Molecular definitions of autophagy and related processes

doi:10.15252/embj.201796697

Review

. 2017 Jul 3;36(13):1811-1836.

doi: 10.15252/embj.201796697. Epub 2017 Jun 8.

Molecular definitions of autophagy and related processes

Lorenzo Galluzzi^{1

2}, Eric H Baehrecke³, Andrea Ballabio^{4

5

6

7}, Patricia Boya⁸, José Manuel Bravo-San Pedro^{2

9

10

11

12}, Francesco Cecconi^{13

14

15}, Augustine M Choi¹⁶, Charleen T Chu¹⁷, Patrice Codogno^{2

18

19

20}, Maria Isabel Colombo^{21

22}, Ana Maria Cuervo²³, Jayanta Debnath²⁴, Vojo Deretic²⁵, Ivan Dikic^{26

27

28}, Eeva-Liisa Eskelinen²⁹, Gian Maria Fimia^{30

31}, Simone Fulda^{32

33

34}, David A Gewirtz^{35

36}, Douglas R Green³⁷, Malene Hansen³⁸, J Wade Harper³⁹, Marja Jäättelä⁴⁰, Terje Johansen⁴¹, Gabor Juhasz^{42

43}, Alec C Kimmelman⁴⁴, Claudine Kraft⁴⁵, Nicholas T Ktistakis⁴⁶, Sharad Kumar⁴⁷, Beth Levine^{48

49}, Carlos Lopez-Otin^{50

51}, Frank Madeo^{52

53}, Sascha Martens⁴⁵, Jennifer Martinez⁵⁴, Alicia Melendez^{55

56}, Noboru Mizushima⁵⁷, Christian Münz⁵⁸, Leon O Murphy⁵⁹, Josef M Penninger⁶⁰, Mauro Piacentini^{13

30}, Fulvio Reggiori⁶¹, David C Rubinsztein⁶², Kevin M Ryan⁶³, Laura Santambrogio⁶⁴, Luca Scorrano^{65

