Mitochondrial Regulation of Cell Death
Open accessAbstract
Although required for life, paradoxically, mitochondria are often essential for initiating apoptotic cell death. Mitochondria regulate caspase activation and cell death through an event termed mitochondrial outer membrane permeabilization (MOMP); this leads to the release of various mitochondrial intermembrane space proteins that activate caspases, resulting in apoptosis. MOMP is often considered a point of no return because it typically leads to cell death, even in the absence of caspase activity. Because of this pivotal role in deciding cell fate, deregulation of MOMP impacts on many diseases and represents a fruitful site for therapeutic intervention. Here we discuss the mechanisms underlying mitochondrial permeabilization and how this key event leads to cell death through caspase-dependent and -independent means. We then proceed to explore how the release of mitochondrial proteins may be regulated following MOMP. Finally, we discuss mechanisms that enable cells sometimes to survive MOMP, allowing them, in essence, to return from the point of no return.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MOMP directly promotes the cytosolic release of apoptogenic factors that normally reside in the mitochondrial intermembrane space, including cytochrome c (CYCS) and SMAC.
“MOMP directly promotes the cytosolic release of apoptogenic factors that normally reside in the mitochondrial intermembrane space [40, 44, 156]. These mitochondrial proteins include (but are not limited to) cytochrome c, somatic (CYCS), which usually operates as an electron shuttle in the mitochondrial respiratory chain [157–160], and diablo IAP-binding mitochondrial protein (DIABLO; also known as”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [156]
Upon apoptotic signals, BAX and BAK become activated and form macropores in the outer mitochondrial membrane, inducing MOMP.
“Upon receiving apoptotic signals, pro-apoptotic proteins BAX and BAK become activated, and form macropores in the outer mitochondrial membrane, inducing mitochondrial outer-membrane permeabilization (MOMP) (Tait and Green, 2013) (Fig. 3).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Tait and Green, 2013
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The BCL-2 protein family: opposing activities that mediate cell death
Youle, R. J., & Strasser, A. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2308 · Cited by 4,704 · see citing works
Parkin is recruited selectively to impaired mitochondria and promotes their autophagy
Narendra, D., Tanaka, A., Suen, D.-F., & Youle, R. J. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200809125 · Cited by 4,026 · see citing works
Proapoptotic BAX and BAK: A Requisite Gateway to Mitochondrial Dysfunction and Death
Wei, M. C., Zong, W.-X., Cheng, E. H.-Y., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., & Korsmeyer, S. J. (2001) · Science · doi:10.1126/science.1059108 · Cited by 3,988 · see citing works
Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses
Jones, S., Zhang, X., Parsons, D. W., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al. (2008) · Science · doi:10.1126/science.1164368 · Cited by 3,969 · see citing works
Du, C., Fang, M., Li, Y., Li, L., & Wang, X. (2000) · Cell · doi:10.1016/s0092-8674(00)00008-8 · Cited by 3,513 · see citing works
The mitochondrial permeability transition pore and its role in cell death
CROMPTON, M. (1999) · Biochemical Journal · doi:10.1042/bj3410233 · Cited by 2,432 · see citing works
Verhagen, A. M., Ekert, P. G., Pakusch, M., Silke, J., Connolly, L. M., Reid, G. E., Moritz, R. L., Simpson, R. J., & Vaux, D. L. (2000) · Cell · doi:10.1016/s0092-8674(00)00009-x · Cited by 2,372 · see citing works
OPA1 Controls Apoptotic Cristae Remodeling Independently from Mitochondrial Fusion
