International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis

Xin Chen; Andrey S. Tsvetkov; Han Ming Shen; Ciro Isidoro; Nicholas T. Ktistakis; Andreas Linkermann; Werner J.H. Koopman; Hans Uwe Simon; Lorenzo Galluzzi; Shouqing Luo; Daqian Xu; Wei Gu; Olivier Peulen; Qian Cai; David C. Rubinsztein; Jen Tsan Chi; Donna D. Zhang; Changfeng Li; Shinya Toyokuni; Jinbao Liu; Jong Lyel Roh; Enyong Dai; Gabor Juhasz; Wei Liu; Jianhua Zhang; Minghua Yang; Jiao Liu; Ling Qiang Zhu; Weiping Zou; Mauro Piacentini; Wen Xing Ding; Zhenyu Yue; Yangchun Xie; Morten Petersen; David A. Gewirtz; Michael A. Mandell; Charleen T. Chu; Debasish Sinha; Eftekhar Eftekharpour; Boris Zhivotovsky; Sébastien Besteiro; Dmitry I. Gabrilovich; Do Hyung Kim; Valerian E. Kagan; Hülya Bayir; Guang Chao Chen; Scott Ayton; Jan D. Lünemann; Masaaki Komatsu; Stefan Krautwald; Ben Loos; Eric H. Baehrecke; Jiayi Wang; Jon D. Lane; Junichi Sadoshima; Wan Seok Yang; Minghui Gao; Christian Münz; Michael Thumm; Martin Kampmann; Di Yu; Marta M. Lipinski; Jace W. Jones; Xuejun Jiang; Herbert J. Zeh; Rui Kang; Daniel J. Klionsky; Guido Kroemer; Daolin Tang

doi:10.1080/15548627.2024.2319901

International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis

Xin Chen
, Andrey S. Tsvetkov
, Han Ming Shen
, Ciro Isidoro
, Nicholas T. Ktistakis
, Andreas Linkermann
, Werner J.H. Koopman
, Hans Uwe Simon
, Lorenzo Galluzzi
, Shouqing Luo
, Daqian Xu
, Wei Gu
, Olivier Peulen
, Qian Cai
, David C. Rubinsztein
, Jen Tsan Chi
, Donna D. Zhang
, Changfeng Li
, Shinya Toyokuni
, Jinbao Liu

Jong Lyel Roh, Enyong Dai, Gabor Juhasz, Wei Liu, Jianhua Zhang, Minghua Yang, Jiao Liu, Ling Qiang Zhu, Weiping Zou, Mauro Piacentini, Wen Xing Ding, Zhenyu Yue, Yangchun Xie, Morten Petersen, David A. Gewirtz, Michael A. Mandell, Charleen T. Chu, Debasish Sinha, Eftekhar Eftekharpour, Boris Zhivotovsky, Sébastien Besteiro, Dmitry I. Gabrilovich, Do Hyung Kim, Valerian E. Kagan, Hülya Bayir, Guang Chao Chen, Scott Ayton, Jan D. Lünemann, Masaaki Komatsu, Stefan Krautwald, Ben Loos, Eric H. Baehrecke, Jiayi Wang, Jon D. Lane, Junichi Sadoshima, Wan Seok Yang, Minghui Gao, Christian Münz, Michael Thumm, Martin Kampmann, Di Yu, Marta M. Lipinski, Jace W. Jones, Xuejun Jiang, Herbert J. Zeh, Rui Kang, Daniel J. Klionsky, Guido Kroemer, Daolin Tang

