Mitochondrial Permeability Transition: New Findings and Persisting Uncertainties
Abstract
Several insults cause the inner mitochondrial membrane to abruptly lose osmotic homeostasis, hence initiating a regulated variant of cell death known as 'mitochondrial permeability transition' (MPT)-driven necrosis. MPT provides an etiological contribution to several human disorders characterized by the acute loss of post-mitotic cells, including cardiac and cerebral ischemia. Nevertheless, the precise molecular determinants of MPT remain elusive, which considerably hampers the development of clinically implementable cardio- or neuroprotective strategies targeting this process. We summarize recent findings shedding new light on the supramolecular entity that mediates MPT, the so-called 'permeability transition pore complex' (PTPC). Moreover, we discuss hitherto unresolved controversies on MPT and analyze the major obstacles that still preclude the complete understanding and therapeutic targeting of this process.
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MPT-driven necrosis is a form of RCD initiated by specific perturbations of intracellular microenvironment such as severe oxidative stress and cytosolic Ca2+ overload, which generally manifests with necrotic morphotype.
“MPT-driven necrosis is a form of RCD initiated by specific perturbations of the intracellular microenvironment such as severe oxidative stress and cytosolic Ca2+ overload, which generally manifests with a necrotic morphotype [373, 374].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [373]
MPT refers to abrupt loss of impermeability of IMM to small solutes, resulting in rapid Δψm dissipation, osmotic breakdown of both mitochondrial membranes, and RCD.
“The term MPT refers to an abrupt loss of the impermeability of the IMM to small solutes, resulting in rapid Δψm dissipation, osmotic breakdown of both mitochondrial membranes, and RCD [373, 374].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [373]
Several other proteins previously hypothesized to mediate non-redundant role within PTPC turned out to be dispensable for MPT in vivo, based on relatively robust genetic models.
“At odds with CYPD, several other proteins that had previously been hypothesized to mediate a non-redundant role within the PTPC turned out to be dispensable for MPT in vivo, based on relatively robust genetic models [373].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [373]
These results reflect a consistent degree of genetic and functional redundancy among components of molecular machinery for MPT.
“These results reflect a consistent degree of genetic and functional redundancy among the components of the molecular machinery for MPT [373].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [373]
Cites
Mitochondrial membrane permeabilization in cell death
Kroemer, G., Galluzzi, L., & Brenner, C. (2007) · Physiological Reviews · doi:10.1152/physrev.00013.2006 · Cited by 3,598 · see citing works
Self-citationClassification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009
Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., El-Deiry, W. S., Golstein, P., Green, D. R., et al. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2008.150 · Cited by 3,399 · see citing works
Self-citationApoptosis: controlled demolition at the cellular level
Taylor, R. C., Cullen, S. P., & Martin, S. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2312 · Cited by 2,617 · see citing works
Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.96 · Cited by 2,421 · see citing works
Self-citationBaines, 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., et al. (2005) · Nature · doi:10.1038/nature03434 · Cited by 2,280 · see citing works