66}, Anna Katharina Simon^{67

68}, Hans-Uwe Simon⁶⁹, Anne Simonsen⁷⁰, Nektarios Tavernarakis^{71

72}, Sharon A Tooze⁷³, Tamotsu Yoshimori^{74

75}, Junying Yuan^{39

76}, Zhenyu Yue⁷⁷, Qing Zhong⁴⁸, Guido Kroemer^{2

9

10

11

12

78

79}

Affiliations

¹ Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA deadoc@vodafone.it.
² Université Paris Descartes/Paris V, Paris, France.
³ Department of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, USA.
⁴ Telethon Institute of Genetics and Medicine (TIGEM), Pozzuoli, Italy.
⁵ Medical Genetics, Department of Pediatrics, Federico II University, Naples, Italy.
⁶ Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.
⁷ Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital, Houston, TX, USA.
⁸ Department of Cellular and Molecular Biology, Centro de Investigaciones Biológicas, CSIC, Madrid, Spain.
⁹ Université Pierre et Marie Curie/Paris VI, Paris, France.
¹⁰ Equipe 11 labellisée Ligue contre le Cancer, Centre de Recherche des Cordeliers, Paris, France.
¹¹ INSERM, U1138, Paris, France.
¹² Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute, Villejuif, France.
¹³ Department of Biology, University of Tor Vergata, Rome, Italy.
¹⁴ Unit of Cell Stress and Survival, Danish Cancer Society Research Center, Copenhagen, Denmark.
¹⁵ Department of Pediatric Hematology and Oncology, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
¹⁶ Division of Pulmonary and Critical Care Medicine, Joan and Sanford I. Weill Department of Medicine, Weill Cornell Medical College, New York, NY, USA.
¹⁷ Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
¹⁸ Institut Necker-Enfants Malades (INEM), Paris, France.
¹⁹ INSERM, U1151, Paris, France.
²⁰ CNRS, UMR8253, Paris, France.
²¹ Laboratorio de Biología Celular y Molecular, Instituto de Histología y Embriología (IHEM)-CONICET, Mendoza, Argentina.
²² Facultad de Ciencias Médicas, Universidad Nacional de Cuyo, Mendoza, Argentina.
²³ Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, Bronx, NY, USA.
²⁴ Department of Pathology, University of California San Francisco, San Francisco, CA, USA.
²⁵ Department of Molecular Genetics and Microbiology, University of New Mexico Health Sciences Center, Albuquerque, NM, USA.
²⁶ Institute of Biochemistry II, School of Medicine, Goethe University Frankfurt, Frankfurt, Germany.
²⁷ Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Frankfurt Main, Germany.
²⁸ Department of Immunology and Medical Genetics, University of Split School of Medicine, Split, Croatia.
²⁹ Department of Biosciences, University of Helsinki, Helsinki, Finland.
³⁰ National Institute for Infectious Diseases "L. Spallanzani" IRCCS, Rome, Italy.
³¹ Department of Biological and Environmental Sciences and Technologies (DiSTeBA), University of Salento, Lecce, Italy.
³² Institute for Experimental Cancer Research in Pediatrics, Goethe-University, Frankfurt, Germany.
³³ German Cancer Consortium (DKTK), Heidelberg, Germany.
³⁴ German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁵ Department of Pharmacology and Toxicology and Medicine, Virginia Commonwealth University, Richmond, VA, USA.
³⁶ Massey Cancer Center, Virginia Commonwealth University, Richmond, VA, USA.
³⁷ Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN, USA.
³⁸ Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, USA.
³⁹ Department of Cell Biology, Harvard Medical School, Boston, MA, USA.
