Guidelines for the use and interpretation of assays for monitoring autophagy

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Bibtex

@article{1941550cfa31428d964695702963e4f6,
title = "Guidelines for the use and interpretation of assays for monitoring autophagy",
abstract = "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. 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 vs. those that measure flux through the autophagy pathway (i.e., the complete process); thus, a block in macroautophagy that results in autophagosome accumulation needs to be differentiated from stimuli that result in increased autophagic activity, defined as increased autophagy induction coupled with increased delivery to, and degradation within, lysosomes (in most 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 field 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. 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. 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.",
keywords = "autolysosome, autophagosome, flux, LC3, lysosome, phagophore, stress, vacuole",
author = "Klionsky, {Daniel J.} and Abdalla, {Fabio C.} and Hagai Abeliovich and Abraham, {Robert T.} and Abraham Acevedo-Arozena and Khosrow Adeli and Lotta Agholme and Maria Agnello and Patrizia Agostinis and Aguirre-Ghiso, {Julio A.} and Ahn, {Hyung Jun} and Ouardia Ait-Mohamed and Slimane Ait-Si-Ali and Takahiko Akematsu and Shizuo Akira and Al-Younes, {Hesham M.} and Al-Zeer, {Munir A.} and Albert, {Matthew L.} and Albin, {Roger L.} and Javier Alegre-Abarrategui and Aleo, {Maria Francesca} and Mehrdad Alirezaei and Alexandru Almasan and Maylin Almonte-Becerril and Atsuo Amano and Ravi Amaravadi and Shoba Amarnath and Amer, {Amal O.} and Nathalie Andrieu-Abadie and Vellareddy Anantharam and Ann, {David K.} and Shailendra Anoopkumar-Dukie and Hiroshi Aoki and Nadezda Apostolova and Giuseppe Arancia and Aris, {John P.} and Katsuhiko Asanuma and Asare, {Nana Y. O.} and Hisashi Ashida and Valerie Askanas and Askew, {David S.} and Patrick Auberger and Misuzu Baba and Backues, {Steven K.} and Baehrecke, {Eric H.} and Bahr, {Ben A.} and Xue-Yuan Bai and Yannick Bailly and Robert Baiocchi and Giulia Baldini and Walter Balduini and Andrea Ballabio and Bamber, {Bruce A.} and Bampton, {Edward T. W.} and Gabor Banhegyi and Bartholomew, {Clinton R.} and Bassham, {Diane C.} and Bast, {Robert C.} and Henri Batoko and Boon-Huat Bay and Isabelle Beau and Bechet, {Daniel M.} and Begley, {Thomas J.} and Christian Behl and Christian Behrends and Soumeya Bekri and Bryan Bellaire and Bendall, {Linda J.} and Luca Benetti and Laura Berliocchi and Henri Bernardi and Francesca Bernassola and Sebastien Besteiro and Ingrid Bhatia-Kissova and Xiaoning Bi and Martine Biard-Piechaczyk and Blum, {Janice S.} and Boise, {Lawrence H.} and Paolo Bonaldo and Boone, {David L.} and Bornhauser, {Beat C.} and Bortoluci, {Karina R.} and Ioannis Bossis and Frederic Bost and Jean-Pierre Bourquin and Patricia Boya and Michael Boyer-Guittaut and Bozhkov, {Peter V.} and Brady, {Nathan R.} and Claudio Brancolini and Andreas Brech and Brenman, {Jay E.} and Ana Brennand and Bresnick, {Emery H.} and Patrick Brest and Dave Bridges and Bristol, {Molly L.} and Brookes, {Paul S.} and Brown, {Eric J.} and Brumell, {John H.} and Nicola Brunetti-Pierri and Brunk, {Ulf T.} and Bulman, {Dennis E.