Autophagic cell death: the story of a misnomer
Abstract
Dying cells often display a large-scale accumulation of autophagosomes and hence adopt a morphology called autophagic cell death. In many cases, it is agreed that this autophagic cell death is cell death with autophagy rather than cell death by autophagy. Here, we evaluate the accumulating body of literature that argues that cell death occurs by autophagy. We also list the caveats that must be considered when deciding whether or not autophagy is an important effector mechanism of cell death.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Claim (c) is stronger than claim (b) because proof is needed that the cell death mechanism is not apoptosis or necrosis.
“Claim (c) is still stronger, because, even if the cell death is blocked by autophagy inhibition, proof needs to be provided that the cell death mechanism is not apoptosis or necrosis.670”
From Guidelines for the use and interpretation of assays for monitoring autophagy (2012) · cites this paper as [670]
Autophagy does not constitute an effector mechanism of cell death but often accompanies cell death.
“Although autophagy does not constitute an effector mechanism of cell death61, it often accompanies cell death 62 (Box 2).”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [62]
Cites
Repertoires of Autophagy in the Pathogenesis of Ocular Diseases
Li, Y., Jiang, Q. L., Cao, G.-F., Yao, J., & Yan, B. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000373980 · Cited by 16,351 · see citing works
Cell Death: The Significance of Apoptosis
Wyllie, A. H., Kerr, J. F. R., & Currie, A. R. (1980) · International review of cytology · doi:10.1016/s0074-7696(08)62312-8 · Cited by 7,235 · see citing works
Autophagy in the Pathogenesis of Disease
Levine, B., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2007.12.018 · Cited by 7,069 · see citing works
Self-citationAutophagy fights disease through cellular self-digestion
Mizushima, N., Levine, B., Cuervo, A. M., & Klionsky, D. J. (2008) · Nature · doi:10.1038/nature06639 · Cited by 6,452 · see citing works
Self-citationAutophagy and Viruses: Adversaries or Allies?
Dong, X., & Levine, B. (2013) · Journal of Innate Immunity · doi:10.1159/000346388 · Cited by 4,441 · see citing works
Self-citationProapoptotic 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
Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis
Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., et al. (1995) · Nature · doi:10.1038/376037a0 · Cited by 3,980 · see citing works
Levine, B., & Klionsky, D. J. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00099-1 · Cited by 3,671 · see citing works
Self-citationSelf-eating and self-killing: crosstalk between autophagy and apoptosis
Maiuri, M. C., Zalckvar, E., Kimchi, A., & Kroemer, G. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2239 · Cited by 3,560 · see citing works
Self-citationBcl-2 Antiapoptotic Proteins Inhibit Beclin 1-Dependent Autophagy
Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., & Levine, B. (2005) · Cell · doi:10.1016/j.cell.2005.07.002 · Cited by 3,536 · see citing works
Self-citationLoss of autophagy in the central nervous system causes neurodegeneration in mice
Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J.-I., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., et al. (2006) · Nature · doi:10.1038/nature04723 · Cited by 3,500 · see citing works
Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009
Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., El-Deiry, W. S., Golstein, P., Green, D. R., et al. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2008.150 · Cited by 3,399 · see citing works
Self-citationAutophagy in Health and Disease: A Double-Edged Sword
Shintani, T., & Klionsky, D. J. (2004) · Science · doi:10.1126/science.1099993 · Cited by 2,531 · see citing works
Identification of RIP1 kinase as a specific cellular target of necrostatins
Degterev, A., Hitomi, J., Germscheid, M., Ch'en, I. L., Korkina, O., Teng, X., Abbott, D., Cuny, G. D., Yuan, C., Wagner, G., et al. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.83 · Cited by 2,059 · see citing works
Autophagy in cell death: an innocent convict?
