Guidelines for the use and interpretation of assays for monitoring autophagy

Daniel J. Klionsky; Fabio C. Abdalla; Hagai Abeliovich; Robert T. Abraham; Abraham Acevedo-Arozena; Khosrow Adeli; Lotta Agholme; Maria Agnello; Patrizia Agostinis; Julio A. Aguirre-Ghiso; Hyung Jun Ahn; Ouardia Ait-Mohamed; Slimane Ait-Si-Ali; Takahiko Akematsu; Shizuo Akira; Hesham M. Al-Younes; Munir A. Al-Zeer; Matthew L. Albert; Roger L. Albin; Javier Alegre-Abarrategui; Maria Francesca Aleo; Mehrdad Alirezaei; Alexandru Almasan; Maylin Almonte-Becerril; Atsuo Amano; Ravi K. Amaravadi; Shoba Amarnath; Amal O. Amer; Nathalie Andrieu-Abadie; Vellareddy Anantharam; David K. Ann; Shailendra Anoopkumar-Dukie; Hiroshi Aoki; Nadezda Apostolova; Giuseppe Arancia; John P. Aris; Katsuhiko Asanuma; Nana Y.O. Asare; Hisashi Ashida; Valerie Askanas; David S. Askew; Patrick Auberger; Misuzu Baba; Steven K. Backues; Eric H. Baehrecke; Ben A. Bahr; Xue-Yuan Bai; Yannick Bailly; Robert Baiocchi; Giulia Baldini; Walter Balduini; Andrea Ballabio; Bruce A. Bamber; Edward T.W. Bampton; Gábor Juhász; Clinton R. Bartholomew; Diane C. Bassham; Robert C. Bast; Henri Batoko; Boon-Huat Bay; Isabelle Beau; Daniel M. Béchet; Thomas J. Begley; Christian Behl; Christian Behrends; Soumeya Bekri; Bryan Bellaire; Linda J. Bendall; Luca Benetti; Laura Berliocchi; Henri Bernardi; Francesca Bernassola; Sébastien Besteiro; Ingrid Bhatia-Kissova; Xiaoning Bi; Martine Biard-Piechaczyk; Janice S. Blum; Lawrence H. Boise; Paolo Bonaldo; David L. Boone; Beat C. Bornhauser; Karina R. Bortoluci; Ioannis Bossis; Frédéric Bost; Jean-Pierre Bourquin; Patricia Boya; Michaël Boyer-Guittaut; Peter V. Bozhkov; Nathan R Brady; Claudio Brancolini; Andreas Brech; Jay E. Brenman; Ana Brennand; Emery H. Bresnick; Patrick Brest; Dave Bridges; Molly L. Bristol; Paul S. Brookes; Eric J. Brown; John H. Brumell; Nicola Brunetti-Pierri; Ulf T. Brunk; Dennis E. Bulman; Scott J. Bultman; Geert Bultynck; Lena F. Burbulla; Wilfried Bursch; Jonathan P. Butchar; Wanda Buzgariu; Sergio P. Bydlowski; Ken Cadwell; Monika Cahová; Dongsheng Cai; Jiyang Cai; Qian Cai; Bruno Calabretta; Javier Calvo-Garrido; Nadine Camougrand; Michelangelo Campanella; Jenny Campos-Salinas; Eleonora Candi; Lizhi Cao; Allan B. Caplan; Simon R. Carding; Sandra M. Cardoso; Jennifer S. Carew; Cathleen R. Carlin; Virginie Carmignac; Leticia A.M. Carneiro; Serena Carra; Rosario A. Caruso; Giorgio Casari; Caty Casas; Roberta Castino; Eduardo Cebollero; Francesco Cecconi; Jean Celli; Hassan Chaachouay; Han-Jung Chae; Chee-Yin Chai; David C. Chan; Edmond Y. Chan; Raymond Chuen-Chung Chang; Chi-Ming Che; Ching-Chow Chen; Guang-Chao Chen; Guo-Qiang Chen; Min Chen; Quan Chen; Steve S.