Frezza, C., Cipolat, S., Martins de Brito, O., Micaroni, M., Beznoussenko, G. V., Rudka, T., Bartoli, D., Polishuck, R. S., Danial, N. N., De Strooper, B., et al. (2006) · Cell · doi:10.1016/j.cell.2006.06.025 · Cited by 1,673 · see citing works
Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Tailor, P., Morimoto, R. I., Cohen, G. M., & Green, D. R. (2000) · Nature Cell Biology · doi:10.1038/35019501 · Cited by 1,513 · see citing works
Self-citationLindsten, T., Ross, A. J., King, A., Zong, W.-X., Rathmell, J. C., Shiels, H. A., Ulrich, E., Waymire, K. G., Mahar, P., Frauwirth, K., et al. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00136-2 · Cited by 1,489 · see citing works
Bid, Bax, and Lipids Cooperate to Form Supramolecular Openings in the Outer Mitochondrial Membrane
Kuwana, T., Mackey, M. R., Perkins, G. A., Ellisman, M. H., Latterich, M., Schneiter, R., Green, D. R., & Newmeyer, D. D. (2002) · Cell · doi:10.1016/s0092-8674(02)01036-x · Cited by 1,480 · see citing works
Self-citationX-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death
Muchmore, S. W., Sattler, M., Liang, H., Meadows, R. P., Harlan, J. E., Yoon, H. S., Nettesheim, D. G., Chang, B. S., Thompson, C. B., Wong, S., et al. (1996) · Nature · doi:10.1038/381335a0 · Cited by 1,467 · see citing works
tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome cPreprint
Wei, M. C., Lindsten, T., Mootha, V. K., Weiler, S., Gross, A., Ashiya, M., Thompson, C. B., & Korsmeyer, S. J. (2000) · Genes & Development · doi:10.1101/gad.14.16.2060 · Cited by 1,265 · see citing works
Bid Induces the Oligomerization and Insertion of Bax into the Outer Mitochondrial Membrane
Eskes, R., Desagher, S., Antonsson, B. E., & Martinou, J. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.3.929-935.2000 · Cited by 1,190 · see citing works
Apaf1 Is Required for Mitochondrial Pathways of Apoptosis and Brain Development
Yoshida, H., Kong, Y., Yoshida, R., Elia, A., Hakem, A., Hakem, R., Penninger, J. M., & Mak, T. W. (1998) · Cell · doi:10.1016/s0092-8674(00)81733-x · Cited by 1,138 · see citing works
Cytosol-to-membrane redistribution of Bax and Bcl-X L during apoptosis
Hsu, Y., Wolter, K. G., & Youle, R. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.8.3668 · Cited by 1,134 · see citing works
Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K., & Takahashi, R. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00341-0 · Cited by 1,116 · see citing works
Suzuki, M., Youle, R. J., & Tjandra, N. (2000) · Cell · doi:10.1016/s0092-8674(00)00167-7 · Cited by 1,104 · see citing works
The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant
Goldstein, J. C., Waterhouse, N. J., Juin, P. P., Evan, G. I., & Green, D. R. (2000) · Nature Cell Biology · doi:10.1038/35004029 · Cited by 1,073 · see citing works
Self-citationA Distinct Pathway Remodels Mitochondrial Cristae and Mobilizes Cytochrome c during Apoptosis
Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S. A., Mannella, C. A., & Korsmeyer, S. J. (2002) · Developmental Cell · doi:10.1016/s1534-5807(01)00116-2 · Cited by 1,072 · see citing works
Ishihara, N., Nomura, M., Jofuku, A., Kato, H., Suzuki, S. O., Masuda, K., Otera, H., Nakanishi, Y., Nonaka, I., Goto, Y.-I., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1907 · Cited by 1,066 · see citing works
Inhibition of Bax Channel-Forming Activity by Bcl-2
Antonsson, B. E., Conti, F., Ciavatta, A., Montessuit, S., Lewis, S., Martinou, I., Bernasconi, L., Bernard, A., Mermod, J., Mazzei, G. J., et al. (1997) · Science · doi:10.1126/science.277.5324.370 · Cited by 1,028 · see citing works
Cytochrome c release from mitochondria proceeds by a two-step process
Ott, M., Robertson, J. D., Gogvadze, V. G., Zhivotovsky, B., & Orrenius, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.241655498 · Cited by 955 · see citing works
