c release and apoptosis induced by heart ischemia. J. Mol. Cell. Cardiol. 2003, 35:357-366.
18. Burwell L.S., Nadtochiy S.M., Tompkins A.J., Young S., Brookes P.S. Direct evidence for S-nitrosation of mitochondrial complex I. Biochem. J. 2006, 394:627-634.
19. Chance B., Williams G.R., Hollunger G. Inhibition of electron and energy transfer in mitochondria. I. Effects of Amytal, thiopental, rotenone, progesterone, and methylene glycol. J. Biol. Chem. 1963, 238:418-431.
20. Chandel N.S. Mitochondrial regulation of oxygen sensing. Adv. Exp. Med. Biol. 2010, 661:339-354.
21. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:11715-11720.
22. Chen L.B. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol. 1988, 4:155-181.
23. Chen Q., Lesnefsky E.J. Depletion of cardiolipin and cytochrome c during ischemia increases hydrogen peroxide production from the electron transport chain. Free Radic. Biol. Med. 2006, 40:976-982.
24. Chen Q., Lesnefsky E.J. Blockade of electron transport preserves the contents of bcl-2 and cytochrome c in subsarcolemmal mitochondria during ischemia. Circulation 2007, 115. (abstract 16690).
25. Chen Q., Lesnefsky E.J. Ischemic damage to the mitochondrial electron transport chain favors opening of the permeability transition pore. FASEB J. 2008, 22:E345. (abstract 750.346).
26. Chen Q., Lesnefsky E. Incubation model for the study of mouse heart mitochondria during ischemia (Abstract). J. Investig. Med. 2009, 57:558.
27. Chen Q., Lesnefsky E. Mitochondria and Cardiac Injury: A Journey from Reperfusion to Ischemia and Back Again. Book chapter 2009, The Research Signpost/Transworld Research Network.
28. Chen Q., Lesnefsky E.J. Blockade of electron transport during ischemia preserves bcl-2 and inhibits opening of the mitochondrial permeability transition pore. FEBS Lett. 2011, 585:921-926.
29. Chen M., He H., Zhan S., Krajewski S., Reed J.C., Gottlieb R.A. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J. Biol. Chem. 2001, 276:30724-30728.
30. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 2003, 278:36027-36031.
31. Chen Q., Hoppel C.L., Lesnefsky E.J. Blockade of electron transport before cardiac ischemia with the reversible inhibitor amobarbital protects rat heart mitochondria. J. Pharmacol. Exp. Ther. 2006, 316:200-207.
32. Chen Q., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Reversible blockade of electron transport during ischemia protects mitochondria and decreases myocardial injury following reperfusion. J. Pharmacol. Exp. Ther. 2006, 319:1405-1412.
33. Chen C.L., Zhang L., Yeh A., Chen C.A., Green-Church K.B., Zweier J.L., Chen Y.R. Site-specific S-glutathiolation of mitochondrial NADH ubiquinone reductase. Biochemistry 2007, 46:5754-5765.
34. Chen Q., Camara A.K., Stowe D.F., Hoppel C.L., Lesnefsky E.J. Modulation of electron transport protects cardiac mitochondria and decreases myocardial injury during ischemia and reperfusion. Am. J. Physiol. Cell Physiol. 2007, 292:C137-C147.
35. Chen Y.R., Chen C.L., Pfeiffer D.R., Zweier J.L. Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J. Biol. Chem. 2007, 282:32640-32654.
36. Chen Q., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am. J. Physiol. Cell Physiol. 2008, 294:C460-C466.
37. Chen Q., Yin G., Stewart S., Hu Y., Lesnefsky E.J. Isolating the segment of the mitochondrial electron transport chain responsible for mitochondrial damage during cardiac ischemia. Biochem. Biophys. Res. Commun. 2010, 397:656-660.
