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      Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018

      , 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 12 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 4 , 5 , 33 , 34 , 16 , 21 , 35 , 4 , 36 , 37 , 38 , 39 , 40 , 6 , 41 , 42 , 43 , 44 , 2 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 49 , 50 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 , 9 , 75 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 42 , 83 , 84 , 85 , 86 , 87 , 88 , 89 , 90 , 91 , 92 , 93 , 94 , 95 , 96 , 97 , 98 , 99 , 100 , 101 , 102 , 103 , 104 , 105 , 106 , 107 , 108 , 109 , 110 , 111 , 3 , 112 , 113 , 114 , 115 , 116 , 117 , 79 , 80 , 81 , 118 , 119 , 120 , 121 , 12 , 122 , 123 , 124 , 125 , 126 , 127 , 128 , 129 , 130 , 131 , 132 , 133 , 134 , 135 , 136 , 137 , 138 , 139 , 140 , 12 , 35 , 141 , 12 , 142 , 4 , 5 , 143 , 144 , 145 , 146 , 147 , 148 , 149 , 150 , 151 , 152 , 153 , 154 , 155 , 156 , 157 , 158 , 159 , 160 , 161 , 162 , 163 , 164 , 165 , 166 , 167 , 168 , 169 , 65 , 170 , 171 , 172 , 173 , 174 , 175 , 176 , 177 , 178 , 179 , 180 , 181 , 182 , 4 , 69 , 60 , 183 , 184 , 185 , 186 , 187 , 188 , 189 , 190 , 191 , 192 , 193 , 194 , 83 , 195 , 196 , 197 , 198 , 199 , 200 , 201 , 47 , 202 , 111 , 55 , 203 , 204 , 205 , 46 , 191 , 206 , 207 , 83 , 208 , 209 , 210 , 211 , 212 , 213 , 214 , 215 , 216 , 217 , 218 , 22 , 23 , 22 , 23 , 219 , 220 , 221 , 222 , 223 , 207 , 224 , 225 , 226 , 227 , 228 , 229 , 230 , 93 , 231 , 232 , 100 , 233 , 112 , 234 , 235 , 236 , 12 , 21 , , 3 , 26 , 113 , 114 , 115 , 116 , 237

      Cell Death and Differentiation

      Nature Publishing Group UK

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Over the past decade, the Nomenclature Committee on Cell Death (NCCD) has formulated guidelines for the definition and interpretation of cell death from morphological, biochemical, and functional perspectives. Since the field continues to expand and novel mechanisms that orchestrate multiple cell death pathways are unveiled, we propose an updated classification of cell death subroutines focusing on mechanistic and essential (as opposed to correlative and dispensable) aspects of the process. As we provide molecularly oriented definitions of terms including intrinsic apoptosis, extrinsic apoptosis, mitochondrial permeability transition (MPT)-driven necrosis, necroptosis, ferroptosis, pyroptosis, parthanatos, entotic cell death, NETotic cell death, lysosome-dependent cell death, autophagy-dependent cell death, immunogenic cell death, cellular senescence, and mitotic catastrophe, we discuss the utility of neologisms that refer to highly specialized instances of these processes. The mission of the NCCD is to provide a widely accepted nomenclature on cell death in support of the continued development of the field.

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          Most cited references 1,084

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          The hallmarks of aging.

          Aging is characterized by a progressive loss of physiological integrity, leading to impaired function and increased vulnerability to death. This deterioration is the primary risk factor for major human pathologies, including cancer, diabetes, cardiovascular disorders, and neurodegenerative diseases. Aging research has experienced an unprecedented advance over recent years, particularly with the discovery that the rate of aging is controlled, at least to some extent, by genetic pathways and biochemical processes conserved in evolution. This Review enumerates nine tentative hallmarks that represent common denominators of aging in different organisms, with special emphasis on mammalian aging. These hallmarks are: genomic instability, telomere attrition, epigenetic alterations, loss of proteostasis, deregulated nutrient sensing, mitochondrial dysfunction, cellular senescence, stem cell exhaustion, and altered intercellular communication. A major challenge is to dissect the interconnectedness between the candidate hallmarks and their relative contributions to aging, with the final goal of identifying pharmaceutical targets to improve human health during aging, with minimal side effects. Copyright © 2013 Elsevier Inc. All rights reserved.
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            Neutrophil extracellular traps kill bacteria.

            Neutrophils engulf and kill bacteria when their antimicrobial granules fuse with the phagosome. Here, we describe that, upon activation, neutrophils release granule proteins and chromatin that together form extracellular fibers that bind Gram-positive and -negative bacteria. These neutrophil extracellular traps (NETs) degrade virulence factors and kill bacteria. NETs are abundant in vivo in experimental dysentery and spontaneous human appendicitis, two examples of acute inflammation. NETs appear to be a form of innate response that binds microorganisms, prevents them from spreading, and ensures a high local concentration of antimicrobial agents to degrade virulence factors and kill bacteria.
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              • Article: not found

              Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).