Shimizu, S., Narita, M., Tsujimoto, Y., & Tsujimoto, Y. (1999) · Nature · doi:10.1038/20959 · Cited by 2,178 · see citing works
Programmed Cell Death in Animal Development and Disease
Fuchs, Y., & Steller, H. (2011) · Cell · doi:10.1016/j.cell.2011.10.033 · Cited by 1,915 · see citing works
Regulated necrosis: the expanding network of non-apoptotic cell death pathways
Berghe, T. V., Linkermann, A., Jouan-Lanhouet, S., Walczak, H., & Vandenabeele, P. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3737 · Cited by 1,735 · see citing works
Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., & Tsujimoto, Y. (2005) · Nature · doi:10.1038/nature03317 · Cited by 1,635 · see citing works
Immunological effects of conventional chemotherapy and targeted anticancer agents
Galluzzi, L., Buqué, A., Kepp, O., Zitvogel, L., & Kroemer, G. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.10.012 · Cited by 1,530 · see citing works
Effect of Cyclosporine on Reperfusion Injury in Acute Myocardial Infarction
Piot, C. A., Croisille, P., Staat, P., Thibault, H., Rioufol, G., Mewton, N., Belghiti, R. E., Cung, T. T., Bonnefoy‐Cudraz, E., Angoulvant, D., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa071142 · Cited by 1,339 · see citing works
Autophagy in malignant transformation and cancer progression
Galluzzi, L., Pietrocola, F., Bravo‐San Pedro, J. M., Amaravadi, R. K., Baehrecke, E. H., Cecconi, F., Codogno, P., Debnath, J., Gewirtz, D. A., Karantza, V., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201490784 · Cited by 1,182 · 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-citationSynchronized renal tubular cell death involves ferroptosis
Linkermann, A., Skouta, R., Himmerkus, N., Mulay, S. R., Dewitz, C., De Zen, F., Prokai, A., Zuchtriegel, G., Krombach, F., Welz, P.-S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415518111 · Cited by 1,126 · see citing works
The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore
Kokoszka, J. E., Waymire, K. G., Levy, S. E., Sligh, J. E., Cai, J., Jones, D. P., MacGregor, G. R., & Wallace, D. C. (2004) · Nature · doi:10.1038/nature02229 · Cited by 1,086 · see citing works
Essential versus accessory aspects of cell death: recommendations of the NCCD 2015
Galluzzi, L., Bravo-San Pedro, J. M., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Alnemri, E. S., Altucci, L., Andrews, D., Annicchiarico-Petruzzelli, M., et al. (2015) · Cell Death & Differentiation · doi:10.1038/cdd.2014.137 · Cited by 1,002 · see citing works
Self-citationVoltage-dependent anion channels are dispensable for mitochondrial-dependent cell death
Baines, C. P., Kaiser, R. A., Sheiko, T., Craigen, W. J., & Molkentin, J. D. (2007) · Nature Cell Biology · doi:10.1038/ncb1575 · Cited by 971 · see citing works
Dimers of mitochondrial ATP synthase form the permeability transition pore
Giorgio, V., von Stockum, S., Antoniel, M., Fabbro, A., Fogolari, F., Forte, M. A., Glick, G. D., Petronilli, V., Zoratti, M., Szabó, I., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217823110 · Cited by 924 · see citing works
VDAC2 Inhibits BAK Activation and Mitochondrial Apoptosis
Cheng, E. H.-Y., Sheiko, T. V., Fisher, J. K., Craigen, W. J., & Korsmeyer, S. J. (2003) · Science · doi:10.1126/science.1083995 · Cited by 852 · see citing works
Mitochondrial permeability transition and oxidative stress
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
Consensus guidelines for the detection of immunogenic cell death
Kepp, O., Senovilla, L., Vitale, I., Vacchelli, E., Adjemian, S., Agostinis, P., Apetoh, L., Aranda, F., Barnaba, V., Bloy, N., et al. (2014) · OncoImmunology · doi:10.4161/21624011.2014.955691 · Cited by 832 · see citing works
