Guidelines for the use and interpretation of assays for monitoring autophagy

Guidelines for the use and interpretation of assays for monitoring autophagy

Author Klionsky, Daniel J. Google Scholar
Abdalla, Fabio Camargo Google Scholar
Abeliovich, Hagai Google Scholar
Abraham, Robert T. Google Scholar
Acevedo-Arozena, Abraham Google Scholar
Adeli, Khosrow Google Scholar
Agholme, Lotta Google Scholar
Agnello, Maria Google Scholar
Agostinis, Patrizia Google Scholar
Aguirre-Ghiso, Julio A. Google Scholar
Ahn, Hyung Jun Google Scholar
Ait-Mohamed, Ouardia Google Scholar
Ait-Si-Ali, Slimane Google Scholar
Akematsu, Takahiko Google Scholar
Akira, Shizuo Google Scholar
Al-Younes, Hesham M. Google Scholar
Al-Zeer, Munir A. Google Scholar
Albert, Matthew L. Google Scholar
Albin, Roger L. Google Scholar
Alegre-Abarrategui, Javier Google Scholar
Aleo, Maria Francesca Google Scholar
Alirezaei, Mehrdad Google Scholar
Almasan, Alexandru Google Scholar
Almonte-Becerril, Maylin Google Scholar
Amano, Atsuo Google Scholar
Amaravadi, Ravi Google Scholar
Amarnath, Shoba Google Scholar
Amer, Amal O. Google Scholar
Andrieu-Abadie, Nathalie Google Scholar
Anantharam, Vellareddy Google Scholar
Ann, David K. Google Scholar
Anoopkumar-Dukie, Shailendra Google Scholar
Aoki, Hiroshi Google Scholar
Apostolova, Nadezda Google Scholar
Arancia, Giuseppe Google Scholar
Aris, John P. Google Scholar
Asanuma, Katsuhiko Google Scholar
Asare, Nana Y. O. Google Scholar
Ashida, Hisashi Google Scholar
Askanas, Valerie Google Scholar
Askew, David S. Google Scholar
Auberger, Patrick Google Scholar
Baba, Misuzu Google Scholar
Backues, Steven K. Google Scholar
Baehrecke, Eric H. Google Scholar
Bahr, Ben A. Google Scholar
Bai, Xue-Yuan Google Scholar
Bailly, Yannick Google Scholar
Baiocchi, Robert Google Scholar
Baldini, Giulia Google Scholar
Balduini, Walter Google Scholar
Ballabio, Andrea Google Scholar
Bamber, Bruce A. Google Scholar
Bampton, Edward T. W. Google Scholar
Banhegyi, Gabor Google Scholar
Bartholomew, Clinton R. Google Scholar
Bassham, Diane C. Google Scholar
Bast, Robert C. Google Scholar
Batoko, Henri Google Scholar
Bay, Boon-Huat Google Scholar
Beau, Isabelle Google Scholar
Bechet, Daniel M. Google Scholar
Begley, Thomas J. Google Scholar
Behl, Christian Google Scholar
Behrends, Christian Google Scholar
Bekri, Soumeya Google Scholar
Bellaire, Bryan Google Scholar
Bendall, Linda J. Google Scholar
Benetti, Luca Google Scholar
Berliocchi, Laura Google Scholar
Bernardi, Henri Google Scholar
Bernassola, Francesca Google Scholar
Besteiro, Sebastien Google Scholar
Bhatia-Kissova, Ingrid Google Scholar
Bi, Xiaoning Google Scholar
Biard-Piechaczyk, Martine Google Scholar
Blum, Janice S. Google Scholar
Boise, Lawrence H. Google Scholar
Bonaldo, Paolo Google Scholar
Boone, David L. Google Scholar
Bornhauser, Beat C. Google Scholar
Bortoluci, Karina Ramalho Autor UNIFESP Google Scholar
Bossis, Ioannis Google Scholar
Bost, Frederic Google Scholar
Bourquin, Jean-Pierre Google Scholar
Boya, Patricia Google Scholar
Boyer-Guittaut, Michael Google Scholar
Bozhkov, Peter V. Google Scholar
Brady, Nathan R. Google Scholar
Brancolini, Claudio Google Scholar
Brech, Andreas Google Scholar
Brenman, Jay E. Google Scholar
Brennand, Ana Google Scholar
Bresnick, Emery H. Google Scholar
Brest, Patrick Google Scholar
Bridges, Dave Google Scholar
Bristol, Molly L. Google Scholar
Brookes, Paul S. Google Scholar
Brown, Eric J. Google Scholar
Brumell, John H. Google Scholar
Brunetti-Pierri, Nicola Google Scholar
Brunk, Ulf T. Google Scholar
Bulman, Dennis E. Google Scholar
