Inhibition of the mitochondrial permeability transition for cytoprotection: Direct versus indirect mechanisms

Biochemistry Research International

Volumn , Issue , 2012, Pages

  Martel, Cécile ^a   Huynh, Le Ha ^a   Garnier, Anne ^a   Ventura Clapier, Renée ^a   Brenner, Catherine ^a  

^a Universite Paris Sud   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84862272377     PISSN: 20902247     EISSN: 20902255     Source Type: Journal    
DOI: 10.1155/2012/213403     Document Type: Review

References (140)

1. Lehninger A. L., The transfer of energy in oxidative phosphorylation Bulletin de la Société de Chimie Biologique 1964 46 1555 1575
2. Kroemer G., Galluzzi L., Brenner C., Mitochondrial membrane permeabilization in cell death Physiological Reviews 2007 87 1 99 163 (Pubitemid 46209992)
3. Martinou J.-C., Youle R., Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics Developmental Cell 2011 21 1 92 101
4. Majno G., Joris I., Apoptosis, oncosis, and necrosis: an overview of cell death American Journal of Pathology 1995 146 1 3 15
5. Papanicolaou K. N., Ngoh G. A., Dabkowski E. R., O'Connell K. A., Ribeiro R. F., Stanley W. C., Walsh K., Cardiomyocyte deletion of mitofusin-1 leads to mitochondrial fragmentation and improves tolerance to ROS-induced mitochondrial dysfunction and cell death American Journal of Physiology 2012 302 1 H167 H179
6. Wallace D. C., Mitochondrial diseases in man and mouse Science 1999 283 5407 1482 1488
7. Ramachandran A., Jha S., Lefer D. J., Review paper: pathophysiology of myocardial reperfusion injury: the role of genetically engineered mouse models Veterinary Pathology 2008 45 5 698 706
8. Matas J., Tien Sing Young N., Bourcier-Lucas C., Ascah A., Marcil M., Deschepper C. F., Burelle Y., Increased expression and intramitochondrial translocation of cyclophilin-D associates with increased vulnerability of the permeability transition pore to stress-induced opening during compensated ventricular hypertrophy Journal of Molecular and Cellular Cardiology 2009 46 3 420 430
9. Begriche K., Igoudjil A., Pessayre D., Fromenty B., Mitochondrial dysfunction in NASH: causes, consequences and possible means to prevent it Mitochondrion 2006 6 1 1 38 (Pubitemid 43250588)
10. Ventura-Clapier R., Garnier A., Veksler V., Joubert F., Bioenergetics of the failing heart Biochimica et Biophysica Acta 2011 1813 7 1360 1372
11. Neubauer S., The failing heart-An engine out of fuel New England Journal of Medicine 2007 356 11 1140 1151 (Pubitemid 46425598)
12. Indran I. R., Tufo G., Pervaiz S., Brenner C., Recent advances in apoptosis, mitochondria and drug resistance in cancer cells Biochimica et Biophysica Acta 2011 1807 6 735 745
13. Palmieri F., The mitochondrial transporter family (SLC25): physiological and pathological implications Pflugers Archiv European Journal of Physiology 2004 447 5 689 709 (Pubitemid 38241455)
14. Klingenberg M., The ADP and ATP transport in mitochondria and its carrier Biochimica et Biophysica Acta 2008 1778 10 1978 2021
15. Gena P., Fanelli E., Brenner C., Svelto M., Calamita G., News and views on mitochondrial water transport Frontiers in Bioscience 2009 14 4189 4198
16. Hunter D. R., Haworth R. A., Southard J. H., Relationship between configuration, function, and permeability in calcium treated mitochondria Journal of Biological Chemistry 1976 251 16 5069 5077
17. Vander Heiden M. G., Chandel N. S., Williamson E. K., Schumacker P. T., Thompson C. B., Bcl-x(L) regulates the membrane potential and volume homeostasis of mitochondria Cell 1997 91 5 627 637 (Pubitemid 27513654)
18. Jacotot E., Ravagnan L., Loeffler M., Ferri K. F., Vieira H. L. A., Zamzami N., Costantini P., Druillennec S., Hoebeke J., Briand J. P., Irinopoulou T., Daugas E., Susin S. A., Cointe D., Xie Z. H., Reed J. C., Roques B. P., Kroemer G., The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore Journal of Experimental Medicine 2000 191 1 33 45 (Pubitemid 30043646)
19. Belzacq-Casagrande A. S., Martel C., Pertuiset C., Borgne-Sanchez A., Jacotot E., Brenner C., Pharmacological screening and enzymatic assays for apoptosis Frontiers in Bioscience 2009 14 3550 3562