-L. Chen; WenLi Chen; Xi Chen; Xiangmei Chen; Xiequn Chen; Ye-Guang Chen; Yingyu Chen; Yongqiang Chen; Yu-Jen Chen; Zhixiang Chen; Alan Cheng; Christopher H.K. Cheng; Yan Cheng; Heesun Cheong; Jae-Ho Cheong; Sara Cherry; Russ Chess-Williams; Zelda H. Cheung; Eric Chevet; Hui-Ling Chiang; Roberto Chiarelli; Tomoki Chiba; Lih-Shen Chin; Shih-Hwa Chiou; Francis V. Chisari; Chi Hin Cho; Dong-Hyung Cho; Augustine M.K. Choi; DooSeok Choi; Kyeong Sook Choi; Mary E. Choi; Salem Chouaib; Divaker Choubey; Vinay Choubey; Charleen T. Chu; Tsung-Hsien Chuang; Sheau-Huei Chueh; Taehoon Chun; Yong-Joon Chwae; Mee-Len Chye; Roberto Ciarcia; Maria R. Ciriolo; Michael J. Clague; Robert S.B. Clark; Peter G.H. Clarke; Robert Clarke; Patrice Codogno; Hilary A. Coller; María I. Colombo; Sergio Comincini; Maria Condello; Fabrizio Condorelli; Mark R. Cookson; Graham H. Coombs; Isabelle Coppens; Ramon Corbalan; Pascale Cossart; Paola Costelli; Safia Costes; Ana Coto-Montes; Eduardo Couve; Fraser P. Coxon; James M. Cregg; José L. Crespo; Marianne J. Cronjé; Ana Maria Cuervo; Joseph J. Cullen; Mark J. Czaja; Marcello D'Amelio; Arlette Darfeuille-Michaud; Lester M. Davids; Faith E. Davies; Massimo De Felici; John F. de Groot; Cornelis A.M. de Haan; Luisa De Martino; Angelo De Milito; Vincenzo De Tata; Jayanta Debnath; Alexei Degterev; Benjamin Dehay; Lea M.D. Delbridge; Francesca Demarchi; Yi Zhen Deng; Jörn Dengjel; Paul Dent; Donna Denton; Vojo Deretic; Shyamal D. Desai; Rodney J. Devenish; Mario Di Gioacchino; Gilbert Di Paolo; Chiara Di Pietro; Guillermo Díaz-Araya; Inés Díaz-Laviada; Maria T. Diaz-Meco; Javier Diaz-Nido; Ivan Dikic; Savithramma P. Dinesh-Kumar; Wen-Xing Ding; Clark W. Distelhorst; Abhinav Diwan; Mojgan Djavaheri-Mergny; Svetlana Dokudovskaya; Zheng Dong; Frank C. Dorsey; Victor Dosenko; James J. Dowling; Stephen Doxsey; Marlène Dreux; Mark E. Drew; Qiuhong Duan; Michel A. Duchosal; Karen E. Duff; Isabelle Dugail; Madeleine Durbeej; Michael Duszenko; Charles L. Edelstein; Aimee L. Edinger; Gustavo Egea; Ludwig Eichinger; N. Tony Eissa; Suhendan Ekmekcioglu; Wafik S. El-Deiry; Zvulun Elazar; Mohamed Elgendy; Lisa M. Ellerby; Kai Er Eng; Anna-Mart Engelbrecht; Simone Engelender; Jekaterina Erenpreisa; Ricardo Escalante; Audrey Esclatine; Eeva-Liisa Eskelinen; Lucile Espert; Virginia Espina; Huizhou Fan; Jia Fan; Qi-Wen Fan; Zhen Fan; Shengyun Fang; Yongqi Fang; Manolis Fanto; Alessandro Fanzani; Thomas Farkas; Jean-Claude Farre; Mathias Faure; Marcus Fechheimer; Carl G. Feng; Jian Feng; Qili Feng; Youji Feng; László Fésüs; Ralph Feuer; Maria E. Figueiredo-Pereira; Gian Maria Fimia; Diane C. Fingar; Steven Finkbeiner; Toren Finkel; Kim D. Finley; Filomena Fiorito; Edward A. Fisher; Paul B. Fisher; Marc Flajolet; Maria L. Florez-McClure; Salvatore Florio; Edward A. Fon; Francesco Fornai; Franco Fortunato; Rati Fotedar; Daniel H. Fowler; Howard S. Fox; Rodrigo Franco; Lisa B. Frankel; Marc Fransen; José M. Fuentes; Juan Fueyo; Jun Fujii; Kozo Fujisaki; Eriko Fujita; Mitsunori Fukuda; Ruth H. Furukawa; Matthias Gaestel; Philippe Gailly; Malgorzata Gajewska; Brigitte Galliot; Vincent Galy; Subramaniam