38. Cimen H., Han M.J., Yang Y., Tong Q., Koc H., Koc E.C. Regulation of Succinate Dehydrogenase Activity by SIRT3 in Mammalian Mitochondria. Biochemistry 2010, 49:304-311.
39. Cooper C.E., Brown G.C. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 2008, 40:533-539.
40. Cooper C.E., Davies N.A., Psychoulis M., Canevari L., Bates T.E., Dobbie M.S., Casley C.S., Sharpe M.A. Nitric oxide and peroxynitrite cause irreversible increases in the K(m) for oxygen of mitochondrial cytochrome oxidase: in vitro and in vivo studies. Biochim. Biophys. Acta 2003, 1607:27-34.
41. Davies M.J. Direct detection of radical production in the ischaemic and reperfused myocardium: current status. Free Radic. Res. Commun. 1989, 7:275-284.
42. Degli Esposti M. Inhibitors of NADH-ubiquinone reductase: an overview. Biochim. Biophys. Acta 1998, 1364:222-235.
43. Edmond J.C. Mitochondrial disorders. Int. Ophthalmol. Clin. 2009, 49:27-33.
44. Elrod J.W., Calvert J.W., Morrison J., Doeller J.E., Kraus D.W., Tao L., Jiao X., Scalia R., Kiss L., Szabo C., Kimura H., Chow C.W., Lefer D.J. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15560-15565.
45. Fannin S.W., Lesnefsky E.J., Slabe T.J., Hassan M.O., Hoppel C.L. Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch. Biochem. Biophys. 1999, 372:399-407.
46. Fantin V.R., St-Pierre J., Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006, 9:425-434.
47. Flameng W., Andres J., Ferdinande P., Mattheussen M., Van Belle H. Mitochondrial function in myocardial stunning. J. Mol. Cell. Cardiol. 1991, 23:1-11.
48. Genova M.L., Ventura B., Giuliano G., Bovina C., Formiggini G., Parenti Castelli G., Lenaz G. The site of production of superoxide radical in mitochondrial Complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2. FEBS Lett. 2001, 505:364-368.
49. Gomez L., Paillard M., Thibault H., Derumeaux G., Ovize M. Inhibition of GSK3beta by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion. Circulation 2008, 117:2761-2768.
50. Gomez L., Paillard M., Price M., Chen Q., Teixeira G., Spiegel S., Lesnefsky E.J. A novel role for mitochondrial sphingosine-1-phosphate produced by sphingosine kinase-2 in PTP-mediated cell survival during cardioprotection. Bas. Res. Cardiol. (In Press). Abstract: (BCVS abstract P173) Published online:, Accessed: December 23, 2010. http://www.americanheart.org/presenter.jhtml?identifier=3074181.
51. Gottlieb R.A. Mitochondrial signaling in apoptosis: mitochondrial daggers to the breaking heart. Basic Res. Cardiol. 2003, 98:242-249.
52. Gottlieb R.A., Burleson K.O., Kloner R.A., Babior B.M., Engler R.L. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J. Clin. Invest. 1994, 94:1621-1628.
53. Gough D.J., Corlett A., Schlessinger K., Wegrzyn J., Larner A.C., Levy D.E. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009, 324:1713-1716.
54. Gustafsson A.B., Gottlieb R.A. Bcl-2 family members and apoptosis, taken to heart. Am. J. Physiol. Cell Physiol. 2007, 292:C45-C51.
55. Hajjar R.J., Samulski R.J. Heart failure: a silver bullet to treat heart failure. Gene Ther. 2006, 13:997.
56. Hajjar R.J., del Monte F., Matsui T., Rosenzweig A. Prospects for gene therapy for heart failure. Circ. Res. 2000, 86:616-621.
57. Han D., Antunes F., Canali R., Rettori D., Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 2003, 278:5557-5563.
58. Hausenloy D.J., Yellon D.M. The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J. Mol. Cell. Cardiol. 2003, 35:339-341.
