Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis
Abstract
Mitochondrial membrane permeabilization is a critical event in the process leading to physiological or chemotherapy-induced apoptosis. This permeabilization event is at least in part under the control of the permeability transition pore complex (PTPC), which interacts with oncoproteins from the Bcl-2 family as well as with tumor suppressor proteins from the Bax family, which inhibit or facilitate membrane permeabilization, respectively. Here we show that thiol crosslinking agents including diazenedicarboxylic acid bis 5N, N-dimethylamide (diamide), dithiodipyridine (DTDP), or bis-maleimido-hexane (BMH) can act on the adenine nucleotide translocator (ANT), one of the proteins within the PTPC. ANT alone reconstituted into artificial lipid bilayers suffices to confer a membrane permeabilization response to thiol crosslinking agents. Diamide, DTDP, and BMH but not tert-butylhydroperoxide or arsenite cause the oxidation of a critical cysteine residue (Cys 56) of ANT. Thiol modification within ANT is observed in intact cells, isolated mitochondria, and purified ANT. Recombinant Bcl-2 fails to prevent thiol modification of ANT. Concomitantly, a series of different thiol crosslinking agents (diamide, DTDP, and BMH, phenylarsine oxide) but not tert-butylhydroperoxide or arsenite induce mitochondrial membrane permeabilization and cell death irrespective of the expression level of Bcl-2. These data indicate that thiol crosslinkers cause a covalent modification of ANT which, beyond any control by Bcl-2, leads to mitochondrial membrane permeabilization and cell death.
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Modification of redox-sensitive thiols in ANT regulates formation of the mitochondrial permeability transition pore and cell death.
“it is known that modification of redox-sensitive thiols in this mitochondrial protein regulates the formation of the mitochondrial permeability transition (MPT) pore and cell death (101).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [101]
The redox-sensitive thiols of ANT are targets for modification by nitric oxide, peroxynitrite, thiol crosslinkers, and other thiol-reactive reagents.
“In contrast, the redox-sensitive thiols of ANT have been well studied as targets for modification by nitric oxide, peroxynitrite, thiol crosslinkers, and other thiol-reactive reagents (101, 435).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [101]
Cites
Green, D. R., & Reed, J. C. (1998) · Science · doi:10.1126/science.281.5381.1309 · Cited by 8,998 · see citing works
Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and Cytochrome c
Liu, X., Kim, C. N., Yang, J., Jemmerson, R., & Wang, X. (1996) · Cell · doi:10.1016/s0092-8674(00)80085-9 · Cited by 5,167 · see citing works
Prevention of Apoptosis by Bcl-2: Release of Cytochrome c from Mitochondria Blocked
Yang, J., Liu, X., Bhalla, K. N., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T.-I., Jones, D. P., & Wang, X. (1997) · Science · doi:10.1126/science.275.5303.1129 · Cited by 4,913 · see citing works
The Release of Cytochrome c from Mitochondria: A Primary Site for Bcl-2 Regulation of Apoptosis
Kluck, R. M., Bossy‐Wetzel, E., Green, D. R., & Newmeyer, D. D. (1997) · Science · doi:10.1126/science.275.5303.1132 · Cited by 4,715 · see citing works
Molecular characterization of mitochondrial apoptosis-inducing factor
Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., et al. (1999) · Nature · doi:10.1038/17135 · Cited by 4,060 · see citing works
Self-citationBcl-2 functions in an antioxidant pathway to prevent apoptosis
Hockenbery, D. M., Oltvai, Z. N., Yin, X., Milliman, C. L., & Korsmeyer, S. J. (1993) · Cell · doi:10.1016/0092-8674(93)80066-n · Cited by 3,420 · see citing works
Shimizu, S., Narita, M., Tsujimoto, Y., & Tsujimoto, Y. (1999) · Nature · doi:10.1038/20959 · Cited by 2,178 · see citing works
THE MITOCHONDRIAL DEATH/LIFE REGULATOR IN APOPTOSIS AND NECROSIS
Kroemer, G., Dallaporta, B., & Resche-Rigon, M. (1998) · Annual Review of Physiology · doi:10.1146/annurev.physiol.60.1.619 · Cited by 1,971 · see citing works
Self-citationBcl-2 inhibition of neural death: decreased generation of reactive oxygen species
Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., Örd, T., & Bredesen, D. E. (1993) · Science · doi:10.1126/science.8235659 · Cited by 1,671 · see citing works
Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A., Hirsch, T., Susin, S. A., Petit, P. X., Mignotte, B., & Kroemer, G. (1995) · The Journal of experimental medicine · doi:10.1084/jem.182.2.367 · Cited by 1,567 · see citing works
Self-citationBcl-xL Regulates the Membrane Potential and Volume Homeostasis of Mitochondria
Heiden, M. G. V., Chandel, N. S., Williamson, E. K., Schumacker, P. T., & Thompson, C. B. (1997) · Cell · doi:10.1016/s0092-8674(00)80450-x · Cited by 1,378 · see citing works
Mitochondrial control of nuclear apoptosis.