Levine, B. (2005) · Journal of Clinical Investigation · doi:10.1172/jci26390 · Cited by 1,671 · 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
Gene silencing in mammals by small interfering RNAs
McManus, M. T., & Sharp, P. A. (2002) · Nature Reviews Genetics · doi:10.1038/nrg908 · Cited by 1,400 · see citing works
DRAM, a p53-Induced Modulator of Autophagy, Is Critical for Apoptosis
Crighton, D., Wilkinson, S., O'Prey, J., Syed, N., Smith, P., Harrison, P. R., Gasco, M., Garrone, O., Crook, T., & Ryan, K. M. (2006) · Cell · doi:10.1016/j.cell.2006.05.034 · Cited by 1,380 · see citing works
Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes
Shimizu, S., Kanaseki, T., Mizushima, N., Mizuta, T., Arakawa-Kobayashi, S., Thompson, C. B., & Tsujimoto, Y. (2004) · Nature Cell Biology · doi:10.1038/ncb1192 · Cited by 1,358 · see citing works
Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis
Yousefi, S., Perozzo, R., Schmid, I., Ziemiecki, A., Schaffner, T. J., Scapozza, L., Brunner, T., & Simon, H. (2006) · Nature Cell Biology · doi:10.1038/ncb1482 · Cited by 1,300 · see citing works
Lysosomes and autophagy in cell death control
Kroemer, G., & Jäättelä, M. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1738 · Cited by 1,291 · see citing works
Self-citationRegulation of an ATG7 - beclin 1 Program of Autophagic Cell Death by Caspase-8
Yu, L., Alva, A. S., Su, H. C., Dutt, P., Freundt, E. C., Welsh, S. J., Baehrecke, E. H., & Lenardo, M. J. (2004) · Science · doi:10.1126/science.1096645 · Cited by 1,220 · see citing works
Functional and physical interaction between Bcl‐XL and a BH3‐like domain in Beclin‐1
Maiuri, M. C., Toumelin-Braizat, G. L., Criollo, A., Rain, J., Gautier, F., Juin, P. P., Tasdemir, E., Pierron, G., Troulinaki, K., Tavernarakis, N., et al. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601689 · Cited by 1,107 · see citing works
Self-citationAutophagy and signaling: their role in cell survival and cell death
Codogno, P., & Meijer, A. J. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401751 · Cited by 1,092 · see citing works
Ambra1 regulates autophagy and development of the nervous system
Fimia, G. M., Stoykova, A., Romagnoli, A., Giunta, L., Bartolomeo, S. D., Nardacci, R., Corazzari, M., Fuoco, C., Uçar, A., Schwartz, P. J., et al. (2007) · Nature · doi:10.1038/nature05925 · Cited by 1,048 · see citing works
Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease.
Anglade, P., Vyas, S., Javoy-Agid, F., Herrero, M. T., Michel, P. P., Marquez, J., Prigent, A., Ruberg, M., Hirsch, É. C., & Agid, Y. (1997) · PubMed · Cited by 1,045 · see citing works
Cell death by necrosis: towards a molecular definition
Golstein, P., & Kroemer, G. (2007) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.11.001 · Cited by 1,044 · see citing works
Self-citationAutophagy: dual roles in life and death?
Baehrecke, E. H. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1666 · Cited by 986 · see citing works
Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells
Kanzawa, T., Germano, I. M., Komata, T., Ito, H., Kondo, Y., & Kondo, S. (2004) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401359 · Cited by 986 · see citing works
Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis
Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H. D., Sun, M., Sato, Y., Liang, C., Jung, J. U., Cheng, J. Q., Mul, J. J., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1634 · Cited by 928 · see citing works
Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice
Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E.-L., Hartmann, D., Lüllmann-Rauch, R., Janssen, P. M. L., Blanz, J., von Figura, K., & Saftig, P. (2000) · Nature · doi:10.1038/35022595 · Cited by 925 · see citing works
Direct Induction of Autophagy by Atg1 Inhibits Cell Growth and Induces Apoptotic Cell Death
Scott, R. C., Juhász, G., & Neufeld, T. P. (2007) · Current Biology · doi:10.1016/j.cub.2006.10.053 · Cited by 852 · see citing works
Classification of cell death: recommendations of the Nomenclature Committee on Cell Death
Kroemer, G., El-Deiry, W. S., Golstein, P., Peter, M. E., Vaux, D., Vandenabeele, P., Zhivotovsky, B., Blagosklonny, M. V., Malorni, W., Knight, R. A., et al. (2005) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4401724 · Cited by 843 · see citing works