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                Author and article information

                Contributors
                +1(212)746-2231 , deadoc@vodafone.it
                +33(1)4427-7667 , kroemer@orange.fr
                Journal
                Cell Death Differ
                Cell Death Differ
                Cell Death and Differentiation
                Nature Publishing Group UK (London )
                1350-9047
                1476-5403
                23 January 2018
                23 January 2018
                March 2018
                : 25
                : 3
                : 486-541
                Affiliations
                [1 ]ISNI 000000041936877X, GRID grid.5386.8, Department of Radiation Oncology, Weill Cornell Medical College, ; New York, NY USA
                [2 ]Sandra and Edward Meyer Cancer Center, New York, NY USA
                [3 ]Paris Descartes/Paris V University, Paris, France
                [4 ]ISNI 0000 0001 2300 0941, GRID grid.6530.0, Department of Biology, University of Rome “Tor Vergata”, ; Rome, Italy
                [5 ]ISNI 0000 0004 1760 5276, GRID grid.417520.5, Unit of Cellular Networks and Molecular Therapeutic Targets, Department of Research, Advanced Diagnostics and Technological Innovation, Regina Elena National Cancer Institute, ; Rome, Italy
                [6 ]ISNI 0000 0001 0670 2351, GRID grid.59734.3c, Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, ; New York, NY USA
                [7 ]ISNI 0000 0000 9482 7121, GRID grid.267313.2, Department of Cell Biology, University of Texas Southwestern Medical Center, ; Dallas, TX USA
                [8 ]ISNI 0000 0001 2153 9986, GRID grid.9764.c, Institute of Immunology, Kiel University, ; Kiel, Germany
                [9 ]ISNI 0000 0001 0668 7884, GRID grid.5596.f, Cell Death Research & Therapy (CDRT) Lab, Department of Cellular & Molecular Medicine, KU Leuven, ; Leuven, Belgium
                [10 ]ISNI 0000 0001 2166 5843, GRID grid.265008.9, Department of Biochemistry and Molecular Biology, Kimmel Cancer Center, Thomas Jefferson University, ; Philadelphia, PA USA
                [11 ]Department of Biochemistry, Biophysics and General Pathology, University of Campania “Luigi Vanvitelli”, Napoli, Italy
                [12 ]ISNI 0000 0004 1936 8411, GRID grid.9918.9, Medical Research Council (MRC) Toxicology Unit, Leicester University, ; Leicester, UK
                [13 ]ISNI 0000 0001 2157 2938, GRID grid.17063.33, Biological Sciences, Sunnybrook Research Institute, ; Toronto, Canada
                [14 ]ISNI 0000 0001 2157 2938, GRID grid.17063.33, Department of Biochemistry, University of Toronto, ; Toronto, Canada
                [15 ]ISNI 0000 0001 2157 2938, GRID grid.17063.33, Department of Medical Biophysics, University of Toronto, ; Toronto, Canada
                [16 ]ISNI 0000 0004 1758 0179, GRID grid.419457.a, Biochemistry Laboratory, Dermopatic Institute of Immaculate (IDI) IRCCS, ; Rome, Italy
                [17 ]ISNI 0000 0004 0604 7563, GRID grid.13992.30, Department of Molecular Genetics, Weizmann Institute of Science, ; Rehovot, Israel
                [18 ]ISNI 0000 0001 0742 0364, GRID grid.168645.8, Department of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, ; Worcester, MA USA
                [19 ]ISNI 0000 0000 9629 3848, GRID grid.418947.7, Institute of Cytology, Russian Academy of Sciences, ; Saint-Petersburg, Russia
                [20 ]ISNI 0000 0000 8954 1233, GRID grid.279863.1, Neuroscience Center of Excellence, Louisiana State University School of Medicine, ; New Orleans, LA USA
                [21 ]ISNI 0000 0001 2300 0941, GRID grid.6530.0, Department of Experimental Medicine and Surgery, University of Rome “Tor Vergata”, ; Rome, Italy
                [22 ]ISNI 0000000104788040, GRID grid.11486.3a, VIB Center for Inflammation Research (IRC), ; Ghent, Belgium
                [23 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Biomedical Molecular Biology, Ghent University, ; Ghent, Belgium
                [24 ]ISNI 0000 0001 2171 1133, GRID grid.4868.2, Centre for Molecular Oncology, Barts Cancer Institute, Queen Mary University of London, ; London, UK
                [25 ]ISNI 0000 0001 2181 8635, GRID grid.240614.5, Cell Stress Biology, Roswell Park Cancer Institute, ; Buffalo, NY USA
                [26 ]ISNI 0000 0004 1937 0626, GRID grid.4714.6, Department of Women’s and Children’s Health, Karolinska Institute, ; Stockholm, Sweden
                [27 ]ISNI 0000 0000 9241 5705, GRID grid.24381.3c, Department of Pediatric Oncology, Karolinska University Hospital, ; Stockholm, Sweden
                [28 ]GRID grid.5963.9, Institute of Molecular Medicine and Cell Research, Albert Ludwigs University, ; Freiburg, Germany
                [29 ]GRID grid.5963.9, Spemann Graduate School of Biology and Medicine (SGBM), Faculty of Medicine, Albert Ludwigs University, ; Freiburg, Germany
                [30 ]ISNI 0000 0001 2183 4846, GRID grid.4711.3, Department of Cellular and Molecular Biology, Center for Biological Investigation (CIB), Spanish National Research Council (CSIC), ; Madrid, Spain
                [31 ]INSERM U1180, Châtenay Malabry, France