} and Bultman, {Scott J.} and Greet Bultynck and Burbulla, {Lena F.} and Wilfried Bursch and Butchar, {Jonathan P.} and Wanda Buzgariu and Bydlowski, {Sergio P.} and Ken Cadwell and Monika Cahova and Dongsheng Cai and Jiyang Cai and Qian Cai and Bruno Calabretta and Javier Calvo-Garrido and Nadine Camougrand and Michelangelo Campanella and Jenny Campos-Salinas and Eleonora Candi and Lizhi Cao and Caplan, {Allan B.} and Carding, {Simon R.} and Cardoso, {Sandra M.} and Carew, {Jennifer S.} and Carlin, {Cathleen R.} and Virginie Carmignac and Carneiro, {Leticia A. M.} and Serena Carra and Caruso, {Rosario A.} and Giorgio Casari and Caty Casas and Roberta Castino and Eduardo Cebollero and Francesco Cecconi and Jean Celli and Hassan Chaachouay and Han-Jung Chae and Chee-Yin Chai and Chan, {David C.} and Chan, {Edmond Y.} and Chang, {Raymond Chuen-Chung} and Chi-Ming Che and Ching-Chow Chen and Guang-Chao Chen and Guo-Qiang Chen and Min Chen and Quan Chen and Chen, {Steve S. -L.} and WenLi Chen and Xi Chen and Xiangmei Chen and Xiequn Chen and Ye-Guang Chen and Yingyu Chen and Yongqiang Chen and Yu-Jen Chen and Zhixiang Chen and Alan Cheng and Cheng, {Christopher H. K.} and Yan Cheng and Heesun Cheong and Jae-Ho Cheong and Sara Cherry and Russ Chess-Williams and Cheung, {Zelda H.} and Eric Chevet and Hui-Ling Chiang and Roberto Chiarelli and Tomoki Chiba and Lih-Shen Chin and Shih-Hwa Chiou and Chisari, {Francis V.} and Cho, {Chi Hin} and Dong-Hyung Cho and Choi, {Augustine M. K.} and DooSeok Choi and Choi, {Kyeong Sook} and Choi, {Mary E.} and Salem Chouaib and Divaker Choubey and Vinay Choubey and Chu, {Charleen T.} and Tsung-Hsien Chuang and Sheau-Huei Chueh and Taehoon Chun and Yong-Joon Chwae and Mee-Len Chye and Roberto Ciarcia and Ciriolo, {Maria R.} and Clague, {Michael J.} and Clark, {Robert S. B.} and Clarke, {Peter G. H.} and Robert Clarke and Patrice Codogno and Coller, {Hilary A.} and Colombo, {Maria I.} and Sergio Comincini and Maria Condello and Fabrizio Condorelli and Cookson, {Mark R.} and Coppens, {Graham H. Coombs Isabelle} and Ramon Corbalan and Pascale Cossart and Paola Costelli and Safia Costes and Ana Coto-Montes and Eduardo Couve and Coxon, {Fraser P.} and Cregg, {James M.} and Crespo, {Jose L.} and Cronje, {Marianne J.} and Cuervo, {Ana Maria} and Cullen, {Joseph J.} and Czaja, {Mark J.} and Marcello D'Amelio and Arlette Darfeuille-Michaud and Davids, {Lester M.} and Davies, {Faith E.} and {De Felici}, Massimo and {de Groot}, {John F.} and {de Haan}, {Cornelis A. M.} and {De Martino}, Luisa and {De Milito}, Angelo and {De Tata}, Vincenzo and Jayanta Debnath and Alexei Degterev and Benjamin Dehay and Delbridge, {Lea M. D.} and Francesca Demarchi and Deng, {Yi Zhen} and Joen Dengjel and Paul Dent and Donna Denton and Vojo Deretic and Desai, {Shyamal D.} and Devenish, {Rodney J.} and {Di Gioacchino}, Mario and {Di Paolo}, Gilbert and {Di Pietro}, Chiara and Guillermo Diaz-Araya and Ines Diaz-Laviada and Diaz-Meco, {Maria T.} and Javier Diaz-Nido and Ivan Dikic and Dinesh-Kumar, {Savithramma P.} and Wen-Xing Ding and Distelhorst, {Clark W.} and Abhinav Diwan and Mojgan Djavaheri-Mergny and Svetlana Dokudovskaya and Zheng Dong and Dorsey, {Frank C.} and Victor Dosenko and Dowling, {James J.} and Stephen Doxsey and Marlene Dreux and Drew, {Mark E.