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Review

Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes

Daniel J. Klionsky, Hagai Abeliovich, Patrizia Agostinis, Devendra K. Agrawal, Gjumrakch Aliev, David S. Askew, Misuzu Baba, Eric H. Baehrecke, Ben A. Bahr, Andrea Ballabio, Bruce A. Bamber, Diane C. Bassham, Ettore Bergamini, Xiaoning Bi, Martine Biard-Piechaczyk, Janice S. Blum, Dale E. Bredesen, Jeffrey L. Brodsky, John H. Brumell, Ulf T. Brunk, Wilfried Bursch, Nadine Camougrand, Eduardo Cebollero, Francesco Cecconi, Yingyu Chen, Lih-Shen Chin, Augustine Choi, Charleen T. Chu, Jongkyeong Chung, Robert S.B. Clark, Peter G.H. Clarke, Steven G. Clarke, Corinne Clave, John L. Cleveland, Patrice Codogno, María Isabel Colombo, Ana Coto-Montes, James M. Cregg, Ana Maria Cuervo, Jayanta Debnath, Patrick B. Dennis, Phillip A. Dennis, Francesca Demarchi, Vojo Deretic, Rodney J. Devenish, Federica Di Sano, J. Fred Dice, Clark W. Distelhorst, Savithramma P. Dinesh-Kumar, N. Tony Eissa, Marian DiFiglia, Mojgan Djavaheri-Mergny, Frank C. Dorsey, Wulf Dröge, Michel Dron, William A. Dunn, Jr., Michael Duszenko, Zvulun Elazar, Audrey Esclatine, Eeva-Liisa Eskelinen, László Fésüs, Kim D. Finley, José M. Fuentes, Juan Fueyo, Kozo Fujisaki, Brigitte Galliot, Fen-Biao Gao, David A. Gewirtz, Spencer B. Gibson, Antje Gohla, Alfred L. Goldberg, Ramon Gonzalez, Cristina González-Estévez, Sharon M. Gorski, Roberta A. Gottlieb, Dieter Häussinger, You-Wen He, Kim Heidenreich, Joseph A. Hill, Maria Høyer-Hansen, Xun Hu, Wei-Pang Huang, Akiko Iwasaki, Marja Jäättelä, William T. Jackson, Xuejun Jiang, Shengkan Jin, Terje Johansen, Jae U. Jung, Motoni Kadowaki, Chanhee Kang, Ameeta Kelekar, David H. Kessel, Jan A.K.W. Kiel, Hong Pyo Kim, Adi Kimchi, Timothy J. Kinsella, Kirill Kiselyov, Katsuhiko Kitamoto, Erwin Knecht, Masaaki Komatsu, Eiki Kominami, Seiji Kondo, Attila L. Kovács, Guido Kroemer, Chia-Yi Kuan, Rakesh Kumar, Mondira Kundu, Jacques Landry, Marianne Laporte, Weidong Le, Huan-Yao Lei, Beth