Guangzhou Medical College
University of Texas Health Science Center at Houston
Faculty of Health Sciences
University of Macau
University of Eastern Piedmont
University of Piemonte Orientale, Novara, Italy
Babraham Institute
Cambridge
Technische Universität Dresden
Yeshiva University
Radboud University Nijmegen
Wageningen University & Research
University of Bern
Brandenburg Medical School Theodor Fontane
Cornell University
University of Plymouth
Zhejiang University
Columbia University
University of Liege
Rutgers - The State University of New Jersey, New Brunswick
University of Cambridge
Duke University
University of Arizona
Jilin University
Nagoya University
CHA University
Szeged Biological Research Centre
Eotvos Lorand University
Second Military Medical University
University of Alabama at Birmingham
Central South University
Hunan Clinical Research Center of Pediatric Cancer
Huazhong University of Science and Technology
University of Michigan, Ann Arbor
University of Rome Tor Vergata
IRCCS Istituto per le Malattie Infettive Lazzaro Spallanzani - Roma
University of Kansas
Icahn School of Medicine at Mount Sinai
University of Copenhagen
Virginia Commonwealth University
University of New Mexico
University of Pittsburgh
University of Manitoba
Metabolomics and Cell Biology Platforms
Karolinska Institutet
Lomonosov Moscow State University
RAS - Engelhardt Institute of Molecular Biology
Université de Montpellier
Assistance publique – Hôpitaux de Paris
AstraZeneca
University of Minnesota Twin Cities
Academia Sinica - Institute of Biological Chemistry
University of Melbourne
University of Münster
Juntendo University
Kiel University
Stellenbosch University
University of Massachusetts Medical School
Shanghai Jiao Tong University
University of Bristol
Rutgers - The State University of New Jersey, Newark
St. John's University
Harbin Institute of Technology
University of Zurich
University of Göttingen
University of California at San Francisco
University of Queensland
University of Maryland
Memorial Sloan-Kettering Cancer Center
University of Texas Southwestern Medical Center
Centre de Recherche des Cordeliers

Research output: Contribution to journal › Review article › peer-review

193 Scopus citations

Abstract

Macroautophagy/autophagy is a complex degradation process with a dual role in cell death that is influenced by the cell types that are involved and the stressors they are exposed to. Ferroptosis is an iron-dependent oxidative form of cell death characterized by unrestricted lipid peroxidation in the context of heterogeneous and plastic mechanisms. Recent studies have shed light on the involvement of specific types of autophagy (e.g. ferritinophagy, lipophagy, and clockophagy) in initiating or executing ferroptotic cell death through the selective degradation of anti-injury proteins or organelles. Conversely, other forms of selective autophagy (e.g. reticulophagy and lysophagy) enhance the cellular defense against ferroptotic damage. Dysregulated autophagy-dependent ferroptosis has implications for a diverse range of pathological conditions. This review aims to present an updated definition of autophagy-dependent ferroptosis, discuss influential substrates and receptors, outline experimental methods, and propose guidelines for interpreting the results. Abbreviation: 3-MA:3-methyladenine; 4HNE: 4-hydroxynonenal; ACD: accidentalcell death; ADF: autophagy-dependentferroptosis; ARE: antioxidant response element; BH2:dihydrobiopterin; BH4: tetrahydrobiopterin; BMDMs: bonemarrow-derived macrophages; CMA: chaperone-mediated autophagy; CQ:chloroquine; DAMPs: danger/damage-associated molecular patterns; EMT,epithelial-mesenchymal transition; EPR: electronparamagnetic resonance; ER, endoplasmic reticulum; FRET: Försterresonance energy transfer; GFP: green fluorescent protein;GSH: glutathione;IF: immunofluorescence; IHC: immunohistochemistry; IOP, intraocularpressure; IRI: ischemia-reperfusion injury; LAA: linoleamide alkyne;MDA: malondialdehyde; PGSK: Phen Green™ SK;RCD: regulatedcell death; PUFAs: polyunsaturated fatty acids; RFP: red fluorescentprotein;ROS: reactive oxygen species; TBA: thiobarbituricacid; TBARS: thiobarbituric acid reactive substances; TEM:transmission electron microscopy.

Original language	English
Pages (from-to)	1213-1246
Number of pages	34
Journal	Autophagy
Volume	20
Issue number	6
DOIs	https://doi.org/10.1080/15548627.2024.2319901
State	Published - Jun 2024
Externally published	Yes

Keywords

Animals
Autophagy/physiology
Consensus
Ferroptosis/physiology
Humans

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10.1080/15548627.2024.2319901

Cite this

Chen, X., Tsvetkov, A. S., Shen, H. M., Isidoro, C., Ktistakis, N. T., Linkermann, A., Koopman, W. J. H., Simon, H. U., Galluzzi, L., Luo, S., Xu, D., Gu, W., Peulen, O., Cai, Q., Rubinsztein, D. C., Chi, J. T., Zhang, D. D., Li, C., Toyokuni, S., ... Tang, D. (2024). International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis. Autophagy, 20(6), 1213-1246. https://doi.org/10.1080/15548627.2024.2319901