} and Qiuhong Duan and Duchosal, {Michel A.} and Karen Duff and Isabelle Dugail and Madeleine Durbeej-Hjalt and Michael Duszenko and Edelstein, {Charles L.} and Edinger, {Aimee L.} and Gustavo Egea and Ludwig Eichinger and Eissa, {N. Tony} and Suhendan Ekmekcioglu and El-Deiry, {Wafik S.} and Zvulun Elazar and Mohamed Elgendy and Ellerby, {Lisa M.} and Eng, {Kai Er} and Anna-Mart Engelbrecht and Simone Engelender and Jekaterina Erenpreisa and Ricardo Escalante and Audrey Esclatine and Eeva-Liisa Eskelinen and Lucile Espert and Virginia Espina and Huizhou Fan and Jia Fan and Qi-Wen Fan and Zhen Fan and Shengyun Fang and Yongqi Fang and Manolis Fanto and Alessandro Fanzani and Thomas Farkas and Jean-Claude Farre and Mathias Faure and Marcus Fechheimer and Feng, {Carl G.} and Jian Feng and Qili Feng and Youji Feng and Laszlo Fesues and Ralph Feuer and Figueiredo-Pereira, {Maria E.} and Fimia, {Gian Maria} and Fingar, {Diane C.} and Steven Finkbeiner and Toren Finkel and Finley, {Kim D.} and Filomena Fiorito and Fisher, {Edward A.} and Fisher, {Paul B.} and Marc Flajolet and Florez-McClure, {Maria L.} and Salvatore Florio and Fon, {Edward A.} and Francesco Fornai and Franco Fortunato and Rati Fotedar and Fowler, {Daniel H.} and Fox, {Howard S.} and Rodrigo Franco and Frankel, {Lisa B.} and Marc Fransen and Fuentes, {Jose M.} and Juan Fueyo and Jun Fujii and Kozo Fujisaki and Eriko Fujita and Mitsunori Fukuda and Furukawa, {Ruth H.} and Matthias Gaestel and Philippe Gailly and Malgorzata Gajewska and Brigitte Galliot and Vincent Galy and Subramaniam Ganesh and Barry Ganetzky and Ganley, {Ian G.} and Fen-Biao Gao and Gao, {George F.} and Jinming Gao and Lorena Garcia and Guillermo Garcia-Manero and Mikel Garcia-Marcos and Marjan Garmyn and Gartel, {Andrei L.} and Evelina Gatti and Mathias Gautel and Gawriluk, {Thomas R.} and Gegg, {Matthew E.} and Jiefei Geng and Marc Germain and Gestwicki, {Jason E.} and Gewirtz, {David A.} and Saeid Ghavami and Pradipta Ghosh and Giammarioli, {Anna M.} and Giatromanolaki, {Alexandra N.} and Gibson, {Spencer B.} and Gilkerson, {Robert W.} and Ginger, {Michael L.} and Ginsberg, {Henry N.} and Jakub Golab and Goligorsky, {Michael S.} and Pierre Golstein and Candelaria Gomez-Manzano and Ebru Goncu and Celine Gongora and Gonzalez, {Claudio D.} and Ramon Gonzalez and Cristina Gonzalez-Estevez and Gonzalez-Polo, {Rosa Ana} and Elena Gonzalez-Rey and Gorbunov, {Nikolai V.} and Sharon Gorski and Sandro Goruppi and Gottlieb, {Roberta A.} and Devrim Gozuacik and Granato, {Giovanna Elvira} and Grant, {Gary D.} and Green, {Kim N.} and Ales Gregorc and Frederic Gros and Charles Grose and Grunt, {Thomas W.} and Philippe Gual and Jun-Lin Guan and Kun-Liang Guan and Guichard, {Sylvie M.} and Gukovskaya, {Anna S.} and Ilya Gukovsky and Jan Gunst and Gustafsson, {Asa B.} and Halayko, {Andrew J.} and Hale, {Amber N.} and Halonen, {Sandra K.} and Maho Hamasaki and Feng Han and Ting Han and Hancock, {Michael K.} and Malene Hansen and Hisashi Harada and Masaru Harada and Hardt, {Stefan E.} and Harper, {J. Wade} and Harris, {Adrian L.} and James Harris and Harris, {Steven D.} and Makoto Hashimoto and Haspel, {Jeffrey A.} and Shin-ichiro Hayashi and Hazelhurst, {Lori A.} and Congcong He and You-Wen He and Marie-Josee Hebert and Heidenreich, {Kim A.} and Helfrich, {Miep H.} and Helgason, {Gudmundur V.