                [32 ]ISNI 0000 0001 2171 2558, GRID grid.5842.b, University of Paris Sud/Paris Saclay, ; Orsay, France
                [33 ]ISNI 0000000121901201, GRID grid.83440.3b, Department of Comparative Biomedical Sciences, The Royal Veterinary College, University of London, ; London, UK
                [34 ]ISNI 0000000121901201, GRID grid.83440.3b, University College London Consortium for Mitochondrial Research, ; London, UK
                [35 ]ISNI 0000000121539003, GRID grid.5110.5, Department Institute of Molecular Biosciences, NAWI Graz, University of Graz, ; Graz, Austria
                [36 ]ISNI 0000 0001 2175 6024, GRID grid.417390.8, Unit of Cell Stress and Survival, Danish Cancer Society Research Center, ; Copenhagen, Denmark
                [37 ]ISNI 0000 0001 0727 6809, GRID grid.414125.7, Department of Pediatric Hematology and Oncology, Bambino Gesù Children’s Hospital IRCCS, ; Rome, Italy
                [38 ]ISNI 0000 0001 0742 0364, GRID grid.168645.8, Department of Pathology, University of Massachusetts Medical School, ; Worcester, MA USA
                [39 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Medicine, Division of Pulmonary and Critical Care Medicine, Northwestern University Feinberg School of Medicine, ; Chicago, IL USA
                [40 ]ISNI 0000 0001 2171 9952, GRID grid.51462.34, Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, ; New York, NY USA
                [41 ]Signal Transduction Laboratory, National Institutes of Environmental Health Sciences, NIH, Research Triangle Park, NC USA
                [42 ]ISNI 0000000121102151, GRID grid.6451.6, Technion Integrated Cancer Center (TICC), The Ruth and Bruce Rappaport Faculty of Medicine and Research Institute, Technion-Israel Institute of Technology, ; Haifa, Israel
                [43 ]ISNI 0000 0004 1936 8470, GRID grid.10025.36, Department of Molecular and Clinical Cancer Medicine, Institute of Translational Medicine, University of Liverpool, ; Liverpool, UK
                [44 ]ISNI 0000 0004 0483 2525, GRID grid.4567.0, Institute of Developmental Genetics, Helmholtz Center Munich, German Research Center for Environmental Health (GmbH), ; Munich, Germany
                [45 ]ISNI 000000041936877X, GRID grid.5386.8, Department of Obstetrics and Gynecology, Weill Cornell Medical College, ; New York, NY USA
                [46 ]GRID grid.1042.7, The Walter and Eliza Hall Institute of Medical Research, Melbourne, ; Victoria, Australia
                [47 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Department of Medical Biology, The University of Melbourne, Melbourne, ; Victoria, Australia
                [48 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Cancer Research UK and Medical Research Council Institute for Radiation Oncology, Department of Oncology, University of Oxford, Old Road Campus Research Building, ; Oxford, UK
                [49 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering, Johns Hopkins University School of Medicine, ; Baltimore, MD USA
                [50 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Department of Neurology, Johns Hopkins University School of Medicine, ; Baltimore, MD USA
                [51 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Department of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, ; Baltimore, MD USA
                [52 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, ; Baltimore, MD USA
                [53 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Department of Physiology, Johns Hopkins University School of Medicine, ; Baltimore, MD USA
                [54 ]Department of Medical, Oral and Biotechnological Sciences, CeSI-MetUniversity of Chieti-Pescara “G. d’Annunzio”, Chieti, Italy
                [55 ]Institute of General Pathology, Catholic University “Sacro Cuore”, Rome, Italy
                [56 ]GRID grid.410712.1, Department of Pediatrics and Adolescent Medicine, Ulm University Medical Center, ; Ulm, Germany
                [57 ]ISNI 0000 0000 9482 7121, GRID grid.267313.2, Children’s Medical Center Research Institute, University of Texas Southwestern Medical Center, ; Dallas, TX USA
                [58 ]ISNI 0000 0001 1034 1720, GRID grid.410711.2, Department of Cell Biology and Physiology, Neuroscience Center, University of North Carolina, ; Chapel Hill, NC USA
                [59 ]ISNI 0000 0001 2300 0941, GRID grid.6530.0, Hypertension and Nephrology Unit, Department of Systems Medicine, University of Rome “Tor Vergata”, ; Rome, Italy
                [60 ]ISNI 0000 0004 1757 2064, GRID grid.8484.0, Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, ; Ferrara, Italy
                [61 ]ISNI 0000 0004 0534 4718, GRID grid.418158.1, Department of Physiological Chemistry, Genentech, ; South San Francisco, CA USA
                [62 ]ISNI 0000000419368956, GRID grid.168010.e, Department of Biology, Stanford University, ; Stanford, CA USA
                [63 ]GRID grid.486749.0, Baylor Scott & White Research Institute, Baylor College of Medicine, ; Dallas, TX USA
                [64 ]ISNI 0000 0004 1936 8753, GRID grid.137628.9, Department of Pathology, New York University School of Medicine, ; New York, NY USA