Zamzami, N., Susín, S. A., Marchetti, P., Hirsch, T., Gomez-Monterrey, I. M., Castedo, M., & Kroemer, G. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.183.4.1533 · Cited by 1,360 · see citing works
Self-citationBax and Adenine Nucleotide Translocator Cooperate in the Mitochondrial Control of Apoptosis
Marzo, I., Brenner, C., Zamzami, N., Jürgensmeier, J. M., Susin, S. A., Vieira, H. L. A., Prévost, M.-C., Xie, Z., Matsuyama, S., Reed, J. C., et al. (1998) · Science · doi:10.1126/science.281.5385.2027 · Cited by 1,168 · see citing works
Self-citationBcl-2 inhibits the mitochondrial release of an apoptogenic protease.
Susín, S. A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, É., Geuskens, M., & Kroemer, G. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.4.1331 · Cited by 1,133 · see citing works
Self-citationNarita, M., Shimizu, S., Ito, T., Chittenden, T., Lutz, R. J., Matsuda, H., & Tsujimoto, Y. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14681 · Cited by 933 · see citing works
Mitochondrial permeability transition is a central coordinating event of apoptosis.
Marchetti, P., Castedo, M., Susín, S. A., Zamzami, N., Hirsch, T., Macho, A., Haeffner, A., Hirsch, F., Geuskens, M., & Kroemer, G. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.3.1155 · Cited by 847 · see citing works
Self-citationMitochondrial Release of Caspase-2 and -9 during the Apoptotic Process
Susín, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Brenner, C., Larochette, N., Prévost, M., Alzari, P. M., & Kroemer, G. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.2.381 · Cited by 710 · see citing works
Self-citationMcEnery, M. W., Snowman, A. M., Trifiletti, R. R., & Snyder, S. H. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.8.3170 · Cited by 708 · see citing works
Marzo, I., Brenner, C., Zamzami, N., Susín, S. A., Beutner, G., Brdiczka, D. G., Rémy, R., Xie, Z.-H., Reed, J. C., & Kroemer, G. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.8.1261 · Cited by 684 · see citing works
Self-citationHalestrap, A. P., Woodfield, K.-Y., & Connern, C. P. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.6.3346 · Cited by 592 · see citing works
Costantini, P., Chernyak, B. V., Petronilli, V., & Bernardi, P. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.12.6746 · Cited by 516 · see citing works
Self-citationCrompton, M., Virji, S., & Ward, J. M. (1998) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1998.2580729.x · Cited by 492 · see citing works
Nicolli, A., Basso, E., Petronilli, V., Wenger, R. M., & Bernardi, P. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.4.2185 · Cited by 482 · see citing works
Pedersen, P. L., Greenawalt, J. W., Reynafarje, B., Hullihen, J. M., Decker, G. L., Soper, J. W., & Bustamente, E. (1978) · Methods in cell biology · doi:10.1016/s0091-679x(08)62030-0 · Cited by 445 · see citing works
Mitochondrial ADP/ATP Carrier Can Be Reversibly Converted into a Large Channel by Ca 2+
Brustovetsky, N., & Klingenberg, M. (1996) · Biochemistry · doi:10.1021/bi960833v · Cited by 423 · see citing works
Mancini, M., Nicholson, D. W., Roy, S., Thornberry, N. A., Peterson, E. P., Casciola-Rosen, L. A., & Rosen, A. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.140.6.1485 · Cited by 408 · see citing works
Woodfield, K., Rück, A., Brdiczka, D. G., & Halestrap, A. P. (1998) · Biochemical Journal · doi:10.1042/bj3360287 · Cited by 386 · see citing works
Mitochondrial Depolarization Accompanies Cytochrome cRelease During Apoptosis in PC6 Cells
