Essential versus accessory aspects of cell death: recommendations of the NCCD 2015
Open accessAbstract
Cells exposed to extreme physicochemical or mechanical stimuli die in an uncontrollable manner, as a result of their immediate structural breakdown. Such an unavoidable variant of cellular demise is generally referred to as 'accidental cell death' (ACD). In most settings, however, cell death is initiated by a genetically encoded apparatus, correlating with the fact that its course can be altered by pharmacologic or genetic interventions. 'Regulated cell death' (RCD) can occur as part of physiologic programs or can be activated once adaptive responses to perturbations of the extracellular or intracellular microenvironment fail. The biochemical phenomena that accompany RCD may be harnessed to classify it into a few subtypes, which often (but not always) exhibit stereotyped morphologic features. Nonetheless, efficiently inhibiting the processes that are commonly thought to cause RCD, such as the activation of executioner caspases in the course of apoptosis, does not exert true cytoprotective effects in the mammalian system, but simply alters the kinetics of cellular demise as it shifts its morphologic and biochemical correlates. Conversely, bona fide cytoprotection can be achieved by inhibiting the transduction of lethal signals in the early phases of the process, when adaptive responses are still operational. Thus, the mechanisms that truly execute RCD may be less understood, less inhibitable and perhaps more homogeneous than previously thought. Here, the Nomenclature Committee on Cell Death formulates a set of recommendations to help scientists and researchers to discriminate between essential and accessory aspects of cell death.
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Regulated cell death (RCD) relies on a dedicated molecular machinery, implying that it can be modulated (delayed or accelerated) by pharmacological or genetic interventions.
“RCD relies on a dedicated molecular machinery, implying that it can be modulated (i.e., delayed or accelerated) by pharmacological or genetic interventions [5, 17].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [17]
Executioner caspases precipitate intrinsic apoptosis, once a point-of-no-return has been trespassed, but are not essential for it.
“Of note, a large body of evidence suggests that executioner caspases precipitate intrinsic apoptosis, once a hitherto poorly defined point-of-no-return has been trespassed, but are not essential for it [17].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [17]
CASP3 and CASP7 mediate a facilitating, rather than indispensable, role in RCD.
“Altogether, these observations suggest that CASP3 and CASP7 mediate a facilitating, rather than indispensable, role in RCD (for an extensive discussion on this topic, please refer to ref [17]).”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [17]
Blocking post-mitochondrial caspase activation by genetic means or with specific pharmacological inhibitors (Z-VAD-fmk and Q-VD-OPh) generally delays (but does not prevent) intrinsic apoptosis in vitro and in vivo (at least in the mammalian system), as it promotes a switch to other types of RCD.
“Accordingly, blocking post-mitochondrial caspase activation by genetic means or with specific pharmacological inhibitors, such as to N-benzyloxycarbonyl-Val-Ala-Asp(O-Me) fluoromethylketone (Z-VAD-fmk) and (3S)-5-(2,6-difluorophenoxy)-3-[[(2S)-3-methyl-1-oxo-2-[(2-quinolinylcarbonyl)amino]butyl]amino]-4-oxo-pentanoic acid hydrate (Q-VD-OPh), generally delays (but does not prevent) intrinsic apopt”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [17]
Cell death in all forms including ACD is ultimately associated with a bioenergetic and redox crisis that may be its actual cause.
“Indeed, cell death in all its forms (including ACD) is ultimately associated with a bioenergetic and redox crisis that may constitute its actual cause [17, 374].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [17]
Enzymes such as caspases, thought to have key causal role in RCD execution, in majority of scenarios only accelerate rather than causally determine cellular demise.
“Moreover, the community has focused for a long time on specific enzymes that were thought to have a key causal role in RCD execution, but in a majority of scenarios only appear to accelerate (rather than causally determine) cellular demise (e.g., caspases) [17, 374].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [17]
Necroptosis and ferroptosis are regulated non-apoptotic death forms that have significant roles in many biological contexts.
“Two regulated forms of non-apoptotic cell death, necroptosis and ferroptosis, have been shown recently to play significant roles in numerous biological contexts [1, 2].”
From Ferroptosis: Death by Lipid Peroxidation (2016) · cites this paper as [2]
In vivo inhibition of caspase activity does not prevent cell death, but shifts the mechanism towards a more necrotic phenotype.