                [65 ]ISNI 0000 0004 1936 8753, GRID grid.137628.9, Laura and Isaac Perlmutter Cancer Center, New York University School of Medicine, ; New York, NY USA
                [66 ]ISNI 0000 0004 0456 6466, GRID grid.412530.1, Laboratory of Translational Oncology and Experimental Cancer Therapeutics, Department of Hematology/Oncology, Fox Chase Cancer Center, ; Philadelphia, PA USA
                [67 ]ISNI 0000 0004 0456 6466, GRID grid.412530.1, Molecular Therapeutics Program, Fox Chase Cancer Center, ; Philadelphia, PA USA
                [68 ]ISNI 0000 0001 2248 3398, GRID grid.264727.2, Center for Translational Medicine, Department of Pharmacology, Lewis Katz School of Medicine at Temple University School of Medicine, ; Philadelphia, PA USA
                [69 ]GRID grid.414603.4, National Institute for Infectious Diseases IRCCS “Lazzaro Spallanzani”, ; Rome, Italy
                [70 ]ISNI 0000 0001 2289 7785, GRID grid.9906.6, Department of Biological and Environmental Sciences and Technologies (DiSTeBA), University of Salento, ; Lecce, Italy
                [71 ]ISNI 0000 0004 1936 9721, GRID grid.7839.5, Institute for Experimental Cancer Research in Pediatrics, Goethe-University Frankfurt, ; Frankfurt, Germany
                [72 ]German Cancer Consortium (DKTK), Partner Site, Frankfurt, Germany
                [73 ]ISNI 0000 0004 0492 0584, GRID grid.7497.d, German Cancer Research Center (DKFZ), ; Heidelberg, Germany
                [74 ]ISNI 0000 0001 2190 1447, GRID grid.10392.39, Interfaculty Institute of Biochemistry, Tübingen University, ; Tübingen, Germany
                [75 ]INSERM U1231 “Lipides Nutrition Cancer”, Dijon, France
                [76 ]ISNI 0000 0001 2298 9313, GRID grid.5613.1, Faculty of Medicine, University of Burgundy France Comté, ; Dijon, France
                [77 ]ISNI 0000 0004 0641 1257, GRID grid.418037.9, Cancer Centre Georges François Leclerc, ; Dijon, France
                [78 ]ISNI 0000000121791997, GRID grid.251993.5, Department of Biochemistry, Albert Einstein College of Medicine, ; Bronx, NY USA
                [79 ]ISNI 0000000121791997, GRID grid.251993.5, Department of Medicine, Albert Einstein College of Medicine, ; Bronx, NY USA
                [80 ]ISNI 0000000121791997, GRID grid.251993.5, Albert Einstein Cancer Center, Albert Einstein College of Medicine, ; Bronx, NY USA
                [81 ]ISNI 0000000121791997, GRID grid.251993.5, Wilf Family Cardiovascular Research Institute, Albert Einstein College of Medicine, ; Bronx, NY USA
                [82 ]ISNI 0000 0001 2176 4817, GRID grid.5399.6, Immunology Center of Marseille-Luminy, Aix Marseille University, ; Marseille, France
                [83 ]ISNI 0000 0000 8821 5196, GRID grid.23636.32, Cancer Research UK Beatson Institute, ; Glasgow, UK
                [84 ]ISNI 0000 0001 0224 711X, GRID grid.240871.8, Department of Immunology, St Jude Children’s Research Hospital, ; Memphis, TN USA
                [85 ]ISNI 0000000419368729, GRID grid.21729.3f, Department of Pathology and Cell Biology, Columbia University College of Physicians and Surgeons, ; New York, NY USA
                [86 ]ISNI 0000 0004 0638 2716, GRID grid.420255.4, Team labeled “Ligue Contre le Cancer”, Department of Functional Genomics and Cancer, Institute of Genetics and Molecular and Cellular Biology (IGBMC), ; Illkirch, France
                [87 ]CNRS UMR 7104, Illkirch, France
                [88 ]INSERM U964, Illkirch, France
                [89 ]ISNI 0000 0001 2157 9291, GRID grid.11843.3f, University of Strasbourg, ; Illkirch, France
                [90 ]ISNI 0000 0004 0604 7563, GRID grid.13992.30, Department of Biological Regulation, Weizmann Institute of Science, ; Rehovot, Israel
                [91 ]ISNI 0000 0001 2166 5843, GRID grid.265008.9, MitoCare Center, Department of Pathology, Anatomy and Cell Biology, Thomas Jefferson University, ; Philadelphia, PA USA
                [92 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Johns Hopkins University Bloomberg School of Public Health, ; Baltimore, MD USA
                [93 ]ISNI 000000041936754X, GRID grid.38142.3c, Department of Cell Biology, Harvard Medical School, ; Boston, MA USA
                [94 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Institute of Molecular Life Sciences, University of Zurich, ; Zurich, Switzerland
                [95 ]ISNI 0000 0004 0385 4466, GRID grid.443909.3, Biomedical Neuroscience Institute, Faculty of Medicine, University of Chile, ; Santiago, Chile
                [96 ]Center for Geroscience, Brain Health and Metabolism, Santiago, Chile
                [97 ]ISNI 0000 0004 0385 4466, GRID grid.443909.3, Cellular and Molecular Biology Program, Institute of Biomedical Sciences, University of Chile, ; Santiago, Chile
                [98 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Laboratory of Cell Signaling, Graduate School of Pharmaceutical Sciences, The University of Tokyo, ; Tokyo, Japan
                [99 ]ISNI 0000 0001 2175 6024, GRID grid.417390.8, Cell Death and Metabolism Unit, Center for Autophagy, Recycling and Disease, Danish Cancer Society Research Center, ; Copenhagen, Denmark