Heiskanen, K. M., Bhat, M. B., Wang, H.-W., Ma, J., & Nieminen, A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.9.5654 · Cited by 348 · see citing works
Beutner, G., Rück, A., Riede, B., & Brdiczka, D. G. (1998) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(97)00175-2 · Cited by 342 · see citing works
Mitochondrial carrier proteins
Palmieri, F. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00329-7 · Cited by 341 · see citing works
Arsenite Induces Apoptosis via a Direct Effect on the Mitochondrial Permeability Transition Pore
Larochette, N., Decaudin, D., Jacotot, E. D., Brenner, C., Marzo, I., Susín, S. A., Zamzami, N., Xie, Z., Reed, J., & Kroemer, G. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4519 · Cited by 301 · see citing works
Self-citationHirsch, T., Decaudin, D., Susín, S. A., Marchetti, P., Larochette, N., Resche-Rigon, M., & Kroemer, G. (1998) · Experimental Cell Research · doi:10.1006/excr.1998.4084 · Cited by 254 · see citing works
Self-citationMitochondrial permeability transition triggers lymphocyte apoptosis
Marchetti, P., Hirsch, T., Zamzami, N., Castedo, M., Decaudin, D., Susín, S. A., Masse, B., & Kroemer, G. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.157.11.4830 · Cited by 230 · see citing works
Self-citationRavagnan, L., Marzo, I., Costantini, P., Susín, S. A., Zamzami, N., PETIT, P. X., Hirsch, F., Goulbern, M., Poupon, M., Miccoli, L., et al. (1999) · Oncogene · doi:10.1038/sj.onc.1202625 · Cited by 210 · see citing works
Self-citationRück, A., Dolder, M., Wallimann, T., & Brdiczka, D. G. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00317-2 · Cited by 151 · see citing works
Zamzami, N., Marzo, I., Susín, S. A., Brenner, C., Larochette, N., Marchetti, P., Reed, J., Kofler, R., & Kroemer, G. (1998) · Oncogene · doi:10.1038/sj.onc.1201864 · Cited by 146 · see citing works
Self-citationMajima, E., Ikawa, K., Takeda, M., Hashimoto, M., Shinohara, Y., & Terada, H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.49.29548 · Cited by 107 · see citing works
Beyer, K., & Nuscher, B. (1996) · Biochemistry · doi:10.1021/bi9610055 · Cited by 102 · see citing works
Dialectics in carrier research: The ADP/ATP carrier and the uncoupling protein
Klingenberg, M. (1993) · Journal of Bioenergetics and Biomembranes · doi:10.1007/bf01108402 · Cited by 95 · see citing works
Costantini, P., Chernyak, B. V., Petronilli, V., & Bernardi, P. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)00256-9 · Cited by 88 · see citing works
Self-citationCostantini, P., Colonna, R., & Bernardi, P. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00090-5 · Cited by 88 · see citing works
Self-citationGirón‐Calle, J., & Schmid, H. H. O. (1996) · Biochemistry · doi:10.1021/bi960840j · Cited by 27 · see citing works
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Fulda, S., Galluzzi, L., & Kroemer, G. (2010) · Nature Reviews Drug Discovery · doi:10.1038/nrd3137 · Cited by 1,638 · see citing works
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Kowaltowski, A. J., Castilho, R. F., & Vercesi, A. E. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02316-x · Cited by 832 · see citing works
Zhao, K., Zhao, G.-M., Wu, D., Soong, Y., Birk, A. V., Schiller, P. W., & Szeto, H. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402999200 · Cited by 782 · see citing works
Imai, H., & Nakagawa, Y. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)01197-8 · Cited by 763 · see citing works
Azad, M. B., Chen, Y., & Gibson, S. B. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2270 · Cited by 761 · see citing works
