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Cell Death Differ. 2015 Jan;22(1):58-73. doi: 10.1038/cdd.2014.137. Epub 2014 Sep 19.

Essential versus accessory aspects of cell death: recommendations of the NCCD 2015.

Galluzzi L1, Bravo-San Pedro JM2, Vitale I3, Aaronson SA4, Abrams JM5, Adam D6, Alnemri ES7, Altucci L8, Andrews D9, Annicchiarico-Petruzzelli M10, Baehrecke EH11, Bazan NG12, Bertrand MJ13, Bianchi K14, Blagosklonny MV15, Blomgren K16, Borner C17, Bredesen DE18, Brenner C19, Campanella M20, Candi E21, Cecconi F22, Chan FK23, Chandel NS24, Cheng EH25, Chipuk JE4, Cidlowski JA26, Ciechanover A27, Dawson TM28, Dawson VL28, De Laurenzi V29, De Maria R3, Debatin KM30, Di Daniele N31, Dixit VM32, Dynlacht BD33, El-Deiry WS34, Fimia GM35, Flavell RA36, Fulda S37, Garrido C38, Gougeon ML39, Green DR40, Gronemeyer H41, Hajnoczky G42, Hardwick JM43, Hengartner MO44, Ichijo H45, Joseph B46, Jost PJ47, Kaufmann T48, Kepp O49, Klionsky DJ50, Knight RA51, Kumar S52, Lemasters JJ53, Levine B54, Linkermann A55, Lipton SA56, Lockshin RA57, López-Otín C58, Lugli E59, Madeo F60, Malorni W61, Marine JC62, Martin SJ63, Martinou JC64, Medema JP65, Meier P66, Melino S67, Mizushima N68, Moll U69, Muñoz-Pinedo C70, Nuñez G71, Oberst A72, Panaretakis T46, Penninger JM73, Peter ME74, Piacentini M75, Pinton P76, Prehn JH77, Puthalakath H78, Rabinovich GA79, Ravichandran KS80, Rizzuto R81, Rodrigues CM82, Rubinsztein DC83, Rudel T84, Shi Y85, Simon HU86, Stockwell BR87, Szabadkai G88, Tait SW89, Tang HL43, Tavernarakis N90, Tsujimoto Y91, Vanden Berghe T13, Vandenabeele P92, Villunger A93, Wagner EF94, Walczak H95, White E96, Wood WG97, Yuan J98, Zakeri Z99, Zhivotovsky B100, Melino G101, Kroemer G102.