Self-citationCell death modalities: classification and pathophysiological implications
Galluzzi, L., Maiuri, M. C., Vitale, I., Zischka, H., Castedo, M., Zitvogel, L., & Kroemer, G. (2007) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4402148 · Cited by 832 · see citing works
Self-citationZong, W., Lindsten, T., Ross, A. J., MacGregor, G. R., & Thompson, C. B. (2001) · Genes & Development · doi:10.1101/gad.897601 · Cited by 809 · see citing works
Another way to die: autophagic programmed cell death
Tsujimoto, Y., & Shimizu, S. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401777 · Cited by 755 · see citing works
Cerebral preconditioning and ischaemic tolerance
Gidday, J. M. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1927 · Cited by 751 · see citing works
Festjens, N., Vanden Berghe, T., & Vandenabeele, P. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.06.014 · Cited by 710 · see citing works
Chen, Y., McMillan‐Ward, E., Kong, J., Israels, S. J., & Gibson, S. B. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402233 · Cited by 689 · see citing works
Autophagic programmed cell death by selective catalase degradation
Yu, L., Wan, F., Dutta, S., Welsh, S., Liu, Z., Freundt, E. C., Baehrecke, E. H., & Lenardo, M. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511288103 · Cited by 668 · see citing works
Autophagy Gene-Dependent Clearance of Apoptotic Cells during Embryonic Development
Qu, X., Zou, Z., Sun, Q., Luby‐Phelps, K., Cheng, P., Hogan, R. N., Gilpin, C. J., & Levine, B. (2007) · Cell · doi:10.1016/j.cell.2006.12.044 · Cited by 655 · see citing works
Self-citationApoptotic and autophagic cell death induced by histone deacetylase inhibitors
Shao, Y., Gao, Z., Marks, P. A., & Jiang, X. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408345102 · Cited by 604 · see citing works
Growth Arrest and Autophagy Are Required for Salivary Gland Cell Degradation in Drosophila
Berry, D. L., & Baehrecke, E. H. (2007) · Cell · doi:10.1016/j.cell.2007.10.048 · Cited by 602 · see citing works
The Atg5–Atg12 conjugate associates with innate antiviral immune responses
Jounai, N., Takeshita, F., Kobiyama, K., Sakaue-Sawano, A., Miyawaki, A., Xin, K.-Q., Ishii, K. J., Kawai, T., Akira, S., Suzuki, K., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704014104 · Cited by 562 · see citing works
Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein
Cao, Y., & Klionsky, D. J. (2007) · Cell Research · doi:10.1038/cr.2007.78 · Cited by 541 · see citing works
Carew, J. S., Nawrocki, S. T., Kahue, C. N., Zhang, H., Yang, C., Chung, L., Houghton, J. A., Huang, P., Giles, F. J., & Cleveland, J. L. (2007) · Blood · doi:10.1182/blood-2006-10-050260 · Cited by 488 · see citing works
Inhibition of Autophagy Prevents Hippocampal Pyramidal Neuron Death after Hypoxic-Ischemic Injury
Koike, M., Shibata, M., Tadakoshi, M., Gotoh, K., Komatsu, M., Waguri, S., Kawahara, N., Kuida, K., Nagata, S., Kominami, E., et al. (2008) · The American Journal of Pathology · doi:10.2353/ajpath.2008.070876 · Cited by 486 · see citing works
Differential Effects of Endoplasmic Reticulum Stress-induced Autophagy on Cell Survival
Ding, W., Ni, H., Gao, W., Hou, Y., Melan, M. A., Chen, X., Stolz, D. B., Shao, Z.-M., & Yin, X. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m609267200 · Cited by 481 · see citing works
Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4
Espert, L. (2006) · Journal of Clinical Investigation · doi:10.1172/jci26185 · Cited by 447 · see citing works
Scarlatti, F., Maffei, R., Beau, I., Codogno, P., & Ghidoni, R. (2008) · Cell Death & Differentiation · doi:10.1038/cdd.2008.51 · Cited by 412 · see citing works
Programmed cell death and apoptosis: origins of the theory
Lockshin, R. A., & Zakeri, Z. F. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35080097 · Cited by 361 · see citing works
Katayama, M., Kawaguchi, T., Berger, M. S., & Pieper, R. O. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402030 · Cited by 353 · see citing works
Kametaka, S., Okano, T., Ohsumi, M., & Ohsumi, Y. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.35.22284 · Cited by 275 · see citing works
Does autophagy have a license to kill mammalian cells?