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Buytaert, E., Dewaele, M., & Agostinis, P. (2007) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2007.07.001 · Cited by 749 · see citing works
The permeability transition pore complex: another view
Halestrap, A. P., McStay, G. P., & Clarke, S. J. (2002) · Biochimie · doi:10.1016/s0300-9084(02)01375-5 · Cited by 709 · see citing works
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Yang, Y., Karakhanova, S., Hartwig, W., D’Haese, J. G., Philippov, P. P., Werner, J., & Bazhin, A. V. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25349 · Cited by 671 · see citing works
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Marchi, S., Giorgi, C., Suski, J. M., Agnoletto, C., Bononi, A., Bonora, M., Marchi, E. D., Missiroli, S., Patergnani, S., Poletti, F., et al. (2011) · Journal of Signal Transduction · doi:10.1155/2012/329635 · Cited by 639 · see citing works
Deniaud, A., Sharaf el dein, O., Maillier, E., Poncet, D., Kroemer, G., Lemaire, C., & Brenner, C. (2008) · Oncogene · doi:10.1038/sj.onc.1210638 · Cited by 586 · see citing works
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Ueda, S., Masutani, H., Nakamura, H., Tanaka, T., Ueno, M., & Yodoi, J. (2002) · Antioxidants and Redox Signaling · doi:10.1089/15230860260196209 · Cited by 581 · see citing works
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Cox, A. G., Winterbourn, C. C., & Hampton, M. B. (2009) · Biochemical Journal · doi:10.1042/bj20091541 · Cited by 530 · see citing works
Mitochondrion as a Novel Target of Anticancer Chemotherapy
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Self-citationRecent advances in apoptosis, mitochondria and drug resistance in cancer cells
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Self-citationLysosomal Membrane Permeabilization Induces Cell Death in a Mitochondrion-dependent Fashion
Boya, P., Andreau, K., Poncet, D., Zamzami, N., Perfettini, J.-L., Metivier, D., Ojcius, D. M., Jäättelä, M., & Kroemer, G. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021952 · Cited by 483 · see citing works
Self-citationZhang, S., Ong, C. N., & Shen, H. (2004) · Cancer Letters · doi:10.1016/j.canlet.2003.11.028 · Cited by 482 · see citing works
Chemotherapy: targeting the mitochondrial cell death pathway
Debatin, K., Poncet, D., & Kroemer, G. (2002) · Oncogene · doi:10.1038/sj.onc.1206039 · Cited by 398 · see citing works
Self-citationThe Mitochondrion in Cell Death Control: Certainties and Incognita
Loeffler, M. W., & Kroemer, G. (2000) · Experimental Cell Research · doi:10.1006/excr.2000.4833 · Cited by 394 · see citing works
Self-citationInteractions between mitochondrial reactive oxygen species and cellular glucose metabolism
Liemburg-Apers, D. C., Willems, P. H. G. M., Koopman, W. J. H., & Grefte, S. (2015) · Archives of Toxicology · doi:10.1007/s00204-015-1520-y · Cited by 391 · see citing works
Chang, T.-S., Cho, C.-S., Park, S., Yu, S., Kang, S. W., & Rhee, S. G. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407707200 · Cited by 388 · see citing works
Jan, G., Belzacq, A.-S., Haouzi, D., Rouault, A., Métivier, D., Kroemer, G., & Brenner, C. (2002) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4400935 · Cited by 385 · see citing works
Self-citationMcSTAY, G. P., CLARKE, S. J., & HALESTRAP, A. P. (2002) · Biochemical Journal · doi:10.1042/bj20011672 · Cited by 367 · see citing works
Glutathione in liver diseases and hepatotoxicity
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Reactive oxygen species and the mitochondrial signaling pathway of cell death.