Bultman, Scott J. Google Scholar
Bultynck, Greet Google Scholar
Burbulla, Lena F. Google Scholar
Bursch, Wilfried Google Scholar
Butchar, Jonathan P. Google Scholar
Buzgariu, Wanda Google Scholar
Bydlowski, Sergio P. Google Scholar
Cadwell, Ken Google Scholar
Cahova, Monika Google Scholar
Cai, Dongsheng Google Scholar
Cai, Jiyang Google Scholar
Cai, Qian Google Scholar
Calabretta, Bruno Google Scholar
Calvo-Garrido, Javier Google Scholar
Camougrand, Nadine Google Scholar
Campanella, Michelangelo Google Scholar
Campos-Salinas, Jenny Google Scholar
Candi, Eleonora Google Scholar
Cao, Lizhi Google Scholar
Caplan, Allan B. Google Scholar
Carding, Simon R. Google Scholar
Cardoso, Sandra M. Google Scholar
Carew, Jennifer S. Google Scholar
Carlin, Cathleen R. Google Scholar
Carmignac, Virgine Google Scholar
Carneiro, Leticia A. M. Google Scholar
Carra, Serena Google Scholar
Caruso, Rosario A. Google Scholar
Casari, Giorgio Google Scholar
Casas, Caty Google Scholar
Castino, Roberta Google Scholar
Cebollero, Eduardo Google Scholar
Cecconi, Francesco Google Scholar
Celli, Jean Google Scholar
Chaachouay, Hassan Google Scholar
Chae, Han-Jung Google Scholar
Chai, Chee-Yin Google Scholar
Chan, David C. Google Scholar
Chan, Edmond Y. Google Scholar
Chang, Raymond Chuen-Chung Google Scholar
Che, Chi-Ming Google Scholar
Chen, Ching-Chow Google Scholar
Chen, Guang-Chao Google Scholar
Chen, Guo-Qiang Google Scholar
Chen, Min Google Scholar
Chen, Quan Google Scholar
Chen, Steve S. -L. Google Scholar
Chen, WenLi Google Scholar
Chen, Xi Google Scholar
Chen, Xiangmei Google Scholar
Chen, Xiequn Google Scholar
Chen, Ye-Guang Google Scholar
Chen, Yingyu Google Scholar
Chen, Yongqiang Google Scholar
Chen, Yu-Jen Google Scholar
Chen, Zhixiang Google Scholar
Cheng, Alan Google Scholar
Cheng, Christopher H. K. Google Scholar
Cheng, Yan Google Scholar
Cheong, Heesun Google Scholar
Cheong, Jae-Ho Google Scholar
Cherry, Sara Google Scholar
Chess-Williams, Russ Google Scholar
Cheung, Zelda H. Google Scholar
Chevet, Eric Google Scholar
Chiang, Hui-Ling Google Scholar
Chiarelli, Roberto Google Scholar
Chiba, Tomoki Google Scholar
Chin, Lih-Shen Google Scholar
Chiou, Shih-Hwa Google Scholar
Chisari, Francis V. Google Scholar
Cho, Chi Hin Google Scholar
Cho, Dong-Hyung Google Scholar
Choi, Augustine M. K. Google Scholar
Choi, DooSeok Google Scholar
Choi, Kyeong Sook Google Scholar
Choi, Mary E. Google Scholar
Chouaib, Salem Google Scholar
Choubey, Divaker Google Scholar
Choubey, Vinay Google Scholar
Chu, Charleen T. Google Scholar
Chuang, Tsung-Hsien Google Scholar
Chueh, Sheau-Huei Google Scholar
Chun, Taehoon Google Scholar
Chwae, Yong-Joon Google Scholar
Chye, Mee-Len Google Scholar
Ciarcia, Roberto Google Scholar
Ciriolo, Maria R. Google Scholar
Clague, Michael J. Google Scholar
Clark, Robert S. B. Google Scholar
Clarke, Peter G. H. Google Scholar
Clarke, Robert Google Scholar
Codogno, Patrice Google Scholar
Coller, Hilary A. Google Scholar
Colombo, Maria I. Google Scholar
Comincini, Sergio Google Scholar
Condello, Maria Google Scholar
Condorelli, Fabrizio Google Scholar
Cookson, Mark R. Google Scholar
Coppens, Graham H. Coombs Isabelle Google Scholar
Corbalan, Ramon Google Scholar
Cossart, Pascale Google Scholar
Costelli, Paola Google Scholar
Costes, Safia Google Scholar
Coto-Montes, Ana Google Scholar
Couve, Eduardo Google Scholar
Coxon, Fraser P. Google Scholar
Cregg, James M. Google Scholar
Crespo, Jose L. Google Scholar
Cronje, Marianne J. Google Scholar
Cuervo, Ana Maria Google Scholar
Cullen, Joseph J. Google Scholar
