Guidelines for the use and interpretation of assays for monitoring autophagy

Research output: Contribution to journalReview article


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. A.} and Hussey, {Patrick J.} and Hwang, {Jung Jin} and Seungmin Hwang and Atsuhiro Ichihara and Shirin Ilkhanizadeh and Ken Inoki and Takeshi Into and Valentine Iovane and Iovanna, {Juan L.} and Ip, {Nancy Y.} and Yoshitaka Isaka and Hiroyuki Ishida and Ciro Isidoro and Ken-ichi Isobe and Akiko Iwasaki and Marta Izquierdo and Yotaro Izumi and Jaakkola, {Panu M.} and Marja Jaattela and Jackson, {George R.} and Jackson, {William T.} and Bassam Janji and Marina Jendrach and Ju-Hong Jeon and Eui-Bae Jeung and Hong Jiang and Hongchi Jiang and Jiang, {Jean X.} and Ming Jiang and Qing Jiang and Xuejun Jiang and Xuejun Jiang and Alberto Jimenez and Meiyan Jin and Shengkan Jin and Joe, {Cheol O.} and Terje Johansen and Johnson, {Daniel E.} and Johnson, {Gail V. 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. W.} and Kiger, {Amy A.} and Akio Kihara and Kim, {Deok Ryong} and Do-Hyung Kim and Dong-Hou Kim and Eun-Kyoung Kim and Hyung-Ryong Kim and Jae-Sung Kim and Kim, {Jeong Hun} and Kim, {Jin Cheon} and Kim, {John K.} and Kim, {Peter K.} and Kim, {Seong Who} and Yong-Sun Kim and Yonghyun Kim and Adi Kimchi and Kimmelman, {Alec C.} and King, {Jason S.} and Kinsella, {Timothy J.} and Vladimir Kirkin and Kirshenbaum, {Lorrie A.} and Katsuhiko Kitamoto and Kaio Kitazato and Ludger Klein and Klimecki, {Walter T.} and Jochen Klucken and Erwin Knecht and Ko, {Ben C. B.} and Koch, {Jan C.} and Hiroshi Koga and Jae-Young Koh and Koh, {Young Ho} and Masato Koike and Masaaki Komatsu and Eiki Kominami and Kong, {Hee Jeong} and Wei-Jia Kong and Korolchuk, {Viktor I.} and Yaichiro Kotake and Koukourakis, {Michael I.} and Flores, {Juan B. 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. X.} and Byung-Wan Lee and Lee, {Gyun Min} and Jongdae Lee and Ju-Hyun Lee and Michael Lee and Myung-Shik Lee and Lee, {Sug Hyung} and Christiaan Leeuwenburgh and Patrick Legembre and Renaud Legouis and Michael Lehmann and Huan-Yao Lei and Qun-Ying Lei and Leib, {David A.} and Jose Leiro and Lemasters, {John J.} and Antoinette Lemoine and Lesniak, {Maciej S.} and Dina Lev and Levenson, {Victor V.} and Beth Levine and Efrat Levy and Faqiang Li and Jun-Lin Li and Lian Li and Sheng Li and Weijie Li and Xue-Jun Li and Yan-bo Li and Yi-Ping Li and Chengyu Liang and Qiangrong Liang and Yung-Feng Liao and Liberski, {Pawel P.} and Andrew Lieberman and Lim, {Hyunjung J.} and Kah-Leong Lim and Kyu Lim and Chiou-Feng Lin and Fu-Cheng Lin and Jian Lin and Lin, {Jiandie D.} and Kui Lin and Wan-Wan Lin and Weei-Chin Lin and Yi-Ling Lin and Rafael Linden and Paul Lingor and Jennifer Lippincott-Schwartz and Lisanti, {Michael P.} and Liton, {Paloma B.} and Bo Liu and Chun-Feng Liu and Kaiyu Liu and Leyuan Liu and Liu, {Qiong A.} and Wei Liu and Young-Chau Liu and Yule Liu and Lockshin, {Richard A.