Scarlatti, F., Granata, R., Meijer, A., & Codogno, P. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2008.101 · Cited by 271 · see citing works
Akar, U., Chaves-Reyez, A., Barria, M., Tari, A. M., Sanguino, A. M., Kondo, Y., Kondo, S., Arun, B. K., Lopez‐Berestein, G., & Özpolat, B. (2008) · Autophagy · doi:10.4161/auto.6083 · Cited by 253 · see citing works
A Molecule Targeting VHL-Deficient Renal Cell Carcinoma that Induces Autophagy
Turcotte, S., Chan, D. A., Sutphin, P. D., Hay, M. P., Denny, W. A., & Giaccia, A. J. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.06.004 · Cited by 251 · see citing works
Active Ras Triggers Death in Glioblastoma Cells through Hyperstimulation of Macropinocytosis
Overmeyer, J. H., Kaul, A., Johnson, E. E., & Maltese, W. A. (2008) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-07-2036 · Cited by 229 · see citing works
A Short Mitochondrial Form of p19ARF Induces Autophagy and Caspase-Independent Cell Death
Reef, S., Zalckvar, E., Shifman, O., Bialik, S., Sabanay, H., Oren, M., & Kimchi, A. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.04.014 · Cited by 226 · see citing works
Zhu, C., Wang, X., Huang, Z., Qiu, L., Xu, F., Vahsen, N., Nilsson, M., Eriksson, P. S., Hagberg, H., Culmsee, C., et al. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402053 · Cited by 213 · see citing works
Self-citationLoss of Bif-1 Suppresses Bax/Bak Conformational Change and Mitochondrial Apoptosis
Takahashi, Y., Karbowski, M., Yamaguchi, H., Kazi, A., Wu, J., Sebti, S. M., Youle, R. J., & Wang, H. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.21.9369-9382.2005 · Cited by 190 · see citing works
Autophagy is required for necrotic cell death in Caenorhabditis elegans
Samara, C., Syntichaki, P., & Tavernarakis, N. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402231 · Cited by 178 · see citing works
Apoptosis and Autophagy in Photoreceptors Exposed to Oxidative Stress
Kunchithapautham, K., & Rohrer, B. (2007) · Autophagy · doi:10.4161/auto.4294 · Cited by 171 · see citing works
Ogura, K., Wicky, C., Magnenat, L., Tobler, H., Mori, I., Müller, F., & Ohshima, Y. (1994) · Genes & Development · doi:10.1101/gad.8.20.2389 · Cited by 165 · see citing works
Massey, D. C. O., & Parkes, M. (2007) · Autophagy · doi:10.4161/auto.5075 · Cited by 141 · see citing works
Nishino, I. (2006) · Seminars in Pediatric Neurology · doi:10.1016/j.spen.2006.06.004 · Cited by 133 · see citing works
A first insight into the molecular mechanisms of apoptosis
Yuan, J., & Horvitz, H. R. (2004) · Cell · doi:10.1016/s0092-8674(04)00028-5 · Cited by 129 · see citing works
Zhou, X., Babu, J. R., da Silva, S., Shu, Q., Graef, I. A., Oliver, T., Tomoda, T., Tani, T., Wooten, M. W., & Wang, F. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701402104 · Cited by 122 · see citing works
Wang, M., Tan, W., Zhou, J., Leow, J., Go, M., Lee, H. S., & Casey, P. J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801855200 · Cited by 115 · see citing works
Kitanaka, C. (2002) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/94.5.358 · Cited by 113 · see citing works
Autophagy occurs upstream or parallel to the apoptosome during histolytic cell death
Akdemir, F., Farkas, R., Chen, P., Juhász, G., Medved'ová, L., Sass, M., Wang, L., Wang, X., Chittaranjan, S., Gorski, S. M., et al. (2006) · Development · doi:10.1242/dev.02332 · Cited by 102 · see citing works
A plant triterpenoid, avicin D, induces autophagy by activation of AMP-activated protein kinase
Xu, Z.-X., Liang, J., Haridas, V., Gaikwad, A. S., Connolly, F. P., Mills, G. B., & Gutterman, J. U. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402207 · Cited by 101 · see citing works
Autophagy Gene Disruption Reveals a Non-vacuolar Cell Death Pathway in Dictyostelium