@article{031bfe354bd64672b27148235bc90549,

title = "International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis",

abstract = "Macroautophagy/autophagy is a complex degradation process with a dual role in cell death that is influenced by the cell types that are involved and the stressors they are exposed to. Ferroptosis is an iron-dependent oxidative form of cell death characterized by unrestricted lipid peroxidation in the context of heterogeneous and plastic mechanisms. Recent studies have shed light on the involvement of specific types of autophagy (e.g. ferritinophagy, lipophagy, and clockophagy) in initiating or executing ferroptotic cell death through the selective degradation of anti-injury proteins or organelles. Conversely, other forms of selective autophagy (e.g. reticulophagy and lysophagy) enhance the cellular defense against ferroptotic damage. Dysregulated autophagy-dependent ferroptosis has implications for a diverse range of pathological conditions. This review aims to present an updated definition of autophagy-dependent ferroptosis, discuss influential substrates and receptors, outline experimental methods, and propose guidelines for interpreting the results. Abbreviation: 3-MA:3-methyladenine; 4HNE: 4-hydroxynonenal; ACD: accidentalcell death; ADF: autophagy-dependentferroptosis; ARE: antioxidant response element; BH2:dihydrobiopterin; BH4: tetrahydrobiopterin; BMDMs: bonemarrow-derived macrophages; CMA: chaperone-mediated autophagy; CQ:chloroquine; DAMPs: danger/damage-associated molecular patterns; EMT,epithelial-mesenchymal transition; EPR: electronparamagnetic resonance; ER, endoplasmic reticulum; FRET: F{\"o}rsterresonance energy transfer; GFP: green fluorescent protein;GSH: glutathione;IF: immunofluorescence; IHC: immunohistochemistry; IOP, intraocularpressure; IRI: ischemia-reperfusion injury; LAA: linoleamide alkyne;MDA: malondialdehyde; PGSK: Phen Green{\texttrademark} SK;RCD: regulatedcell death; PUFAs: polyunsaturated fatty acids; RFP: red fluorescentprotein;ROS: reactive oxygen species; TBA: thiobarbituricacid; TBARS: thiobarbituric acid reactive substances; TEM:transmission electron microscopy.",

keywords = "Animals, Autophagy/physiology, Consensus, Ferroptosis/physiology, Humans",

author = "Xin Chen and Tsvetkov, \{Andrey S.\} and Shen, \{Han Ming\} and Ciro Isidoro and Ktistakis, \{Nicholas T.\} and Andreas Linkermann and Koopman, \{Werner J.H.\} and Simon, \{Hans Uwe\} and Lorenzo Galluzzi and Shouqing Luo and Daqian Xu and Wei Gu and Olivier Peulen and Qian Cai and Rubinsztein, \{David C.\} and Chi, \{Jen Tsan\} and Zhang, \{Donna D.\} and Changfeng Li and Shinya Toyokuni and Jinbao Liu and Roh, \{Jong Lyel\} and Enyong Dai and Gabor Juhasz and Wei Liu and Jianhua Zhang and Minghua Yang and Jiao Liu and Zhu, \{Ling Qiang\} and Weiping Zou and Mauro Piacentini and Ding, \{Wen Xing\} and Zhenyu Yue and Yangchun Xie and Morten Petersen and Gewirtz, \{David A.\} and Mandell, \{Michael A.\} and Chu, \{Charleen T.\} and Debasish Sinha and Eftekhar Eftekharpour and Boris Zhivotovsky and S{\'e}bastien Besteiro and Gabrilovich, \{Dmitry I.\} and Kim, \{Do Hyung\} and Kagan, \{Valerian E.\} and H{\"u}lya Bayir and Chen, \{Guang Chao\} and Scott Ayton and L{\"u}nemann, \{Jan D.\} and Masaaki Komatsu and Stefan Krautwald and Ben Loos and Baehrecke, \{Eric H.\} and Jiayi Wang and Lane, \{Jon D.\} and Junichi Sadoshima and Yang, \{Wan Seok\} and Minghui Gao and Christian M{\"u}nz and Michael Thumm and Martin Kampmann and Di Yu and Lipinski, \{Marta M.\} and Jones, \{Jace W.\} and Xuejun Jiang and Zeh, \{Herbert J.\} and Rui Kang and Klionsky, \{Daniel J.\} and Guido Kroemer and Daolin Tang",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s). Published by Informa UK Limited, trading as Taylor \& Francis Group.",