59. Hausenloy D.J., Yellon D.M. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc. Res. 2004, 61:448-460.
60. Henze K., Martin W. Evolutionary biology: essence of mitochondria. Nature 2003, 426:127-128.
61. Hilfiker-Kleiner D., Hilfiker A., Drexler H. Many good reasons to have STAT3 in the heart. Pharmacol. Ther. 2005, 107:131-137.
62. Hilfiker-Kleiner D., Kaminski K., Podewski E., Bonda T., Schaefer A., Sliwa K., Forster O., Quint A., Landmesser U., Doerries C., Luchtefeld M., Poli V., Schneider M.D., Balligand J.L., Desjardins F., Ansari A., Struman I., Nguyen N.Q., Zschemisch N.H., Klein G., Heusch G., Schulz R., Hilfiker A., Drexler H. A cathepsin D-cleaved 16kDa form of prolactin mediates postpartum cardiomyopathy. Cell 2007, 128:589-600.
63. Hoppel C.L., Tandler B., Fujioka H., Riva A. Dynamic organization of mitochondria in human heart and in myocardial disease. Int. J. Biochem. Cell Biol. 2009, 41:1949-1956.
64. Horgan D.J., Singer T.P., Casida J.E. Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase. 13. Binding sites of rotenone, piericidin A, and amytal in the respiratory chain. J. Biol. Chem. 1968, 243:834-843.
65. Ilangovan G., Liebgott T., Kutala V.K., Petryakov S., Zweier J.L., Kuppusamy P. EPR oximetry in the beating heart: myocardial oxygen consumption rate as an index of postischemic recovery. Magn. Reson. Med. 2004, 51:835-842.
66. Ingraham C.A., Burwell L.S., Skalska J., Brookes P.S., Howell R.L., Sheu S.S., Pinkert C.A. NDUFS4: creation of a mouse model mimicking a Complex I disorder. Mitochondrion 2009, 9:204-210.
67. Jacoby J.J., Kalinowski A., Liu M.G., Zhang S.S., Gao Q., Chai G.X., Ji L., Iwamoto Y., Li E., Schneider M., Russell K.S., Fu X.Y. Cardiomyocyte-restricted knockout of STAT3 results in higher sensitivity to inflammation, cardiac fibrosis, and heart failure with advanced age. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:12929-12934.
68. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., Vlasova I.I., Zhao Q., Zou M., Di P., Svistunenko D.A., Kurnikov I.V., Borisenko G.G. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 2005, 1:223-232.
69. 2 radicals in intact hearts with ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 2003, 284:H566-H574.
70. Koopman W.J., Nijtmans L.G., Dieteren C.E., Roestenberg P., Valsecchi F., Smeitink J.A., Willems P.H. Mammalian mitochondrial complex I: biogenesis, regulation and reactive oxygen species generation. Antioxid. Redox Signal. 2010, 12:1431-1470.
71. Korsmeyer S.J., Wei M.C., Saito M., Weiler S., Oh K.J., Schlesinger P.H. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ. 2000, 7:1166-1173.
72. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
73. Kruse S.E., Watt W.C., Marcinek D.J., Kapur R.P., Schenkman K.A., Palmiter R.D. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008, 7:312-320.
74. Kudin A.P., Bimpong-Buta N.Y., Vielhaber S., Elger C.E., Kunz W.S. Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 2004, 279:4127-4135.
75. Kunisada K., Negoro S., Tone E., Funamoto M., Osugi T., Yamada S., Okabe M., Kishimoto T., Yamauchi-Takihara K. Signal transducer and activator of transcription 3 in the heart transduces not only a hypertrophic signal but a protective signal against doxorubicin-induced cardiomyopathy. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:315-319.
76. Kushnareva Y., Murphy A.N., Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+oxidation-reduction state. Biochem. J. 2002, 368:545-553.