“Recent studies in mice reveal that in vivo inhibition of caspase activity does not prevent cell death, but rather shifts the mechanism towards a more necrotic phenotype (Galluzzi et al., 2015).”
From Programmed cell death in aging (2015) · cites this paper as Galluzzi et al., 2015
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Self-citationBID, BIM, and PUMA Are Essential for Activation of the BAX- and BAK-Dependent Cell Death Program
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Self-citationRole of the c subunit of the F O ATP synthase in mitochondrial permeability transition
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Self-citationRedefining viruses: lessons from Mimivirus
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Mitochondria and cell signalling
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Self-citationMlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis
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Regulation of the Apaf-1–caspase-9 apoptosome
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BCL-2 Family Proteins: Critical Checkpoints of Apoptotic Cell Death
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Self-citationQ-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties
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Many stimuli pull the necrotic trigger, an overview
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Self-citationThe CD95 Receptor: Apoptosis Revisited
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Self-citationAutophagy, Not Apoptosis, Is Essential for Midgut Cell Death in Drosophila
Denton, D., Shravage, B., Simin, R., Mills, K., Berry, D. L., Baehrecke, E. H., & Kumar, S. (2009) · Current Biology · doi:10.1016/j.cub.2009.08.042 · Cited by 385 · 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
Cell death by autophagy: facts and apparent artefacts
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Self-citationTherapeutic applications of PARP inhibitors: Anticancer therapy and beyond
Curtin, N. J., & Szabo, C. (2013) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2013.01.006 · Cited by 369 · see citing works
Die another way – non-apoptotic mechanisms of cell death
Tait, S. W. G., Ichim, G., & Green, D. R. (2014) · Journal of Cell Science · doi:10.1242/jcs.093575 · Cited by 366 · cited 1× · see citing works
“Taken together with the notion that the absence of either Ripk3, Casp8 or Fadd fails to rescue Ripk1 / mice from neonatal lethality,(180,185) these results pointed to the existence of a switch mechanism that regulates cell fate upon TNFR1 ligation.(204,205) Intriguingly, such switch may not operate in all cell types,…”
BackgroundSelf-citationIntracellular ATP, a switch in the decision between apoptosis and necrosis
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TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation
Jouan-Lanhouet, S., Arshad, M. I., Piquet-Pellorce, C., Martin-Chouly, C., Le Moigne-Muller, G., Van Herreweghe, F., Takahashi, N., Sergent, O., Lagadic-Gossmann, D., Vandenabeele, P., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2012.90 · Cited by 357 · see citing works
Self-citationRong, Y., & Distelhorst, C. (2007) · Annual Review of Physiology · doi:10.1146/annurev.physiol.70.021507.105852 · Cited by 357 · see citing works
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Self-citationDCP-1, a Drosophila Cell Death Protease Essential for Development
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Self-citationInterdigital cell death can occur through a necrotic and caspase-independent pathway
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Self-citation
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Ferroptosis: A Regulated Cell Death Nexus Linking Metabolism, Redox Biology, and Disease
Stockwell, B. R., Friedmann Angeli, J. P., Bayir, H., Bush, A. I., Conrad, M., Dixon, S. J., Fulda, S., Gascón, S., Hatzios, S. K., Kagan, V. E., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.021 · Cited by 7,695 · see citing works
Self-citationGalluzzi, 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-citationGuidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Self-citationFerroptosis: Death by Lipid Peroxidation