Negative regulation of the Apaf-1 apoptosome by Hsp70
Saleh, A., Srinivasula, S. M., Balkir, L., Robbins, P. D., & Alnemri, E. S. (2000) · Nature Cell Biology · doi:10.1038/35019510 · Cited by 823 · see citing works
Caspase-independent cell death
Kroemer, G., & Martin, S. J. (2005) · Nature Medicine · doi:10.1038/nm1263 · Cited by 719 · see citing works
BAX activation is initiated at a novel interaction site
Gavathiotis, E., Suzuki, M., Davis, M. L., Pitter, K., Bird, G. H., Katz, S. G., Tu, H.-C., Kim, H., Cheng, E. H.-Y., Tjandra, N., et al. (2008) · Nature · doi:10.1038/nature07396 · Cited by 700 · see citing works
Gray, M. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011403 · Cited by 639 · see citing works
AIF deficiency compromises oxidative phosphorylation
Vahsen, N., Candé, C., Brière, J.-J., Bénit, P., Joza, N. A., Larochette, N., Mastroberardino, P. G., Péquignot, M. O., Casares, N., Lazar, V., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600461 · Cited by 622 · see citing works
Czabotar, P. E., Westphal, D., Dewson, G., Ma, S., Hockings, C., Fairlie, W. D., Lee, E. F., Yao, S., Robin, A. Y., Smith, B. J., et al. (2013) · Cell · doi:10.1016/j.cell.2012.12.031 · Cited by 573 · see citing works
Pandey, P., Saleh, A., Nakazawa, A., Kumar, S., Srinivasula, S. M., Kumar, V., Weichselbaum, R. R., Nalin, C. M., Alnemri, E. S., Kufe, D. W., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.16.4310 · Cited by 556 · see citing works
Colell, A., Ricci, J.-E., Tait, S., Milasta, S., Maurer, U., Bouchier-Hayes, L., Fitzgerald, P., Guio-Carrion, A., Waterhouse, N. J., Li, C. W., et al. (2007) · Cell · doi:10.1016/j.cell.2007.03.045 · Cited by 516 · see citing works
Self-citationCytochrome c Deficiency Causes Embryonic Lethality and Attenuates Stress-Induced Apoptosis
Li, K., Li, Y., Shelton, J. M., Richardson, J. A., Spencer, E., Chen, Z. J., Wang, X., & Williams, R. S. (2000) · Cell · doi:10.1016/s0092-8674(00)80849-1 · Cited by 509 · see citing works
XIAP discriminates between type I and type II FAS-induced apoptosis
Jost, P. J., Grabow, S., Gray, D., McKenzie, M. D., Nachbur, U., Huang, D. C. S., Bouillet, P., Thomas, H. E., Borner, C., Silke, J., et al. (2009) · Nature · doi:10.1038/nature08229 · Cited by 482 · see citing works
Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK
Allan, L. A., MORRICE, N. A., Brady, S. C., Magee, G. J., Pathak, S., & Clarke, P. R. (2003) · Nature Cell Biology · doi:10.1038/ncb1005 · Cited by 474 · see citing works
Arnoult, D., Gaume, B. R., Karbowski, M., Sharpe, J. C., Cecconi, F., & Youle, R. J. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg423 · Cited by 451 · see citing works
Calpain I Induces Cleavage and Release of Apoptosis-inducing Factor from Isolated Mitochondria
Polster, B. M., Basáñez, G., Etxebarria, A., Hardwick, J. M., & Nicholls, D. G. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m413269200 · Cited by 438 · see citing works
Regulation of the Apaf-1–caspase-9 apoptosome
Bratton, S. B., & Salvesen, G. S. (2010) · Journal of Cell Science · doi:10.1242/jcs.073643 · Cited by 434 · see citing works
Membrane Remodeling Induced by the Dynamin-Related Protein Drp1 Stimulates Bax Oligomerization
Montessuit, S., Somasekharan, S. P., Terrones, O., Lucken‐Ardjomande, S., Herzig, S., Schwarzenbacher, R., Manstein, D. J., Bossy‐Wetzel, E., Basáñez, G., Meda, P., et al. (2010) · Cell · doi:10.1016/j.cell.2010.08.017 · Cited by 422 · see citing works
Vaughn, A. E., & Deshmukh, M. (2008) · Nature Cell Biology · doi:10.1038/ncb1807 · Cited by 408 · see citing works
Martins, L. M., Morrison, A., Klupsch, K., Fedele, V., Moisoi, N., Teismann, P., Abuin, A., Grau, E., Geppert, M., Livi, G. P., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.22.9848-9862.2004 · Cited by 395 · see citing works