Ganesh; Barry Ganetzky; Ian G. Ganley; Fen-Biao Gao; George F. Gao; Jinming Gao; Lorena Garcia; Guillermo Garcia-Manero; Mikel Garcia-Marcos; Marjan Garmyn; Andrei L. Gartel; Evelina Gatti; Mathias Gautel; Thomas R. Gawriluk; Matthew E. Gegg; Jiefei Geng; Marc Germain; Jason E. Gestwicki; David A. Gewirtz; Saeid Ghavami; Pradipta Ghosh; Anna M. Giammarioli; Alexandra N. Giatromanolaki; Spencer B. Gibson; Robert W. Gilkerson; Michael L. Ginger; Henry N. Ginsberg; Jakub Golab; Michael S. Goligorsky; Pierre Golstein; Candelaria Gomez-Manzano; Ebru Goncu; Céline Gongora; Claudio D. Gonzalez; Ramon Gonzalez; Cristina González-Estévez; Rosa Ana González-Polo; Elena Gonzalez-Rey; Nikolai V. Gorbunov; Sharon Gorski; Sandro Goruppi; Roberta A. Gottlieb; Devrim Gozuacik; Giovanna Elvira Granato; Gary D. Grant; Kim N. Green; Ales Gregorc; Frédéric Gros; Charles Grose; Thomas W. Grunt; Philippe Gual; Jun-Lin Guan; Kun-Liang Guan; Sylvie M. Guichard; Anna S. Gukovskaya; Ilya Gukovsky; Jan Gunst; Åsa B. Gustafsson; Andrew J. Halayko; Amber N. Hale; Sandra K. Halonen; Maho Hamasaki; Feng Han; Ting Han; Michael K. Hancock; Malene Hansen; Hisashi Harada; Masaru Harada; Stefan E. Hardt; J. Wade Harper; Adrian L. Harris; James Harris; Steven D. Harris; Makoto Hashimoto; Jeffrey A. Haspel; Shin-ichiro Hayashi; Lori A. Hazelhurst; Congcong He; You-Wen He; Marie-Josée Hébert; Kim A. Heidenreich; Miep H. Helfrich; Gudmundur V. Helgason; Elizabeth P. Henske; Brian Herman; Paul K. Herman; Claudio Hetz; Sabine Hilfiker; Joseph A. Hill; Lynne J. Hocking; Paul Hofman; Thomas G. Hofmann; Jörg Höhfeld; Tessa L. Holyoake; Ming-Huang Hong; David A. Hood; Gökhan S. Hotamisligil; Ewout J. Houwerzijl; Maria Høyer-Hansen; Bingren Hu; Chien-an A. Hu; Hong-Ming Hu; Ya Hua; Canhua Huang; Ju Huang; Shengbing Huang; Wei-Pang Huang; Tobias B. Huber; Won-Ki Huh; Tai-Ho Hung; Ted R. Hupp; Gang Min Hur; James B. Hurley; Sabah N.A. Hussain; Patrick J. Hussey; Jung Jin Hwang; Seungmin Hwang; Atsuhiro Ichihara; Shirin Ilkhanizadeh; Ken Inoki; Takeshi Into; Valentina Iovane; Juan L. Iovanna; Nancy Y. Ip; Yoshitaka Isaka; Hiroyuki Ishida; Ciro Isidoro; Ken-ichi Isobe; Akiko Iwasaki; Marta Izquierdo; Yotaro Izumi; Panu M. Jaakkola; Marja Jäättelä; George R. Jackson; William T. Jackson; Bassam Janji; Marina Jendrach; Ju-Hong Jeon; Eui-Bae Jeung; Hong Jiang; Hongchi Jiang; Jean X. Jiang; Ming Jiang; Qing Jiang; Xuejun Jiang; Alberto Jiménez; Meiyan Jin; Shengkan V. Jin; Cheol O. Joe; Terje Johansen; Daniel E. Johnson; Gail V.W. Johnson; Nicola L. Jones; Bertrand Joseph; Suresh K. Joseph; Annie M. Joubert; Lucienne Juillerat-Jeanneret; Chang Hwa Jung; Yong-Keun Jung; Kai Kaarniranta; Allen Kaasik; Tomohiro Kabuta; Motoni Kadowaki; Katarina Kågedal; Yoshiaki Kamada; Vitaliy O. Kaminskyy; Harm H. Kampinga; Hiromitsu Kanamori; Chanhee Kang; Khong Bee Kang; Kwang Il Kang; Rui Kang; Yoon-A Kang; Tomotake Kanki; Thirumala-Devi