Bras, M. L., Clément, M.-V., Pervaiz, S., & Brenner, C. (2005) · PubMed · doi:10.14670/hh-20.205 · Cited by 359 · see citing works
Self-citationMitochondria as therapeutic targets for cancer chemotherapy
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Self-citationBonora, M., Wieckowski, M. R., Chinopoulos, C., Kepp, O., Kroemer, G., Galluzzi, L., & Pinton, P. (2015) · Oncogene · doi:10.1038/onc.2014.96 · Cited by 330 · see citing works
Self-citationLeung, A. W. C., & Halestrap, A. P. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.03.009 · Cited by 323 · see citing works
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Signalling apoptosis: a radical approach
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Jacotot, E. D., Ferri, K. F., Hamel, C. E., Brenner, C., Druillennec, S., Hoebeke, J., Rustin, P., Métivier, D., Lenoir, C., Geuskens, M., et al. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.4.509 · Cited by 273 · see citing works
Self-citationYang, Z., Schumaker, L. M., Egorin, M. J., Zuhowski, E. G., Guo, Z., & Cullen, K. J. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1037 · Cited by 270 · see citing works
Zhao, K., Luo, G., Giannelli, S., & Szeto, H. H. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.08.022 · Cited by 251 · see citing works
The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal
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Salvi, M., Battaglia, V., Brunati, A. M., La Rocca, N., Tibaldi, E., Pietrangeli, P., Marcocci, L., Mondovi, B., Rossi, C. A., & Toninello, A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701589200 · Cited by 231 · see citing works
Arsenic trioxide, a therapeutic agent for APL
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Knockout mice heterozygous forSod2show alterations in cardiac mitochondrial function and apoptosis
Remmen, H. V., Williams, M. D., Guo, Z., Estlack, L. E., Yang, H. C., Carlson, E. J., Epstein, C. J., Huang, T., & Richardson, A. G. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.3.h1422 · Cited by 230 · see citing works
Vieira, H. L. A., Haouzi, D., Hamel, C. E., Jacotot, E. D., Belzacq, A.-S., Brenner, C., & Kroemer, G. (2000) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400778 · Cited by 229 · see citing works
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Odin, J. A., Huebert, R. C., Casciola-Rosen, L., LaRusso, N. F., & Rosen, A. (2001) · Journal of Clinical Investigation · doi:10.1172/jci200110716 · Cited by 220 · see citing works
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Mitochondrial and Cell Death Mechanisms in Neurodegenerative Diseases
Martin, L. J. (2010) · Pharmaceuticals · doi:10.3390/ph3040839 · Cited by 208 · see citing works
Oxygen free radicals and redox biology of organelles
Moldovan, L., & Moldovan, N. I. (2004) · Histochemistry and Cell Biology · doi:10.1007/s00418-004-0676-y · Cited by 207 · see citing works
Ketone bodies are protective against oxidative stress in neocortical neurons
Kim, D. Y., Davis, L. M., Sullivan, P. G., Maalouf, M., Simeone, T. A., van Brederode, J. F. M., & Rho, J. M. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04483.x · Cited by 205 · see citing works
Mitochondria as a critical target of the chemotheraputic agent cisplatin in head and neck cancer
Cullen, K. J., Yang, Z., Schumaker, L. M., & Guo, Z. (2007) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-006-9059-5 · Cited by 194 · see citing works
Belzacq, A.-S., Hamel, C. E., Vieira, H. L. A., Cohen, I., Haouzi, D., Métivier, D., Marchetti, P., Brenner, C., & Kroemer, G. (2001) · Oncogene · doi:10.1038/sj.onc.1204953 · Cited by 194 · see citing works
Self-citationPrinciples in Redox Signaling: From Chemistry to Functional Significance
Bindoli, A., & Rigobello, M. P. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4655 · Cited by 189 · see citing works
Apoptotic effect of eugenol in human colon cancer cell lines
Jaganathan, S. K., Mazumdar, A., Mondhe, D. M., & Mandal, M. (2010) · Cell Biology International · doi:10.1042/cbi20100118 · Cited by 189 · see citing works
Redox active calcium ion channels and cell death
Waring, P. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2004.08.001 · Cited by 189 · see citing works
Martin, L. J., Gertz, B., Pan, Y. H., Price, A. C., Molkentin, J. D., & Chang, Q. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.02.015 · Cited by 181 · see citing works
Bid acts on the permeability transition pore complex to induce apoptosis
Zamzami, N., Hamel, C. E., Maisse, C., Brenner, C., Muñoz-Pinedo, C., Belzacq, A.-S., Costantini, P., Vieira, H., Loeffler, M., Molle, G., et al. (2000) · Oncogene · doi:10.1038/sj.onc.1204030 · Cited by 178 · see citing works
Self-citationPhysiological Roles of the Permeability Transition Pore
Brenner, C., & Moulin, M. (2012) · Circulation Research · doi:10.1161/circresaha.112.265942 · Cited by 179 · see citing works
Self-citationDimmeler, S., & Zeiher, A. M. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(00)00105-1 · Cited by 178 · see citing works
Disruption of mitochondrial redox circuitry in oxidative stress
Jones, D. P. (2006) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2006.07.008 · Cited by 176 · see citing works
Brar, S. S., Grigg, C., Wilson, K. S., Holder, W. D., Dréau, D., Austin, C. E., Foster, M., Ghio, A. J., Whorton, A. R., Stowell, G. W., et al. (2004) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.1049.3.9 · Cited by 172 · see citing works
Burwell, L. S., & Brookes, P. S. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1845 · Cited by 172 · see citing works
Lluis, J. M., Colell, A., García‐Ruiz, C., Kaplowitz, N., & Fernández-Checa, J. C. (2003) · Gastroenterology · doi:10.1053/gast.2003.50089 · Cited by 172 · see citing works
The Role of Reactive Oxygen Species in the Life Cycle of the Mitochondrion
Venditti, P., & Meo, S. D. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062173 · Cited by 170 · see citing works
Programmed Death Phenomena: From Organelle to Organism
Skulachev, V. P. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02095.x · Cited by 171 · see citing works
Inhibition of energy-producing pathways of HepG2 cells by 3-bromopyruvate1
Silva, A. P. P. D., El‐Bacha, T., Kyaw, N., dos Santos, R. S., da‐Silva, W. S., Almeida, F. C. L., Poian, A. T. D., & Galina, A. (2008) · Biochemical Journal · doi:10.1042/bj20080805 · Cited by 170 · see citing works
Bcl-2 and Bax modulate adenine nucleotide translocase activity.