20. Halestrap A. R., Connern C. R., Griffiths E. J., Kerr P. M., Cyclosporin A binding to mitochondrial cyclophilin inhibits the permeability transition pore and protects hearts from ischaemia/reperfusion injury Molecular and Cellular Biochemistry 1997 174 1-2 167 172 (Pubitemid 27404185)
21. Piot C., Croisille P., Staat P., Thibault H., Rioufol G., Mewton N., Elbelghiti R., Thien T. C., Bonnefoy E., Angoulvant D., Macia C., Raczka F., Sportouch C., Gahide G., Finet G., André-Fout X., Revel D., Kirkorian G., Monassier J. P., Derumeaux G., Ovize M., Effect of cyclosporine on reperfusion injury in acute myocardial infarction New England Journal of Medicine 2008 359 5 473 481
22. Nieminen A. L., Petrie T. G., Lemasters J. J., Selman W. R., Cyclosporin A delays mitochondrial depolarization induced by N-methyl-D-aspartate in cortical neurons: evidence of the mitochondrial permeability transition Neuroscience 1996 75 4 993 997 (Pubitemid 26377087)
23. Blattner J. R., He L., Lemasters J. J., Screening assays for the mitochondrial permeability transition using a fluorescence multiwell plate reader Analytical Biochemistry 2001 295 2 220 226 (Pubitemid 32756977)
24. Frezza C., Cipolat S., Scorrano L., Organelle isolation: functional mitochondria from mouse liver, muscle and cultured filroblasts Nature Protocols 2007 2 2 287 295 (Pubitemid 47040043)
25. Buron N., Porceddu M., Brabant M., Desgué D., Racoeur C., Lassalle M., Péchoux C., Rustin P., Jacotot E., Borgne-Sanchez A., Use of human cancer cell lines mitochondria to explore the mechanisms of BH3 peptides and ABT-737-induced mitochondrial membrane permeabilization PloS One 2010 5 3, article e9924
26. Picard M., Taivassalo T., Gouspillou G., Hepple R. T., Mitochondria: isolation, structure and function Journal of Physiology 2011 589 18 4413 4421
27. Petronilli V., Miotto G., Canton M., Brini M., Colonna R., Bernardi P., Di Lisa F., Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence Biophysical Journal 1999 76 2 725 734 (Pubitemid 29264555)
28. Zahrebelski G., Nieminen A. L., Al-Ghoul K., Qian T., Herman B., Lemasters J. J., Progression of subcellular changes during chemical hypoxia to cultured rat hepatocytes: a laser scanning confocal microscopic study Hepatology 1995 21 5 1361 1372
29. Nieminen A. L., Saylor A. K., Tesfai S. A., Herman B., Lemasters J. J., Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide Biochemical Journal 1995 307 1 99 106
30. Dedkova E. N., Blatter L. A., Measuring mitochondrial function in intact cardiac myocytes Journal of Molecular and Cellular Cardiology 2012 52 1 48 61
31. Rama Rao K. V., Jayakumar A. R., Norenberg M. D., Ammonia neurotoxicity: role of the mitochondrial permeability transition Metabolic Brain Disease 2003 18 2 113 127 (Pubitemid 36718124)
32. Galluzzi L., Zamzami N., De La Motte Rouge T., Lemaire C., Brenner C., Kroemer G., Methods for the assessment of mitochondrial membrane permeabilization in apoptosis Apoptosis 2007 12 5 803 813 (Pubitemid 46653289)
33. Griffiths E. J., Halestrap A. P., Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion Biochemical Journal 1995 307 1 93 98
34. Halestrap A. P., Brenner C., The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death Current Medicinal Chemistry 2003 10 16 1507 1525 (Pubitemid 36896553)
35. Baines C. P., Kaiser R. A., Purcell N. H., Blair N. S., Osinska H., Hambleton M. A., Brunskill E. W., Sayen M. R., Gottlieb R. A., Dorn G. W., Bobbins J., Molkentin J. D., Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death Nature 2005 434 7033 658 662 (Pubitemid 40488559)
36. Crompton M., Mitochondrial intermembrane junctional complexes and their role in cell death Journal of Physiology 2000 529 1 11 21
37. Brdiczka D., Beutner G., Rck A., Dolder M., Wallimann T., The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition BioFactors 1998 8 3-4 235 242 (Pubitemid 29021354)
38. Halestrap A. P., What is the mitochondrial permeability transition pore? Journal of Molecular and Cellular Cardiology 2009 46 6 821 831