Kanneganti; Haruo Kanno; Anumantha G. Kanthasamy; Arthi Kanthasamy; Vassiliki Karantza; Gur P. Kaushal; Susmita Kaushik; Yoshinori Kawazoe; Po-Yuan Ke; John H. Kehrl; Ameeta Kelekar; Claus Kerkhoff; David H. Kessel; Hany Khalil; Jan A.K.W. Kiel; Amy A. Kiger; Akio Kihara; Deok Ryong Kim; Do-Hyung Kim; Dong-Hou Kim; Eun-Kyoung Kim; Hyung-Ryong Kim; Jae-Sung Kim; Jeong Hun Kim; Jin Cheon Kim; John K. Kim; Peter K. Kim; Seong Who Kim; Yong-Sun Kim; Yonghyun Kim; Adi Kimchi; Alec C. Kimmelman; Jason S. King; Timothy J. Kinsella; Vladimir Kirkin; Lorrie A. Kirshenbaum; Katsuhiko Kitamoto; Kaio Kitazato; Ludger Klein; Walter T. Klimecki; Jochen Klucken; Erwin Knecht; Ben C.B. Ko; Jan C. Koch; Hiroshi Koga; Jae-Young Koh; Young Ho Koh; Masato Koike; Masaaki Komatsu; Eiki Kominami; Hee Jeong Kong; Wei-Jia Kong; Viktor I. Korolchuk; Yaichiro Kotake; Michael I. Koukourakis; Juan B. Kouri Flores; Attila L. Kovács; Claudine Kraft; Dimitri Krainc; Helmut Krämer; Carole Kretz-Remy; Anna M. Krichevsky; Guido Kroemer; Rejko Krüger; Oleg Krut; Nicholas T. Ktistakis; Chia-Yi Kuan; Roza Kucharczyk; Ashok Kumar; Raj Kumar; Sharad Kumar; Mondira Kundu; Hsing-Jien Kung; Tino Kurz; Ho Jeong Kwon; Albert R. La Spada; Frank Lafont; Trond Lamark; Jacques Landry; Jon D. Lane; Pierre Lapaquette; Jocelyn F. Laporte; Lajos László; Sergio Lavandero; Josée N. Lavoie; Robert Layfield; Pedro A. Lazo; Weidong Le; Laurent Le Cam; Daniel J. Ledbetter; Alvin J.X. Lee; Byung-Wan Lee; Gyun Min Lee; Jongdae Lee; Ju-hyun lee; Michael Lee; Myung-Shik Lee; Sug Hyung Lee; Christiaan Leeuwenburgh; Patrick Legembre; Renaud Legouis; Michael Lehmann; Huan-Yao Lei; Qun-Ying Lei; David A. Leib; José Leiro; John J. Lemasters; Antoinette Lemoine; Maciej S. Lesniak; Dina Lev; Victor V. Levenson; Beth Levine; Efrat Levy; Faqiang Li; Jun-Lin Li; Lian Li; Sheng Li; Weijie Li; Xue-Jun Li; Yan-Bo Li; Yi-Ping Li; Chengyu Liang; Qiangrong Liang; Yung-Feng Liao; Pawel P. Liberski; Andrew Lieberman; Hyunjung J. Lim; Kah-Leong Lim; Kyu Lim; Chiou-Feng Lin; Fu-Cheng Lin; Jian Lin; Jiandie D. Lin; Kui Lin; Wan-Wan Lin; Weei-Chin Lin; Yi-Ling Lin; Rafael Linden; Paul Lingor; Jennifer Lippincott-Schwartz; Michael P. Lisanti; Paloma B. Liton; Bo Liu; Chun-Feng Liu; Kaiyu Liu; Leyuan Liu; Qiong A. Liu; Wei Liu; Young-Chau Liu; Yule Liu; Richard A. Lockshin; Chun-Nam Lok; Sagar Lonial; Benjamin Loos; Gabriel Lopez-Berestein; Carlos López-Otín; Laura Lossi; Michael T. Lotze; Peter Low; Binfeng Lu; Bingwei Lu; Bo Lu; Zhen Lu; Fréderic Luciano; Nicholas W. Lukacs; Anders H. Lund; Melinda A. Lynch-Day; Yong Ma; Fernando Macian; Jeff P. MacKeigan; Kay F. Macleod; Frank Madeo; Luigi Maiuri; Maria Chiara Maiuri; Davide Malagoli; May Christine V. Malicdan; Walter Malorni; Na Man; Eva-Maria Mandelkow; Stephen Manon; Irena Manov; Kai Mao; Xiang Mao; Zixu Mao; Philippe Marambaud; Daniela Marazziti; Yves L. Marcel; Katie Marchbank; Piero