⁴⁰ Cell Death and Metabolism Unit, Center for Autophagy, Recycling and Disease, Danish Cancer Society Research Center, Copenhagen, Denmark.
⁴¹ Molecular Cancer Research Group, Institute of Medical Biology, University of Tromsø - The Arctic University of Norway, Tromsø, Norway.
⁴² Department of Anatomy, Cell and Developmental Biology, Eotvos Lorand University, Budapest, Hungary.
⁴³ Institute of Genetics, Biological Research Center of the Hungarian Academy of Sciences, Szeged, Hungary.
⁴⁴ Department of Radiation Oncology, Perlmutter Cancer Center, NYU Langone Medical Center, New York, NY, USA.
⁴⁵ Max F. Perutz Laboratories, Department of Biochemistry and Cell Biology, Vienna Biocenter, University of Vienna, Vienna, Austria.
⁴⁶ Signalling Programme, Babraham Institute, Cambridge, UK.
⁴⁷ Centre for Cancer Biology, University of South Australia, Adelaide, SA, Australia.
⁴⁸ Center for Autophagy Research, Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX, USA.
⁴⁹ Howard Hughes Medical Institute (HHMI), Dallas, TX, USA.
⁵⁰ Department de Bioquímica y Biología Molecular, Facultad de Medicina, Instituto Universitario de Oncología (IUOPA), Universidad de Oviedo, Oviedo, Spain.
⁵¹ Centro de Investigación en Red de Cáncer, Oviedo, Spain.
⁵² Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
⁵³ BioTechMed Graz, Graz, Austria.
⁵⁴ Immunity, Inflammation, and Disease Laboratory, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
⁵⁵ Department of Biology, Queens College, Queens, NY, USA.
⁵⁶ Graduate Center, City University of New York, New York, NY, USA.
⁵⁷ Department of Biochemistry and Molecular Biology, Graduate School and Faculty of Medicine, The University of Tokyo, Tokyo, Japan.
⁵⁸ Viral Immunobiology, Institute of Experimental Immunology, University of Zürich, Zurich, Switzerland.
⁵⁹ Novartis Institutes for BioMedical Research, Cambridge, MA, USA.
⁶⁰ Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Campus Vienna BioCentre, Vienna, Austria.
⁶¹ Department of Cell Biology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.
⁶² Department of Medical Genetics, Cambridge Institute for Medical Research, University of Cambridge, Cambridge, UK.
⁶³ Cancer Research UK Beatson Institute, Glasgow, UK.
⁶⁴ Department of Pathology, Albert Einstein College of Medicine, Bronx, NY, USA.
⁶⁵ Department of Biology, University of Padova, Padova, Italy.
⁶⁶ Venetian Institute of Molecular Medicine, Padova, Italy.
⁶⁷ Kennedy Institute of Rheumatology, University of Oxford, Oxford, UK.
⁶⁸ MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, UK.
⁶⁹ Institute of Pharmacology, University of Bern, Bern, Switzerland.
⁷⁰ Department of Molecular Medicine, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway.
⁷¹ Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece.
⁷² Department of Basic Sciences, Faculty of Medicine, University of Crete, Heraklion, Greece.
⁷³ Molecular Cell Biology of Autophagy Laboratory, The Francis Crick Institute, London, UK.
⁷⁴ Department of Genetics, Graduate School of Medicine, Osaka University, Osaka, Japan.
⁷⁵ Laboratory of Intracellular Membrane Dynamics, Graduate School of Frontier Biosciences Osaka University, Osaka, Japan.
⁷⁶ Ludwig Cancer Center, Harvard Medical School, Boston, MA, USA.
⁷⁷ Department of Neurology, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁷⁸ Department of Women's and Children's Health, Karolinska Institute, Karolinska University Hospital, Stockholm, Sweden.
⁷⁹ Pôle de Biologie, Hopitâl Européen George Pompidou, AP-HP, Paris, France.