Kosta, A., Roisin-Bouffay, C., Luciani, M., Otto, G. P., Kessin, R. H., & Golstein, P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408924200 · Cited by 92 · see citing works
Autophagy functions in programmed cell death
Berry, D. L., & Baehrecke, E. H. (2008) · Autophagy · doi:10.4161/auto.5575 · Cited by 67 · see citing works
Rashmi, R., Pillai, S. G., Vijayalingam, S., et al. (2007) · Oncogene · doi:10.1038/sj.onc.1210783 · Cited by 63 · see citing works
Chatterjee, T., Muhkopadhyay, A., Khan, K. A., et al. (1998) · Mutagenesis · doi:10.1093/mutage/13.6.619 · Cited by 54 · see citing works
Kim, K. W., Moretti, L., & Lu, J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002275 · Cited by 51 · see citing works
Xue, L., Borutaite, V., & Tolkovsky, A. M. (2002) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)01181-4 · Cited by 45 · see citing works
Bolaños‐Meade, J., Zhou, L., Höke, A., Corse, A. M., Vogelsang, G. B., & Wagner, K. R. (2005) · American Journal of Hematology · doi:10.1002/ajh.20294 · Cited by 43 · see citing works
Comprehensive proteomics analysis of autophagy-deficient mouse liver
Matsumoto, N., Ezaki, J., Komatsu, M., Takahashi, K., Mineki, R., Taka, H., Kikkawa, M., Fujimura, T., Takeda‐Ezaki, M., Ueno, T., et al. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.01.112 · Cited by 39 · see citing works
Iida, A., Emi, M., Matsuoka, R., et al. (2000) · Human Genetics · doi:10.1007/s004390051038 · Cited by 37 · see citing works
Perelman, B., Dafni, N., Naiman, T., et al. (1997) · Genomics · doi:10.1006/geno.1997.4623 · Cited by 35 · see citing works
Studying autophagy’s relationship to cell death
Thorburn, A. M. (2008) · Autophagy · doi:10.4161/auto.5661 · Cited by 17 · see citing works
From autophagic to necrotic cell death in Dictyostelium
Tresse, E., Kosta, A., Luciani, M., & Golstein, P. (2006) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2006.10.010 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Guidelines 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-citationMethods in Mammalian Autophagy Research
Mizushima, N., Yoshimori, T., & Levine, B. (2010) · Cell · doi:10.1016/j.cell.2010.01.028 · Cited by 4,497 · see citing works
Self-citationGuidelines for the use and interpretation of assays for monitoring autophagy
Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J. A., et al. (2012) · Autophagy · doi:10.4161/auto.19496 · Cited by 3,996 · see citing works
Self-citationGalluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.96 · Cited by 2,421 · see citing works
Self-citationSelf-consumption: the interplay of autophagy and apoptosis
Mariño, G., Niso-Santano, M., Baehrecke, E. H., & Kroemer, G. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3735 · Cited by 2,172 · see citing works
Self-citationRubinsztein, D. C., Mariño, G., & Kroemer, G. (2011) · Cell · doi:10.1016/j.cell.2011.07.030 · Cited by 2,107 · see citing works
Self-citationImmunogenic and tolerogenic cell death
Green, D. R., Ferguson, T., Zitvogel, L., & Kroemer, G. (2009) · Nature Reviews Immunology · doi:10.1038/nri2545 · Cited by 1,176 · see citing works
Self-citationEssential 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-citationKang, R., Chen, R., Zhang, Q., Hou, W., Wu, S., Cao, L., Huang, J., Yu, Y., Fan, X.-G., Yan, Z., et al. (2014) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2014.05.001 · Cited by 956 · see citing works
Autophagy‐based unconventional secretory pathway for extracellular delivery of IL‐1β
Dupont, N., Jiang, S., Pilli, M., Ornatowski, W., Bhattacharya, D., & Deretic, V. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.398 · Cited by 967 · see citing works
Mitotic catastrophe: a mechanism for avoiding genomic instability
Vitale, I., Galluzzi, L., Castedo, M., & Kroemer, G. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3115 · Cited by 834 · see citing works