Levine, Andrew Lieberman, Kah-Leong Lim, Fu-Cheng Lin, Willisa Liou, Leroy F. Liu, Gabriel Lopez-Berestein, Carlos López-Otín, Bo Lu, Kay F. Macleod, Walter Malorni, Wim Martinet, Ken Matsuoka, Josef Mautner, Alfred J. Meijer, Alicia Meléndez, Paul Michels, Giovanni Miotto, Wilhelm P. Mistiaen, Noboru Mizushima, Baharia Mograbi, Michael N. Moore, Paula I. Moreira, Yuji Moriyasu, Tomasz Motyl, Christian Münz, Leon O. Murphy, Naweed I. Naqvi, Thomas P. Neufeld, Ichizo Nishino, Ralph A. Nixon, Takeshi Noda, Bernd Nürnberg, Michinaga Ogawa, Nancy L. Oleinick, Laura J. Olsen, Bulent Ozpolat, Shoshana Paglin, Glen E. Palmer, Issidora S. Papassideri, Miles Parkes, David H. Perlmutter, George Perry, Mauro Piacentini, Ronit Pinkas-Kramarski, Mark Prescott, Tassula Proikas-Cezanne, Nina Raben, Abdelhaq Rami, Fulvio Reggiori, Bärbel Rohrer, David C. Rubinsztein, Kevin M. Ryan, Junichi Sadoshima, Hiroshi Sakagami, Yasuyoshi Sakai, Marco Sandri, Chihiro Sasakawa, Miklós Sass, Claudio Schneider, Per O. Seglen, Oleksandr Seleverstov, Jeffrey Settleman, John J. Shacka, Irving M. Shapiro, Andrei A. Sibirny, Elaine C.M. Silva-Zacarin, Hans-Uwe Simon, Cristiano Simone, Anne Simonsen, Mark A. Smith, Katharina Spanel-Borowski, Vickram Srinivas, Meredith Steeves, Harald Stenmark, Per E. Stromhaug, Carlos S. Subauste, Seiichiro Sugimoto, David Sulzer, Toshihiko Suzuki, Michele S. Swanson, Ira Tabas, Fumihiko Takeshita, Nicholas J. Talbot, Zsolt Tallóczy, Keiji Tanaka, Kozo Tanaka, Isei Tanida, Graham S. Taylor, J. Paul Taylor, Alexei Terman, Gianluca Tettamanti, Craig B. Thompson, Michael Thumm, Aviva M. Tolkovsky, Sharon A. Tooze, Ray Truant, Lesya V. Tumanovska, Yasuo Uchiyama, Takashi Ueno, Néstor L. Uzcátegui, Ida J. van der Klei, Eva C. Vaquero, Tibor Vellai, Michael W. Vogel, Hong-Gang Wang, Paul Webster, Zhijun Xi, Gutian Xiao, Joachim Yahalom, Jin-Ming Yang, George S. Yap, Xiao-Ming Yin, Tamotsu Yoshimori, Zhenyu Yue, Michisuke Yuzaki, Olga Zabirnyk, Xiaoxiang Zheng, Xiongwei Zhu and Russell L. Deter