Marchetti; Stefan J. Marciniak; Mateus Marcondes; Mohsen Mardi; Gabriella Marfe; Guillermo Mariño; Maria Markaki; Mark R. Marten; Seamus J. Martin; Camille Martinand-Mari; Wim Martinet; Marta Martinez-Vicente; Matilde Masini; Paola Matarrese; Saburo Matsuo; Raffaele Matteoni; Andreas Mayer; Nathalie M. Mazure; David J. McConkey; Melanie J. McConnell; Catherine McDermott; Christine McDonald; Gerald M. McInerney; Sharon L. McKenna; BethAnn McLaughlin; Pamela J. McLean; Christopher R. McMaster; G. Angus McQuibban; Alfred J. Meijer; Miriam H. Meisler; Alicia Meléndez; Thomas J. Melia; Gerry Melino; Maria A. Mena; Javier A. Menendez; Rubem F. S. Menna-Barreto; Manoj B. Menon; Fiona M. Menzies; Carol A. Mercer; Adalberto Merighi; Diane E. Merry; Stefania Meschini; Christian G. Meyer; Thomas F. Meyer; Chao-Yu Miao; Jun-Ying Miao; Paul A.M. Michels; Carine Michiels; Dalibor Mijaljica; Ana Milojkovic; Saverio Minucci; Clelia Miracco; Cindy K. Miranti; Ioannis Mitroulis; Keisuke Miyazawa; Noboru Mizushima; Baharia Mograbi; Simin Mohseni; Xavier Molero; Bertrand Mollereau; Faustino Mollinedo; Takashi Momoi; Iryna Monastyrska; Martha M. Monick; Mervyn J. Monteiro; Michael N. Moore; Rodrigo Mora; Kevin Moreau; Paula I. Moreira; Yuji Moriyasu; Jorge Moscat; Serge Mostowy; Jeremy C. Mottram; Tomasz Motyl; Charbel E.-H. Moussa; Sylke Müller; Sylviane Muller; Karl Münger; Christian Münz; Leon O. Murphy; Maureen E. Murphy; Antonio Musarò; Indira Mysorekar; Eiichiro Nagata; Kazuhiro Nagata; Aimable Nahimana; Usha Nair; Toshiyuki Nakagawa; Kiichi Nakahira; Hiroyasu Nakano; Hitoshi Nakatogawa; Meera Nanjundan; Naweed I. Naqvi; Derek P. Narendra; Masashi Narita; Miguel Navarro; Steffan T. Nawrocki; Taras Y. Nazarko; Andriy Nemchenko; Mihai G. Netea; Thomas P. Neufeld; Paul A. 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Schätzl; Wiep Scheper; Stefano Schiaffino; Claudio Schneider; Marion E. Schneider; Regine Schneider-Stock; Patricia V. Schoenlein; Daniel F. Schorderet; Christoph Schüller; Gary K. Schwartz; Luca Scorrano; Linda Sealy; Per O. Seglen; Juan Segura-Aguilar; Iban Seiliez; Oleksandr Seleverstov; Christian Sell; Jong Bok Seo; Duska Separovic; Vijayasaradhi Setaluri; Takao Setoguchi; Carmine Settembre; John J. Shacka; Mala Shanmugam; Irving M. Shapiro; Eitan Shaulian; Reuben J. Shaw; James H. Shelhamer; Han-Ming Shen; Wei-Chiang Shen; Zu-Hang Sheng; Yang Shi; Kenichi Shibuya; Yoshihiro Shidoji; Jeng-Jer Shieh; Chwen-Ming Shih; Yohta Shimada; Shigeomi Shimizu; Takahiro Shintani; Orian S. Shirihai; Gordon C. Shore; Andriy A. Sibirny; Stan B. Sidhu; Beata Sikorska; Elaine C.M. Silva-Zacarin; Alison Simmons; Anna Katharina Simon; Hans-Uwe Simon; Cristiano Simone; Anne Simonsen; David A. Sinclair; Rajat Singh; Debasish Sinha; Frank A. Sinicrope; Agnieszka Sirko; Parco M. 