Self-citationSchinzel, A. C., Takeuchi, O., Huang, Z., Fisher, J. K., Zhou, Z., Rubens, J., Hetz, C., Danial, N. N., Moskowitz, M. A., & Korsmeyer, S. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505294102 · Cited by 820 · see citing works
Properties of the Permeability Transition Pore in Mitochondria Devoid of Cyclophilin D
Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M. A., & Bernardi, P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.c500089200 · Cited by 808 · see citing works
p53 Opens the Mitochondrial Permeability Transition Pore to Trigger Necrosis
Vaseva, A. V., Marchenko, N. D., Ji, K., Tsirka, S. E., Holzmann, S., & Moll, U. M. (2012) · Cell · doi:10.1016/j.cell.2012.05.014 · Cited by 740 · see citing works
Cyclosporine before PCI in Patients with Acute Myocardial Infarction
Cung, T.-T., Morel, O., Cayla, G., Rioufol, G., Garcia-Dorado, D., Angoulvant, D., Bonnefoy-Cudraz, E., Guérin, P., Elbaz, M., Delarche, N., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1505489 · Cited by 713 · see citing works
Live to die another way: modes of programmed cell death and the signals emanating from dying cells
Fuchs, Y., & Steller, H. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3999 · Cited by 632 · see citing works
Regulated necrosis: disease relevance and therapeutic opportunities
Conrad, M., Angeli, J. P. F., Vandenabeele, P., & Stockwell, B. R. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2015.6 · Cited by 630 · see citing works
Alavian, K. N., Beutner, G., Lazrove, E., Sacchetti, S., Park, H., Licznerski, P., Li, H., Nabili, P., Hockensmith, K., Graham, M. M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1401591111 · Cited by 595 · see citing works
Bernardi, P., Rasola, A., Forte, M. A., & Lippe, G. (2015) · Physiological Reviews · doi:10.1152/physrev.00001.2015 · Cited by 586 · see citing works
Two independent pathways of regulated necrosis mediate ischemia–reperfusion injury
Linkermann, A., Bräsen, J. H., Darding, M., Jin, M. K., Sanz, A. B., Heller, J.-O., Zen, F. D., Weinlich, R., Ortíz, A., Walczak, H., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305538110 · Cited by 568 · see citing works
Regulated cell death and inflammation: an auto-amplification loop causes organ failure
Linkermann, A., Stockwell, B. R., Krautwald, S., & Anders, H.-J. (2014) · Nature Reviews Immunology · doi:10.1038/nri3743 · Cited by 522 · see citing works
Inducible in vivo genome editing with CRISPR-Cas9
Dow, L. E., Fisher, J., O’Rourke, K. P., Muley, A., Kastenhuber, E. R., Livshits, G., Tschaharganeh, D. F., Socci, N. D., & Lowe, S. W. (2015) · Nature Biotechnology · doi:10.1038/nbt.3155 · Cited by 482 · see citing works
Cardiolipin provides specificity for targeting of tBid to mitochondria
Lutter, M. L., Fang, M., Luo, X., Nishijima, M., Xie, X., & Wang, X. (2000) · Nature Cell Biology · doi:10.1038/35036395 · Cited by 472 · see citing works
Physiological and Pathological Roles of the Mitochondrial Permeability Transition Pore in the Heart
Kwong, J. Q., & Molkentin, J. D. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2014.12.001 · Cited by 463 · see citing works
Role of the c subunit of the F O ATP synthase in mitochondrial permeability transition
Bonora, M., Bononi, A., Marchi, E. D., Giorgi, C., Lebiedzińska, M., Marchi, S., Patergnani, S., Rimessi, A., Suski, J. M., Wojtala, A., et al. (2013) · Cell Cycle · doi:10.4161/cc.23599 · Cited by 454 · see citing works
Self-citationBaines, C. P., Song, C., Zheng, Y.-T., Wang, G.-W., Zhang, J., Wang, O.-L., Guo, Y., Bolli, R., Cardwell, E. M., & Ping, P. (2003) · Circulation Research · doi:10.1161/01.res.0000069215.36389.8d · Cited by 450 · see citing works