Yang, W. S., & Stockwell, B. R. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.10.014 · Cited by 3,088 · see citing works
Self-citationImmunogenic cell death in cancer and infectious disease
Galluzzi, L., Buqué, A., Kepp, O., Zitvogel, L., & Kroemer, G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.107 · Cited by 3,119 · see citing works
Self-citationKlionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Self-citationMolecular definitions of autophagy and related processes
Galluzzi, L., Baehrecke, E. H., Ballabio, A., Boya, P., Bravo‐San Pedro, J. M., Cecconi, F., Choi, A. M., Chu, C. T., Codogno, P., Colombo, M. I., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201796697 · Cited by 1,646 · see citing works
Self-citationNLRP3 inflammasome activation and cell death
Huang, Y., Xu, W., & Zhou, R. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-021-00740-6 · Cited by 1,527 · 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
Old, new and emerging functions of caspases
Shalini, S., Dorstyn, L., Dawar, S., & Kumar, S. (2015) · Cell Death & Differentiation · doi:10.1038/cdd.2014.216 · Cited by 1,267 · see citing works
Self-citationAutophagy 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-citationMetabolic control of autophagy
Galluzzi, L., Pietrocola, F., Levine, B., & Kroemer, G. (2014) · Cell · doi:10.1016/j.cell.2014.11.006 · Cited by 855 · see citing works
Self-citationAutophagy and mitophagy in cardiovascular disease
Bravo-San Pedro, J. M., Kroemer, G., & Galluzzi, L. (2017) · Circulation Research · doi:10.1161/circresaha.117.311082 · Cited by 843 · see citing works
Self-citationPharmacological modulation of autophagy: therapeutic potential and persisting obstacles
Galluzzi, L., Bravo-San Pedro, J. M., Levine, B., Green, D. R., & Kroemer, G. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.22 · Cited by 842 · see citing works
Self-citationHSPB1 as a novel regulator of ferroptotic cancer cell death
Sun, X., Ou, Z., Xie, M., Kang, R., Fan, Y., Niu, X., Wang, H., Cao, L., & Tang, D. (2015) · Oncogene · doi:10.1038/onc.2015.32 · Cited by 666 · see citing works
Initiation and execution mechanisms of necroptosis: an overview
Grootjans, S., Vanden Berghe, T., & Vandenabeele, P. (2017) · Cell Death & Differentiation · doi:10.1038/cdd.2017.65 · Cited by 566 · see citing works
Self-citationInterleukin 1α and the inflammatory process
Di Paolo, N. C., & Shayakhmetov, D. M. (2016) · Nature Immunology · doi:10.1038/ni.3503 · Cited by 568 · see citing works
Programmed cell death in aging
Tower, J. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.04.002 · Cited by 426 · see citing works
Immunological impact of cell death signaling driven by radiation on the tumor microenvironment
Rodriguez-Ruiz, M. E., Vitale, I., Harrington, K. J., Melero, I., & Galluzzi, L. (2020) · Nature Immunology · doi:10.1038/s41590-019-0561-4 · Cited by 385 · see citing works
Self-citationTNFα blockade overcomes resistance to anti-PD-1 in experimental melanoma
Bertrand, F., Montfort, A., Marcheteau, E., Imbert, C., Gilhodes, J., Filleron, T., Rochaix, P., Andrieu-Abadie, N., Levade, T., Meyer, N., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02358-7 · Cited by 384 · see citing works
“This was associated with an increased plasma membrane permeability, re fl ecting the permanent loss of plasma membrane barrier function and indicates that TILs indeed died, according to recent criteria for cell death 41 .”
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-citationAutophagy and Microglia: Novel Partners in Neurodegeneration and Aging
Plaza-Zabala, A., Sierra-Torre, V., & Sierra, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030598 · Cited by 323 · see citing works
Dixon, S. J. (2017) · Immunological Reviews · doi:10.1111/imr.12533 · Cited by 314 · see citing works
The Autophagy Machinery Controls Cell Death Switching between Apoptosis and Necroptosis
Goodall, M. L., Fitzwalter, B. E., Zahedi, S., Wu, M., Rodriguez, D., Mulcahy-Levy, J. M., Green, D. R., Morgan, M., Cramer, S. D., & Thorburn, A. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.04.018 · Cited by 314 · see citing works