77. Lacerda L., Somers S., Opie L.H., Lecour S. Ischaemic postconditioning protects against reperfusion injury via the SAFE pathway. Cardiovasc. Res. 2009, 84:201-208.
78. Lee J.W., Bobst E.V., Wang Y.G., Ashraf M.M., Bobst A.M. Increased endogenous ascorbyl free radical formation with singlet oxygen scavengers in reperfusion injury: an EPR and functional recovery study in rat hearts. Cell. Mol. Biol. (Noisy-le-Grand) 2000, 46:1383-1395.
79. Lesnefsky E.J., Gallo D.S., Ye J., Whittingham T.S., Lust W.D. Aging increases ischemia-reperfusion injury in the isolated, buffer-perfused heart. J. Lab. Clin. Med. 1994, 124:843-851.
80. Lesnefsky E.J., Lundergan C.F., Hodgson J.M., Nair R., Reiner J.S., Greenhouse S.W., Califf R.M., Ross A.M. Increased left ventricular dysfunction in elderly patients despite successful thrombolysis: the GUSTO-I angiographic experience. J. Am. Coll. Cardiol. 1996, 28:331-337.
81. Lesnefsky E.J., Tandler B., Ye J., Slabe T.J., Turkaly J., Hoppel C.L. Myocardial ischemia decreases oxidative phosphorylation through cytochrome oxidase in subsarcolemmal mitochondria. Am. J. Physiol. 1997, 273:H1544-H1554.
82. Lesnefsky E.J., Gudz T.I., Migita C.T., Ikeda-Saito M., Hassan M.O., Turkaly P.J., Hoppel C.L. 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. 2001, 385:117-128.
83. Lesnefsky E.J., Gudz T.I., Moghaddas S., Migita C.T., Ikeda_Saito M., Turkaly P.J., Hoppel C.L. Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J. Mol. Cell. Cardiol. 2001, 33:37-47.
84. Lesnefsky E.J., Moghaddas S., Tandler B., Kerner J., Hoppel C.L. Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J. Mol. Cell. Cardiol. 2001, 33:1065-1089.
85. Lesnefsky E.J., Slabe T.J., Stoll M.S., Minkler P.E., Hoppel C.L. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am. J. Physiol. 2001, 280:H2770-H2778.
86. Lesnefsky E.J., Chen Q., Moghaddas S., Hassan M.O., Tandler B., Hoppel C.L. Blockade of electron transport during ischemia protects cardiac mitochondria. J. Biol. Chem. 2004, 279:47961-47967.
87. Lesnefsky E.J., Chen Q., Slabe T.J., Stoll M.S., Minkler P.E., Hassan M.O., Tandler B., Hoppel C.L. Ischemia, rather than reperfusion, inhibits respiration through cytochrome oxidase in the isolated, perfused rabbit heart: role of cardiolipin. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H258-H267.
88. Lesnefsky E.J., He D., Moghaddas S., Hoppel C.L. Reversal of mitochondrial defects before ischemia protects the aged heart. FASEB J. 2006, 20:1543-1545.
89. Levy D.E., Lee C.K. What does Stat3 do?. J. Clin. Invest. 2002, 109:1143-1148.
90. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., Robinson J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 2003, 278:8516-8525.
91. Liao Z., Brar B.K., Cai Q., Stephanou A., O'Leary R.M., Pennica D., Yellon D.M., Latchman D.S. Cardiotrophin-1 (CT-1) can protect the adult heart from injury when added both prior to ischaemia and at reperfusion. Cardiovasc. Res. 2002, 53:902-910.
92. Lucas D.T., Szweda L.I. Cardiac reperfusion injury: aging, lipid peroxidation, and mitochondrial dysfunction. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:510-514.
93. Maupoil V., Rochette L., Tabard A., Clauser P., Harpey C. Evolution of free radical formation during low-flow ischemia and reperfusion in isolated rat heart. Cardiovasc. Drugs Ther. 1990, 4:791-795.