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Taylor; J. Paul Taylor; Lance S. Terada; Alexei Terman; Gianluca Tettamanti; Karin Thevissen; Craig B. Thompson; Andrew Thorburn; Michael Thumm; FengFeng Tian; Yuan Tian; Glauco Tocchini-Valentini; Aviva M. Tolkovsky; Yasuhiko Tomino; Lars Tönges; Sharon A. Tooze; Cathy Tournier; John Tower; Roberto Towns; Vladimir Trajkovic; Leonardo H. Travassos; Ting-Fen Tsai; Mario P. Tschan; Takeshi Tsubata; Allan Tsung; Boris Turk; Lorianne S. Turner; Suresh C. Tyagi; Yasuo Uchiyama; Takashi Ueno; Midori Umekawa; Rika Umemiya-Shirafuji; Vivek K. Unni; Maria I. Vaccaro; Enza Maria Valente; Greet Van den Berghe; Ida J. van der Klei; Wouter G. van Doorn; Linda F. van Dyk; Marjolein van Egmond; Leo A. van Grunsven; Peter Vandenabeele; Wim P. Vandenberghe; Ilse Vanhorebeek; Eva C. Vaquero; Guillermo Velasco; Tibor Vellai; José Miguel Vicencio; Richard D. Vierstra; Miquel Vila; Cécile Vindis; Giampietro Viola; Maria Teresa Viscomi; Olga V. Voitsekhovskaja; Clarissa von Haefen; Marcela Votruba; Keiji Wada; Richard Wade-Martins; Cheryl L. Walker; Craig M. Walsh; Jochen Walter; Xiang-Bo Wan; Aimin Wang; Chenguang Wang; Dawei Wang; Fan Wang; Fen Wang; Guanghui Wang; Haichao Wang; Hong-Gang Wang; Horng-Dar Wang; Jin Wang; Ke Wang; Mei Wang; Richard C. Wang; Xinglong Wang; Xiujie J. Wang; Ying-Jan Wang; Yipeng Wang; Zhen-Bo Wang; Zhigang Charles Wang; Zhinong Wang; Derick G. Wansink; Diane M. Ward; Hirotaka Watada; Sarah L. Waters; Paul Webster; Lixin Wei; Conrad C. Weihl; William A. Weiss; Scott M. Welford; Long-Ping Wen; Caroline A. Whitehouse; J. Lindsay Whitton; Alexander J. Whitworth; Tom Wileman; John W. Wiley; Simon Wilkinson; Dieter Willbold; Roger L. Williams; Peter R. Williamson; Bradly G. Wouters; Chenghan Wu; Dao-Cheng Wu; William K.K. Wu; Andreas Wyttenbach; Ramnik J. Xavier; Zhijun Xi; Pu Xia; Gengfu Xiao; Zhiping Xie; Zhonglin Xie; Da-zhi Xu; Jianzhen Xu; Liang Xu; Xiaolei Xu; Ai Yamamoto; Akitsugu Yamamoto; Shunhei Yamashina; Michiaki Yamashita; Xianghua Yan; Mitsuhiro Yanagida; Dun-Sheng Yang; Elizabeth Yang; Jin-Ming Yang; Shi Yu Yang; Wannian Yang; Wei Yuan Yang; Zhifen Yang; Meng-Chao Yao; Tso-Pang Yao; Behzad Yeganeh; Wei-Lien Yen; Jia-Jing Yin; Xiao-Ming Yin; Ook-Joon Yoo; Gyesoon Yoon; Seung-Yong Yoon; Tomohiro Yorimitsu; Yuko Yoshikawa; Tamotsu Yoshimori; Kohki Yoshimoto; Ho Jin You; Richard J. Youle; Anas Younes; Li Yu; Long Yu; Seong-Woon Yu; Wai Haung Yu; Zhi-Min Yuan; Zhenyu Yue; Cheol-Heui Yun; Michisuke Yuzaki; Olga Zabirnyk; Elaine Silva-Zacarin; David Zacks; Eldad Zacksenhaus; Nadia Zaffaroni; Zahra Zakeri; Herbert J. Zeh, III; Scott O. Zeitlin; Hong Zhang; Hui-Ling Zhang; Jianhua Zhang; Jing-Pu Zhang; Lin Zhang; Long Zhang; Ming-Yong Zhang; Xu Dong Zhang; Mantong Zhao; Yi-Fang Zhao; Ying Zhao; Zhizhuang J. Zhao; Xiaoxiang Zheng; Boris Zhivotovsky; Qing Zhong; Cong-Zhao Zhou; Changlian Zhu; Wei-Guo Zhu; Xiao-Feng Zhu; Xiongwei Zhu; Yuangang Zhu; Teresa Zoladek; Wei-Xing Zong; Antonio Zorzano; Jürgen Zschocke; Brian Zuckerbraun