} and Chun-Nam Lok and Sagar Lonial and Benjamin Loos and Gabriel Lopez-Berestein and Carlos Lopez-Otin and Laura Lossi and Lotze, {Michael T.} and Peter Low and Binfeng Lu and Bingwei Lu and Bo Lu and Zhen Lu and Frederic Luciano and Lukacs, {Nicholas W.} and Lund, {Anders H.} and Lynch-Day, {Melinda A.} and Yong Ma and Fernando Macian and MacKeigan, {Jeff P.} and Macleod, {Kay F.} and Frank Madeo and Luigi Maiuri and Maiuri, {Maria Chiara} and Davide Malagoli and Malicdan, {May Christine V.} and Walter Malorni and Na Man and Eva-Maria Mandelkow and Stephen Manon and Irena Manov and Kai Mao and Xiang Mao and Zixu Mao and Philippe Marambaud and Daniela Marazziti and Marcel, {Yves L.} and Katie Marchbank and Piero Marchetti and Marciniak, {Stefan J.} and Mateus Marcondes and Mohsen Mardi and Gabriella Marfe and Guillermo Marino and Maria Markaki and Marten, {Mark R.} and Martin, {Seamus J.} and Camille Martinand-Mari and Wim Martinet and Marta Martinez-Vicente and Matilde Masini and Paola Matarrese and Saburo Matsuo and Raffaele Matteoni and Andreas Mayer and Mazure, {Nathalie M.} and McConkey, {David J.} and McConnell, {Melanie J.} and Catherine McDermott and Christine McDonald and McInerney, {Gerald M.} and McKenna, {Sharon L.} and BethAnn McLaughlin and McLean, {Pamela J.} and McMaster, {Christopher R.} and McQuibban, {G. Angus} and Meijer, {Alfred J.} and Meisler, {Miriam H.} and Alicia Melendez and Melia, {Thomas J.} and Gerry Melino and Mena, {Maria A.} and Menendez, {Javier A.} and Menna-Barreto, {Rubem F. S.} and Menon, {Manoj B.} and Menzies, {Fiona M.} and Mercer, {Carol A.} and Adalberto Merighi and Merry, {Diane E.} and Stefania Meschini and Meyer, {Christian G.} and Meyer, {Thomas F.} and Chao-Yu Miao and Jun-Ying Miao and Michels, {Paul A. 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. Javier} and Olsen, {Laura J.} and Stefan Olsson and Onya Opota and Osborne, {Timothy F.} and Ostrander, {Gary K.} and Kinya Otsu and Ou, {Jing-hsiung James} and Mireille Ouimet and Michael Overholtzer and Bulent Ozpolat and Paolo Paganetti and Ugo Pagnini and Nicolas Pallet and Palmer, {Glen E.} and Camilla Palumbo and Tianhong Pan and Theocharis Panaretakis and Pandey, {Udai Bhan} and Zuzana Papackova and Issidora Papassideri and Irmgard Paris and Junsoo Park and Park, {Ohkmae K.} and Parys, {Jan B.} and Parzych, {Katherine R.} and Susann Patschan and Cam Patterson and Sophie Pattingre and Pawelek, {John M.} and Jianxin Peng and Perlmutter, {David H.} and Ida Perrotta and George Perry and Shazib Pervaiz and Matthias Peter and Peters, {Godefridus J.} and Morten Petersen and Goran Petrovski and Phang, {James M.} and Mauro Piacentini and Philippe Pierre and Valerie Pierrefite-Carle and Gerard Pierron and Ronit Pinkas-Kramarski and Antonio Piras and Natik Piri and Platanias, {Leonidas C.