year = "2024",

month = jun,

doi = "10.1080/15548627.2024.2319901",

language = "English",

volume = "20",

pages = "1213--1246",

journal = "Autophagy",

issn = "1554-8627",

publisher = "Taylor and Francis Ltd.",

number = "6",

}

Chen, X, Tsvetkov, AS, Shen, HM, Isidoro, C, Ktistakis, NT, Linkermann, A, Koopman, WJH, Simon, HU, Galluzzi, L, Luo, S, Xu, D, Gu, W, Peulen, O, Cai, Q, Rubinsztein, DC, Chi, JT, Zhang, DD, Li, C, Toyokuni, S, Liu, J, Roh, JL, Dai, E, Juhasz, G, Liu, W, Zhang, J, Yang, M, Liu, J, Zhu, LQ, Zou, W, Piacentini, M, Ding, WX, Yue, Z, Xie, Y, Petersen, M, Gewirtz, DA, Mandell, MA, Chu, CT, Sinha, D, Eftekharpour, E, Zhivotovsky, B, Besteiro, S, Gabrilovich, DI, Kim, DH, Kagan, VE, Bayir, H, Chen, GC, Ayton, S, Lünemann, JD, Komatsu, M, Krautwald, S, Loos, B, Baehrecke, EH, Wang, J, Lane, JD, Sadoshima, J, Yang, WS, Gao, M, Münz, C, Thumm, M, Kampmann, M, Yu, D, Lipinski, MM, Jones, JW, Jiang, X, Zeh, HJ, Kang, R, Klionsky, DJ, Kroemer, G & Tang, D 2024, 'International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis', Autophagy, vol. 20, no. 6, pp. 1213-1246. https://doi.org/10.1080/15548627.2024.2319901

TY - JOUR

T1 - International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis

AU - Chen, Xin

AU - Tsvetkov, Andrey S.

AU - Shen, Han Ming

AU - Isidoro, Ciro

AU - Ktistakis, Nicholas T.

AU - Linkermann, Andreas

AU - Koopman, Werner J.H.

AU - Simon, Hans Uwe

AU - Galluzzi, Lorenzo

AU - Luo, Shouqing

AU - Xu, Daqian

AU - Gu, Wei

AU - Peulen, Olivier

AU - Cai, Qian

AU - Rubinsztein, David C.

AU - Chi, Jen Tsan

AU - Zhang, Donna D.

AU - Li, Changfeng

AU - Toyokuni, Shinya

AU - Liu, Jinbao

AU - Roh, Jong Lyel

AU - Dai, Enyong

AU - Juhasz, Gabor

AU - Liu, Wei

AU - Zhang, Jianhua

AU - Yang, Minghua

AU - Liu, Jiao

AU - Zhu, Ling Qiang

AU - Zou, Weiping

AU - Piacentini, Mauro

AU - Ding, Wen Xing

AU - Yue, Zhenyu

AU - Xie, Yangchun

AU - Petersen, Morten

AU - Gewirtz, David A.

AU - Mandell, Michael A.

AU - Chu, Charleen T.

AU - Sinha, Debasish

AU - Eftekharpour, Eftekhar

AU - Zhivotovsky, Boris

AU - Besteiro, Sébastien

AU - Gabrilovich, Dmitry I.

AU - Kim, Do Hyung

AU - Kagan, Valerian E.

AU - Bayir, Hülya

AU - Chen, Guang Chao

AU - Ayton, Scott

AU - Lünemann, Jan D.

AU - Komatsu, Masaaki

AU - Krautwald, Stefan

AU - Loos, Ben

AU - Baehrecke, Eric H.

AU - Wang, Jiayi

AU - Lane, Jon D.

AU - Sadoshima, Junichi

AU - Yang, Wan Seok

AU - Gao, Minghui

AU - Münz, Christian

AU - Thumm, Michael

AU - Kampmann, Martin

AU - Yu, Di

AU - Lipinski, Marta M.

AU - Jones, Jace W.

AU - Jiang, Xuejun

AU - Zeh, Herbert J.

AU - Kang, Rui

AU - Klionsky, Daniel J.