He, L., & Lemasters, J. J. (2002) · FEBS Letters · doi:10.1016/s0014-5793(01)03314-2 · Cited by 435 · see citing works
Shimizu, S., Konishi, A., Kodama, T. S., & Tsujimoto, Y. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3100 · Cited by 433 · see citing works
Elrod, J. W., Wong, R., Mishra, S., Vagnozzi, R. J., Sakthievel, B., Goonasekera, S. A., Karch, J., Gabel, S., Farber, J., Force, T., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci43171 · Cited by 384 · see citing works
Vander Heiden, M. G., Li, X. X., Gottleib, E., Hill, R. B., Thompson, C. B., & Colombini, M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101590200 · Cited by 372 · see citing works
Caspases Connect Cell-Death Signaling to Organismal Homeostasis
Galluzzi, L., López-Soto, A., Kumar, S., & Kroemer, G. (2016) · Immunity · doi:10.1016/j.immuni.2016.01.020 · Cited by 350 · see citing works
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., Varanyuwatana, P., & Halestrap, A. P. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805235200 · Cited by 315 · see citing works
Ferreirinha, F., Quattrini, A., Pirozzi, M., Valsecchi, V., Dina, G., Broccoli, V., Auricchio, A., Piemonte, F., Tozzi, G., Gaeta, L., et al. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200420138 · Cited by 308 · see citing works
Giorgio, V., Bisetto, E., Soriano, M. E., Dabbeni‐Sala, F., Basso, E., Petronilli, V., Forte, M. A., Bernardi, P., & Lippe, G. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.020115 · Cited by 306 · see citing works
Hom, J., Quintanilla, R. A., Hoffman, D. L., Bentley, K. L. D. M., Molkentin, J. D., Sheu, S., & Porter, G. A., Jr. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.08.008 · Cited by 293 · see citing works
Karch, J., Kwong, J. Q., Burr, A. R., Sargent, M. A., Elrod, J. W., Peixoto, P. M., Martinez-Caballero, S., Osinska, H., Cheng, E. H.-Y., Robbins, J., et al. (2013) · eLife · doi:10.7554/elife.00772 · Cited by 290 · cited 1× · see citing works
“Moreover, mice lacking specifically Bax and Bak1 in cardiomyocytes have been attributed an increased resistance to cardiac ischemia/reperfusion, as compared to their wild-type littermates, and isolated Bax / Bak1 / mitochondria were unable to normally undergo MPT in vitro [40].”
Alavian, K. N., Li, H., Collis, L. P., Bonanni, L., Zeng, L., Sacchetti, S., Lazrove, E., Nabili, P., Flaherty, B., Graham, M. M., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2330 · Cited by 283 · see citing works
Hao, Z., Duncan, G. S., Chang, C., Elia, A., Fang, M., Wakeham, A. C., Okada, H., Calzascia, T., Jang, Y., You-Ten, A. J., et al. (2005) · Cell · doi:10.1016/j.cell.2005.03.016 · Cited by 278 · see citing works
Ferreirinha, F., Quattrini, A., Pirozzi, M., et al. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20138 · Cited by 264 · see citing works
Molecular mechanisms of regulated necrosis
Galluzzi, L., Kepp, O., Krautwald, S., Kroemer, G., & Linkermann, A. (2014) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2014.02.006 · Cited by 258 · see citing works
Self-citationOrganelle-specific initiation of cell death
Galluzzi, L., Bravo-San Pedro, J. M., & Kroemer, G. (2014) · Nature Cell Biology · doi:10.1038/ncb3005 · Cited by 239 · see citing works
Self-citationNishihara, M., Miura, T., Miki, T., Tanno, M., Yano, T., Naitoh, K., Ohori, K., Hotta, H., Terashima, Y., & Shimamoto, K. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2007.08.010 · Cited by 235 · see citing works
Mukherjee, R., Mareninova, O. A., Odinokova, I. V., Huang, W., Murphy, J., Chvanov, M., Javed, M. A., Wen, L., Booth, D. M., Cane, M. C., et al. (2015) · Gut · doi:10.1136/gutjnl-2014-308553 · Cited by 233 · see citing works