Czaja, Mark J. Google Scholar
D'Amelio, Marcello Google Scholar
Darfeuille-Michaud, Arlette Google Scholar
Davids, Lester M. Google Scholar
Davies, Faith E. Google Scholar
De Felici, Massimo Google Scholar
Groot, John F. de Google Scholar
Haan, Cornelis A. M. de Google Scholar
De Martino, Luisa Google Scholar
De Milito, Angelo Google Scholar
De Tata, Vincenzo Google Scholar
Debnath, Jayanta Google Scholar
Degterev, Alexei Google Scholar
Dehay, Benjamin Google Scholar
Delbridge, Lea M. D. Google Scholar
Demarchi, Francesca Google Scholar
Deng, Yi Zhen Google Scholar
Dengjel, Joen Google Scholar
Dent, Paul Google Scholar
Denton, Donna Google Scholar
Deretic, Vojo Google Scholar
Desai, Shyamal D. Google Scholar
Devenish, Rodney J. Google Scholar
Di Gioacchino, Mario Google Scholar
Di Paolo, Gilbert Google Scholar
Di Pietro, Chiara Google Scholar
Diaz-Araya, Guillermo Google Scholar
Diaz-Laviada, Ines Google Scholar
Diaz-Meco, Maria T. Google Scholar
Diaz-Nido, Javier Google Scholar
Dikic, Ivan Google Scholar
Dinesh-Kumar, Savithramma P. Google Scholar
Ding, Wen-Xing Google Scholar
Distelhorst, Clark W. Google Scholar
Diwan, Abhinav Google Scholar
Djavaheri-Mergny, Mojgan Google Scholar
Dokudovskaya, Svetlana Google Scholar
Dong, Zheng Google Scholar
Dorsey, Frank C. Google Scholar
Dosenko, Victor Google Scholar
Dowling, James J. Google Scholar
Doxsey, Stephen Google Scholar
Dreux, Marlene Google Scholar
Drew, Mark E. Google Scholar
Duan, Qiuhong Google Scholar
Duchosal, Michel A. Google Scholar
Duff, Karen Google Scholar
Dugail, Isabelle Google Scholar
Durbeej, Madeleine Google Scholar
Duszenko, Michael Google Scholar
Edelstein, Charles L. Google Scholar
Edinger, Aimee L. Google Scholar
Egea, Gustavo Google Scholar
Eichinger, Ludwig Google Scholar
Eissa, N. Tony Google Scholar
Ekmekcioglu, Suhendan Google Scholar
El-Deiry, Wafik S. Google Scholar
Elazar, Zvulun Google Scholar
Elgendy, Mohamed Google Scholar
Ellerby, Lisa M. Google Scholar
Eng, Kai Er Google Scholar
Engelbrecht, Anna-Mart Google Scholar
Engelender, Simone Google Scholar
Erenpreisa, Jekaterina Google Scholar
Escalante, Ricardo Google Scholar
Esclatine, Audrey Google Scholar
Eskelinen, Eeva-Liisa Google Scholar
Espert, Lucile Google Scholar
Espina, Virginia Google Scholar
Fan, Huizhou Google Scholar
Fan, Jia Google Scholar
Fan, Qi-Wen Google Scholar
Fan, Zhen Google Scholar
Fang, Shengyun Google Scholar
Fang, Yongqi Google Scholar
Fanto, Manolis Google Scholar
Fanzani, Alessandro Google Scholar
Farkas, Thomas Google Scholar
Farre, Jean-Claude Google Scholar
Faure, Mathias Google Scholar
Fechheimer, Marcus Google Scholar
Feng, Carl G. Google Scholar
Feng, Jian Google Scholar
Feng, Qili Google Scholar
Feng, Youji Google Scholar
Fesues, Laszlo Google Scholar
Feuer, Ralph Google Scholar
Figueiredo-Pereira, Maria E. Google Scholar
Fimia, Gian Maria Google Scholar
Fingar, Diane C. Google Scholar
Finkbeiner, Steven Google Scholar
Finkel, Toren Google Scholar
Finley, Kim D. Google Scholar
Fiorito, Filomena Google Scholar
Fisher, Edward A. Google Scholar
Fisher, Paul B. Google Scholar
Flajolet, Marc Google Scholar
Florez-McClure, Maria L. Google Scholar
Florio, Salvatore Google Scholar
Fon, Edward A. Google Scholar
Fornai, Francesco Google Scholar
Fortunato, Franco Google Scholar
Fotedar, Rati Google Scholar
Fowler, Daniel H. Google Scholar
Fox, Howard S. Google Scholar
Franco, Rodrigo Google Scholar
Frankel, Lisa B. Google Scholar
Fransen, Marc Google Scholar
Fuentes, Jose M. Google Scholar
Fueyo, Juan Google Scholar
Fujii, Jun Google Scholar
Fujisaki, Kozo Google Scholar