Self-citationActivating autophagy to potentiate immunogenic chemotherapy and radiation therapy
Galluzzi, L., Bravo-San Pedro, J. M., Demaria, S., Formenti, S. C., & Kroemer, G. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.183 · Cited by 314 · see citing works
Self-citationAnti-DNA antibodies–quintessential biomarkers of SLE
Pisetsky, D. S. (2016) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2015.151 · Cited by 267 · see citing works
Autophagy in acute brain injury
Galluzzi, L., Bravo-San Pedro, J. M., Blomgren, K., & Kroemer, G. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.51 · Cited by 234 · see citing works
Self-citationMitochondrial Permeability Transition: New Findings and Persisting Uncertainties
Izzo, V., Bravo-San Pedro, J. M., Sica, V., Kroemer, G., & Galluzzi, L. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.04.006 · Cited by 205 · 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-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-citationZanzottera, E. C., Messinger, J. D., Ach, T., Smith, R. T., Freund, K. B., & Curcio, C. A. (2015) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.15-16431 · Cited by 164 · see citing works
Prognostic and predictive value of DAMPs and DAMP-associated processes in cancer
Fucikova, J., Moserova, I., Urbanova, L., Bezu, L., Kepp, O., Cremer, I., Salek, C., Strnad, P., Kroemer, G., Galluzzi, L., et al. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00402 · Cited by 159 · see citing works
Self-citationRodriguez-Ruiz, M. E., Buqué, A., Hensler, M., Chen, J., Bloy, N., Petroni, G., Sato, A., Yamazaki, T., Fucikova, J., & Galluzzi, L. (2019) · OncoImmunology · doi:10.1080/2162402x.2019.1655964 · Cited by 147 · see citing works
Self-citationBazan, N. G. (2018) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2018.09.003 · Cited by 148 · see citing works
Self-citationPathophysiological role of different tubular epithelial cell death modes in acute kidney injury
Sancho-Martínez, S. M., López-Novoa, J. M., & López-Hernández, F. J. (2015) · Clinical Kidney Journal · doi:10.1093/ckj/sfv069 · Cited by 130 · see citing works
Wang, Z., Liu, D., Varin, A., Nicolas, V, Courilleau, D., Mateo, P., Caubere, C., Rouet, P., Gomez, A.-M., Vandecasteele, G., et al. (2016) · Cell Death & Disease · doi:10.1038/cddis.2016.106 · Cited by 106 · see citing works
Self-citationAn Overview of Pathways of Regulated Necrosis in Acute Kidney Injury
Kers, J., Leemans, J. C., & Linkermann, A. (2016) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2016.03.002 · Cited by 80 · see citing works
Self-citationCocaine elicits autophagic cytotoxicity via a nitric oxide-GAPDH signaling cascade
Guha, P., Harraz, M. M., & Snyder, S. H. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1524860113 · Cited by 70 · see citing works
Machado, M. D., & Soares, E. V. (2019) · Aquatic Toxicology · doi:10.1016/j.aquatox.2019.01.014 · Cited by 68 · see citing works
Lerner, L. K., Francisco, G., Soltys, D. T., Rocha, C. R. R., Quinet, A., Vessoni, A. T., Castro, L. P., David, T. I. P., Bustos, S. O., Strauss, B. E., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1196 · Cited by 53 · see citing works
“The cell cycle and apoptosis (SubG1) (27,31) were monitored 24 and 72 h after the challenging doses, respectively.”
High mobility group A1 protein modulates autophagy in cancer cells
Conte, A., Paladino, S., Bianco, G., Fasano, D., Gerlini, R., Tornincasa, M., Renna, M., Fusco, A., Tramontano, D., & Pierantoni, G. M. (2017) · Cell Death & Differentiation · doi:10.1038/cdd.2017.117 · Cited by 52 · see citing works
Karyotypic Aberrations in Oncogenesis and Cancer Therapy
Vitale, I., Manic, G., Senovilla, L., Kroemer, G., & Galluzzi, L. (2015) · Trends in Cancer · doi:10.1016/j.trecan.2015.08.001 · Cited by 34 · see citing works
Self-citationApoptotic caspases cut down the immunogenicity of radiation
Buqué, A., Rodriguez-Ruiz, M. E., Fucikova, J., & Galluzzi, L. (2019) · OncoImmunology · doi:10.1080/2162402x.2019.1655364 · Cited by 28 · see citing works