} and Henske, {Elizabeth P.} and Brian Herman and Herman, {Paul K.} and Claudio Hetz and Sabine Hilfiker and Hill, {Joseph A.} and Hocking, {Lynne J.} and Paul Hofman and Hofmann, {Thomas G.} and Joerg Hoehfeld and Holyoake, {Tessa L.} and Ming-Huang Hong and Hood, {David A.} and Hotamisligil, {Goekhan S.} and Houwerzijl, {Ewout J.} and Maria Hoyer-Hansen and Bingren Hu and Hu, {Chien-An A.} and Hong-Ming Hu and Ya Hua and Canhua Huang and Ju Huang and Shengbing Huang and Wei-Pang Huang and Huber, {Tobias B.} and Won-Ki Huh and Tai-Ho Hung and Hupp, {Ted R.} and Hur, {Gang Min} and Hurley, {James B.} and Hussain, {Sabah N. 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W.} and Jones, {Nicola L.} and Bertrand Joseph and Joseph, {Suresh K.} and Joubert, {Annie M.} and Gabor Juhasz and Lucienne Juillerat-Jeanneret and Jung, {Chang Hwa} and Yong-Keun Jung and Kai Kaarniranta and Allen Kaasik and Tomohiro Kabuta and Motoni Kadowaki and Katarina Kagedal and Yoshiaki Kamada and Kaminskyy, {Vitaliy O.} and Kampinga, {Harm H.} and Hiromitsu Kanamori and Chanhee Kang and Kang, {Khong Bee} and Kang, {Kwang Il} and Rui Kang and Yoon-A Kang and Tomotake Kanki and Thirumala-Devi Kanneganti and Haruo Kanno and Kanthasamy, {Anumantha G.} and Arthi Kanthasamy and Vassiliki Karantza and Kaushal, {Gur P.} and Susmita Kaushik and Yoshinori Kawazoe and Po-Yuan Ke and Kehrl, {John H.} and Ameeta Kelekar and Claus Kerkhoff and Kessel, {David H.} and Hany Khalil and Kiel, {Jan A. K. 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Kouri} and Kovacs, {Attila L.} and Claudine Kraft and Dimitri Krainc and Helmut Kraemer and Carole Kretz-Remy and Krichevsky, {Anna M.} and Guido Kroemer and Rejko Krueger and Oleg Krut and Ktistakis, {Nicholas T.} and Chia-Yi Kuan and Roza Kucharczyk and Ashok Kumar and Raj Kumar and Sharad Kumar and Mondira Kundu and Hsing-Jien Kung and Tino Kurz and Kwon, {Ho Jeong} and {La Spada}, {Albert R.} and Frank Lafont and Trond Lamark and Jacques Landry and Lane, {Jon D.} and Pierre Lapaquette and Laporte, {Jocelyn F.} and Lajos Laszlo and Sergio Lavandero and Lavoie, {Josee N.} and Robert Layfield and Lazo, {Pedro A.} and Weidong Le and {Le Cam}, Laurent and Ledbetter, {Daniel J.} and Lee, {Alvin J. 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M.} and Carine Michiels and Dalibor Mijaljica and Ana Milojkovic and Saverio Minucci and Clelia Miracco and Miranti, {Cindy K.} and Ioannis Mitroulis and Keisuke Miyazawa and Noboru Mizushima and Baharia Mograbi and Simin Mohseni and Xavier Molero and Bertrand Mollereau and Faustino Mollinedo and Takashi Momoi and Iryna Monastyrska and Monick, {Martha M.} and Monteiro, {Mervyn J.} and Moore, {Michael N.} and Rodrigo Mora and Kevin Moreau and Moreira, {Paula I.} and Yuji Moriyasu and Jorge Moscat and Serge Mostowy and Mottram, {Jeremy C.} and Tomasz Motyl and Moussa, {Charbel E. -H.} and Sylke Mueller and Karl Muenger and Christian Muenz and Murphy, {Leon O.} and Murphy, {Maureen E.} and Antonio Musaro and Indira Mysorekar and Eiichiro Nagata and Kazuhiro Nagata and Aimable Nahimana and Usha Nair and Toshiyuki Nakagawa and Kiichi Nakahira and Hiroyasu Nakano and Hitoshi Nakataogawa and Meera Nanjundan and Naqvi, {Naweed I.} and Narendra, {Derek P.} and Masashi Narita and Miguel Navarro and Nawrocki, {Steffan T.} and Nazarko, {Taras Y.