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In 2008 we published the first set of guidelines for standardizing research in autophagy. Since then, research on this topic has continued to accelerate, and many new scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Accordingly, it is important to update these guidelines for monitoring autophagy in different organisms. Various reviews have described the range of assays that have been used for this purpose. Nevertheless, there continues to be confusion regarding acceptable methods to measure autophagy, especially in multicellular eukaryotes. For example, a key point that needs to be emphasized is that there is a difference between measurements that monitor the numbers or volume of autophagic elements (e.g., autophagosomes or autolysosomes) at any stage of the autophagic process versus those that measure fl ux through the autophagy pathway (i.e., the complete process including the amount and rate of cargo sequestered and degraded). In particular, a block in macroautophagy that results in autophagosome accumulation must be differentiated from stimuli that increase autophagic activity, defi ned as increased autophagy induction coupled with increased delivery to, and degradation within, lysosomes (inmost higher eukaryotes and some protists such as Dictyostelium ) or the vacuole (in plants and fungi). In other words, it is especially important that investigators new to the fi eld understand that the appearance of more autophagosomes does not necessarily equate with more autophagy. In fact, in many cases, autophagosomes accumulate because of a block in trafficking to lysosomes without a concomitant change in autophagosome biogenesis, whereas an increase in autolysosomes may reflect a reduction in degradative activity. It is worth emphasizing here that lysosomal digestion is a stage of autophagy and evaluating its competence is a crucial part of the evaluation of autophagic flux, or complete autophagy. Here, we present a set of guidelines for the selection and interpretation of methods for use by investigators who aim to examine macroautophagy and related processes, as well as for reviewers who need to provide realistic and reasonable critiques of papers that are focused on these processes. These guidelines are 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 monitor autophagy. Along these lines, because of the potential for pleiotropic effects due to blocking autophagy through genetic manipulation it is imperative to delete or knock down more than one autophagy-related gene. In addition, some individual Atg proteins, or groups of proteins, are involved in other cellular pathways so not all Atg proteins can be used as a specific marker for an autophagic process. In these guidelines, we consider these various methods of assessing autophagy and what information can, or cannot, be obtained from them. Finally, by discussing the merits and limits of particular autophagy assays, we hope to encourage technical innovation in the field.
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
Daniel J. Klionsky;Kotb Abdelmohsen;Akihisa Abe;Md Joynal Abedin;Hagai Abeliovich;Abraham Acevedo Arozena;Hiroaki Adachi;Christopher M. Adams;Peter D. Adams;Khosrow Adeli;Peter J. Adhihetty;Sharon G. Adler;Galila Agam;Rajesh Agarwal;Manish K. Aghi;Maria Agnello;Patrizia Agostinis;Patricia V. Aguilar;Julio Aguirre Ghiso;Edoardo M. Airoldi;Slimane Ait Si Ali;Takahiko Akematsu;Emmanuel T. Akporiaye;Mohamed Al Rubeai;Guillermo M. Albaiceta;Chris Albanese;Diego Albani;Matthew L. Albert;Jesus Aldudo;Hana Algül;Mehrdad Alirezaei;Iraide Alloza;Alexandru Almasan;Maylin Almonte Beceril;Emad S. Alnemri;Covadonga Alonso;Nihal Altan Bonnet;Dario C. Altieri;Silvia Alvarez;Lydia Alvarez Erviti;Sandro Alves;Giuseppina Amadoro;Atsuo Amano;Consuelo Amantini;Santiago Ambrosio;Ivano Amelio;Amal O. Amer;Mohamed Amessou;Angelika Amon;Zhenyi An;Frank A. Anania;Stig U. Andersen;Usha P. Andley;Catherine K. Andreadi;Nathalie Andrieu Abadie;Alberto Anel;David K. Ann;Shailendra Anoopkumar Dukie;Manuela Antonioli;Hiroshi Aoki;Nadezda Apostolova;Saveria Aquila;Katia Aquilano;Koichi Araki;Eli Arama;Agustin Aranda;Jun Araya;Alexandre Arcaro;Esperanza Arias;Hirokazu Arimoto;Aileen R. Ariosa;Jane L. Armstrong;Thierry Arnould;Ivica Arsov;Katsuhiko Asanuma;Valerie Askanas;Eric Asselin;Ryuichiro Atarashi;Sally S. Atherton;Julie D. Atkin;Laura D. Attardi;Patrick Auberger;Georg Auburger;Laure Aurelian;Riccardo Autelli;Laura Avagliano;Maria Laura Avantaggiati;Limor Avrahami;Suresh Awale;Neelam Azad;Tiziana Bachetti;Jonathan M. Backer;Dong Hun Bae;Jae sung Bae;Ok Nam Bae;Soo Han Bae;Eric H. Baehrecke;Seung Hoon Baek;Stephen Baghdiguian;Agnieszka BagniewskaZadworna;Hua Bai;Jie Bai;Xue Yuan Bai;Yannick Bailly;Kithiganahalli Narayanaswamy Balaji;Walter Balduini;Andrea Ballabio;Rena Balzan;Rajkumar Banerjee;Gábor Bánhegyi;Haijun Bao;Benoit Barbeau;Maria D. Barrachina;Esther Barreiro;Bonnie Bartel;Alberto Bartolomé;Diane C. Bassham;Maria Teresa Bassi;Robert C. 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Wang;Shuo Wang;Ting Fang Wang;Xian Wang;Xiao jia Wang;Xiao Wei Wang;Xin Wang;Xuejun Wang;Yan Wang;Yanming Wang;Ying Wang;Ying Jan Wang;Yipeng Wang;Yu Wang;Yu Tian Wang;Yuqing Wang;Zhi Nong Wang;Pablo Wappner;Carl Ward;Diane McVey Ward;Gary Warnes;Hirotaka Watada;Yoshihisa Watanabe;Kei Watase;Timothy E. Weaver;Colin D. Weekes;Jiwu Wei;Thomas Weide;Conrad C. Weihl;Günther Weindl;Simone Nardin Weis;Longping Wen;Xin Wen;Yunfei Wen;Benedikt Westermann;Cornelia M. Weyand;Anthony R. White;Eileen White;J. Lindsay Whitton;Alexander J. Whitworth;Joëlle Wiels;Franziska Wild;Manon E. Wildenberg;Tom Wileman;Deepti Srinivas Wilkinson;Simon Wilkinson;Dieter Willbold;