} and Stefanie Poeggeler and Marc Poirot and Angelo Poletti and Christian Poues and Mercedes Pozuelo-Rubio and Mette Praetorius-Ibba and Anil Prasad and Mark Prescott and Muriel Priault and Nathalie Produit-Zengaffinen and Ann Progulske-Fox and Tassula Proikas-Cezanne and Serge Przedborski and Karin Przyklenk and Rosa Puertollano and Julien Puyal and Shu-Bing Qian and Liang Qin and Zheng-Hong Qin and Quaggin, {Susan E.} and Nina Raben and Hannah Rabinowich and Rabkin, {Simon W.} and Irfan Rahman and Abdelhaq Rami and Georg Ramm and Glenn Randall and Felix Randow and Rao, {V. 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. M.} and Alison Simmons and Simon, {Anna Katharina} and Hans-Uwe Simon and Cristiano Simone and Anne Simonsen and Sinclair, {David A.} and Rajat Singh and Debasish Sinha and Sinicrope, {Frank A.} and Agnieszka Sirko and Siu, {Parco M.} and Efthimios Sivridis and Vojtech Skop and Skulachev, {Vladimir P.} and Slack, {Ruth S.} and Smaili, {Soraya S.} and Smith, {Duncan R.} and Soengas, {Maria S.} and Thierry Soldati and Xueqin Song and Sood, {Anil K.} and Soong, {Tuck Wah} and Federica Sotgia and Spector, {Stephen A.} and Spies, {Claudia D.} and Wolfdieter Springer and Srinivasula, {Srinivasa M.} and Leonidas Stefanis and Steffan, {Joan S.} and Ruediger Stendel and Harald Stenmark and Anastasis Stephanou and Stern, {Stephan T.} and Cinthya Sternberg and Bjoern Stork and Peter Stralfors and Subauste, {Carlos S.} and Xinbing Sui and David Sulzer and Jiaren Sun and Shi-Yong Sun and Zhi-Jun Sun and Sung, {Joseph J. Y.} and Kuninori Suzuki and Toshihiko Suzuki and Swanson, {Michele S.} and Charles Swanton and Sweeney, {Sean T.} and Lai-King Sy and Gyorgy Szabadkai and Ira Tabas and Heinrich Taegtmeyer and Marco Tafani and Krisztina Takacs-Vellai and Yoshitaka Takano and Kaoru Takegawa and Genzou Takemura and Fumihiko Takeshita and Talbot, {Nicholas J.} and Tan, {Kevin S. W.} and Keiji Tanaka and Kozo Tanaka and Daolin Tang and Dingzhong Tang and Isei Tanida and Tannous, {Bakhos A.} and Nektarios Tavernarakis and Taylor, {Graham S.} and Taylor, {Gregory A.} and Taylor, {J. Paul} and Terada, {Lance S.} and Alexei Terman and Gianluca Tettamanti and Karin Thevissen and Thompson, {Craig B.} and Andrew Thorburn and Michael Thumm and FengFeng Tian and Yuan Tian and Glauco Tocchini-Valentini and Tolkovsky, {Aviva M.} and Yasuhiko Tomino and Lars Toenges and Tooze, {Sharon A.} and Cathy Tournier and John Tower and Roberto Towns and Vladimir Trajkovic and Travassos, {Leonardo H.} and Ting-Fen Tsai and Tschan, {Mario P.} and Takeshi Tsubata and Allan Tsung and Boris Turk and Turner, {Lorianne S.} and Tyagi, {Suresh C.} and Yasuo Uchiyama and Takashi Ueno and Midori Umekawa and Rika Umemiya-Shirafuji and Unni, {Vivek K.} and Vaccaro, {Maira I.} and Valente, {Enza Maria} and {Van den Berghe}, Greet and {van der Klei}, {Ida J.} and {van Doorn}, {Wouter G.} and {van Dyk}, {Linda F.} and {van Egmond}, Marjolein and {van Grunsven}, {Leo A.} and Peter Vandenabeele and Vandenberghe, {Wim P.