AU - Kroemer, Guido

AU - Tang, Daolin

PY - 2024/6

Y1 - 2024/6

N2 - Macroautophagy/autophagy is a complex degradation process with a dual role in cell death that is influenced by the cell types that are involved and the stressors they are exposed to. Ferroptosis is an iron-dependent oxidative form of cell death characterized by unrestricted lipid peroxidation in the context of heterogeneous and plastic mechanisms. Recent studies have shed light on the involvement of specific types of autophagy (e.g. ferritinophagy, lipophagy, and clockophagy) in initiating or executing ferroptotic cell death through the selective degradation of anti-injury proteins or organelles. Conversely, other forms of selective autophagy (e.g. reticulophagy and lysophagy) enhance the cellular defense against ferroptotic damage. Dysregulated autophagy-dependent ferroptosis has implications for a diverse range of pathological conditions. This review aims to present an updated definition of autophagy-dependent ferroptosis, discuss influential substrates and receptors, outline experimental methods, and propose guidelines for interpreting the results. Abbreviation: 3-MA:3-methyladenine; 4HNE: 4-hydroxynonenal; ACD: accidentalcell death; ADF: autophagy-dependentferroptosis; ARE: antioxidant response element; BH2:dihydrobiopterin; BH4: tetrahydrobiopterin; BMDMs: bonemarrow-derived macrophages; CMA: chaperone-mediated autophagy; CQ:chloroquine; DAMPs: danger/damage-associated molecular patterns; EMT,epithelial-mesenchymal transition; EPR: electronparamagnetic resonance; ER, endoplasmic reticulum; FRET: Försterresonance energy transfer; GFP: green fluorescent protein;GSH: glutathione;IF: immunofluorescence; IHC: immunohistochemistry; IOP, intraocularpressure; IRI: ischemia-reperfusion injury; LAA: linoleamide alkyne;MDA: malondialdehyde; PGSK: Phen Green™ SK;RCD: regulatedcell death; PUFAs: polyunsaturated fatty acids; RFP: red fluorescentprotein;ROS: reactive oxygen species; TBA: thiobarbituricacid; TBARS: thiobarbituric acid reactive substances; TEM:transmission electron microscopy.

AB - Macroautophagy/autophagy is a complex degradation process with a dual role in cell death that is influenced by the cell types that are involved and the stressors they are exposed to. Ferroptosis is an iron-dependent oxidative form of cell death characterized by unrestricted lipid peroxidation in the context of heterogeneous and plastic mechanisms. Recent studies have shed light on the involvement of specific types of autophagy (e.g. ferritinophagy, lipophagy, and clockophagy) in initiating or executing ferroptotic cell death through the selective degradation of anti-injury proteins or organelles. Conversely, other forms of selective autophagy (e.g. reticulophagy and lysophagy) enhance the cellular defense against ferroptotic damage. Dysregulated autophagy-dependent ferroptosis has implications for a diverse range of pathological conditions. This review aims to present an updated definition of autophagy-dependent ferroptosis, discuss influential substrates and receptors, outline experimental methods, and propose guidelines for interpreting the results. Abbreviation: 3-MA:3-methyladenine; 4HNE: 4-hydroxynonenal; ACD: accidentalcell death; ADF: autophagy-dependentferroptosis; ARE: antioxidant response element; BH2:dihydrobiopterin; BH4: tetrahydrobiopterin; BMDMs: bonemarrow-derived macrophages; CMA: chaperone-mediated autophagy; CQ:chloroquine; DAMPs: danger/damage-associated molecular patterns; EMT,epithelial-mesenchymal transition; EPR: electronparamagnetic resonance; ER, endoplasmic reticulum; FRET: Försterresonance energy transfer; GFP: green fluorescent protein;GSH: glutathione;IF: immunofluorescence; IHC: immunohistochemistry; IOP, intraocularpressure; IRI: ischemia-reperfusion injury; LAA: linoleamide alkyne;MDA: malondialdehyde; PGSK: Phen Green™ SK;RCD: regulatedcell death; PUFAs: polyunsaturated fatty acids; RFP: red fluorescentprotein;ROS: reactive oxygen species; TBA: thiobarbituricacid; TBARS: thiobarbituric acid reactive substances; TEM:transmission electron microscopy.

KW - Animals

KW - Autophagy/physiology

KW - Consensus

KW - Ferroptosis/physiology

KW - Humans

UR - https://www.scopus.com/pages/publications/85189958829

U2 - 10.1080/15548627.2024.2319901

DO - 10.1080/15548627.2024.2319901

M3 - Review article

C2 - 38442890

AN - SCOPUS:85189958829

SN - 1554-8627

VL - 20

SP - 1213

EP - 1246

JO - Autophagy

JF - Autophagy

IS - 6

ER -

International consensus guidelines for the definition, detection, and interpretation of autophagy-dependent ferroptosis

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Keywords

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