39. Ricchelli F., ileikyte J., Bernardi P., Shedding light on the mitochondrial permeability transition Biochimica et Biophysica Acta 2011 1807 5 482 490
40. Szabo I., Zoratti M., The mitochondrial megachannel is the permeability transition pore Journal of Bioenergetics and Biomembranes 1992 24 1 111 117
41. Ko Y. H., Delannoy M., Hullihen J., Chiu W., Pedersen P. L., Mitochondrial ATP synthasome: cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP Journal of Biological Chemistry 2003 278 14 12305 12309 (Pubitemid 36800213)
42. Jacotot E., Deniaud A., Borgne-Sanchez A., Touat Z., Briand J. P., Le Bras M., Brenner C., Therapeutic peptides: targeting the mitochondrion to modulate apoptosis Biochimica et Biophysica Acta 2006 1757 9-10 1312 1323 (Pubitemid 44442138)
43. Loor G., Schumacker P. T., Role of hypoxia-inducible factor in cell survival during myocardial ischemia-reperfusion Cell Death and Differentiation 2008 15 4 686 690 (Pubitemid 351405073)
44. Tokarska-Schlattner M., Zaugg M., Zuppinger C., Wallimann T., Schlattner U., New insights into doxorubicin-induced cardiotoxicity: the critical role of cellular energetics Journal of Molecular and Cellular Cardiology 2006 41 3 389 405 (Pubitemid 44362995)
45. Broekemeier K. M., Dempsey M. E., Pfeiffer D. R., Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria Journal of Biological Chemistry 1989 264 14 7826 7830 (Pubitemid 19137258)
46. Griffiths E. J., Halestrap A. P., Protection by cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts Journal of Molecular and Cellular Cardiology 1993 25 12 1461 1469 (Pubitemid 24049454)
47. Clarke S. J., McStay G. P., Halestrap A. P., Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A Journal of Biological Chemistry 2002 277 38 34793 34799
48. Hausenloy D. J., Duchen M. R., Yellon D. M., Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury Cardiovascular Research 2003 60 3 617 625 (Pubitemid 37501119)
49. Henderson P. J., Lardy H. A., Bongkrekic acid. An inhibitor of the adenine nucleotide translocase of mitochondria Journal of Biological Chemistry 1970 245 6 1319 1326
50. Narita M., Shimizu S., Ito T., Chittenden T., Lutz R. J., Matsuda H., Tsujimoto Y., Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria Proceedings of the National Academy of Sciences of the United States of America 1998 95 25 14681 14686 (Pubitemid 29003690)
51. Zamzami N., Hamel C. E., Maisse C., Brenner C., Moz-Pinedo C., Belzacq A. S., Costantini P., Vieira H., Loeffler M., Molle G., Kroemer G., Bid acts on the permeability transition pore complex to induce apoptosis Oncogene 2000 19 54 6342 6350 (Pubitemid 32641848)
52. Novgorodov S. A., Gudz T. I., Milgrom Y. M., Brierley G. P., The permeability transition in heart mitochondria is regulated synergistically by ADP and cyclosporin A Journal of Biological Chemistry 1992 267 23 16274 16282
53. Haworth R. A., Hunter D. R., Control of the mitochondrial permeability transition pore by high- affinity ADP binding at the ADP/ATP translocase in permeabilized mitochondria Journal of Bioenergetics and Biomembranes 2000 32 1 91 96 (Pubitemid 30241261)
54. Lee A. C., Zizi M., Colombini M., -NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6 Journal of Biological Chemistry 1994 269 49 30974 30980 (Pubitemid 24377586)
55. Deniaud A., Rossi C., Berquand A., Homand J., Campagna S., Knoll W., Brenner C., Chopineau J., Voltage-dependent anion channel transports calcium ions through biomimetic membranes Langmuir 2007 23 7 3898 3905 (Pubitemid 46581919)
56. Deniaud A., Sharaf El Dein O., Maillier E., Poncet D., Kroemer G., Lemaire C., Brenner C., Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis Oncogene 2008 27 3 285 299
57. Thinnes F. P., Florke H., Winkelbach H., Stadtmuller U., Heiden M., Karabinos A., Hesse D., Kratzin H. D., Fleer E., Hilschmann N., Channel active mammalian porin, purified from crude membrane fractions of human B lymphocytes or bovine skeletal muscle, reversibly binds the stilbene-disulfonate group of the chloride channel blocker DIDS Biological Chemistry Hoppe-Seyler 1994 375 5 315 322 (Pubitemid 2089188)