94. McBride H.M., Neuspiel M., Wasiak S. Mitochondria: more than just a powerhouse. Curr. Biol. 2006, 16:R551-R560.
95. Merrill G.F. Acetaminophen and low-flow myocardial ischemia: efficacy and antioxidant mechanisms. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H1341-H1349.
96. Murphy E., Steenbergen C. Cardioprotection in females: a role for nitric oxide and altered gene expression. Heart Fail. Rev. 2007, 12:293-300.
97. Nadtochiy S.M., Burwell L.S., Brookes P.S. Cardioprotection and mitochondrial S-nitrosation: effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury. J. Mol. Cell. Cardiol. 2007, 42:812-825.
98. Nadtochiy S.M., Burwell L.S., Ingraham C.A., Spencer C.M., Friedman A.E., Pinkert C.A., Brookes P.S. In vivo cardioprotection by S-nitroso-2-mercaptopropionyl glycine. J. Mol. Cell. Cardiol. 2009, 46:960-968.
99. Negoro S., Kunisada K., Fujio Y., Funamoto M., Darville M.I., Eizirik D.L., Osugi T., Izumi M., Oshima Y., Nakaoka Y., Hirota H., Kishimoto T., Yamauchi-Takihara K. Activation of signal transducer and activator of transcription 3 protects cardiomyocytes from hypoxia/reoxygenation-induced oxidative stress through the upregulation of manganese superoxide dismutase. Circulation 2001, 104:979-981.
100. Ohnishi S.T., Ohnishi T., Muranaka S., Fujita H., Kimura H., Uemura K., Yoshida K., Utsumi K. A possible site of superoxide generation in the complex I segment of rat heart mitochondria. J. Bioenerg. Biomembr. 2005, 37:1-15.
101. O'Rourke B., Cortassa S., Aon M.A. Mitochondrial ion channels: gatekeepers of life and death. Physiology (Bethesda) 2005, 20:303-315.
102. Oshima Y., Fujio Y., Nakanishi T., Itoh N., Yamamoto Y., Negoro S., Tanaka K., Kishimoto T., Kawase I., Azuma J. STAT3 mediates cardioprotection against ischemia/reperfusion injury through metallothionein induction in the heart. Cardiovasc. Res. 2005, 65:428-435.
103. Ott M., Robertson J.D., Gogvadze V., Zhivotovsky B., Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1259-1263.
104. Paillard M., Gomez L., Augeul L., Loufouat J., Lesnefsky E.J., Ovize M. Postconditioning inhibits mPTP opening independent of oxidative phosphorylation and membrane potential. J. Mol. Cell. Cardiol. 2009, 46:902-909.
105. Paradies G., Ruggiero F.M., Petrosillo G., Quagliariello E. Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett. 1998, 424:155-158.
106. Park J.W., Chun Y.S., Kim Y.H., Kim C.H., Kim M.S. Ischemic preconditioning reduces Op6 generation and prevents respiratory impairment in the mitochondria of post-ischemic reperfused heart of rat. Life Sci. 1997, 60:2207-2219.
107. Pasdois P., Beauvoit B., Costa A.D., Vinassa B., Tariosse L., Bonoron-Adele S., Garlid K.D., Dos Santos P. Sarcoplasmic ATP-sensitive potassium channel blocker HMR1098 protects the ischemic heart: implication of calcium, complex I, reactive oxygen species and mitochondrial ATP-sensitive potassium channel. J. Mol. Cell. Cardiol. 2007, 42:631-642.
108. Phillips D., Reilley M.J., Aponte A.M., Wang G., Boja E., Gucek M., Balaban R.S. Stoichiometry of STAT3 and mitochondrial proteins: implications for the regulation of oxidative phosphorylation by protein-protein interactions. J. Biol. Chem. 2010, 285:23532-23536.