Self-citationMorselli, E., Maiuri, M. C., Markaki, M., Megalou, E., Pasparaki, A., Palikaras, K., Criollo, A., Galluzzi, L., Malik, S. A., Vitale, I., et al. (2010) · Cell Death & Disease · doi:10.1038/cddis.2009.8 · Cited by 613 · see citing works
Self-citationRegulation of lipid stores and metabolism by lipophagy
Liu, K., & Czaja, M. J. (2013) · Cell Death & Differentiation · doi:10.1038/cdd.2012.63 · Cited by 542 · see citing works
HMGB1 release and redox regulates autophagy and apoptosis in cancer cells
Tang, D., Kang, R., Cheh, C.-W., Livesey, K. M., Liang, X., Schapiro, N. E., Benschop, R., Sparvero, L. J., Amoscato, A. A., Tracey, K. J., et al. (2010) · Oncogene · doi:10.1038/onc.2010.261 · Cited by 461 · see citing works
Elgendy, M., Sheridan, C., Brumatti, G., & Martin, S. J. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.02.009 · Cited by 426 · see citing works
Molecular Mechanisms of Radiation-Induced Cancer Cell Death: A Primer
Sia, J., Szmyd, R., Hau, E., & Gee, H. E. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00041 · Cited by 378 · see citing works
Mi, S., Li, Z., Yang, H.-Z., Liu, H., Wang, J.-P., Ma, Y.-G., Wang, X.-X., Liu, H.-Z., Sun, W., & Hu, Z.-W. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1004081 · Cited by 370 · 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 · see citing works
Cardiac Aging: From Molecular Mechanisms to Significance in Human Health and Disease
Dai, D.-F., Chen, T., Johnson, S. C., Szeto, H., & Rabinovitch, P. S. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4179 · Cited by 334 · see citing works
Bacterial programmed cell death: making sense of a paradox
Bayles, K. W. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3136 · Cited by 315 · see citing works
Autophagy 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
Recent advances in our understanding of neurodegeneration
Jellinger, K. A. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0240-y · Cited by 274 · see citing works
Yu, K.-N., Yoon, T.-J., Minai-Tehrani, A., Kim, J.-E., Park, S. J., Jeong, M. S., Ha, S.-W., Lee, J.-K., Kim, J. S., & Cho, M.-H. (2013) · Toxicology in Vitro · doi:10.1016/j.tiv.2013.02.010 · Cited by 268 · see citing works
Molecular mechanisms of regulated necrosis
Galluzzi, L., Kepp, O., Krautwald, S., Kroemer, G., & Linkermann, A. (2014) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2014.02.006 · Cited by 258 · see citing works
Self-citationAutophagy 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-citationAutophagic protein LC3B confers resistance against hypoxia-induced pulmonary hypertension.
Lee, S.-J., Smith, A., Guo, L., Alastalo, T.-P., Li, M., Sawada, H., Liu, X., Chen, Z.-H., Ifedigbo, E., Jin, Y., et al. (2011) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201005-0746oc · Cited by 217 · see citing works
Autophagy mediates pharmacological lifespan extension by spermidineand resveratrol
Morselli, E., Galluzzi, L., Kepp, O., Criollo, A., Maiuri, M. C., Tavernarakis, N., Madeo, F., & Kroemer, G. (2009) · Aging · doi:10.18632/aging.100110 · Cited by 213 · see citing works
Self-citationLysosomal cell death mechanisms in aging
Gómez-Sintes, R., Ledesma, M. D., & Boya, P. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.02.009 · Cited by 216 · see citing works
The relationship of autophagy defects to cartilage damage during joint aging in a mouse model
Caramés, B., Olmer, M., Kiosses, W. B., & Lotz, M. K. (2015) · Arthritis & Rheumatology · doi:10.1002/art.39073 · Cited by 204 · see citing works
Jung, S., Choe, S., Woo, H., Jeong, H., An, H.-K., Moon, H., Ryu, H. Y., Yeo, B. K., Lee, Y. W., Choi, H., et al. (2020) · Autophagy · doi:10.1080/15548627.2019.1630222 · Cited by 183 · see citing works
Gao, W., Shen, Z., Shang, L., & Wang, X. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2011.33 · Cited by 178 · see citing works