Author information

1
1] Gustave Roussy Cancer Center, Villejuif, France [2] Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France [3] Université Paris Descartes/Paris V, Sorbonne Paris Cité, Paris, France.
2
1] Gustave Roussy Cancer Center, Villejuif, France [2] Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France [3] INSERM, U1138, Gustave Roussy, Paris, France.
3
Regina Elena National Cancer Institute, Rome, Italy.
4
Department of Oncological Sciences, The Tisch Cancer Institute, Ichan School of Medicine at Mount Sinai, New York, NY, USA.
5
Department of Cell Biology, UT Southwestern Medical Center, Dallas, TX, USA.
6
Institute of Immunology, Christian-Albrechts University, Kiel, Germany.
7
Department of Biochemistry and Molecular Biology, Thomas Jefferson University, Philadelphia, PA, USA.
8
Dipartimento di Biochimica, Biofisica e Patologia Generale, Seconda Università degli Studi di Napoli, Napoli, Italy.
9
Department of Biochemistry and Medical Biophysics, University of Toronto, Toronto, ON, Canada.
10
Biochemistry Laboratory, Istituto Dermopatico dell'Immacolata - Istituto Ricovero Cura Carattere Scientifico (IDI-IRCCS), Rome, Italy.
11
Department of Cancer Biology, University of Massachusetts Medical School, Worcester, MA, USA.
12
Neuroscience Center of Excellence, School of Medicine, New Orleans, LA, USA.
13
1] VIB Inflammation Research Center, Ghent, Belgium [2] Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.
14
1] Barts Cancer Institute, Cancer Research UK Centre of Excellence, London, UK [2] Queen Mary University of London, John Vane Science Centre, London, UK.
15
Department of Cell Stress Biology, Roswell Park Cancer Institute, Buffalo, NY, USA.
16
Karolinska University Hospital, Karolinska Institute, Stockholm, Sweden.
17
Institute of Molecular Medicine and Spemann Graduate School of Biology and Medicine, Albert-Ludwigs University, Freiburg, Germany.
18
1] Buck Institute for Research on Aging, Novato, CA, USA [2] Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA.
19
1] INSERM, UMRS769, Châtenay Malabry, France [2] LabEx LERMIT, Châtenay Malabry, France [3] Université Paris Sud/Paris XI, Orsay, France.
20
Department of Comparative Biomedical Sciences and Consortium for Mitochondrial Research, University College London (UCL), London, UK.
21
Department of Experimental Medicine and Surgery, University of Rome Tor Vergata, Rome, Italy.
22
1] Laboratory of Molecular Neuroembryology, IRCCS Fondazione Santa Lucia, Rome, Italy [2] Department of Biology, University of Rome Tor Vergata; Rome, Italy [3] Unit of Cell Stress and Survival, Danish Cancer Society Research Center, Copenhagen, Denmark.
23
Department of Pathology, University of Massachusetts Medical School, Worcester, MA, USA.
24
Department of Medicine, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
25
Human Oncology and Pathogenesis Program and Department of Pathology, Memorial Sloan Kettering Cancer Center (MSKCC), New York, NY, USA.
26
Laboratory of Signal Transduction, National Institute of Environmental Health Sciences (NIEHS), National Institute of Health (NIH), North Carolina, NC, USA.
27
Tumor and Vascular Biology Research Center, The Rappaport Faculty of Medicine and Research Institute, Technion Israel Institute of Technology, Haifa, Israel.
28
1] Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering (ICE), Departments of Neurology, Pharmacology and Molecular Sciences, Solomon H Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD, USA [2] Adrienne Helis Malvin Medical Research Foundation, New Orleans, LA, USA.
29
Department of Experimental and Clinical Sciences, Gabriele d'Annunzio University, Chieti, Italy.
30
Department of Pediatrics and Adolescent Medicine, Ulm University Medical Center, Ulm, Germany.
31
Department of Systems Medicine, University of Rome Tor Vergata, Rome, Italy.
32
Department of Physiological Chemistry, Genentech, South San Francisco, CA, USA.
33
Department of Pathology and Cancer Institute, Smilow Research Center, New York University School of Medicine, New York, NY, USA.
34
Laboratory of Translational Oncology and Experimental Cancer Therapeutics, Department of Medicine (Hematology/Oncology), Penn State Hershey Cancer Institute, Penn State College of Medicine, Hershey, PA, USA.
35