58. Shoshan-Barmatz V., Keinan N., Abu-Hamad S., Tyomkin D., Aram L., Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: release of cytochrome c, AIF and Smac/Diablo Biochimica et Biophysica Acta 2010 1797 6-7 1281 1291
59. Rigobello M. P., Turcato F., Bindoli A., Inhibition of rat liver mitochondrial permeability transition by respiratory substrates Archives of Biochemistry and Biophysics 1995 319 1 225 230
60. Gincel D., Silberberg S., Shoshan-Barmatz V., Modulation of the voltagedependent anion channel (VDAC) by glutamate Journal of Bioenergetics and Biomembranes 2000 32 571 583 (Pubitemid 32204234)
61. Gincel D., Shoshan-Barmatz V., Glutamate interacts with VDAC and modulates opening of the mitochondrial permeability transition pore Journal of Bioenergetics and Biomembranes 2004 36 2 179 186 (Pubitemid 39023635)
62. Cesura A. M., Pinard E., Schubenel R., Goetschy V., Friedlein A., Langen H., Polcic P., Forte M. A., Bernardi P., Kemp J. A., The voltage-dependent anion channel is the target for a new class of inhibitors of the mitochondrial permeability transition pore Journal of Biological Chemistry 2003 278 50 49812 49818 (Pubitemid 37548815)
63. Krauskopf A., Eriksson O., Craigen W. J., Forte M. A., Bernardi P., Properties of the permeability transition in VDAC1 -/- mitochondria Biochimica et Biophysica Acta 2006 1757 5-6 590 595 (Pubitemid 43993836)
64. Leung A. W. C., Varanyuwatana P., Halestrap A. P., The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition Journal of Biological Chemistry 2008 283 39 26312 26323
65. Fontaine E., Ichas F., Bernardi P., A ubiquinone-binding site regulates the mitochondrial permeability transition pore Journal of Biological Chemistry 1998 273 40 25734 25740 (Pubitemid 28475797)
66. Elimadi A., Sapena R., Settaf A., Le Louet H., Tillement J. P., Morin D., Attenuation of liver normothermic ischemiareperfusion injury by preservation of mitochondrial functions with S-15176, a potent trimetazidine derivative Biochemical Pharmacology 2001 62 4 509 516 (Pubitemid 32607734)
67. Elimadi A., Jullien V., Tillement J. P., Morin D., S-15176 inhibits mitochondrial permeability transition via a mechanism independent of its antioxidant properties European Journal of Pharmacology 2003 468 2 93 101 (Pubitemid 36556252)
68. Ascah A., Khairallah M., Daussin F., Bourcier-Lucas C., Godin R., Allen B. G., Petrof B. J., Des Rosiers C., Burelle Y., Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil American Journal of Physiology 2011 300 1 H144 H153
69. Millay D. P., Sargent M. A., Osinska H., Baines C. P., Barton E. R., Vuagniaux G., Sweeney H. L., Robbins J., Molkentin J. D., Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy Nature Medicine 2008 14 4 442 447 (Pubitemid 351499389)
70. Bordet T., Buisson B., Michaud M., Drouot C., Galéa P., Delaage P., Akentieva N. P., Evers A. S., Covey D. F., Ostuni M. A., Lacapre J. J., Massaad C., Schumacher M., Steidl E. M., Maux D., Delaage M., Henderson C. E., Pruss R. M., Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis Journal of Pharmacology and Experimental Therapeutics 2007 322 2 709 720 (Pubitemid 47105813)
71. Queiroga C. S. F., Almeida A. S., Martel C., Brenner C., Alves P. M., Vieira H. L. A., Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis Journal of Biological Chemistry 2010 285 22 17077 17088
72. Azzolin L., Antolini N., Calderan A., Ruzza P., Sciacovelli M., Marin O., Mammi S., Bernardi P., Rasola A., Antamanide, a derivative of amanita phalloides, is a novel inhibitor of the mitochondrial permeability transition pore PLoS One 2011 6 1, article e16280
73. Mewton N., Croisille P., Gahide G., Rioufol G., Bonnefoy E., Sanchez I., Cung T. T., Sportouch C., Angoulvant D., Finet G., André-Fout X., Derumeaux G., Piot C., Vernhet H., Revel D., Ovize M., Effect of cyclosporine on left ventricular remodeling after reperfused myocardial infarction Journal of the American College of Cardiology 2010 55 12 1200 1205