                [100 ]ISNI 0000 0004 1937 0626, GRID grid.4714.6, Toxicology Unit, Institute of Environmental Medicine, Karolinska Institute, ; Stockholm, Sweden
                [101 ]ISNI 0000000123222966, GRID grid.6936.a, III Medical Department for Hematology and Oncology, Technical University Munich, ; Munich, Germany
                [102 ]Team 8 “Stress adaptation and tumor escape”, CRCINA-INSERM U1232, Nantes, France
                [103 ]GRID grid.4817.a, University of Nantes, ; Nantes, France
                [104 ]ISNI 0000 0001 2248 3363, GRID grid.7252.2, University of Angers, ; Angers, France
                [105 ]Institute of Cancer Research in Western France, Saint-Herblain, France
                [106 ]ISNI 0000 0001 0629 5880, GRID grid.267309.9, Department of Microbiology, Immunology and Molecular Genetics, University of Texas Health Science Center, ; San Antonio, TX USA
                [107 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Laboratory of Gene Regulation and Signal Transduction, University of California San Diego, ; La Jolla, CA USA
                [108 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Department of Pathology, University of California San Diego, ; La Jolla, CA USA
                [109 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Department of Pharmacology, University of California San Diego, ; La Jolla, CA USA
                [110 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Moores Cancer Center, University of California San Diego, ; La Jolla, CA USA
                [111 ]ISNI 0000 0001 0726 5157, GRID grid.5734.5, Institute of Pharmacology, University of Bern, ; Bern, Switzerland
                [112 ]Faculty of Medicine, Paris Sud/Paris XI University, Kremlin-Bicêtre, France
                [113 ]Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Campus, Villejuif, France
                [114 ]GRID grid.417925.c, Team 11 labeled “Ligue Nationale contre le Cancer”, Cordeliers Research Center, ; Paris, France
                [115 ]INSERM U1138, Paris, France
                [116 ]Pierre et Marie Curie/Paris VI University, Paris, France
                [117 ]ISNI 0000 0004 0604 7563, GRID grid.13992.30, Department of Molecular Genetics, Weizmann Institute of Science, ; Rehovot, Israel
                [118 ]ISNI 0000000121791997, GRID grid.251993.5, Department of Cell Biology, Albert Einstein College of Medicine, ; Bronx, NY USA
                [119 ]ISNI 0000000121791997, GRID grid.251993.5, Einstein-Mount Sinai Diabetes Research Center, Albert Einstein College of Medicine, ; Bronx, NY USA
                [120 ]ISNI 0000000086837370, GRID grid.214458.e, Department of Molecular, Cellular, and Developmental Biology, University of Michigan, ; Ann Arbor, MI USA
                [121 ]ISNI 0000000086837370, GRID grid.214458.e, Life Sciences Institute, University of Michigan, ; Ann Arbor, MI USA
                [122 ]ISNI 0000 0004 0450 082X, GRID grid.470344.0, Centre for Cancer Biology, University of South Australia and SA Pathology, Adelaide, ; South Australia, Australia
                [123 ]ISNI 000000041936754X, GRID grid.38142.3c, Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, ; Charlestown, MA USA
                [124 ]ISNI 0000 0001 2189 3475, GRID grid.259828.c, Center for Cell Death, Injury and Regeneration, Department of Drug Discovery & Biomedical Sciences, Medical University of South Carolina, ; Charleston, SC USA
                [125 ]ISNI 0000 0001 2189 3475, GRID grid.259828.c, Center for Cell Death, Injury and Regeneration, Department of Biochemistry & Molecular Biology, Medical University of South Carolina, ; Charleston, SC USA
                [126 ]ISNI 0000 0000 9482 7121, GRID grid.267313.2, Center for Autophagy Research, University of Texas Southwestern Medical Center, ; Dallas, TX USA
                [127 ]ISNI 0000 0000 9482 7121, GRID grid.267313.2, Department of Internal Medicine, University of Texas Southwestern Medical Center, ; Dallas, TX USA
                [128 ]ISNI 0000 0000 9482 7121, GRID grid.267313.2, Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, ; Dallas, TX USA
                [129 ]ISNI 0000 0001 1091 2917, GRID grid.412282.f, Division of Nephrology, University Hospital Carl Gustav Carus Dresden, ; Dresden, Germany
                [130 ]ISNI 0000000122199231, GRID grid.214007.0, Department of Molecular Medicine, The Scripps Research Institute, ; La Jolla, CA USA
                [131 ]ISNI 0000000122199231, GRID grid.214007.0, Department of Neuroscience, The Scripps Research Institute, ; La Jolla, CA USA
                [132 ]ISNI 0000000122199231, GRID grid.214007.0, Neuroscience Translational Center, The Scripps Research Institute, ; La Jolla, CA USA
                [133 ]ISNI 0000 0001 1954 7928, GRID grid.264091.8, Department of Biology, St. John’s University, ; Queens, NY USA
                [134 ]ISNI 0000 0001 2188 3760, GRID grid.262273.0, Queens College of the City University of New York, ; Queens, NY USA
                [135 ]ISNI 0000 0001 2164 6351, GRID grid.10863.3c, Departament of Biochemistry and Molecular Biology, Faculty of Medicine, University Institute of Oncology of Asturias (IUOPA), University of Oviedo, ; Oviedo, Spain