Inhibition of the Mitochondrial Permeability Transition by Creatine Kinase Substrates
Dolder, M., Walzel, B., Speer, O., Schlattner, U., & Wallimann, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208705200 · Cited by 219 · see citing works
SPG7 Is an Essential and Conserved Component of the Mitochondrial Permeability Transition Pore
Shanmughapriya, S., Rajan, S., Hoffman, N. E., Higgins, A. M., Tomar, D., Nemani, N., Hines, K. J., Smith, D. J., Eguchi, A., Vallem, S., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.08.009 · Cited by 209 · see citing works
Hierarchical involvement of Bak, VDAC1 and Bax in cisplatin-induced cell death
Tajeddine, N., Galluzzi, L., Kepp, O., Hangen, E., Morselli, E., Senovilla, L., Araujo, N., Pinna, G., Larochette, N., Zamzami, N., et al. (2008) · Oncogene · doi:10.1038/onc.2008.63 · Cited by 207 · see citing works
Self-citationOrganelle-Specific Initiation of Autophagy
Sica, V., Galluzzi, L., Bravo-San Pedro, J. M., Izzo, V., Maiuri, M. C., & Kroemer, G. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.021 · Cited by 205 · see citing works
Self-citationDas, S., Wong, R. P., Rajapakse, N. C., Murphy, E., & Steenbergen, C. (2008) · Circulation Research · doi:10.1161/circresaha.108.178970 · Cited by 197 · see citing works
Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein
Arbel, N., Ben-Hail, D., & Shoshan-Barmatz, V. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.345918 · Cited by 179 · 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-citationRegulated cell death and adaptive stress responses
Galluzzi, L., Bravo-San Pedro, J. M., Kepp, O., & Kroemer, G. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2209-y · Cited by 177 · see citing works
Self-citationKwong, J. Q., Davis, J., Baines, C. P., Sargent, M. A., Karch, J., Wang, X., Huang, T., & Molkentin, J. D. (2014) · Cell Death & Differentiation · doi:10.1038/cdd.2014.36 · Cited by 174 · see citing works
Decaudin, D., Castedo, M., Némati, F., Beurdeley‐Thomas, A., Pinieux, G. D. B. D., Caron, A., Pouillart, P., Wijdenes, J., Rouillard, D., Kroemer, G., et al. (2002) · PubMed · Cited by 155 · see citing works
Self-citationA yeast BH3-only protein mediates the mitochondrial pathway of apoptosis
Büttner, S., Ruli, D., Vögtle, F., Galluzzi, L., Moitzi, B., Eisenberg, T., Kepp, O., Habernig, L., Carmona‐Gutierrez, D., Rockenfeller, P., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.197 · Cited by 133 · see citing works
Self-citationGutiérrez‐Aguilar, M., Douglas, D. L., Gibson, A. K., Domeier, T. L., Molkentin, J. D., & Baines, C. P. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.04.008 · Cited by 120 · see citing works
Physiological roles of the mitochondrial permeability transition pore
Mnatsakanyan, N., Beutner, G., Porter, G. A., Alavian, K. N., & Jonas, E. A. (2016) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-016-9652-1 · Cited by 113 · see citing works
Non‐apoptotic functions of apoptosis‐regulatory proteins
Galluzzi, L., Kepp, O., Trojel‐Hansen, C., & Kroemer, G. (2012) · The EMBO Reports · doi:10.1038/embor.2012.19 · Cited by 109 · see citing works
Self-citationIndividual Cardiac Mitochondria Undergo Rare Transient Permeability Transition Pore Openings
Lu, X., Kwong, J. Q., Molkentin, J. D., & Bers, D. M. (2015) · Circulation Research · doi:10.1161/circresaha.115.308093 · Cited by 109 · see citing works
Mitochondrial regulation of cell death: a phylogenetically conserved control
Galluzzi, L., Kepp, O., & Kroemer, G. (2016) · Microbial Cell · doi:10.15698/mic2016.03.483 · Cited by 106 · see citing works