} and Andriy Nemchenko and Netea, {Mihai G.} and Neufeld, {Thomas P.} and Ney, {Paul A.} and Nezis, {Ioannis P.} and Nguyen, {Huu Phuc} and Daotai Nie and Ichizo Nishino and Corey Nislow and Nixon, {Ralph A.} and Takeshi Noda and Noegel, {Angelika A.} and Anna Nogalska and Satoru Noguchi and Lucia Notterpek and Ivana Novak and Tomoyoshi Nozaki and Nobuyuki Nukina and Thorsten Nuernberger and Beat Nyfeler and Keisuke Obara and Oberley, {Terry D.} and Salvatore Oddo and Michinaga Ogawa and Toya Ohashi and Koji Okamoto and Oleinick, {Nancy L.} and Oliver, {F. 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Ashutosh} and Rathmell, {Jeffrey C.} and Brinda Ravikumar and Ray, {Swapan K.} and Reed, {Bruce H.} and Reed, {John C.} and Fulvio Reggiori and Anne Regnier-Vigouroux and Reichert, {Andreas S.} and Reiners, {John J.} and Reiter, {Russel J.} and Jun Ren and Revuelta, {Jose L.} and Rhodes, {Christopher J.} and Konstantinos Ritis and Elizete Rizzo and Jeffrey Robbins and Michel Roberge and Hernan Roca and Roccheri, {Maria C.} and Stephane Rocchi and Rodemann, {H. Peter} and {de Cordoba}, {Santiago Rodriguez} and Baerbel Rohrer and Roninson, {Igor B.} and Kirill Rosen and Rost-Roszkowska, {Magdalena M.} and Mustapha Rouis and Rouschop, {Kasper M. A.} and Francesca Rovetta and Rubin, {Brian P.} and Rubinsztein, {David C.} and Klaus Ruckdeschel and Rucker, {Edmund B} and Assaf Rudich and Emil Rudolf and Nelson Ruiz-Opazo and Rossella Russo and Rusten, {Tor Erik} and Ryan, {Kevin M.} and Ryter, {Stefan W.} and Sabatini, {David M.} and Junichi Sadoshima and Tapas Saha and Tatsuya Saitoh and Hiroshi Sakagami and Yasuyoshi Sakai and Salekdeh, {Ghasem Hoseini} and Paolo Salomoni and Salvaterra, {Paul M.} and Guy Salvesen and Rosa Salvioli and Sanchez, {Anthony M. J.} and Sanchez-Alcazar, {Jose A.} and Ricardo Sanchez-Prieto and Marco Sandri and Uma Sankar and Poonam Sansanwal and Laura Santambrogio and Shweta Saran and Sovan Sarkar and Minnie Sarwal and Chihiro Sasakawa and Ausra Sasnauskiene and Miklos Sass and Ken Sato and Miyuki Sato and Schapira, {Anthony H. V.} and Michael Scharl and Schaetzl, {Hermann M.} and Wiep Scheper and Stefano Schiaffino and Claudio Schneider and Schneider, {Marion E.} and Regine Schneider-Stock and Schoenlein, {Patricia V.} and Schorderet, {Daniel F.} and Christoph Schueller and Schwartz, {Gary K.} and Luca Scorrano and Linda Sealy and Seglen, {Per O.} and Juan Segura-Aguilar and Iban Seiliez and Oleksandr Seleverstov and Christian Sell and Seo, {Jong Bok} and Duska Separovic and Vijayasaradhi Setaluri and Takao Setoguchi and Carmine Settembre and Shacka, {John J.} and Mala Shanmugam and Shapiro, {Irving M.} and Eitan Shaulian and Shaw, {Reuben J.} and Shelhamer, {James H.} and Han-Ming Shen and Wei-Chiang Shen and Zu-Hang Sheng and Yang Shi and Kenichi Shibuya and Yoshihiro Shidoji and Jeng-Jer Shieh and Chwen-Ming Shih and Yohta Shimada and Shigeomi Shimizu and Takahiro Shintani and Shirihai, {Orian S.} and Shore, {Gordon C.} and Sibirny, {Andriy A.} and Sidhu, {Stan B.} and Beata Sikorska and Silva-Zacarin, {Elaine C. 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year = "2012",
doi = "10.4161/auto.19496",
language = "English",
volume = "8",
pages = "445--544",
journal = "Autophagy",
issn = "1554-8635",
publisher = "Landes Bioscience",
number = "4",

}