1] Department of Biological and Environmental Sciences and Technologies (DiSTeBA), University of Salento, Lecce, Italy [2] Department of Epidemiology and Preclinical Research, National Institute for Infectious Diseases Lazzaro Spallanzani, Istituto Ricovero Cura Carattere Scientifico (IRCCS), Rome, Italy.
36
Department of Immunobiology, Yale School of Medicine, New Haven, CT, USA.
37
Institute for Experimental Cancer Research in Pediatrics, Goethe University, Frankfurt, Germany.
38
1] INSERM, U866, Dijon, France [2] Faculty of Medicine, University of Burgundy, Dijon, France.
39
Antiviral Immunity, Biotherapy and Vaccine Unit, Infection and Epidemiology Department, Institut Pasteur, Paris, France.
40
Department of Immunology, St Jude's Children's Research Hospital, Memphis, TN, USA.
41
Department of Functional Genomics and Cancer, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France.
42
Department of Pathology, Anatomy and Cell Biology, Thomas Jefferson University, Philadelphia, PA, USA.
43
W Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins University, Baltimore, MD, USA.
44
Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland.
45
Laboratory of Cell Signaling, Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan.
46
Department of Oncology-Pathology, Cancer Centrum Karolinska (CCK), Karolinska Institute, Stockholm, Sweden.
47
Medical Department for Hematology, Technical University of Munich, Munich, Germany.
48
Institute of Pharmacology, Medical Faculty, University of Bern, Bern, Switzerland.
49
1] Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France [2] INSERM, U1138, Gustave Roussy, Paris, France [3] Metabolomics and Cell Biology Platforms, Gustave Roussy Cancer Center, Villejuif, France.
50
Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA.
51
1] Medical Molecular Biology Unit, Institute of Child Health, University College London (UCL), London, UK [2] Medical Research Council Toxicology Unit, Leicester, UK.
52
1] Centre for Cancer Biology, University of South Australia, Adelaide, SA, Australia [2] School of Medicine and School of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA, Australia.
53
Departments of Drug Discovery and Biomedical Sciences and Biochemistry and Molecular Biology, Medical University of South Carolina, Charleston, SC, USA.
54
1] Center for Autophagy Research, University of Texas, Southwestern Medical Center, Dallas, TX, USA [2] Howard Hughes Medical Institute (HHMI), Chevy Chase, MD, USA.
55
Division of Nephrology and Hypertension, Christian-Albrechts University, Kiel, Germany.
56
1] The Scripps Research Institute, La Jolla, CA, USA [2] Sanford-Burnham Center for Neuroscience, Aging, and Stem Cell Research, La Jolla, CA, USA [3] Salk Institute for Biological Studies, La Jolla, CA, USA [4] University of California, San Diego (UCSD), San Diego, CA, USA.
57
Department of Biological Sciences, St. John's University, Queens, NY, USA.
58
Department of Biochemistry and Molecular Biology, Faculty of Medecine, Instituto Universitario de Oncología (IUOPA), University of Oviedo, Oviedo, Spain.
59
Unit of Clinical and Experimental Immunology, Humanitas Clinical and Research Center, Milan, Italy.
60
Institute of Molecular Biosciences, University of Graz, Graz, Austria.
61
1] Department of Therapeutic Research and Medicine Evaluation, Istituto Superiore di Sanita (ISS), Roma, Italy [2] San Raffaele Institute, Sulmona, Italy.
62
1] Laboratory for Molecular Cancer Biology, Center for the Biology of Disease, Leuven, Belgium [2] Laboratory for Molecular Cancer Biology, Center of Human Genetics, Leuven, Belgium.
63
Department of Genetics, The Smurfit Institute, Trinity College, Dublin, Ireland.
64
Department of Cell Biology, University of Geneva, Geneva, Switzerland.
65
Laboratory for Experiments Oncology and Radiobiology (LEXOR), Academic Medical Center (AMC), Amsterdam, The Netherlands.
66
Institute of Cancer Research, The Breakthrough Toby Robins Breast Cancer Research Centre, London, UK.
67
Department of Chemical Sciences and Technologies, University of Rome Tor Vergata, Rome, Italy.
68
Graduate School and Faculty of Medicine, University of Tokyo, Tokyo, Japan.
69
Department of Pathology, Stony Brook University, Stony Brook, NY, USA.
70
Cell Death Regulation Group, Bellvitge Biomedical Research Institute (IDIBELL), Barcelona, Spain.
71