                [136 ]ISNI 0000 0001 2166 1519, GRID grid.134907.8, Howard Hughes Medical Institute, The Rockefeller University, ; New York, NY USA
                [137 ]ISNI 0000 0001 2171 9952, GRID grid.51462.34, Memorial Sloan Kettering Cancer Center, ; New York, NY USA
                [138 ]ISNI 0000 0000 8653 1507, GRID grid.412301.5, Division of Gastroenterology, Hepatology and Hepatobiliary Oncology, University Hospital RWTH Aachen, ; Aachen, Germany
                [139 ]ISNI 0000 0004 1756 8807, GRID grid.417728.f, Laboratory of Translational Immunology, Humanitas Clinical and Research Center, Rozzano, ; Milan, Italy
                [140 ]ISNI 0000 0004 1756 8807, GRID grid.417728.f, Humanitas Flow Cytometry Core, Humanitas Clinical and Research Center, Rozzano, ; Milan, Italy
                [141 ]GRID grid.452216.6, BioTechMed Graz, ; Graz, Austria
                [142 ]ISNI 0000 0000 9120 6856, GRID grid.416651.1, National Centre for Gender Medicine, Italian National Institute of Health (ISS), ; Rome, Italy
                [143 ]ISNI 0000000104788040, GRID grid.11486.3a, Laboratory for Molecular Cancer Biology, VIB Center for Cancer Biology, ; Leuven, Belgium
                [144 ]ISNI 0000 0001 0668 7884, GRID grid.5596.f, Laboratory for Molecular Cancer Biology, Department of Oncology, KU Leuven, ; Leuven, Belgium
                [145 ]ISNI 0000 0004 1936 9705, GRID grid.8217.c, Departments of Genetics, Trinity College, University of Dublin, ; Dublin 2, Ireland
                [146 ]ISNI 0000 0001 2322 4988, GRID grid.8591.5, Department of Cell Biology, Faculty of Sciences, University of Geneva, ; Geneva, Switzerland
                [147 ]Laboratory for Experimental Oncology and Radiobiology (LEXOR), Center for Experimental Molecular Medicine (CEMM), Academic Medical Center (AMC), University of Amsterdam, Amsterdam, The Netherlands
                [148 ]Cancer Genomics Center, Amsterdam, The Netherlands
                [149 ]ISNI 0000 0004 0384 0005, GRID grid.462282.8, Apoptosis, Cancer and Development laboratory, CRCL, ; Lyon, France
                [150 ]Team labeled “La Ligue contre le Cancer”, Lyon, France
                [151 ]LabEx DEVweCAN, Lyon, France
                [152 ]INSERM U1052, Lyon, France
                [153 ]CNRS UMR5286, Lyon, France
                [154 ]Department of Translational Research and Innovation, Léon Bérard Cancer Center, Lyon, France
                [155 ]ISNI 0000 0001 1271 4623, GRID grid.18886.3f, The Breast Cancer Now Toby Robins Research Centre, Institute of Cancer Research, Mary-Jean Mitchell Green Building, Chester Beatty Laboratories, ; London, UK
                [156 ]GRID grid.7841.a, Department of Chemical Sciences and Technologies, University of Rome, Tor Vergata, ; Rome, Italy
                [157 ]ISNI 0000 0001 1034 1720, GRID grid.410711.2, Department of Microbiology and Immunology, University of North Carolina, ; Chapel Hill, NC USA
                [158 ]ISNI 0000000122483208, GRID grid.10698.36, Lineberger Comprehensive Cancer Center, University of North Carolina, ; Chapel Hill, NC USA
                [159 ]ISNI 0000 0001 1034 1720, GRID grid.410711.2, Center for Gastrointestinal Biology and Disease, University of North Carolina, ; Chapel Hill, NC USA
                [160 ]ISNI 0000 0000 9025 8099, GRID grid.239573.9, Howard Hughes Medical Institute, Cincinnati Children’s Hospital Medical Center, ; Cincinnati, OH USA
                [161 ]ISNI 0000 0001 2216 9681, GRID grid.36425.36, Department of Pathology, Stony Brook University, ; Stony Brook, NY USA
                [162 ]ISNI 0000 0004 0427 2257, GRID grid.418284.3, Cell Death Regulation Group, Oncobell Program, Bellvitge Biomedical Research Institute (IDIBELL), Hospitalet de Llobregat, ; Barcelona, Spain
                [163 ]ISNI 0000 0004 0373 3971, GRID grid.136593.b, Laboratory of Biochemistry and Immunology, World Premier International (WPI) Immunology Frontier Research Center, Osaka University, Suita, ; Osaka, Japan
                [164 ]ISNI 0000000086837370, GRID grid.214458.e, Department of Pathology, University of Michigan Medical School, ; Ann Arbor, MI USA
                [165 ]ISNI 0000000086837370, GRID grid.214458.e, Comprehensive Cancer Center, University of Michigan Medical School, ; Ann Arbor, MI USA
                [166 ]ISNI 0000000122986657, GRID grid.34477.33, Department of Immunology, University of Washington, ; Seattle, WA USA
                [167 ]Center for Innate Immunity and Immune Disease, Seattle, WA USA
                [168 ]ISNI 0000 0004 0604 7563, GRID grid.13992.30, Department of Molecular Cell Biology, Weizmann Institute, ; Rehovot, Israel
                [169 ]ISNI 0000 0001 2171 9952, GRID grid.51462.34, Cell Biology Program, Memorial Sloan Kettering Cancer Center, ; New York, NY USA
                [170 ]ISNI 0000 0004 1936 8753, GRID grid.137628.9, Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, ; New York, NY USA
                [171 ]ISNI 0000 0004 1936 8753, GRID grid.137628.9, Howard Hughes Medical Institute, New York University School of Medicine, ; New York, NY USA
                [172 ]Department of Genitourinary Medical Oncology, University of Texas, MD Anderson Cancer Center, Houston, TX USA