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Authors

Daniel J. Klionsky

University of Michigan; Ann Arbor, MI USA

Hagai Abeliovich

Hebrew University

Patrizia Agostinis

Catholic University of Leuven

Devendra K. Agrawal

Creighton University School of Medicine

Gjumrakch Aliev

University of Texas at San Antonio

David S. Askew

University of Cincinati

Misuzu Baba

Eric H. Baehrecke

University of Massachusetts Medical School

Ben A. Bahr

University of Connecticut

Andrea Ballabio

Telethon Institute of Genetics and Medicine (TIGEM)

Bruce A. Bamber

University of Toledo

Diane C. Bassham

Iowa State University

Ettore Bergamini

Center for Research on Biology and Pathology of Aging

Xiaoning Bi

Western University of Health Sciences

Martine Biard-Piechaczyk

Centre d\'études d\'agents Pathogènes et Biotechnologies pour la Santé, CNRS UM1, UM2

Janice S. Blum

Indiana University School of Medicine

Dale E. Bredesen

Buck Institute for Age Research

Jeffrey L. Brodsky

University of Pittsburgh

John H. Brumell

Hospital for Sick Children

Ulf T. Brunk

Linköping University

Wilfried Bursch

Medical University of Vienna

Nadine Camougrand

Université de Bordeaux 2

Eduardo Cebollero

Instituto de Fermentaciones Industriales

Francesco Cecconi

University of Rome Tor Vergata

Yingyu Chen

Peking University

Lih-Shen Chin

Emory University School of Medicine

Augustine Choi

Brigham & Womens Hospital, Harvard Medical School

Charleen T. Chu

University of Pittsburgh

Jongkyeong Chung

Korea advanced institute of science and technology

Robert S.B. Clark

Safar Center for Resuscitation Research

Peter G.H. Clarke

Université de Lausanne

Steven G. Clarke

University of California, Los Angeles

Corinne Clave

University of California, Los Angeles

John L. Cleveland

The Scripps Research Institute

Patrice Codogno

35INSERM U756 and the Université Paris-Sud 11

María Isabel Colombo

Universidad Nacional de Cuyo

Ana Coto-Montes

Universidad de Oviedo

James M. Cregg

Keck Graduate Institute of Applied Sciences

Ana Maria Cuervo

Albert Einstein College of Medicine

Jayanta Debnath

University of California, San Francisco

Patrick B. Dennis

University of Cincinnati

Phillip A. Dennis

National Cancer Institute/Navy Medical Oncology

Francesca Demarchi

Laboratorio Nazionale Consorzio Interuniversitario Biotecnologie

Vojo Deretic

University of New Mexico Health Science Center

Rodney J. Devenish

Monash University

Federica Di Sano

University of Tor Vergata

J. Fred Dice

Tufts University

Clark W. Distelhorst

Case Western Reserve University and University Hospitals of Cleveland

Savithramma P. Dinesh-Kumar

Yale University

N. Tony Eissa

Baylor College of Medicine

Marian DiFiglia

Massachusetts General Hospital

Mojgan Djavaheri-Mergny

Université Paris-Sud 11

Frank C. Dorsey

The Scripps Research Institute

Wulf Dröge

Immunotec Research Ltd.

Michel Dron

INRA UR892

William A. Dunn, Jr.