doi:10.4161/auto.19496

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Guidelines for the use and interpretation of assays for monitoring autophagy

Journal article

Open access

Peer reviewed

Guidelines for the use and interpretation of assays for monitoring autophagy

Daniel J. Klionsky, Fabio C. Abdalla, Hagai Abeliovich, Robert T. Abraham, Abraham Acevedo-Arozena, Khosrow Adeli, Lotta Agholme, Maria Agnello, Patrizia Agostinis, Julio A. Aguirre-Ghiso, …

Autophagy, Vol.8(4), pp.445-544

2012-04-01

DOI: https://doi.org/10.4161/auto.19496

PMCID: PMC3404883

PMID: 22966490

Abstract

autolysosome

autophagosome

flux

LC3

lysosome

phagophore

Review

stress

vacuole

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.

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Collaboration types: Industry collaboration; Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.25 Molecular & Cell Biology - Cancer, Autophagy & Apoptosis; 1.25.797 Autophagy
Web Of Science research areas: Cell Biology
ESI research areas: Molecular Biology & Genetics

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Title: Guidelines for the use and interpretation of assays for monitoring autophagy
Creators: Daniel J. Klionsky
Fabio C. Abdalla
Hagai Abeliovich
Robert T. Abraham
Abraham Acevedo-Arozena
Khosrow Adeli
Lotta Agholme
Maria Agnello
Patrizia Agostinis
Julio A. Aguirre-Ghiso
Hyung Jun Ahn
Ouardia Ait-Mohamed
Slimane Ait-Si-Ali
Takahiko Akematsu
Shizuo Akira
Hesham M. Al-Younes
Munir A. Al-Zeer
Matthew L. Albert
Roger L. Albin
Javier Alegre-Abarrategui
Maria Francesca Aleo
Mehrdad Alirezaei
Alexandru Almasan
Maylin Almonte-Becerril
Atsuo Amano
Ravi K. Amaravadi
Shoba Amarnath
Amal O. Amer
Nathalie Andrieu-Abadie
Vellareddy Anantharam
David K. Ann
Shailendra Anoopkumar-Dukie
Hiroshi Aoki
Nadezda Apostolova
Giuseppe Arancia
John P. Aris
Katsuhiko Asanuma
Nana Y.O. Asare
Hisashi Ashida
Valerie Askanas
David S. Askew
Patrick Auberger
Misuzu Baba
Steven K. Backues
Eric H. Baehrecke
Ben A. Bahr
Xue-Yuan Bai
Yannick Bailly
Robert Baiocchi
Giulia Baldini
Walter Balduini
Andrea Ballabio
Bruce A. Bamber
Edward T.W. Bampton
Gábor Juhász
Clinton R. Bartholomew
Diane C. Bassham
Robert C. Bast
Henri Batoko
Boon-Huat Bay
Isabelle Beau
Daniel M. Béchet
Thomas J. Begley
Christian Behl
Christian Behrends
Soumeya Bekri
Bryan Bellaire
Linda J. Bendall
Luca Benetti
Laura Berliocchi