                [173 ]ISNI 0000 0004 1937 0626, GRID grid.4714.6, Department of Oncology-Pathology, Karolinska Institute, ; Stockholm, Sweden
                [174 ]ISNI 0000 0000 8580 3777, GRID grid.6190.e, Institute for Genetics, Center for Molecular Medicine (CMMC), University of Cologne, ; Cologne, Germany
                [175 ]ISNI 0000 0000 8580 3777, GRID grid.6190.e, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, ; Cologne, Germany
                [176 ]ISNI 0000 0001 0008 2788, GRID grid.417521.4, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Campus Vienna BioCentre, ; Vienna, Austria
                [177 ]ISNI 0000 0001 1503 7226, GRID grid.5808.5, REQUIMTE/LAQV, Laboratory of Pharmacognosy, Department of Chemistry, Faculty of Pharmacy, University of Porto, ; Porto, Portugal
                [178 ]ISNI 0000 0001 2180 6431, GRID grid.4280.e, Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore, ; Singapore, Singapore
                [179 ]ISNI 0000 0001 2180 6431, GRID grid.4280.e, NUS Graduate School for Integrative Sciences and Engineering, National University of Singapore, ; Singapore, Singapore
                [180 ]National University Cancer Institute, National University Health System (NUHS), Singapore, Singapore
                [181 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Division of Hematology/Oncology, Department of Medicine, Northwestern University Feinberg School of Medicine, ; Chicago, IL USA
                [182 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine, ; Chicago, IL USA
                [183 ]ISNI 0000 0004 1757 2064, GRID grid.8484.0, LTTA center, University of Ferrara, ; Ferrara, Italy
                [184 ]Maria Cecilia Hospital, GVM Care & Research, Health Science Foundation, Cotignola, Italy
                [185 ]ISNI 0000 0004 0488 7120, GRID grid.4912.e, Department of Physiology, Royal College of Surgeons in Ireland, ; Dublin, Ireland
                [186 ]ISNI 0000 0001 2342 0938, GRID grid.1018.8, Department of Biochemistry, La Trobe University, ; Victoria, Australia
                [187 ]ISNI 0000 0001 1945 2152, GRID grid.423606.5, Laboratory of Immunopathology, Institute of Biology and Experimental Medicine (IBYME), National Council of Scientific and Technical Research (CONICET), ; Buenos Aires, Argentina
                [188 ]ISNI 0000 0001 0056 1981, GRID grid.7345.5, Department of Biological Chemistry, Faculty of Exact and Natural Sciences, University of Buenos Aires, ; Buenos Aires, Argentina
                [189 ]ISNI 0000 0004 1936 9713, GRID grid.5719.a, Institute of Cell Biology and Immunology, University of Stuttgart, ; Stuttgart, Germany
                [190 ]Stuttgart Research Center Systems Biology, Stuttgart, Germany
                [191 ]ISNI 0000 0004 1757 3470, GRID grid.5608.b, Department of Biomedical Sciences, University of Padua, ; Padua, Italy
                [192 ]ISNI 0000 0001 2181 4263, GRID grid.9983.b, Research Institute for Medicines (iMed.ULisboa), Faculty of Pharmacy, University of Lisbon, ; Lisbon, Portugal
                [193 ]ISNI 0000000121885934, GRID grid.5335.0, Department of Medical Genetics, Cambridge Institute for Medical Research (CIMR), University of Cambridge, ; Cambridge, UK
                [194 ]ISNI 0000 0001 1958 8658, GRID grid.8379.5, Department of Microbiology, Biocenter, University of Würzburg, ; Würzburg, Germany
                [195 ]ISNI 0000 0004 1936 9297, GRID grid.5491.9, Cancer Sciences Unit, Faculty of Medicine, University of Southampton, ; Southampton, UK
                [196 ]ISNI 0000 0004 1757 3470, GRID grid.5608.b, Department of Biology, University of Padua, ; Padua, Italy
                [197 ]GRID grid.428736.c, Venetian Institute of Molecular Medicine, ; Padua, Italy
                [198 ]ISNI 0000 0004 0644 5086, GRID grid.410717.4, National Institute of Biological Sciences, ; Beijing, China
                [199 ]ISNI 0000 0004 0626 5341, GRID grid.452350.5, Key Laboratory of Stem Cell Biology, Institute of Health Sciences, Chinese Academy of Sciences, ; Shanghai, China
                [200 ]ISNI 0000 0001 0198 0694, GRID grid.263761.7, Jiangsu Key Laboratory of Stem Cells and Medicinal Biomaterials, Institutes for Translational Medicine, Soochow University, ; Suzhou, China
                [201 ]ISNI 0000 0001 0198 0694, GRID grid.263761.7, The First Affiliated Hospital of Soochow University, Institutes for Translational Medicine, Soochow University, ; Suzhou, China
                [202 ]GRID grid.1042.7, Division of Inflammation, Walter and Eliza Hall Institute of Medical Research, Melbourne, ; Victoria, Australia
                [203 ]ISNI 0000 0004 1760 5276, GRID grid.417520.5, Unit of Tumor Immunology and Immunotherapy, Department of Research, Advanced Diagnostics and Technological Innovation, Regina Elena National Cancer Institute, ; Rome, Italy
                [204 ]ISNI 0000000419368729, GRID grid.21729.3f, Department of Biological Sciences, Columbia University, ; New York, NY USA
                [205 ]ISNI 0000000419368729, GRID grid.21729.3f, Department of Chemistry, Columbia University, ; New York, NY USA