109. Phillips D., Aponte A.M., Covian R., Balaban R.S. Intrinsic protein kinase activity in mitochondrial oxidative phosphorylation complexes. Biochemistry 2011, 50:2515-2529.
110. Pietri S., Culcasi M., Cozzone P.J. Real-time continuous-flow spin trapping of hydroxyl free radical in the ischemic and post-ischemic myocardium. Eur. J. Biochem. 1989, 186:163-173.
111. Piper H.M., Sezer O., Schleyer M., Schwartz P., Hutter J.F., Spieckermann P.G. Development of ischemia-induced damage in defined mitochondrial subpopulations. J. Mol. Cell. Cardiol. 1985, 17:885-896.
112. 2+] levels during short-term 17 degrees C ischemia in intact hearts. Cardiovasc. Res. 2004, 61:580-590.
113. Robinson N.C., Strey F., Talbert L. Investigation of the essential boundary layer phospholipids of cytochrome c oxidase using Triton X-100 delipidation. Biochemistry 1980, 19:3656-3661.
114. Rouslin W. Mitochondrial complexes I, II, III, IV, and V in myocardial ischemia and autolysis. Am. J. Physiol. 1983, 244:H743-H748.
115. Salloum F.N., Chau V.Q., Hoke N.N., Abbate A., Varma A., Ockaili R.A., Toldo S., Kukreja R.C. Phosphodiesterase-5 inhibitor, tadalafil, protects against myocardial ischemia/reperfusion through protein-kinase g-dependent generation of hydrogen sulfide. Circulation 2009, 120:S31-S36.
116. Sarafian T.A., Montes C., Imura T., Qi J., Coppola G., Geschwind D.H., Sofroniew M.V. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 2010, 5:e9532.
117. Sauve A.A., Wolberger C., Schramm V.L., Boeke J.D. The biochemistry of sirtuins. Annu. Rev. Biochem. 2006, 75:435-465.
118. Schulman D., Latchman D.S., Yellon D.M. Effect of aging on the ability of preconditioning to protect rat hearts from ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H1630-H1636.
119. Shidoji Y., Hayashi K., Komura S., Ohishi N., Yagi K. Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation. Biochem. Biophys. Res. Commun. 1999, 264:343-347.
120. Shiva S., Sack M.N., Greer J.J., Duranski M., Ringwood L.A., Burwell L., Wang X., MacArthur P.H., Shoja A., Raghavachari N., Calvert J.W., Brookes P.S., Lefer D.J., Gladwin M.T. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J. Exp. Med. 2007, 204:2089-2102.
121. Smith R.M., Suleman N., Lacerda L., Opie L.H., Akira S., Chien K.R., Sack M.N. Genetic depletion of cardiac myocyte STAT-3 abolishes classical preconditioning. Cardiovasc. Res. 2004, 63:611-616.
122. Spiegel H.E., Wainio W.W. Some features of barbiturate interaction and inhibition of NADH-cytochrome C oxidoreductase in respiring systems. J. Pharmacol. Exp. Ther. 1969, 165:23-29.
123. Stephanou A., Brar B., Heads R., Knight R.D., Marber M.S., Pennica D., Latchman D.S. Cardiotrophin-1 induces heat shock protein accumulation in cultured cardiac cells and protects them from stressful stimuli. J. Mol. Cell. Cardiol. 1998, 30:849-855.
124. Stewart S., Lesnefsky E.J., Chen Q. Reversible blockade of electron transport with amobarbital at the onset of reperfusion attenuates cardiac injury. Transl. Res. 2009, 153:224-231.
125. + channel opening requires superoxide radical generation. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H434-H440.
126. Strub G.M., Paillard M., Liang J., Gomez L., Allegood J.C., Hait N.C., Maceyka M., Price M.M., Chen Q., Simpson D.C., Kordula T., Milstien S., Lesnefsky E.J., Spiegel S. Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J 2011, 25:600-612.