Belzacq, A.-S., Vieira, H. L. A., Verrier, F., Vandecasteele, G., Cohen, I., Prévost, M., Larquet, É., Pariselli, F., PETIT, P. X., Kahn, A., et al. (2003) · PubMed · Cited by 167 · see citing works
Self-citationBiology of Mitochondria in Neurodegenerative Diseases
Martin, L. J. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-385883-2.00005-9 · Cited by 162 · see citing works
Gerasimenko, J. V., Gerasimenko, O. V., Palejwala, A. A., Tepikin, A. V., Petersen, O. H., & Watson, A. J. M. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.3.485 · Cited by 163 · see citing works
Anderson, E. J., Rodríguez, E., Anderson, C. A., Thayne, K. A., Chitwood, W. R., & Kypson, A. P. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00932.2010 · Cited by 163 · see citing works
Chen, Y., Cai, J.-Y., Murphy, T., & Jones, D. P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202026200 · Cited by 166 · see citing works
Mitochondria and aging: A role for the mitochondrial transition pore?
Panel, M., Ghaleh, B., & Morin, D. (2018) · Aging Cell · doi:10.1111/acel.12793 · Cited by 149 · see citing works
Apoptosis and necrosis in health and disease: Role of mitochondria
Nieminen, A. (2003) · International review of cytology · doi:10.1016/s0074-7696(05)24002-0 · Cited by 145 · see citing works
Disulfiram induces apoptosis in human melanoma cells: a redox-related process.
Cen, D., Gonzalez, R. I., Buckmeier, J. A., Kahlon, R. S., Tohidian, N. B., & Meyskens, F. L. (2002) · PubMed · Cited by 145 · see citing works
Local Melatoninergic System as the Protector of Skin Integrity
Slominski, A. T., Kleszczyński, K., Semak, I. V., Janjetović, Z., Zmijewski, M. A., Kim, T., Slominski, R. M., Reiter, R. J., & Fischer, T. W. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms151017705 · Cited by 145 · see citing works
Mitochondriotoxic compounds for cancer therapy
Fantin, V. R., & Leder, P. (2006) · Oncogene · doi:10.1038/sj.onc.1209599 · Cited by 144 · see citing works
3-bromopyruvate: Targets and outcomes
Shoshan, M. C. (2012) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-012-9419-2 · Cited by 144 · see citing works
Li, M., Xia, T., Jiang, C.-S., Li, L.-J., Fu, J.-L., & Zhou, Z.-C. (2003) · Toxicology · doi:10.1016/s0300-483x(03)00327-5 · Cited by 137 · see citing works
Mitochondrial permeability transition in apoptosis and necrosis
Zamzami, N., Larochette, N., & Kroemer, G. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401682 · Cited by 136 · see citing works
Self-citationThe mitochondrial permeability transition: Recent progress and open questions
Bernardi, P., Carraro, M., & Lippe, G. (2021) · FEBS Journal · doi:10.1111/febs.16254 · Cited by 135 · see citing works
The programmed death phenomena, aging, and the Samurai law of biology
Skulachev, V. P. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(01)00109-7 · Cited by 134 · see citing works
Queiroga, C. S. F., Almeida, A. S., Martel, C., Brenner, C., Alves, P. M., & Vieira, H. L. A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.065052 · Cited by 133 · see citing works
Self-citationHansen, J. M., Zhang, H., & Jones, D. P. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfj175 · Cited by 131 · see citing works
Agostinelli, E., Arancia, G., Vedova, L. D., Belli, F., Marra, M., Salvi, M., & Toninello, A. (2004) · Amino Acids · doi:10.1007/s00726-004-0114-4 · Cited by 129 · see citing works