Kluck, R. M., Martin, S. J., Hoffman, B. M., Zhou, J. S., Green, D. R., & Newmeyer, D. D. (1997) · The EMBO Journal · doi:10.1093/emboj/16.15.4639 · Cited by 383 · see citing works
Self-citationQuantitative Analysis of Pathways Controlling Extrinsic Apoptosis in Single Cells
Albeck, J. G., Burke, J. M., Aldridge, B. B., Zhang, M., Lauffenburger, D. A., & Sorger, P. K. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.02.012 · Cited by 382 · see citing works
Distinctive Roles of PHAP Proteins and Prothymosin-α in a Death Regulatory Pathway
Jiang, X., Kim, H.-E., Shu, H., Zhao, Y., Zhang, H., Kofron, J. L., Donnelly, J. B., Burns, D., Ng, S., Rosenberg, S. H., et al. (2003) · Science · doi:10.1126/science.1076807 · Cited by 378 · see citing works
Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice
Jones, J. M., Datta, P., Srinivasula, S. M., Ji, W., Gupta, S., Zhang, Z., Davies, E., Hajnóczky, G., Saunders, T. L., Keuren, M. L. V., et al. (2003) · Nature · doi:10.1038/nature02052 · Cited by 378 · see citing works
Caspase-independent cell death: leaving the set without the final cut
Tait, S. W. G., & Green, D. R. (2008) · Oncogene · doi:10.1038/onc.2008.311 · Cited by 353 · see citing works
Self-citationTo Trigger Apoptosis, Bak Exposes Its BH3 Domain and Homodimerizes via BH3:Groove Interactions
Dewson, G., Kratina, T., Sim, H. W., Puthalakath, H., Adams, J. M., Colman, P. M., & Kluck, R. M. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.04.005 · Cited by 348 · see citing works
Germain, M., Mathai, J. P., McBride, H. M., & Shore, G. C. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600592 · Cited by 337 · see citing works
Estaquier, J., & Arnoult, D. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402107 · Cited by 330 · see citing works
Interdigital cell death can occur through a necrotic and caspase-independent pathway
Chautan, M., Chazal, G., Cecconi, F., Gruß, P., & Golstein, P. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80425-4 · Cited by 325 · see citing works
BH3-Triggered Structural Reorganization Drives the Activation of Proapoptotic BAX
Gavathiotis, E., Reyna, D. E., Davis, M. L., Bird, G. H., & Walensky, L. D. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.019 · Cited by 310 · see citing works
Martinou, I., Desagher, S., Eskes, R., Antonsson, B. E., André, É., Fakan, S., & Martinou, J. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.144.5.883 · Cited by 308 · see citing works
Yamaguchi, R., Lartigue, L., Perkins, G. A., Scott, R. T., Dixit, A., Kushnareva, Y., Kuwana, T., Ellisman, M. H., & Newmeyer, D. D. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.07.010 · Cited by 290 · see citing works
Evidence of a Novel Event during Neuronal Death
Deshmukh, M., & Johnson, E. M. (1998) · Neuron · doi:10.1016/s0896-6273(00)80587-5 · Cited by 281 · see citing works
Sun, M., Williams, J. M., Muñoz‐Pinedo, C., Perkins, G. A., Brown, J. M., Ellisman, M. H., Green, D. R., & Frey, T. (2007) · Nature Cell Biology · doi:10.1038/ncb1630 · Cited by 279 · see citing works
Self-citationHao, 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
Basáñez, G., Nechushtan, A., Drozhinin, O., Chanturiya, A., Choe, E., Tutt, S., Wood, K. A., Hsu, Y.-T., Zimmerberg, J. J., & Youle, R. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5492 · Cited by 270 · see citing works
The Apoptosome: Physiological, Developmental, and Pathological Modes of Regulation
Schafer, Z. T., & Kornbluth, S. A. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.04.008 · Cited by 247 · see citing works
Muñoz‐Pinedo, C., Guío-Carrión, A., Goldstein, J. C., FITZGERALD, P. J., Newmeyer, D. D., & Green, D. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603007103 · Cited by 247 · see citing works
Self-citationPhosphorylation of Caspase-9 by CDK1/Cyclin B1 Protects Mitotic Cells against Apoptosis
Allan, L. A., & Clarke, P. R. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.03.019 · Cited by 238 · see citing works