PMID: 28596378
PMCID: PMC5494474
DOI: 10.15252/embj.201796697

Review

Molecular definitions of autophagy and related processes

Lorenzo Galluzzi et al. EMBO J. 2017.

. 2017 Jul 3;36(13):1811-1836.

doi: 10.15252/embj.201796697. Epub 2017 Jun 8.

Authors

Affiliations

¹ Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA deadoc@vodafone.it.
² Université Paris Descartes/Paris V, Paris, France.
³ Department of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, USA.
⁴ Telethon Institute of Genetics and Medicine (TIGEM), Pozzuoli, Italy.
⁵ Medical Genetics, Department of Pediatrics, Federico II University, Naples, Italy.
⁶ Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.
⁷ Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital, Houston, TX, USA.
⁸ Department of Cellular and Molecular Biology, Centro de Investigaciones Biológicas, CSIC, Madrid, Spain.
⁹ Université Pierre et Marie Curie/Paris VI, Paris, France.
¹⁰ Equipe 11 labellisée Ligue contre le Cancer, Centre de Recherche des Cordeliers, Paris, France.
¹¹ INSERM, U1138, Paris, France.
¹² Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute, Villejuif, France.
¹³ Department of Biology, University of Tor Vergata, Rome, Italy.
¹⁴ Unit of Cell Stress and Survival, Danish Cancer Society Research Center, Copenhagen, Denmark.
¹⁵ Department of Pediatric Hematology and Oncology, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
¹⁶ Division of Pulmonary and Critical Care Medicine, Joan and Sanford I. Weill Department of Medicine, Weill Cornell Medical College, New York, NY, USA.
¹⁷ Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
¹⁸ Institut Necker-Enfants Malades (INEM), Paris, France.
¹⁹ INSERM, U1151, Paris, France.
²⁰ CNRS, UMR8253, Paris, France.
²¹ Laboratorio de Biología Celular y Molecular, Instituto de Histología y Embriología (IHEM)-CONICET, Mendoza, Argentina.
²² Facultad de Ciencias Médicas, Universidad Nacional de Cuyo, Mendoza, Argentina.
²³ Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, Bronx, NY, USA.
²⁴ Department of Pathology, University of California San Francisco, San Francisco, CA, USA.
²⁵ Department of Molecular Genetics and Microbiology, University of New Mexico Health Sciences Center, Albuquerque, NM, USA.
²⁶ Institute of Biochemistry II, School of Medicine, Goethe University Frankfurt, Frankfurt, Germany.
²⁷ Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Frankfurt Main, Germany.
²⁸ Department of Immunology and Medical Genetics, University of Split School of Medicine, Split, Croatia.
²⁹ Department of Biosciences, University of Helsinki, Helsinki, Finland.
³⁰ National Institute for Infectious Diseases "L. Spallanzani" IRCCS, Rome, Italy.
³¹ Department of Biological and Environmental Sciences and Technologies (DiSTeBA), University of Salento, Lecce, Italy.
³² Institute for Experimental Cancer Research in Pediatrics, Goethe-University, Frankfurt, Germany.
³³ German Cancer Consortium (DKTK), Heidelberg, Germany.
³⁴ German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁵ Department of Pharmacology and Toxicology and Medicine, Virginia Commonwealth University, Richmond, VA, USA.
³⁶ Massey Cancer Center, Virginia Commonwealth University, Richmond, VA, USA.
³⁷ Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN, USA.
³⁸ Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, USA.
³⁹ Department of Cell Biology, Harvard Medical School, Boston, MA, USA.
⁴⁰ Cell Death and Metabolism Unit, Center for Autophagy, Recycling and Disease, Danish Cancer Society Research Center, Copenhagen, Denmark.
⁴¹ Molecular Cancer Research Group, Institute of Medical Biology, University of Tromsø - The Arctic University of Norway, Tromsø, Norway.
⁴² Department of Anatomy, Cell and Developmental Biology, Eotvos Lorand University, Budapest, Hungary.
⁴³ Institute of Genetics, Biological Research Center of the Hungarian Academy of Sciences, Szeged, Hungary.
⁴⁴ Department of Radiation Oncology, Perlmutter Cancer Center, NYU Langone Medical Center, New York, NY, USA.
⁴⁵ Max F. Perutz Laboratories, Department of Biochemistry and Cell Biology, Vienna Biocenter, University of Vienna, Vienna, Austria.
⁴⁶ Signalling Programme, Babraham Institute, Cambridge, UK.
⁴⁷ Centre for Cancer Biology, University of South Australia, Adelaide, SA, Australia.
⁴⁸ Center for Autophagy Research, Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX, USA.
⁴⁹ Howard Hughes Medical Institute (HHMI), Dallas, TX, USA.
⁵⁰ Department de Bioquímica y Biología Molecular, Facultad de Medicina, Instituto Universitario de Oncología (IUOPA), Universidad de Oviedo, Oviedo, Spain.
⁵¹ Centro de Investigación en Red de Cáncer, Oviedo, Spain.
⁵² Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
⁵³ BioTechMed Graz, Graz, Austria.
⁵⁴ Immunity, Inflammation, and Disease Laboratory, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
⁵⁵ Department of Biology, Queens College, Queens, NY, USA.
⁵⁶ Graduate Center, City University of New York, New York, NY, USA.
⁵⁷ Department of Biochemistry and Molecular Biology, Graduate School and Faculty of Medicine, The University of Tokyo, Tokyo, Japan.
⁵⁸ Viral Immunobiology, Institute of Experimental Immunology, University of Zürich, Zurich, Switzerland.
⁵⁹ Novartis Institutes for BioMedical Research, Cambridge, MA, USA.
⁶⁰ Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Campus Vienna BioCentre, Vienna, Austria.
⁶¹ Department of Cell Biology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.
⁶² Department of Medical Genetics, Cambridge Institute for Medical Research, University of Cambridge, Cambridge, UK.
⁶³ Cancer Research UK Beatson Institute, Glasgow, UK.
⁶⁴ Department of Pathology, Albert Einstein College of Medicine, Bronx, NY, USA.
⁶⁵ Department of Biology, University of Padova, Padova, Italy.
⁶⁶ Venetian Institute of Molecular Medicine, Padova, Italy.
⁶⁷ Kennedy Institute of Rheumatology, University of Oxford, Oxford, UK.
⁶⁸ MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, UK.
⁶⁹ Institute of Pharmacology, University of Bern, Bern, Switzerland.
⁷⁰ Department of Molecular Medicine, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway.
⁷¹ Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece.
⁷² Department of Basic Sciences, Faculty of Medicine, University of Crete, Heraklion, Greece.
⁷³ Molecular Cell Biology of Autophagy Laboratory, The Francis Crick Institute, London, UK.
⁷⁴ Department of Genetics, Graduate School of Medicine, Osaka University, Osaka, Japan.
⁷⁵ Laboratory of Intracellular Membrane Dynamics, Graduate School of Frontier Biosciences Osaka University, Osaka, Japan.
⁷⁶ Ludwig Cancer Center, Harvard Medical School, Boston, MA, USA.
⁷⁷ Department of Neurology, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁷⁸ Department of Women's and Children's Health, Karolinska Institute, Karolinska University Hospital, Stockholm, Sweden.
⁷⁹ Pôle de Biologie, Hopitâl Européen George Pompidou, AP-HP, Paris, France.