Boscolo, A., Milanović, D., Starr, J. A., Sanchez, V., Oklopcic, A., Moy, L., Ori, C., Erişir, A., & Jevtović‐Todorović, V. (2013) · Anesthesiology · doi:10.1097/aln.0b013e318289bc9b · Cited by 128 · see citing works
Precise Subcellular Organelle Targeting for Boosting Endogenous‐Stimuli‐Mediated Tumor Therapy
Zhen, W., An, S., Wang, S., Hu, W., Li, Y., Jiang, X., & Li, J. (2021) · Advanced Materials · doi:10.1002/adma.202101572 · Cited by 128 · see citing works
Oxygen toxicity: cellular mechanisms in normobaric hyperoxia
Alva, R., Mirza, M., Baiton, A., Lazuran, L., Samokysh, L., Bobinski, A. R., Cowan, C., Jaimon, A., Obioru, D., Makhoul, T. A., et al. (2022) · Cell Biology and Toxicology · doi:10.1007/s10565-022-09773-7 · Cited by 128 · see citing works
The Modes of Cell Death Induced by PDT: An Overview
Plaetzer, K., Kiesslich, T., Verwanger, T., & Krammer, B. E. (2003) · Medical Laser Application · doi:10.1078/1615-1615-00082 · Cited by 126 · see citing works
Siegmund, S., Qian, T., Minicis, S. D., Harvey-White, J. D., Kunos, G., Vinod, K. Y., Hungund, B. L., & Schwabe, R. F. (2007) · The FASEB Journal · doi:10.1096/fj.06-7717com · Cited by 123 · see citing works
Apoptosis Following Photodynamic Tumor Therapy: Induction, Mechanisms and Detection
Plaetzer, K., Kiesslich, T., Oberdanner, C. B., & Krammer, B. E. (2005) · Current Pharmaceutical Design · doi:10.2174/1381612053507648 · Cited by 122 · see citing works
Gottlieb, R. A. (2001) · Neurosignals · doi:10.1159/000046884 · Cited by 120 · see citing works
Redox regulation and signaling lipids in mitochondrial apoptosis.
Fernández-Checa, J. (2003) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/s0006-291x(03)00619-3 · Cited by 120 · see citing works
Targeting mitochondria for cancer therapy
Hockenbery, D. M. (2010) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20552 · Cited by 121 · see citing works
The adenine nucleotide translocator in apoptosis
Belzacq, A.-S., Vieira, H. L. A., Kroemer, G., & Brenner, C. (2002) · Biochimie · doi:10.1016/s0300-9084(02)01366-4 · Cited by 117 · see citing works
Self-citationKorotkov, S. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914459 · Cited by 115 · see citing works
- Authors
- Costantini, P., Belzacq, A.-S., Vieira, H. L., Larochette, N., de Pablo, M. A., Zamzami, N., Susin, S. A., Brenner, C., & Kroemer, G.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Université de Technologie de Compiègne (FR)
- Venue
- Oncogene
- Published
- 2000-01-13
- Volume
- 19
- Issue
- 2
- Pages
- 307-314
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- OpenAlex
- W2053090763
- Cited by
- 284
- References
- 42
- Citations by year
- 2026: 2 · 2024: 1 · 2023: 3 · 2022: 3 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 8 · 2017: 2 · 2016: 6 · 2015: 9 · 2014: 3 · 2013: 6 · 2012: 11
- FWCI
- 9.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Keywords
- adenine nucleotide translocase, mitochondrial permeability transition pore, mitochondrial membrane permeabilization, apoptosis, cysteine oxidation, Bcl-2, Bax, mitochondrial permeability transition, covalent modification, diamide, phenylarsine oxide, tert-butyl hydroperoxide, arsenite
- MeSH terms
- Mitochondrial ADP, ATP Translocases, Animals, Cell Line, Cross-Linking Reagents, Humans, Hybridomas, Intracellular Membranes, Oxidation-Reduction, Permeability, Sulfhydryl Compounds, Rats, Wistar, Apoptosis, Proto-Oncogene Proteins c-bcl-2, Macromolecular Substances, Rats
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