} and Ilse Vanhorebeek and Vaquero, {Eva C.} and Guillermo Velasco and Tibor Vellai and Vicencio, {Jose Miguel} and Vierstra, {Richard D.} and Miquel Vila and Cecile Vindis and Giampietro Viola and Viscomi, {Maria Teresa} and Voitsekhovskaja, {Olga V.} and {von Haefen}, Clarissa and Marcela Votruba and Keiji Wada and Richard Wade-Martins and Walker, {Cheryl L.} and Walsh, {Craig M.} and Jochen Walter and Xiang-Bo Wan and Aimin Wang and Chenguang Wang and Dawei Wang and Fan Wang and Fen Wang and Guanghui Wang and Haichao Wang and Hong-Gang Wang and Horng-Dar Wang and Jin Wang and Ke Wang and Mei Wang and Wang, {Richard C.} and Xinglong Wang and Xuejun Wang and Ying-Jan Wang and Yipeng Wang and Zhen Wang and Wang, {Zhigang Charles} and Zhinong Wang and Wansink, {Derick G.} and Ward, {Diane M.} and Hirotaka Watada and Waters, {Sarah L.} and Paul Webster and Lixin Wei and Weihl, {Conrad C.} and Weiss, {William A.} and Welford, {Scott M.} and Long-Ping Wen and Whitehouse, {Caroline A.} and Whitton, {J. Lindsay} and Whitworth, {Alexander J.} and Tom Wileman and Wiley, {John W.} and Simon Wilkinson and Dieter Willbold and Williams, {Roger L.} and Williamson, {Peter R.} and Wouters, {Bradly G.} and Chenghan Wu and Dao-Cheng Wu and Wu, {William K. K.} and Andreas Wyttenbach and Xavier, {Ramnik J.} and Zhijun Xi and Pu Xia and Gengfu Xiao and Zhiping Xie and Zhonglin Xie and Da-zhi Xu and Jianzhen Xu and Liang Xu and Xiaolei Xu and Ai Yamamoto and Akitsugu Yamamoto and Shunhei Yamashina and Michiaki Yamashita and Xianghua Yan and Mitsuhiro Yanagida and Dun-Sheng Yang and Elizabeth Yang and Jin-Ming Yang and Yang, {Shi Yu} and Wannian Yang and Yang, {Wei Yuan} and Zhifen Yang and Meng-Chao Yao and Tso-Pang Yao and Behzad Yeganeh and Wei-Lien Yen and Jia-jing Yin and Xiao-Ming Yin and Ook-Joon Yoo and Gyesoon Yoon and Seung-Yong Yoon and Tomohiro Yorimitsu and Yuko Yoshikawa and Tamotsu Yoshimori and Kohki Yoshimoto and You, {Ho Jin} and Youle, {Richard J.} and Anas Younes and Li Yu and Long Yu and Seong-Woon Yu and Yu, {Wai Haung} and Zhi-Min Yuan and Zhenyu Yue and Cheol-Heui Yun and Michisuke Yuzaki and Olga Zabirnyk and Elaine Silva-Zacarin and David Zacks and Eldad Zacksenhaus and Nadia Zaffaroni and Zahra Zakeri and {Zeh III}, {Herbert J.} and Zeitlin, {Scott O.} and Hong Zhang and Hui-Ling Zhang and Jianhua Zhang and Jing-Pu Zhang and Lin Zhang and Long Zhang and Ming-Yong Zhang and Zhang, {Xu Dong} and Mantong Zhao and Yi-Fang Zhao and Ying Zhao and Zhao, {Zhizhuang J.} and Xiaoxiang Zheng and Boris Zhivotovsky and Qing Zhong and Cong-Zhao Zhou and Changlian Zhu and Wei-Guo Zhu and Xiao-Feng Zhu and Xiongwei Zhu and Yuangang Zhu and Teresa Zoladek and Wei-Xing Zong and Antonio Zorzano and Juergen Zschocke and Brian Zuckerbraun",
year = "2012",
doi = "10.4161/auto.19496",
language = "English",
volume = "8",
pages = "445--544",
journal = "Autophagy",
issn = "1554-8635",
publisher = "Landes Bioscience",
number = "4",