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

Research in autophagy continues to accelerate,(1) and as a result many new scientists are entering the field. Accordingly, it is important to establish a standard set of criteria for monitoring macroautophagy in different organisms. Recent reviews have described the range of assays that have been used for this purpose.(2,3) There are many useful and convenient methods that can be used to monitor macroautophagy in yeast, but relatively few in other model systems, and there is much confusion regarding acceptable methods to measure macroautophagy in higher eukaryotes. A key point that needs to be emphasized is that there is a difference between measurements that monitor the numbers of autophagosomes versus those that measure flux through the autophagy pathway; thus, a block in macroautophagy that results in autophagosome accumulation needs to be differentiated from fully functional autophagy that includes delivery to, and degradation within, lysosomes (in most higher eukaryotes) or the vacuole (in plants and fungi). Here, we present a set of guidelines for the selection and interpretation of the methods that can be used by investigators who are attempting to examine macroautophagy and related processes, as well as by reviewers who need to provide realistic and reasonable critiques of papers that investigate these processes. This set of guidelines is not meant to be a formulaic set of rules, because the appropriate assays depend in part on the question being asked and the system being used. In addition, we emphasize that no individual assay is guaranteed to be the most appropriate one in every situation, and we strongly recommend the use of multiple assays to verify an autophagic response.

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

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