Department of Pathology and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, MI, USA.
72
Department of Immunology, University of Washington, Seattle, WA, USA.
73
Institute of Molecular Biotechnology of the Austrian Academy of Sciences, Vienna, Austria.
74
Department of Hematology/Oncology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
75
1] Department of Biology, University of Rome Tor Vergata; Rome, Italy [2] Department of Epidemiology and Preclinical Research, National Institute for Infectious Diseases Lazzaro Spallanzani, Istituto Ricovero Cura Carattere Scientifico (IRCCS), Rome, Italy.
76
Department of Morphology, Surgery and Experimental Medicine, Section of Pathology, Oncology and Experimental Biology and LTTA Center, University of Ferrara, Ferrara, Italy.
77
Department of Physiology and Medical Physics, Royal College of Surgeons, Dublin, Ireland.
78
Department of Biochemistry, La Trobe Institute of Molecular Science, La Trobe University, Melbourne, Australia.
79
Laboratory of Immunopathology, Instituto de Biología y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.
80
Department of Microbiology, Immunology and Cancer Biology, University of Virginia, Charlottesville, VA, USA.
81
Department Biomedical Sciences, University of Padova, Padova, Italy.
82
Research Institute for Medicines, Faculty of Pharmacy, University of Lisbon, Lisbon, Portugal.
83
Department of Medical Genetics, Cambridge Institute for Medical Research, University of Cambridge School of Clinical Medicine, Cambridge, UK.
84
Department of Microbiology, University of Würzburg; Würzburg, Germany.
85
Soochow Institute for Translational Medicine, Soochow University, Suzhou, China.
86
Institute of Pharmacology, University of Bern, Bern, Switzerland.
87
1] Howard Hughes Medical Institute (HHMI), Chevy Chase, MD, USA [2] Departments of Biological Sciences and Chemistry, Columbia University, New York, NY, USA.
88
1] Department Biomedical Sciences, University of Padova, Padova, Italy [2] Department of Cell and Developmental Biology and Consortium for Mitochondrial Research, University College London (UCL), London, UK.
89
1] Cancer Research UK Beatson Institute, Glasgow, UK [2] Institute of Cancer Sciences, University of Glasgow, Glasgow, UK.
90
1] Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece [2] Department of Basic Sciences, Faculty of Medicine, University of Crete, Heraklion, Crete, Greece.
91
Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka, Japan.
92
1] VIB Inflammation Research Center, Ghent, Belgium [2] Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium [3] Methusalem Program, Ghent University, Ghent, Belgium.
93
Division of Developmental Immunology, Biocenter, Medical University Innsbruck, Innsbruck, Austria.
94
Cancer Cell Biology Program, Spanish National Cancer Research Centre (CNIO), Madrid, Spain.
95
Centre for Cell Death, Cancer and Inflammation (CCCI), UCL Cancer Institute, University College London (UCL), London, UK.
96
Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA.
97
1] Department of Pharmacology, University of Minnesota School of Medicine, Minneapolis, MN, USA [2] Geriatric Research, Education and Clinical Center, VA Medical Center, Minneapolis, MN, USA.
98
Department of Cell Biology, Harvard Medical School, Boston, MA, USA.
99
1] Department of Biology, Queens College, Queens, NY, USA [2] Graduate Center, City University of New York (CUNY), Queens, NY, USA.
100
1] Division of Toxicology, Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden [2] Faculty of Fundamental Medicine, Lomonosov Moscow State University, Moscow, Russia.
101
1] Department of Experimental Medicine and Surgery, University of Rome Tor Vergata, Rome, Italy [2] Medical Research Council Toxicology Unit, Leicester, UK.
102
1] Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France [2] Université Paris Descartes/Paris V, Sorbonne Paris Cité, Paris, France [3] INSERM, U1138, Gustave Roussy, Paris, France [4] Metabolomics and Cell Biology Platforms, Gustave Roussy Cancer Center, Villejuif, France [5] Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP, Paris, France.

Abstract

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.

PMID:
25236395
PMCID:
PMC4262782
DOI:
10.1038/cdd.2014.137
[Indexed for MEDLINE]
Free PMC Article
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