Basáñez, G., Sharpe, J. C., Galanis, J., Brandt, T. B., Hardwick, J. M., & Zimmerberg, J. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206069200 · Cited by 234 · see citing works
Living with death: the evolution of the mitochondrial pathway of apoptosis in animals
Oberst, A., Bender, C., & Green, D. R. (2008) · Cell Death and Differentiation · doi:10.1038/cdd.2008.65 · Cited by 234 · see citing works
Self-citationInhibiting the Mitochondrial Fission Machinery Does Not Prevent Bax/Bak-Dependent Apoptosis
Parone, P. A., James, D. I., Cruz, S. D., Mattenberger, Y., Donzé, O., Barja, F., & Martinou, J. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02282-05 · Cited by 231 · see citing works
Means to an end: apoptosis and other cell death mechanisms
(2011) · Choice Reviews Online · doi:10.5860/choice.48-5678 · Cited by 224 · see citing works
Bak Activation for Apoptosis Involves Oligomerization of Dimers via Their α6 Helices
Dewson, G., Kratina, T., Czabotar, P. E., Day, C. L., Adams, J. M., & Kluck, R. M. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.11.008 · Cited by 220 · see citing works
tRNA Binds to Cytochrome c and Inhibits Caspase Activation
Mei, Y., Yong, J., Liu, H., Shi, Y., Meinkoth, J. L., Dreyfuss, G., & Yang, X. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.023 · Cited by 207 · see citing works
Resistance to Caspase-Independent Cell Death Requires Persistence of Intact Mitochondria
Tait, S. W. G., Parsons, M. J., Llambi, F., Bouchier‐Hayes, L., Connell, S., Muñoz‐Pinedo, C., & Green, D. R. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.03.014 · Cited by 204 · see citing works
Self-citationBID-induced structural changes in BAK promote apoptosis
Moldoveanu, T., Grace, C. R., Llambi, F., Nourse, A., Fitzgerald, P., Gehring, K., Kriwacki, R. W., & Green, D. R. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2563 · Cited by 201 · see citing works
Self-citationPhysiological Concentrations of K+ Inhibit Cytochrome c-dependent Formation of the Apoptosome
Cain, K., Langlais, C., Sun, X.-M., Brown, D. G., & Cohen, G. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107419200 · Cited by 197 · see citing works
Cheung, E. C., Joza, N. A., Steenaart, N. A. E., McClellan, K. A., Neuspiel, M., McNamara, S., MacLaurin, J. G., Rippstein, P. U., Park, D. S., Shore, G. C., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601276 · Cited by 191 · see citing works
Bax dimerizes via a symmetric BH3:groove interface during apoptosis
Dewson, G., Ma, S., Frederick, P., Hockings, C., Tan, I., Kratina, T., & Kluck, R. M. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.138 · Cited by 189 · see citing works
Generation and Characterization of Smac/DIABLO-Deficient Mice
Okada, H., Suh, W., Jin, J., Woo, M., Du, C., Elia, A., Duncan, G. S., Wakeham, A. C., Itié, A., Lowe, S. W., et al. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.10.3509-3517.2002 · Cited by 172 · see citing works
Mitochondrial Disruption in Drosophila Apoptosis
Abdelwahid, E., Yokokura, T., Krieser, R. J., Balasundaram, S., Fowle, W. H., & White, K. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.04.004 · Cited by 165 · see citing works
Direct activation of full-length proapoptotic BAK
Leshchiner, E. S., Braun, C. R., Bird, G. H., & Walensky, L. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214313110 · Cited by 157 · see citing works
Potts, P. R., Singh, S., Knezek, M., Thompson, C. B., & Deshmukh, M. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200307130 · Cited by 149 · see citing works
Real-time single cell analysis of Smac/DIABLO release during apoptosis
Rehm, M., Düßmann, H., & Prehn, J. H. M. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200303123 · Cited by 146 · see citing works
Dynamics of outer mitochondrial membrane permeabilization during apoptosis