Henri Bernardi
Francesca Bernassola
Sébastien Besteiro
Ingrid Bhatia-Kissova
Xiaoning Bi
Martine Biard-Piechaczyk
Janice S. Blum
Lawrence H. Boise
Paolo Bonaldo
David L. Boone
Beat C. Bornhauser
Karina R. Bortoluci
Ioannis Bossis
Frédéric Bost
Jean-Pierre Bourquin
Patricia Boya
Michaël Boyer-Guittaut
Peter V. Bozhkov
Nathan R Brady
Claudio Brancolini
Andreas Brech
Jay E. Brenman
Ana Brennand
Emery H. Bresnick
Patrick Brest
Dave Bridges
Molly L. Bristol
Paul S. Brookes
Eric J. Brown
John H. Brumell
Nicola Brunetti-Pierri
Ulf T. Brunk
Dennis E. Bulman
Scott J. Bultman
Geert Bultynck
Lena F. Burbulla
Wilfried Bursch
Jonathan P. Butchar
Wanda Buzgariu
Sergio P. Bydlowski
Ken Cadwell
Monika Cahová
Dongsheng Cai
Jiyang Cai
Qian Cai
Bruno Calabretta
Javier Calvo-Garrido
Nadine Camougrand
Michelangelo Campanella
Jenny Campos-Salinas
Eleonora Candi
Lizhi Cao
Allan B. Caplan
Simon R. Carding
Sandra M. Cardoso
Jennifer S. Carew
Cathleen R. Carlin
Virginie Carmignac
Leticia A.M. Carneiro
Serena Carra
Rosario A. Caruso
Giorgio Casari
Caty Casas
Roberta Castino
Eduardo Cebollero
Francesco Cecconi
Jean Celli
Hassan Chaachouay
Han-Jung Chae
Chee-Yin Chai
David C. Chan
Edmond Y. Chan
Raymond Chuen-Chung Chang
Chi-Ming Che
Ching-Chow Chen
Guang-Chao Chen
Guo-Qiang Chen
Min Chen
Quan Chen
Steve S.-L. Chen
WenLi Chen
Xi Chen
Xiangmei Chen
Xiequn Chen
Ye-Guang Chen
Yingyu Chen
Yongqiang Chen
Yu-Jen Chen
Zhixiang Chen
Alan Cheng
Christopher H.K. Cheng
Yan Cheng
Heesun Cheong
Jae-Ho Cheong
Sara Cherry
Russ Chess-Williams
Zelda H. Cheung
Eric Chevet
Hui-Ling Chiang
Roberto Chiarelli
Tomoki Chiba
Lih-Shen Chin
Shih-Hwa Chiou
Francis V. Chisari
Chi Hin Cho
Dong-Hyung Cho
Augustine M.K. Choi
DooSeok Choi
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Salem Chouaib
Divaker Choubey
Vinay Choubey
Charleen T. Chu
Tsung-Hsien Chuang
Sheau-Huei Chueh
Taehoon Chun
Yong-Joon Chwae
Mee-Len Chye
Roberto Ciarcia
Maria R. Ciriolo
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Patrice Codogno
Hilary A. Coller
María I. Colombo
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Publication Details: Autophagy, Vol.8(4), pp.445-544
Publisher: Landes Bioscience
Academic Unit: Miller School of Medicine; UMMG Dept of Radiation Oncology; Microbiology and Immunology Research
Language: English
Resource Type: Journal article
PMID: 22966490
PMCID: PMC3404883
Record Identifier: 991031713453802976