Self-citationBencze, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010362 · Cited by 20 · see citing works
Molecular Perspectives of Mitochondrial Adaptations and Their Role in Cardiac Proteostasis
Alam, S., Abdullah, C. S., Aishwarya, R., Morshed, M., & Bhuiyan, M. S. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.01054 · Cited by 12 · see citing works
- Authors
- 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., Baehrecke, E. H., Bazan, N. G., Bertrand, M. J., Bianchi, K., Blagosklonny, M. V., Blomgren, K., Borner, C., Bredesen, D. E., Brenner, C., Campanella, M., Candi, E., Cecconi, F., Chan, F. K., Chandel, N. S., Cheng, E. H., Chipuk, J. E., Cidlowski, J. A., Ciechanover, A., Dawson, T. M., Dawson, V. L., De Laurenzi, V, De Maria, R., Debatin, K.-M., Di Daniele, N., Dixit, V. M., Dynlacht, B. D., El-Deiry, W. S., Fimia, G. M., Flavell, R. A., Fulda, S., Garrido, C., Gougeon, M.-L., Green, D. R., Gronemeyer, H., Hajnoczky, G., Hardwick, J. M., Hengartner, M. O., Ichijo, H., Joseph, B., Jost, P. J., Kaufmann, T., Kepp, O., Klionsky, D. J., Knight, R. A., Kumar, S., Lemasters, J. J., Levine, B., Linkermann, A., Lipton, S. A., Lockshin, R. A., López-Otín, C., Lugli, E., Madeo, F., Malorni, W., Marine, J.-C., Martin, S. J., Martinou, J.-C., Medema, J. P., Meier, P., Melino, S., Mizushima, N., Moll, U., Muñoz-Pinedo, C., Nuñez, G., Oberst, A., Panaretakis, T., Penninger, J. M., Peter, M. E., Piacentini, M., Pinton, P., Prehn, J. H., Puthalakath, H., Rabinovich, G. A., Ravichandran, K. S., Rizzuto, R., Rodrigues, C. M., Rubinsztein, D. C., Rudel, T., Shi, Y., Simon, H.-U., Stockwell, B. R., Szabadkai, G., Tait, S. W., Tang, H. L., Tavernarakis, N., Tsujimoto, Y., Vanden Berghe, T., Vandenabeele, P., Villunger, A., Wagner, E. F., Walczak, H., White, E., Wood, W. G., Yuan, J., Zakeri, Z., Zhivotovsky, B., Melino, G., & Kroemer, G.
- Affiliations
- Institut Gustave Roussy (FR)
- Instituto Nazionale Tumori Regina Elena (IT)
- Tisch Cancer Institute (US)
- The University of Texas Southwestern Medical Center (US)
- Christian-Albrechts-Universität zu Kiel (DE)
- Thomas Jefferson University (US)
- University of Campania "Luigi Vanvitelli" (IT)
- University of Toronto (CA)
- University of Massachusetts Chan Medical School (US)
- Ghent University (BE)
- Queen Mary University of London (GB)
- Roswell Park Comprehensive Cancer Center (US)
- Karolinska University Hospital (SE)
- University of Freiburg (DE)
- Buck Institute for Research on Aging (US)
- Université Paris-Sud (FR)
- University College London (GB)
- University of Rome Tor Vergata (IT)
- Northwestern University (US)
- Memorial Sloan Kettering Cancer Center (US)
- National Institutes of Health (US)
- Technion – Israel Institute of Technology (IL)
- Johns Hopkins University (US)
- University Hospital Ulm (DE)
- Genentech (US)
- New York University (US)
- University of Salento (IT)
- Yale University (US)
- Goethe University Frankfurt (DE)
- Inserm (FR)
- Institut Pasteur (FR)
- St. Jude Children's Research Hospital (US)
- Institut de génétique et de biologie moléculaire et cellulaire (FR)
- University of Zurich (CH)
- The University of Tokyo (JP)
- Karolinska Institutet (SE)
- Technical University of Munich (DE)
- University of Bern (CH)
- University of Michigan (US)
- University of South Australia (AU)
- Medical University of South Carolina (US)
- Howard Hughes Medical Institute (US)
- Scripps Research Institute (US)
- St. John's University (US)
- University of Graz (AT)
- Istituto Superiore di Sanità (IT)
- VIB-KU Leuven Center for Cancer Biology (BE)
- Trinity College Dublin (IE)
- University of Geneva (CH)
- Amsterdam UMC Location University of Amsterdam (NL)
- Institute of Cancer Research (GB)
- Stony Brook University (US)
- University of Washington (US)
- Institute of Molecular Biotechnology (AT)
- University of Ferrara (IT)
- Royal College of Surgeons in Ireland (IE)
- La Trobe University (AU)
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- University of Virginia (US)
- University of Padua (IT)
- University of Lisbon (PT)
- University of Cambridge (GB)
- University of Würzburg (DE)
- Soochow University (CN)
- Cancer Research UK Scotland Institute (GB)
- University of Crete (GR)