University of Florida College of Medicine

Michael Duszenko

University of Tubingen

Zvulun Elazar

The Weizmann Institute of Science

Audrey Esclatine

Université Paris-Sud 11

Eeva-Liisa Eskelinen

University of Helsinki

László Fésüs

University of Debrecen

Kim D. Finley

The Salk Institute for Biological Studies

José M. Fuentes

Univeridad de Extremadura

Juan Fueyo

University of Texas MD Anderson Cancer Center

Kozo Fujisaki

Kagoshima University

Brigitte Galliot

University of Geneva

Fen-Biao Gao

The J. David Gladstone Institutes at University of California, San Francisco

David A. Gewirtz

Virginia Commonwealth University

Spencer B. Gibson

University of Manitoba

Antje Gohla

Heinrich-Heine-Universitaet

Alfred L. Goldberg

Harvard Medical School

Ramon Gonzalez

Instituto de Fermentaciones Industriales

Cristina González-Estévez

The University of Nottingham

Sharon M. Gorski

BC Cancer Agency

Roberta A. Gottlieb

San Diego State University

Dieter Häussinger

Heinrich Heine Universität

You-Wen He

Duke University Medical Center

Kim Heidenreich

University of Colorado Health Sciences Center

Joseph A. Hill

University of Texas Southwestern Medical Center

Maria Høyer-Hansen

Danish Cancer Society

Xun Hu

Zhejiang University School of Medicine

Wei-Pang Huang

National Taiwan University

Akiko Iwasaki

Yale University School of Medicine

Marja Jäättelä

Danish Cancer Society

William T. Jackson

Medical College of Wisconsin

Xuejun Jiang

Memorial Sloan-Kettering Cancer Center

Shengkan Jin

University of Medicine and Dentistry of New Jersey

Terje Johansen

University of Tromsø

Jae U. Jung

University of Southern California Keck Medical School

Motoni Kadowaki

Niigata University

Chanhee Kang

University of Texas Southwestern Medical Center

Ameeta Kelekar

University of Minnesota

David H. Kessel

Wayne State University School of Medicine

Jan A.K.W. Kiel

University of Groningen

Hong Pyo Kim

University of Pittsburgh Medical Center

Adi Kimchi

Weizmann Institute of Science

Timothy J. Kinsella

University Hospitals of Cleveland

Kirill Kiselyov

University of Pittsburgh

Katsuhiko Kitamoto

The University of Tokyo

Erwin Knecht

Centro de Investigación Princípe Felipe

Masaaki Komatsu

Tokyo Metropolitan Institute of Medical Science

Eiki Kominami

Juntendo University School of Medicine

Seiji Kondo

University of Texas MD Anderson Cancer Center

Attila L. Kovács

Eötvös Loránd University

Guido Kroemer

Institut Gustave Roussy and the Université Paris-Sud 11

Chia-Yi Kuan

Children’s Hospital Medical Center

Rakesh Kumar

University of Texas MD Anderson Cancer Center

Mondira Kundu

University of Pennsylvania School of Medicine

Jacques Landry

Laval Universtity

Marianne Laporte

Eastern Michigan University

Weidong Le

Chinese Academy of Sciences

Huan-Yao Lei

National Cheng Kung University

Beth Levine

University of Texas Southwestern Medical Center

Andrew Lieberman

University of Michigan Medical School

Kah-Leong Lim

National Neuroscience Institute

Fu-Cheng Lin

Biotechnology Institute; Huajiachi Campus of Zhejiang University; Kaixuan Road 268#; Hangzhou 310029, Zhejiang, China.

Willisa Liou

Chang Gung University

Leroy F. Liu

University of Medicine and Dentistry of New Jersey

Gabriel Lopez-Berestein

University of Texas MD Anderson Cancer Center

Carlos López-Otín

Universidad de Oviedo

Bo Lu

Vanderbilt University

Kay F. Macleod

University of Chicago

Walter Malorni

Istituto Superiore di Sanita

Wim Martinet

University of Antwerp

Ken Matsuoka

Kyushu University

Josef Mautner

GSF-National Research Center for Environment and Health

Alfred J. Meijer

Academic Medical Center

Alicia Meléndez

City University of New York

Paul Michels

Research Unit for Tropical Diseases, de Duve Institute, Université catholique de Louvain

Giovanni Miotto

University of Padua

Wilhelm P. Mistiaen

The University College of Antwerp

Noboru Mizushima

Tokyo Medical and Dental University

Baharia Mograbi

INSERM ERI 21, and the Laboratoire de Pathologie Clinique et Expérimentale

Michael N. Moore

Plymouth Marine Laboratory

Paula I. Moreira

Center for Neuroscience and Cell Biology

Yuji Moriyasu

Saitama University

Tomasz Motyl

Warsaw Agricultural University

Christian Münz

The Rockefeller University

Leon O. Murphy

Novartis Institutes for Biomedical Research Inc.

Naweed I. Naqvi

National University of Singapore

Thomas P. Neufeld

University of Minnesota

Ichizo Nishino

National Institute of Neuroscience

Ralph A. Nixon

New York University School of Medicine

Takeshi Noda

Osaka University

Bernd Nürnberg

Clinic for Dermatology, Venerology and Allergology, The Saarland University Hospital