PMID: 28596378
PMCID: PMC5494474
DOI: 10.15252/embj.201796697

Abstract

Over the past two decades, the molecular machinery that underlies autophagic responses has been characterized with ever increasing precision in multiple model organisms. Moreover, it has become clear that autophagy and autophagy-related processes have profound implications for human pathophysiology. However, considerable confusion persists about the use of appropriate terms to indicate specific types of autophagy and some components of the autophagy machinery, which may have detrimental effects on the expansion of the field. Driven by the overt recognition of such a potential obstacle, a panel of leading experts in the field attempts here to define several autophagy-related terms based on specific biochemical features. The ultimate objective of this collaborative exchange is to formulate recommendations that facilitate the dissemination of knowledge within and outside the field of autophagy research.

Keywords: LC3‐associated phagocytosis; chaperone‐mediated autophagy; microautophagy; mitophagy; xenophagy.

PubMed Disclaimer

Figures

**Figure 1. Autophagy substrates**
A wide and heterogeneous set of cytoplasmic entities—be they of endogenous/intracellular or exogenous/extracellular origin—can be targeted to lysosomal degradation by non‐selective or selective forms of autophagy. ER, endoplasmic reticulum.

See this image and copyright information in PMC

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References

1. Agarraberes FA, Terlecky SR, Dice JF (1997) An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 137: 825–834 - PMC - PubMed
1. Al Rawi S, Louvet‐Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334: 1144–1147 - PubMed
1. Amaravadi R, Kimmelman AC, White E (2016) Recent insights into the function of autophagy in cancer. Genes Dev 30: 1913–1930 - PMC - PubMed
1. Amaya C, Fader CM, Colombo MI (2015) Autophagy and proteins involved in vesicular trafficking. FEBS Lett 589: 3343–3353 - PubMed
1. Antonioli M, Di Rienzo M, Piacentini M, Fimia GM (2016) Emerging mechanisms in initiating and terminating autophagy. Trends Biochem Sci 42: 28–41 - PubMed

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[1] Agarraberes FA, Terlecky SR, Dice JF (1997) An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 137: 825–834 - PMC - PubMed

[2] Agarraberes FA, Terlecky SR, Dice JF (1997) An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 137: 825–834 - PMC - PubMed

[3] Al Rawi S, Louvet‐Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334: 1144–1147 - PubMed

[4] Al Rawi S, Louvet‐Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334: 1144–1147 - PubMed

[5] Amaravadi R, Kimmelman AC, White E (2016) Recent insights into the function of autophagy in cancer. Genes Dev 30: 1913–1930 - PMC - PubMed

[6] Amaravadi R, Kimmelman AC, White E (2016) Recent insights into the function of autophagy in cancer. Genes Dev 30: 1913–1930 - PMC - PubMed

[7] Amaya C, Fader CM, Colombo MI (2015) Autophagy and proteins involved in vesicular trafficking. FEBS Lett 589: 3343–3353 - PubMed

[8] Amaya C, Fader CM, Colombo MI (2015) Autophagy and proteins involved in vesicular trafficking. FEBS Lett 589: 3343–3353 - PubMed

[9] Antonioli M, Di Rienzo M, Piacentini M, Fimia GM (2016) Emerging mechanisms in initiating and terminating autophagy. Trends Biochem Sci 42: 28–41 - PubMed

[10] Antonioli M, Di Rienzo M, Piacentini M, Fimia GM (2016) Emerging mechanisms in initiating and terminating autophagy. Trends Biochem Sci 42: 28–41 - PubMed

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Molecular definitions of autophagy and related processes

Affiliations

Molecular definitions of autophagy and related processes

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