Rehm, M., Huber, H. J., Hellwig, C. T., Anguissola, S., Düßmann, H., & Prehn, J. H. M. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2008.187 · Cited by 141 · see citing works
The Apaf‐1•procaspase‐9 apoptosome complex functions as a proteolytic‐based molecular timer
Malladi, S., Challa-Malladi, M., Fearnhead, H. O., & Bratton, S. B. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.152 · Cited by 140 · see citing works
Lartigue, L., Kushnareva, Y., Seong, Y., Lin, H. H., Faustin, B., & Newmeyer, D. D. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-07-0649 · Cited by 134 · see citing works
George, N. M., Evans, J. J. D., & Luo, X. (2007) · Genes & Development · doi:10.1101/gad.1553607 · Cited by 132 · see citing works
Chandra, D., Bratton, S. B., Person, M. D., Tian, Y., Martín, Á. G., Ayres, M., Fearnhead, H. O., Gandhi, V. V., & Tang, D. G. (2006) · Cell · doi:10.1016/j.cell.2006.05.026 · Cited by 127 · see citing works
Substrates of IAP Ubiquitin Ligases Identified with a Designed Orthogonal E3 Ligase, the NEDDylator
Zhuang, M., Guan, S., Wang, H., Burlingame, A. L., & Wells, J. A. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.10.022 · Cited by 125 · see citing works
Mitochondrial Outer Membrane Proteins Assist Bid in Bax-mediated Lipidic Pore Formation
Schafer, B., Quispe, J. D., Choudhary, V., Chipuk, J. E., Ajero, T. G., Du, H., Schneiter, R., & Kuwana, T. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-10-1056 · Cited by 119 · see citing works
Reduced Apaf-1 levels in cardiomyocytes engage strict regulation of apoptosis by endogenous XIAP
Potts, M. B., Vaughn, A. E., McDonough, H., Patterson, C., & Deshmukh, M. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200504082 · Cited by 116 · see citing works
Assembly of the Mitochondrial Apoptosis-induced Channel, MAC
Martinez‐Caballero, S., Dejean, L. M., Kinnally, M., Oh, K. J., Mannella, C. A., & Kinnally, K. W. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m806610200 · Cited by 115 · see citing works
Mitochondrial pathway of apoptosis is ancestral in metazoans
Bender, C. E., FITZGERALD, P. J., Tait, S. W. G., Llambi, F., McStay, G. P., Tupper, D. O., Pellettieri, J., Alvarado, A. S., Salvesen, G. S., & Green, D. R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120680109 · Cited by 115 · see citing works
Self-citationKim, H.-E., Jiang, X., Du, F., & Wang, X. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.03.014 · Cited by 104 · see citing works
Borutaitė, V., & Brown, G. C. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700322200 · Cited by 98 · see citing works
Wright, K. M., Linhoff, M. W., Potts, P. R., & Deshmukh, M. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200406073 · Cited by 95 · see citing works
Calcium Blocks Formation of Apoptosome by Preventing Nucleotide Exchange in Apaf-1
Bao, Q., Lu, W., Rabinowitz, J. D., & Shi, Y. (2007) · Molecular Cell · doi:10.1016/j.molcel.2006.12.013 · Cited by 90 · see citing works
Garcı́a-Pérez, C., Roy, S. S., Naghdi, S., Lin, X., Davies, E., & Hajnóczky, G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118244109 · Cited by 86 · see citing works
Distinct death mechanisms in Drosophila development
Ryoo, H. D., & Baehrecke, E. H. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.08.022 · Cited by 72 · see citing works
Analysis of redox regulation of cytochrome c-induced apoptosis in a cell-free system
Pan, Z., Voehringer, D. W., & Meyn, R. E. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400544 · Cited by 69 · see citing works
XIAP impairs Smac release from the mitochondria during apoptosis
Flanagan, L., Sebastià, J., Tuffy, L. P., Spring, A., Lichawska-Cieślar, A., Devocelle, M. C., Prehn, J. H. M., & Rehm, M. (2010) · Cell Death and Disease · doi:10.1038/cddis.2010.26 · Cited by 63 · see citing works