- Osaka International Cancer Institute (JP)
- Innsbruck Medical University (AT)
- Spanish National Cancer Research Centre (ES)
- Rutgers, The State University of New Jersey (US)
- University of Minnesota (US)
- Harvard University (US)
- Queens College, CUNY (US)
- Lomonosov Moscow State University (RU)
- Corresponding author
- Galluzzi, L
- Kroemer, G
- ORCID
- Galluzzi, L
- Vitale, I
- Aaronson, S A
- Abrams, J M
- Adam, D
- Alnemri, E S
- Altucci, L
- Andrews, D
- Baehrecke, E H
- Bazan, N G
- Bertrand, M J
- Bianchi, K
- Blomgren, K
- Borner, C
- Bredesen, D E
- Brenner, C
- Campanella, M
- Candi, E
- Cecconi, F
- Chan, F K
- Chandel, N S
- Cheng, E H
- Chipuk, J E
- Cidlowski, J A
- Ciechanover, A
- Dawson, T M
- Dawson, V L
- Dixit, V M
- Dynlacht, B D
- Fimia, G M
- Flavell, R A
- Fulda, S
- Garrido, C
- Green, D R
- Gronemeyer, H
- Hardwick, J M
- Ichijo, H
- Joseph, B
- Jost, P J
- Kaufmann, T
- Kepp, O
- Klionsky, D J
- Knight, R A
- Kumar, S
- Lemasters, J J
- Levine, B
- Linkermann, A
- Lipton, S A
- Lockshin, R A
- Lugli, E
- Madeo, F
- Malorni, W
- Marine, J-C
- Martin, S J
- Martinou, J-C
- Medema, J P
- Meier, P
- Melino, S
- Mizushima, N
- Moll, U
- Oberst, A
- Panaretakis, T
- Penninger, J M
- Peter, M E
- Pinton, P
- Prehn, J H
- Puthalakath, H
- Rabinovich, G A
- Ravichandran, K S
- Rizzuto, R
- Rodrigues, C M
- Rubinsztein, D C
- Rudel, T
- Shi, Y
- Stockwell, B R
- Szabadkai, G
- Tait, S W
- Tang, H L
- Vandenabeele, P
- Villunger, A
- Wagner, E F
- Walczak, H
- White, E
- Yuan, J
- Zhivotovsky, B
- Melino, G
- Kroemer, G
- Venue
- Cell Death & Differentiation
- Published
- 2014-09-19
- Volume
- 22
- Issue
- 1
- Pages
- 58-73
- ISSN
- 1350-9047 (ISSN-L)
- 1476-5403
- PMC
- PMC4262782
- OpenAlex
- W1997128330
- Cited by
- 1,002
- References
- 342
- Citations by year
- 2026: 34 · 2025: 71 · 2024: 56 · 2023: 80 · 2022: 68 · 2021: 70 · 2020: 74 · 2019: 77 · 2018: 104 · 2017: 118 · 2016: 134 · 2015: 105 · 2014: 11
- FWCI
- 11.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Death and Differentiation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, other-oa)
- PubliCatt (Università Cattolica del Sacro Cuore) (submittedVersion, cc-by)
- PubliCatt (Università Cattolica del Sacro Cuore) (submittedVersion, other-oa)
- RVC Research Online (Royal Veterinary College) (submittedVersion, cc-by)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- HAL (submittedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion, other-oa)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- BORIS (University Library Bern) (submittedVersion, cc-by)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
- Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- CONICET Digital (CONICET) (submittedVersion, cc-by)
- Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion, cc-by)
- UniSA Research Outputs Repository (University of South Australia) (submittedVersion, cc-by)
- Open Access CRIS of the University of Bern
- Funders
- Wellcome Trust (100140, 095317)
- Medical Research Council (MR/M019217/1)
- Biotechnology and Biological Sciences Research Council (BB/I013695/1)
- Japan Society for the Promotion of Science (25221302)
- National Institute on Alcohol Abuse and Alcoholism (R01AA021191)
- National Institute on Drug Abuse (P50DA000266)
- National Cancer Institute (R01CA169291, R01CA097061, R01CA170702, P01CA080058, R01CA130893, R01CA163591)
- National Institute of General Medical Sciences (R01GM096208, R01GM072124, R01GM053396)
- National Institute of Allergy and Infectious Diseases (R01AI044828)
- National Institute of Diabetes and Digestive and Kidney Diseases (R56DK037034, R01DK073336)
- National Institute of Neurological Disorders and Stroke (R01NS086890, P50NS038377)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD066319, P01HD029587)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Social Sciences › Anthropology › Death, Funerary Practices, and Mourning
- Keywords
- regulated cell death, apoptosis, caspases, cytoprotection, cell death mechanisms
- MeSH terms
- Animals, Humans, Terminology as Topic, Signal Transduction, Apoptosis
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