Upregulation of Rubicon promotes autosis during myocardial ischemia/reperfusion injury
Nah, J., Zhai, P., Huang, C.-Y., Fernández, Á. F., Mareedu, S., Levine, B., & Sadoshima, J. (2020) · Journal of Clinical Investigation · doi:10.1172/jci132366 · Cited by 150 · see citing works
Self-citationChen, X., Wang, K., Xing, Y., Tu, J., Yang, X., Zhao, Q., Li, K., & Chen, Z. (2014) · Protein & Cell · doi:10.1007/s13238-014-0104-6 · Cited by 130 · see citing works
Pathophysiological 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
Hypoxia-inducible factor-1α (HIF-1α) and autophagy in polycystic kidney disease (PKD)
Belibi, F., Zafar, I., Ravichandran, K., Segvic, A. B., Jani, A., Ljubanovic, D. G., & Edelstein, C. L. (2011) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00348.2010 · Cited by 107 · see citing works
Autophagy as a Potential Target for Sarcopenia: AUTOPHAGY REGULATION IN SARCOPENIA
Fan, J., Kou, X., Jia, S., Yang, X., Yang, Y., & Chen, N. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25260 · Cited by 101 · see citing works
BAX channel activity mediates lysosomal disruption linked to Parkinson disease
Bové, J., Martínez-Vicente, M., Dehay, B., Perier, C., Recasens, A., Bombrun, A., Antonsson, B., & Vila, M. (2014) · Autophagy · doi:10.4161/auto.28286 · Cited by 89 · see citing works
Autophagy in Pulmonary Diseases
Nakahira, K., Pabon Porras, M. A., & Choi, A. M. K. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201512-2468so · Cited by 78 · see citing works
Apoptosis and autophagy in polycystic kidney disease (PKD)
Nowak, K. L., & Edelstein, C. L. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2019.109518 · Cited by 71 · see citing works
Verma, N. K., Conroy, J., Lyons, P. E., Coleman, J., O'Sullivan, M. P., Kornfeld, H., Kelleher, D., & Volkov, Y. (2012) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2012.08.023 · Cited by 68 · see citing works
Shah, S. Z. A., Zhao, D., Hussain, T., & Yang, L. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.09.004 · Cited by 55 · see citing works
Natural antioxidants’ effects on endoplasmic reticulum stress-related diseases
Reyes-Fermín, L. M., Aparicio-Trejo, O. E., Avila-Rojas, S. H., Gómez-Sierra, T., Martínez-Klimova, E., & Pedraza-Chaverri, J. (2020) · Food and Chemical Toxicology · doi:10.1016/j.fct.2020.111229 · Cited by 50 · see citing works
Pontrelli, P., Oranger, A., Barozzino, M., Divella, C., Conserva, F., Fiore, M. G., Rossi, R., Papale, M., Castellano, G., Simone, S., et al. (2018) · Journal of Molecular Medicine · doi:10.1007/s00109-018-1656-3 · Cited by 26 · see citing works
Taurine Rescues Cisplatin-Induced Muscle Atrophy in Vitro: A Morphological Study
Stacchiotti, A., Rovetta, F., Ferroni, M., Corsetti, G., Lavazza, A., Sberveglieri, G., & Aleo, M. F. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/840951 · Cited by 21 · see citing works
- Authors
- Kroemer, G., & Levine, B.
- Affiliations
- Institut Gustave Roussy (FR)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Kroemer, Guido
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2008-10-30
- Volume
- 9
- Issue
- 12
- Pages
- 1004-1010
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- OpenAlex
- W1989051519
- Cited by
- 1,453
- References
- 83
- Citations by year
- 2026: 29 · 2025: 48 · 2024: 42 · 2023: 63 · 2022: 71 · 2021: 74 · 2020: 82 · 2019: 81 · 2018: 83 · 2017: 87 · 2016: 93 · 2015: 108 · 2014: 120 · 2013: 116 · 2012: 104
- FWCI
- 8.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Cancer Institute (R01CA109618, R01CA084254)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- autophagic cell death, autophagy, cell death, autophagosomes, terminology
- MeSH terms
- Animals, Autophagy, Lysosomes, Necrosis, Terminology as Topic, Phagosomes, Cell Death, Apoptosis
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