Discovery and molecular characterization of a Bcl-2–regulated cell death pathway in schistosomes
Lee, E. F., Clarke, O. B., Evangelista, M., Feng, Z., Speed, T. P., Tchoubrieva, E. B., Strasser, A., Kalinna, B. H., Colman, P. M., & Fairlie, W. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100652108 · Cited by 57 · see citing works
Ferraro, E., Pulicati, A., Cencioni, M. T., Cozzolino, M., Navoni, F., Martino, S. D., Nardacci, R., Carrı̀, M. T., & Cecconi, F. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-09-0858 · Cited by 55 · see citing works
MAC inhibitors suppress mitochondrial apoptosis
Peixoto, P. M. V., Ryu, S.-Y., Bombrun, A., Antonsson, B. E., & Kinnally, K. W. (2009) · Biochemical Journal · doi:10.1042/bj20090664 · Cited by 51 · see citing works
Rsk‐mediated phosphorylation and 14‐3‐3ε binding of Apaf‐1 suppresses cytochrome c‐induced apoptosis
Kim, J., Parrish, A. B., Kurokawa, M., Matsuura, K., Freel, C. D., Andersen, J. L., Johnson, C. E., & Kornbluth, S. A. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.491 · Cited by 49 · see citing works
pp32/PHAPI determines the apoptosis response of non-small-cell lung cancer
Hoffarth, S., Zitzer, A. O., Wiewrodt, R. G., Hähnel, P. S., Beyer, V., Kreft, A., Biesterfeld, S., & Schüler, M. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402256 · Cited by 46 · see citing works
An intracellular wave of cytochrome c propagates and precedes Bax redistribution during apoptosis
Lartigue, L., Medina, C. F., Schembri, L., Chabert, P., Zanese, M., Tomasello, M. F., Dalibart, R., Thoraval, D. H., Crouzet, M., Ichas, F., et al. (2008) · Journal of Cell Science · doi:10.1242/jcs.029587 · Cited by 46 · see citing works
Spatial and Temporal Dynamics of Mitochondrial Membrane Permeability Waves during Apoptosis
Bhola, P. D., Mattheyses, A. L., & Simon, S. M. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2009.07.056 · Cited by 45 · see citing works
Niimi, S., Arakawa-Takeuchi, S., Uranbileg, B., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.347690 · Cited by 44 · see citing works
Bax, along with Lipid Conspirators, Allows Cytochrome c to Escape Mitochondria
Hardwick, J. M., & Polster, B. M. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00751-7 · Cited by 43 · see citing works
Infection and the origins of apoptosis
James, E. R., & Green, D. R. (2002) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400986 · Cited by 42 · see citing works
Self-citationKhodjakov, A. L., Rieder, C. L., Mannella, C. A., & Kinnally, K. W. (2003) · Mitochondrion · doi:10.1016/j.mito.2003.10.002 · Cited by 39 · see citing works
Genome-wide silencing in Drosophila captures conserved apoptotic effectors
Chew, S. K., Chen, P., Link, N., Galindo, K. A., Pogue, K., & Abrams, J. (2009) · Nature · doi:10.1038/nature08087 · Cited by 38 · see citing works
Requirement of cytochrome c for apoptosis in human cells
Matapurkar, A., & Lazebnik, Y. A. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401968 · Cited by 34 · see citing works
Lavallard, V., Pradelli, L. A., Paul, A., Bénéteau, M., Jacquel, A., Auberger, P., & Ricci, J. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2731 · Cited by 30 · see citing works
Regulation of apoptosis by C. elegans CED-9 in the absence of the C-terminal transmembrane domain
Tan, F. J., Fire, A. Z., & Hill, R. B. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402215 · Cited by 27 · see citing works
Goemans, C. G., Boya, P., Skirrow, C. J., & Tolkovsky, A. M. (2008) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402290 · Cited by 26 · see citing works
Colell, A., Ricci, J., Tait, S. W. G., et al. (2007) · Cell · doi:10.1016/j.cell.2007.07.012 · Cited by 23 · see citing works
Self-citationGillick, K., & Crompton, M. (2008) · Journal of Cell Science · doi:10.1242/jcs.021303 · Cited by 18 · see citing works
[Regulation of apoptosis by p53].