74. Okorie M., Bhavsar D., Ridout D., Postconditioning protects against human endothelial ischaemia-reperfusion injury via subtype-specific KATP channel activation and is mimicked by inhibition of the mitochondrial permeability transition pore European Heart Journal 2011 1266 1274
75. Kim J. S., He L., Qian T., Lemasters J. J., Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes Current Molecular Medicine 2003 3 6 527 535 (Pubitemid 37173382)
76. Qian T., Nieminen A. L., Herman B., Lemasters J. J., Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes American Journal of Physiology 1997 273 6 C1783 C1792
77. Friberg H., Ferrand-Drake M., Bengtsson F., Halestrap A. P., Wieloch T., Cyclosporin A, but not FK 506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death Journal of Neuroscience 1998 18 14 5151 5159 (Pubitemid 28311932)
78. Khaspekov L., Friberg H., Halestrap A., Viktorov I., Wieloch T., Cyclosporin A and its nonimmunosuppressive analogue N-Me-Val-4-cyclosporin A mitigate glucose/oxygen deprivation-induced damage to rat cultured hippocampal neurons European Journal of Neuroscience 1999 11 9 3194 3198 (Pubitemid 29431654)
79. Matsumoto S., Friberg H., Ferrand-Drake M., Wieloch T., Blockade of the mitochondrial permeability transition pore diminishes infarct size in the rat after transient middle cerebral artery occlusion Journal of Cerebral Blood Flow and Metabolism 1999 19 7 736 741 (Pubitemid 30159798)
80. Malouitre S., Dube H., Selwood D., Crompton M., Mitochondrial targeting of cyclosporin A enables selective inhibition of cyclophilin-D and enhanced cytoprotection after glucose and oxygen deprivation Biochemical Journal 2010 425 1 137 148
81. Dube H., Selwood D., Malouitre S., Capano M., Simone M. I., Crompton M., A mitochondrial-targeted cyclosporin A with high binding affinity for cyclophilin D yields improved cytoprotection of cardiomyocytes Biochemical Journal 2012 441 3 901 907
82. Porteous C. M., Logan A., Evans C., Ledgerwood E. C., Menon D. K., Aigbirhio F., Smith R. A. J., Murphy M. P., Rapid uptake of lipophilic triphenylphosphonium cations by mitochondria in vivo following intravenous injection: implications for mitochondria-specific therapies and probes Biochimica et Biophysica Acta 2010 1800 9 1009 1017
83. Miura T., Tanno M., Sato T., Mitochondrial kinase signalling pathways in myocardial protection from ischaemia/reperfusion-induced necrosis Cardiovascular Research 2010 88 1 7 15
84. Feng J., Lucchinetti E., Ahuja P., Pasch T., Perriard J. C., Zaugg M., Isoflurane postconditioning prevents opening of the mitochondrial permeability transition pore through inhibition of glycogen synthase kinase 3 Anesthesiology 2005 103 5 987 995 (Pubitemid 41552054)
85. Javadov S., Rajapurohitam V., Kili A., Zeidan A., Choi A., Karmazyn M., Anti-hypertrophic effect of NHE-1 inhibition involves GSK-3 -dependent attenuation of mitochondrial dysfunction Journal of Molecular and Cellular Cardiology 2009 46 6 998 1007
86. Gomez L., Paillard M., Thibault H., Derumeaux G., Ovize M., Inhibition of GSK3 by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion Circulation 2008 117 21 2761 2768 (Pubitemid 351770456)
87. Pastorino J. G., Hoek J. B., Shulga N., Activation of glycogen synthase kinase 3 disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity Cancer Research 2005 65 22 10545 10554 (Pubitemid 41743749)
88. Rasola A., Sciacovelli M., Chiara F., Pantic B., Brusilow W. S., Bernardi P., Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition Proceedings of the National Academy of Sciences of the United States of America 2010 107 2 726 731
89. Pediaditakis P., Kim J. S., He L., Zhang X., Graves L. M., Lemasters J. J., Inhibition of the mitochondrial permeability transition by protein kinase A in rat liver mitochondria and hepatocytes Biochemical Journal 2010 431 3 411 421
90. Baines C. P., Song C. X., Zheng Y. T., Wang G. W., Zhang J., Wang O. L., Guo Y., Bolli R., Cardwell E. M., Ping P., Protein kinase C interacts with and inhibits the permeability transition pore in cardiac mitochondria Circulation Research 2003 92 8 873 880 (Pubitemid 36542528)