127. Szczepanek K., Chen Q., Derecka M., Salloum F.N., Zhang Q., Szelag M., Cichy J., Kukreja R.C., Dulak J., Lesnefsky E.J., Larner A.C. Mitochondrial-targeted signal transducer and activator of transcription (STAT3) protects against ischemia-induced changes in the electron transport chain and the generation of reactive oxygen species. J. Biol. Chem. 2011, 286:29610-29620.
128. Taylor E.R., Hurrell F., Shannon R.J., Lin T.K., Hirst J., Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 2003, 278:19603-19610.
129. Tompkins A.J., Burwell L.S., Digerness S.B., Zaragoza C., Holman W.L., Brookes P.S. Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim. Biophys. Acta 2006, 1762:223-231.
130. - spin trapping on cardiac submitochondrial particles isolated from ischemic and non-ischemic myocardium. J. Mol. Cell. Cardiol. 1990, 22:893-899.
131. Uren R.T., Dewson G., Chen L., Coyne S.C., Huang D.C., Adams J.M., Kluck R.M. Mitochondrial permeabilization relies on BH3 ligands engaging multiple prosurvival Bcl-2 relatives, not Bak. J. Cell Biol. 2007, 177:277-287.
132. Vanden Hoek T.L., Li C., Shao Z., Schumacker P.T., Becker L.B. Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J. Mol. Cell. Cardiol. 1997, 29:2571-2583.
133. Verdin E., Hirschey M.D., Finley L.W., Haigis M.C. Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010, 35:669-675.
134. Vessey D.A., Kelley M., Li L., Huang Y. Sphingosine protects aging hearts from ischemia/reperfusion injury: superiority to sphingosine 1-phosphate and ischemic pre- and post-conditioning. Oxid. Med. Cell. Longev. 2009, 2:146-151.
135. Vessey D.A., Li L., Jin Z.-Q., Kelley M., Honbo N., Zhang J., Karliner S. A sphingosine kinase form 2 knockout sensitizes mouse myocardium to ischemia/reoxygenation injury and diminishes responsiveness to ischemic preconditioning. Oxid. Med. Cell. Longev. 2011, 2011.
136. Vik S.B., Capaldi R.A. Lipid requirements for cytochrome c oxidase activity. Biochemistry 1977, 16:5755-5759.
137. Vlasova I.I., Tyurin V.A., Kapralov A.A., Kurnikov I.V., Osipov A.N., Potapovich M.V., Stoyanovsky D.A., Kagan V.E. Nitric oxide inhibits peroxidase activity of cytochrome c.cardiolipin complex and blocks cardiolipin oxidation. J. Biol. Chem. 2006, 281:14554-14562.
138. Wegrzyn J., Potla R., Chwae Y.J., Sepuri N.B., Zhang Q., Koeck T., Derecka M., Szczepanek K., Szelag M., Gornicka A., Moh A., Moghaddas S., Chen Q., Bobbili S., Cichy J., Dulak J., Baker D.P., Wolfman A., Stuehr D., Hassan M.O., Fu X.Y., Avadhani N., Drake J.I., Fawcett P., Lesnefsky E.J., Larner A.C. Function of mitochondrial Stat3 in cellular respiration. Science 2009, 323:793-797.
139. Willis S.N., Adams J.M. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 2005, 17:617-625.
140. Xiong Y., Liu X., Lee C.P., Chua B.H., Ho Y.S. Attenuation of doxorubicin-induced contractile and mitochondrial dysfunction in mouse heart by cellular glutathione peroxidase. Free Radic. Biol. Med. 2006, 41:46-55.
141. Zhu S.G., Kukreja R.C., Das A., Chen Q., Lesnefsky E.J., Xi L. Dietary nitrate supplementation protects against Doxorubicin-induced cardiomyopathy by improving mitochondrial function. J. Am. Coll. Cardiol. 2011, 57:2181-2189.