Ohtsuka, T. (2004) · PubMed · Cited by 11 · see citing works
Kim, H.-E., Jiang, X., Du, F., et al. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.12.018 · Cited by 5 · see citing works
Niimi, S., Arakawa-Takeuchi, S., Uranbileg, B., et al. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.a112.347690 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
Self-citationRegulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins
Singh, R., Letai, A., & Sarosiek, K. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0089-8 · Cited by 2,111 · 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-citationMitochondrial 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
Self-citationA fate worse than death: apoptosis as an oncogenic process
Ichim, G., & Tait, S. W. G. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.58 · Cited by 451 · see citing works
Self-citationMitochondria: diversity in the regulation of the NLRP3 inflammasome
Gurung, P., Lukens, J. R., & Kanneganti, T.-D. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.11.008 · Cited by 393 · see citing works
Interleukin-1β Induces mtDNA Release to Activate Innate Immune Signaling via cGAS-STING
Aarreberg, L. D., Esser-Nobis, K., Driscoll, C., Shuvarikov, A., Roby, J. A., & Gale, M. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.02.038 · Cited by 328 · see citing works
Cytoplasmic DNA: sources, sensing, and role in aging and disease
Miller, K. N., Victorelli, S. G., Salmonowicz, H., Dasgupta, N., Liu, T., Passos, J. F., & Adams, P. D. (2021) · Cell · doi:10.1016/j.cell.2021.09.034 · Cited by 288 · see citing works
Distribution and Apoptotic Function of Outer Membrane Proteins Depend on Mitochondrial Fusion
Weaver, D., Eisner, V., Liu, X., Várnai, P., Hunyady, L., Gross, A., & Hajnóczky, G. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.048 · Cited by 58 · see citing works
Mullane, K., & Williams, M. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.09.027 · Cited by 32 · see citing works
- Authors
- Tait, S. W. G., & Green, D. R.
- Affiliations
- Cancer Research UK Scotland Institute (GB)
- St. Jude Children's Research Hospital (US)
- Venue
- Cold Spring Harbor Perspectives in Biology
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2013-09-01
- Volume
- 5
- Issue
- 9
- Pages
- a008706-a008706
- ISSN
- 1943-0264 (ISSN-L)
- PMC
- PMC3753705
- OpenAlex
- W2157965986
- Cited by
- 530
- References
- 114
- Citations by year
- 2026: 29 · 2025: 48 · 2024: 38 · 2023: 57 · 2022: 52 · 2021: 57 · 2020: 46 · 2019: 51 · 2018: 50 · 2017: 26 · 2016: 37 · 2015: 17 · 2014: 20 · 2013: 2
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cold Spring Harbor Perspectives in Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI044828)
- 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 › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- mitochondrial outer membrane permeabilization, apoptosis, caspase activation, caspase-independent cell death, mitochondrial permeability transition pore, cell fate
- MeSH terms
- Enzyme Activation, Mitochondria, Models, Biological, Permeability, Gene Expression Regulation, Enzymologic, Apoptosis, Proto-Oncogene Proteins c-bcl-2, Caspases, Mitochondrial Proteins, Mitochondrial Membranes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