91. Takuma K., Phuagphong P., Lee E., Mori K., Baba A., Matsuda T., Anti-apoptotic effect of cGMP in cultured astrocytes: inhibition by cGMP-dependent protein kinase of mitochondrial permeable transition pore Journal of Biological Chemistry 2001 276 51 48093 48099
92. Borutaite V., Morkuniene R., Arandarcikaite O., Jekabsone A., Barauskaite J., Brown G. C., Nitric oxide protects the heart from ischemia-induced apoptosis and mitochondrial damage via protein kinase G mediated blockage of permeability transition and cytochrome c release Journal of Biomedical Science 2009 16 1, article 70
93. Wyss M., Smeitink J., Wevers R. A., Wallimann T., Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism Biochimica et Biophysica Acta 1992 1102 2 119 166
94. O'Gorman E., Beutner G., Dolder M., Koretsky A. P., Brdiczka D., Wallimann T., The role of creatine kinase in inhibition of mitochondrial permeability transition FEBS Letters 1997 414 2 253 257 (Pubitemid 27389373)
95. Beutner G., Rck A., Riede B., Brdiczka D., Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases Biochimica et Biophysica Acta 1998 1368 1 7 18 (Pubitemid 28031936)
96. Miura T., Nishihara M., Miki T., Drug development targeting the glycogen synthase kinase-3 (GSK-3 )-mediated signal transduction pathway: role of GSK-3 in myocardial protection against ischemia/reperfusion injury Journal of Pharmacological Sciences 2009 109 2 162 167
97. Fajardo G., Zhao M., Berry G., Wong L.-J., Mochly-Rosen D., Bernstein D., 2-adrenergic receptors mediate cardioprotection through crosstalk with mitochondrial cell death pathways Journal of Molecular and Cellular Cardiology 2011 51 5 781 789
98. Adams J. M., Cory S., Life-or-death decisions by the Bcl-2 protein family Trends in Biochemical Sciences 2001 26 1 61 66 (Pubitemid 32124712)
99. Chonghaile T. N., Sarosiek K. A., Vo T.-T., Ryan J. A., Tammareddi A., Moore V. D.G., Deng J., Anderson K. C., Richardson P., Tai Y.-T., Mitsiades C. S., Matulonis U. A., Drapkin R., Stone R., DeAngelo D. J., McConkey D. J., Sallan S. E., Silverman L., Hirsch M. S., Carrasco D. R., Letai A., Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy Science 2011 334 6059 1129 1133
100. Llambi F., Moldoveanu T., Tait S., Bouchier-Hayes L., Temirov J., McCormick L., Dillon C., Green D., A unified model of mammalian BCL-2 protein family interactions at the mitochondria Molecular Cell 2011 44 4 517 531
101. Marzo I., Brenner C., Zamzami N., Susin S. A., Beutner G., Brdiczka D., Rémy R., Xie Z. H., Reed J. C., Kroemer G., The permeability transition pore complex: a target for apoptosis regulation by caspases and Bcl-2-related proteins Journal of Experimental Medicine 1998 187 8 1261 1271 (Pubitemid 28189115)
102. Shimizu S., Narita M., Tsujimoto Y., Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC Nature 1999 399 6735 483 487 (Pubitemid 29258855)
103. Chen Z. X., Pervaiz S., Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells Cell Death and Differentiation 2007 14 9 1617 1627 (Pubitemid 47278847)
104. Alavian K. N., Li H., Collis L., Bonanni L., Zeng L., Sacchetti S., Lazrove E., Nabili P., Flaherty B., Graham M., Chen Y., Messerli S. M., Mariggio M. A., Rahner C., McNay E., Shore G. C., Smith P. J.S., Hardwick J. M., Jonas E. A., Bcl-x L regulates metabolic efficiency of neurons through interaction with the mitochondrial F 1 F O ATP synthase Nature Cell Biology 2011 13 10 1224 1233
105. Marzo I., Brenner C., Zamzami N., Jrgensmeier J. M., Susin S. A., Vieira H. L. A., Prévost M. C., Xie Z., Matsuyama S., Reed J. C., Kroemer G., Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis Science 1998 281 5385 2027 2031 (Pubitemid 28475490)
106. Brenner C., Cadiou H., Vieira H. L. A., Zamzami N., Marzo I., Xie Z., Leber B., Andrews D., Duclohier H., Reed J. C., Kroemer G., Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator Oncogene 2000 19 3 329 336 (Pubitemid 30077332)