Michinaga Ogawa

Tokyo Daigaku Seikyo, Ikaken Shisho

Nancy L. Oleinick

Case Western Reserve University

Laura J. Olsen

University of Michigan

Bulent Ozpolat

University of Texas MD Anderson Cancer Center

Shoshana Paglin

Memorial Sloan-Kettering Cancer Center

Glen E. Palmer

LSU School of Dentistry

Issidora S. Papassideri

University of Athens

Miles Parkes

Addenbrooke's NHS Trust

David H. Perlmutter

Childrens Hospital of Pittsburgh

George Perry

Case Western Reserve University

Mauro Piacentini

University of Rome Tor Vergata

Ronit Pinkas-Kramarski

Tel Aviv University

Mark Prescott

Monash University

Tassula Proikas-Cezanne

University of Tüebingen

Nina Raben

National Institutes of Health

Abdelhaq Rami

Klinikum der Johann Wolfgang von Goethe-Universität

Fulvio Reggiori

University Medical Centre Utrecht

Bärbel Rohrer

Medical University of South Carolina

David C. Rubinsztein

Cambridge Institute for Medical Research

Kevin M. Ryan

Beatson Institute for Cancer Research; Glasgow, UK

Junichi Sadoshima

University of Medicine and Dentistry of New Jersey

Hiroshi Sakagami

Meikai University School of Dentistry

Yasuyoshi Sakai

Kyoto University, Kyoto, Japan; CREST, Japan

Marco Sandri

University of Padova

Chihiro Sasakawa

University of Tokyo

Miklós Sass

Eötvös Loránd University

Claudio Schneider

Laboratorio Nazionale Consorzio Interuniversitario Biotecnologie

Per O. Seglen

The Norwegian Radium Hospital

Oleksandr Seleverstov

University of Wyoming, Department of Animal Science

Jeffrey Settleman

Massachusetts General Hospital Cancer Center

John J. Shacka

University of Alabama at Birmingham

Irving M. Shapiro

Thomas Jefferson University

Andrei A. Sibirny

National Academy of Sciences of Ukraine

Elaine C.M. Silva-Zacarin

Universidade Federal de São Carlos

Hans-Uwe Simon

University of Bern

Cristiano Simone

Consorzio Mario Negri Sud

Anne Simonsen

The Norwegian Radium Hospital

Mark A. Smith

Case Western Reserve University

Katharina Spanel-Borowski

University of Leipzig

Vickram Srinivas

Thomas Jefferson University

Meredith Steeves

The Scripps Research Institute

Harald Stenmark

The Norwegian Radium Hospital

Per E. Stromhaug

University of Missouri

Carlos S. Subauste

Case Western Reserve University

Seiichiro Sugimoto

National Hospital Organization, Miyazaki Higashi Hospital

David Sulzer

Columbia University

Toshihiko Suzuki

University of the Ryukyus

Michele S. Swanson

University of Michigan

Ira Tabas

Columbia University

Fumihiko Takeshita

Yokohama City University Graduate School of Medicine

Nicholas J. Talbot

University of Exeter

Zsolt Tallóczy

Columbia University

Keiji Tanaka

Tokyo Metropolitan Institute of Medical Science

Kozo Tanaka

Tohoku University

Isei Tanida

National Institute of Infectious Diseases

Graham S. Taylor

CRUK Institute for Cancer Studies, University of Birmingham

J. Paul Taylor

University of Pennsylvania School of Medicine

Alexei Terman

Linköping University

Gianluca Tettamanti

University of Insubria

Craig B. Thompson

University of Pennsylvania School of Medicine

Michael Thumm

Georg-August-Universitaet

Aviva M. Tolkovsky

University of Cambridge

Sharon A. Tooze

Cancer Research UK

Ray Truant

McMaster University

Lesya V. Tumanovska

Bogomoletz Institute of Physiology

Yasuo Uchiyama

Osaka University

Takashi Ueno

Department of Biochemistry, Juntendo University School of Medicne

Néstor L. Uzcátegui

Universidad Central de Venezuela

Ida J. van der Klei

University of Groningen

Eva C. Vaquero

Hospital Clínic

Tibor Vellai

Eötvös Loránd University

Michael W. Vogel

Maryland Psychiatric Research Center

Hong-Gang Wang

H. Lee Moffitt Cancer Center & Research Institute

Paul Webster

House Ear Institute

Zhijun Xi

Peking University First Hospital

Gutian Xiao

University of Pittsburgh Cancer Institute

Joachim Yahalom

Memorial Sloan-Kettering Cancer Center

Jin-Ming Yang

University of Medicine and Dentistry of New Jersey-Robert Wood Johnson Medical School

George S. Yap

University of Medicine and Dentistry of New Jersey-New Jersey Medical School

Xiao-Ming Yin

University of Pittsburgh

Tamotsu Yoshimori

Osaka University

Zhenyu Yue

Mount Sinai School of Medicine

Michisuke Yuzaki

Keio University School of Medicine

Olga Zabirnyk

National Institutes of Health

Xiaoxiang Zheng

Zhejiang University

Xiongwei Zhu

Case Western Reserve University

Russell L. Deter

Baylor College of Medicine

 Download PDF

If the document does not open, please right-click on the link (control-click on a Macintosh) and select the option to save the file to disk.