                [206 ]ISNI 0000000121901201, GRID grid.83440.3b, Department of Cell and Developmental Biology, University College London Consortium for Mitochondrial Research, ; London, UK
                [207 ]ISNI 0000 0004 1795 1830, GRID grid.451388.3, Francis Crick Institute, ; London, UK
                [208 ]ISNI 0000 0000 8653 1072, GRID grid.410737.6, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, ; Guangdong, China
                [209 ]ISNI 0000 0000 8653 1072, GRID grid.410737.6, Center for DAMP Biology, Guangzhou Medical University, Guangzhou, ; Guangdong, China
                [210 ]ISNI 0000 0000 8653 1072, GRID grid.410737.6, Key Laboratory for Major Obstetric Diseases of Guangdong Province, Guangzhou Medical University, Guangzhou, ; Guangdong, China
                [211 ]ISNI 0000 0000 8653 1072, GRID grid.410737.6, Key Laboratory of Reproduction and Genetics of Guangdong Higher Education Institutes, Guangzhou Medical University, Guangzhou, ; Guangdong, China
                [212 ]ISNI 0000 0000 8653 1072, GRID grid.410737.6, Key Laboratory for Protein Modification and Degradation of Guangdong Province, Guangzhou Medical University, Guangzhou, ; Guangdong, China
                [213 ]ISNI 0000 0004 1936 9000, GRID grid.21925.3d, Department of Surgery, University of Pittsburgh, ; Pittsburgh, PA USA
                [214 ]Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas Medical School, University of Crete, Heraklion, Greece
                [215 ]ISNI 0000 0001 0703 675X, GRID grid.430503.1, Department of Pharmacology, University of Colorado, ; Aurora, CO USA
                [216 ]Research Center, Osaka International Cancer Institute, Osaka, Japan
                [217 ]ISNI 0000 0001 0706 0012, GRID grid.11375.31, Department Biochemistry and Molecular Biology, “Jozef Stefan” Institute, ; Ljubljana, Slovenia
                [218 ]ISNI 0000 0001 0721 6013, GRID grid.8954.0, Faculty of Chemistry and Chemical Technology, University of Ljubljana, ; Ljubljana, Slovenia
                [219 ]ISNI 0000 0001 2341 2786, GRID grid.116068.8, Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, ; Cambridge, MA USA
                [220 ]ISNI 0000 0001 2341 2786, GRID grid.116068.8, Department of Biology, Massachusetts Institute of Technology, ; Cambridge, MA USA
                [221 ]ISNI 0000 0001 2106 9910, GRID grid.65499.37, Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, ; Boston, MA USA
                [222 ]ISNI 0000 0000 8853 2677, GRID grid.5361.1, Division of Developmental Immunology, Innsbruck Medical University, ; Innsbruck, Austria
                [223 ]ISNI 0000 0001 2355 7002, GRID grid.4367.6, Department of Pathology and Immunology, Washington University School of Medicine, ; St. Louis, MO USA
                [224 ]ISNI 0000 0004 0534 4718, GRID grid.418158.1, Department of Early Discovery Biochemistry, Genentech, ; South San Francisco, CA USA
                [225 ]ISNI 0000 0000 8700 1153, GRID grid.7719.8, Genes, Development and Disease Group, Cancer Cell Biology Program, Spanish National Cancer Research Centre (CNIO), ; Madrid, Spain
                [226 ]ISNI 0000000121901201, GRID grid.83440.3b, Centre for Cell Death, Cancer and Inflammation, UCL Cancer Institute, University College London, ; London, UK
                [227 ]ISNI 0000 0004 0604 7563, GRID grid.13992.30, Department of Biomolecular Sciences, Weizmann Institute of Science, ; Rehovot, Israel
                [228 ]ISNI 0000 0004 0467 2285, GRID grid.419092.7, Institute of Health Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, ; Shanghai, China
                [229 ]ISNI 0000 0001 2297 6811, GRID grid.266102.1, Department of Pharmaceutical Chemistry, University of California, San Francisco, ; San Francisco, CA USA
                [230 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, School of Cellular and Molecular Medicine, Faculty of Biomedical Sciences, University of Bristol, ; Bristol, UK
                [231 ]ISNI 0000 0001 1015 4378, GRID grid.422150.0, Interdisciplinary Research Center on Biology and Chemistry, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, ; Shanghai, China
                [232 ]ISNI 0000 0001 2188 3760, GRID grid.262273.0, Department of Biology, Queens College of the City University of New York, ; Queens, NY USA
                [233 ]ISNI 0000 0001 2342 9668, GRID grid.14476.30, Faculty of Fundamental Medicine, Lomonosov Moscow State University, ; Moscow, Russia
                [234 ]ISNI 0000 0001 2284 9388, GRID grid.14925.3b, Gustave Roussy Comprehensive Cancer Institute, ; Villejuif, France
                [235 ]INSERM U1015, Villejuif, France
                [236 ]Center of Clinical Investigations in Biotherapies of Cancer (CICBT) 1428, Villejuif, France
                [237 ]ISNI 0000 0001 2175 4109, GRID grid.50550.35, Biology Pole, European Hospital George Pompidou, AP-HP, ; Paris, France
                Article
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                10.1038/s41418-017-0012-4
                5864239
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                © ADMC Associazione Differenziamento e Morte Cellulare 2018

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