107. Belzacq A. S., Vieira H. L. A., Verrier F., Vandecasteele G., Cohen I., Prévost M. C., Larquet E., Pariselli F., Petit P. X., Kahn A., Rizzuto R., Brenner C., Kroemer G., Bcl-2 and Bax modulate adenine nucleotide translocase activity Cancer Research 2003 63 2 541 546 (Pubitemid 36152519)
108. Shimizu S., Konishi A., Kodama T., Tsujimoto Y., BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death Proceedings of the National Academy of Sciences of the United States of America 2000 97 7 3100 3105 (Pubitemid 30183262)
109. Vieira H. L. A., Boya P., Cohen I., El Hamel C., Haouzi D., Druillenec S., Belzacq A. S., Brenner C., Roques B., Kroemer G., Cell permeable BH3-peptides overcome the cytoprotective effect of Bcl-2 and Bcl-XL Oncogene 2002 21 13 1963 1977 (Pubitemid 34270885)
110. Sugioka R., Shimizu S., Funatsu T., Tamagawa H., Sawa Y., Kawakami T., Tsujimoto Y., BH4-domain peptide from Bcl-xL exerts anti-apoptotic activity in vivo Oncogene 2003 22 52 8432 8440 (Pubitemid 37523895)
111. Ono M., Sawa Y., Ryugo M., Alechine A. N., Shimizu S., Sugioka R., Tsujimoto Y., Matsuda H., BH4 peptide derivative from Bcl-xL attenuates ischemia/reperfusion injury thorough anti-apoptotic mechanism in rat hearts European Journal of Cardio-thoracic Surgery 2005 27 1 117 121 (Pubitemid 40038539)
112. Morin D., Assaly R., Paradis S., Berdeaux A., Inhibition of mitochondrial membrane permeability as a putative pharmacological target for cardioprotection Current Medicinal Chemistry 2009 16 33 4382 4398
113. Plin C., Tillement J. P., Berdeaux A., Morin D., Resveratrol protects against cold ischemia-warm reoxygenation-induced damages to mitochondria and cells in rat liver European Journal of Pharmacology 2005 528 13 162 168 (Pubitemid 41773668)
114. Ligeret H., Barthelemy S., Zini R., Tillement J. P., Labidalle S., Morin D., Effects of curcumin and curcumin derivatives on mitochondrial permeability transition pore Free Radical Biology and Medicine 2004 36 7 919 929 (Pubitemid 38401063)
115. Ungvari Z., Sonntag W. E., De Cabo R., Baur J. A., Csiszar A., Mitochondrial protection by resveratrol Exercise and Sport Sciences Reviews 2011 39 3 128 132
116. Rimbaud S., Ruiz M., Piquereau J., Mateo P., Fortin D., Veksler V., Garnier A., Ventura-Clapier R., Resveratrol improves survival, hemodynamics and energetics in a rat model of hypertension leading to heart failure PLoS One 2011 6 10, article e26391
117. Izem-Meziane M., Djerdjouri B., Rimbaud S., Caffin F., Fortin D., Garnier A., Veksler V., Joubert F., Ventura-Clapier R., Catecholamine-induced cardiac mitochondrial dysfunction and mPTP opening: protective effect of curcumin American Journal of Physiology 2012 302 3 H665 H674
118. Tanwar V., Sachdeva J., Golechha M., Kumari S., Arya D. S., Curcumin protects rat myocardium against isoproterenol-induced ischemic injury: attenuation of ventricular dysfunction through increased expression of hsp27 alongwith strengthening antioxidant defense system Journal of Cardiovascular Pharmacology 2010 55 4 377 384
119. Manikandan P., Sumitra M., Aishwarya S., Manohar B. M., Lokanadam B., Puvanakrishnan R., Curcumin modulates free radical quenching in myocardial ischaemia in rats The International Journal of Biochemistry amp; Cell Biology 2004 36 10 1967 1980
120. Kelso G. F., Porteous C. M., Coulter C. V., Hughes G., Porteous W. K., Ledgerwood E. C., Smith R. A. J., Murphy M. P., Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties Journal of Biological Chemistry 2001 276 7 4588 4596
121. Graham D., Huynh N. N., Hamilton C. A., Beattie E., Smith R. A. J., Cochemé H. M., Murphy M. P., Dominiczak A. F., Mitochondria-targeted antioxidant mitoq10 improves endothelial function and attenuates cardiac hypertrophy Hypertension 2009 54 2 322 328
122. Vergeade A., Mulder P., Vendeville-Dehaudt C., Estour F., Fortin D., Ventura-Clapier R., Thuillez C., Monteil C., Mitochondrial impairment contributes to cocaine-induced cardiac dysfunction: prevention by the targeted antioxidant MitoQ Free Radical Biology and Medicine 2010 49 5 748 756