Self-citationThe Inhibitor Protein (IF1) Promotes Dimerization of the Mitochondrial F1F0-ATP Synthase
García, J. J., Morales‐Ríos, E., Cortés-Hernández, P., et al. (2006) · Biochemistry · doi:10.1021/bi060339j · Cited by 97 · see citing works
Alcalá, S., Klee, M., Fernández, J., Fleischer, A., & Pimentel‐Muiños, F. X. (2007) · Oncogene · doi:10.1038/sj.onc.1210600 · Cited by 97 · see citing works
Weaver, J., Tarze, A., Moffat, T. C., Bras, M. L., Deniaud, A., Brenner, C., Bren, G. D., Morin, M. Y., Phenix, B. N., Dong, L. M., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci22954 · Cited by 91 · see citing works
Self-citationVerrier, F., Deniaud, A., Bras, M. L., Métivier, D., Kroemer, G., Mignotte, B., Jan, G., & Brenner, C. (2004) · Oncogene · doi:10.1038/sj.onc.1208001 · Cited by 87 · see citing works
Self-citationSmeele, K. M., Southworth, R., Wu, R., et al. (2011) · Circulation Research · doi:10.1161/circresaha.111.244962 · Cited by 83 · see citing works
Induction of the permeability transition pore in cells depleted of mitochondrial DNA
Masgras, I., Rasola, A., & Bernardi, P. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.02.022 · Cited by 57 · see citing works
Richardson, A. P., & Halestrap, A. P. (2016) · Biochemical Journal · doi:10.1042/bcj20160070 · Cited by 42 · see citing works
Linkermann, A., Konstantinidis, K., & Kitsis, R. N. (2016) · Cell Death & Differentiation · doi:10.1038/cdd.2015.151 · Cited by 36 · see citing works
Datler, C., Pazarentzos, E., Mahul‐Mellier, A., Chaisaklert, W., Hwang, M., Osborne, F. N., & Grimm, S. (2014) · Journal of Cell Science · doi:10.1242/jcs.140467 · Cited by 33 · see citing works
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Self-citationWang, C., Guan, Y., Lv, M., Zhang, R., Guo, Z., Wei, X., Du, X., Yang, J., Li, T., Wan, Y., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.03.017 · Cited by 869 · see citing works
Mitochondrial inner membrane permeabilisation enables mtDNA release during apoptosis
Riley, J. S., Quarato, G., Cloix, C., Lopez, J., O'Prey, J., Pearson, M., Chapman, J., Sesaki, H., Carlin, L. M., Passos, J. F., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201899238 · Cited by 551 · see citing works
Mitochondria in innate immune signaling
Banoth, B., & Cassel, S. L. (2018) · Translational Research · doi:10.1016/j.trsl.2018.07.014 · Cited by 410 · see citing works
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Holmström, K. M., Kostov, R. V., & Dinkova-Kostova, A. T. (2016) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2016.10.002 · Cited by 368 · see citing works
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- Authors
- Izzo, V., Bravo-San Pedro, J. M., Sica, V., Kroemer, G., & Galluzzi, L.
- Affiliations
- Inserm (FR)
- Université Paris-Sud (FR)
- Karolinska University Hospital (SE)
- Corresponding author
- Kroemer, Guido
- Galluzzi, Lorenzo
- Venue
- Trends in Cell Biology
- Publisher
- Elsevier BV
- Published
- 2016-09
- Volume
- 26
- Issue
- 9
- Pages
- 655-667
- ISSN
- 0962-8924 (ISSN-L)
- OpenAlex
- W2345712655
- Cited by
- 205
- References
- 79
- Citations by year
- 2026: 6 · 2025: 14 · 2024: 13 · 2023: 24 · 2022: 27 · 2021: 23 · 2020: 20 · 2019: 28 · 2018: 26 · 2017: 18 · 2016: 6
- FWCI
- 2.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Keywords
- mitochondrial permeability transition, mitochondrial permeability transition pore, regulated cell death, myocardial ischemia, cerebral ischemia, neuroprotection, cardioprotection
- MeSH terms
- Mitochondrial Permeability Transition Pore, Animals, Humans, Models, Biological, Mitochondrial Diseases, Mitochondrial Membrane Transport Proteins
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