123. Plecit-Hlavat L., Jeek J., Jeek P., Pro-oxidant mitochondrial matrix-targeted ubiquinone MitoQ10 acts as anti-oxidant at retarded electron transport or proton pumping within Complex I International Journal of Biochemistry and Cell Biology 2009 41 8-9 1697 1707
124. Nez-Crdoba J. M., Martnez-Gonzlez M. A., Antioxidant vitamins and cardiovascular disease Current Topics in Medicinal Chemistry 2011 11 14 1861 1869
125. Chen J. Q., Cammarata P. R., Baines C. P., Yager J. D., Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications Biochimica et Biophysica Acta 2009 1793 10 1540 1570
126. Regitz-Zagrosek V., Oertelt-Prigione S., Seeland U., Hetzer R., Sex and gender differences in myocardial hypertrophy and heart failure Wiener Medizinische Wochenschrift 2011 161 109 116
127. Maas A. H. E. M., Van Der Schouw Y. T., Regitz-Zagrosek V., Swahn E., Appelman Y. E., Pasterkamp G., Ten Cate H., Nilsson P. M., Huisman M. V., Stam H. C.G., Eizema K., Stramba-Badiale M., Red alert for womens heart: the urgent need for more research and knowledge on cardiovascular disease in women European Heart Journal 2011 32 11 1362 1368
128. Duckles S. P., Krause D. N., Mechanisms of cerebrovascular protection: oestrogen, inflammation and mitochondria Acta Physiologica 2011 203 1 149 154
129. Klinge C. M., Estrogenic control of mitochondrial function and biogenesis Journal of Cellular Biochemistry 2008 105 6 1342 1351
130. Mattingly K. A., Ivanova M. M., Riggs K. A., Wickramasinghe N. S., Barch M. J., Klinge C. M., Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis Molecular Endocrinology 2008 22 3 609 622 (Pubitemid 351397789)
131. Morkuniene R., Arandarcikaite O., Ivanoviene L., Borutaite V., Estradiol-induced protection against ischemia-induced heart mitochondrial damage and caspase activation is mediated by protein kinase G Biochimica et Biophysica Acta 2010 1797 6-7 1012 1017
132. Borrs C., Gambini J., Lpez-Grueso R., Pallard F. V., Via J., Direct antioxidant and protective effect of estradiol on isolated mitochondria Biochimica et Biophysica Acta 2010 1802 1 205 211
133. Morkuniene R., Jekabsone A., Borutaite V., Estrogens prevent calcium-induced release of cytochrome c from heart mitochondria FEBS Letters 2002 521 1-3 53 56 (Pubitemid 34628457)
134. Muoz-Castaeda J. R., Montilla P., Muoz M. C., Bujalance I., Muntané J., Tnez I., Effect of 17- -estradiol administration during adriamycin-induced cardiomyopathy in ovariectomized rat European Journal of Pharmacology 2005 523 13 86 92 (Pubitemid 41562382)
135. Ventura-Clapier R., Mettauer B., Bigard X., Beneficial effects of endurance training on cardiac and skeletal muscle energy metabolism in heart failure Cardiovascular Research 2007 73 1 10 18 (Pubitemid 44937180)
136. Garnier A., Fortin D., Zoll J., N'Guessan B., Mettauer B., Lampert E., Veksler V., Ventura-Clapier R., Coordinated changes in mitochondrial function and biogenesis in healthy and diseased human skeletal muscle FASEB Journal 2005 19 1 43 52 (Pubitemid 40069919)
137. Ascenso A., Ferreira R., Magalhes J., Exercise-induced cardioprotectionbiochemical, morphological and functional evidence in whole tissue and isolated mitochondria International Journal of Cardiology 2007 117 1 16 30 (Pubitemid 46420357)
138. Ciminelli M., Ascah A., Bourduas K., Burelle Y., Short term training attenuates opening of the mitochondrial permeability transition pore without affecting myocardial function following ischemia-reperfusion Molecular and Cellular Biochemistry 2006 291 1-2 39 47 (Pubitemid 44725300)
139. Marcil M., Bourduas K., Ascah A., Burelle Y., Exercise training induces respiratory substrate-specific decrease in Ca 2+ -induced permeability transition pore opening in heart mitochondria American Journal of Physiology 2006 290 4 H1549 H1557
140. Ascenso A., Lumini-Oliveira J., Machado N. G., Ferreira R. M., Gonalves I. O., Moreira A. C., Marques F., Sardo V. A., Oliveira P. J., Magalhes J., Acute exercise protects against calcium-induced cardiac mitochondrial permeability transition pore opening in doxorubicin-treated rats Clinical Science 2011 120 1 37 49