Fujita, Eriko Google Scholar
Fukuda, Mitsunori Google Scholar
Furukawa, Ruth H. Google Scholar
Gaestel, Matthias Google Scholar
Gailly, Philippe Google Scholar
Gajewska, Malgorzata Google Scholar
Galliot, Brigitte Google Scholar
Galy, Vincent Google Scholar
Ganesh, Subramaniam Google Scholar
Ganetzky, Barry Google Scholar
Ganley, Ian G. Google Scholar
Gao, Fen-Biao Google Scholar
Gao, George F. Google Scholar
Gao, Jinming Google Scholar
Garcia, Lorena Google Scholar
Garcia-Manero, Guillermo Google Scholar
Garcia-Marcos, Mikel Google Scholar
Garmyn, Marjan Google Scholar
Gartel, Andrei L. Google Scholar
Gatti, Evelina Google Scholar
Gautel, Mathias Google Scholar
Gawriluk, Thomas R. Google Scholar
Gegg, Matthew E. Google Scholar
Geng, Jiefei Google Scholar
Germain, Marc Google Scholar
Gestwicki, Jason E. Google Scholar
Gewirtz, David A. Google Scholar
Ghavami, Saeid Google Scholar
Ghosh, Pradipta Google Scholar
Giammarioli, Anna M. Google Scholar
Giatromanolaki, Alexandra N. Google Scholar
Gibson, Spencer B. Google Scholar
Gilkerson, Robert W. Google Scholar
Ginger, Michael L. Google Scholar
Ginsberg, Henry N. Google Scholar
Golab, Jakub Google Scholar
Goligorsky, Michael S. Google Scholar
Golstein, Pierre Google Scholar
Gomez-Manzano, Candelaria Google Scholar
Goncu, Ebru Google Scholar
Gongora, Celine Google Scholar
Gonzalez, Claudio D. Google Scholar
Gonzalez, Ramon Google Scholar
Gonzalez-Estevez, Cristina Google Scholar
Gonzalez-Polo, Rosa Ana Google Scholar
Gonzalez-Rey, Elena Google Scholar
Gorbunov, Nikolai V. Google Scholar
Gorski, Sharon Google Scholar
Goruppi, Sandro Google Scholar
Gottlieb, Roberta A. Google Scholar
Gozuacik, Devrim Google Scholar
Granato, Giovanna Elvira Google Scholar
Grant, Gary D. Google Scholar
Green, Kim N. Google Scholar
Gregorc, Ales Google Scholar
Gros, Frederic Google Scholar
Grose, Charles Google Scholar
Grunt, Thomas W. Google Scholar
Gual, Philippe Google Scholar
Guan, Jun-Lin Google Scholar
Guan, Kun-Liang Google Scholar
Guichard, Sylvie M. Google Scholar
Gukovskaya, Anna S. Google Scholar
Gukovsky, Ilya Google Scholar
Gunst, Jan Google Scholar
Gustafsson, Asa B. Google Scholar
Halayko, Andrew J. Google Scholar
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Halonen, Sandra K. Google Scholar
Hamasaki, Maho Google Scholar
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Hansen, Malene Google Scholar
Harada, Hisashi Google Scholar
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Hardt, Stefan E. Google Scholar
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Johansen, Terje Google Scholar
Johnson, Daniel E. Google Scholar
Johnson, Gail V. W. Google Scholar
Jones, Nicola L. Google Scholar
Joseph, Bertrand Google Scholar
Joseph, Suresh K. Google Scholar
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Juhasz, Gabor Google Scholar
Juillerat-Jeanneret, Lucienne Google Scholar
Jung, Chang Hwa Google Scholar
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Kaarniranta, Kai Google Scholar
Kaasik, Allen Google Scholar
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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
Language English
Sponsor National Institutes of Health Public Health Service
Grant number National Institutes of Health Public Health Service: GM53396
Date 2012-04-01
Published in Autophagy. Philadelphia: Taylor & Francis Inc, v. 8, n. 4, p. 445-544, 2012.
ISSN 1554-8627 (Sherpa/Romeo, impact factor)
Publisher Taylor & Francis Inc
Extent 445-544
Origin http://dx.doi.org/10.4161/auto.19496
Access rights Open access Open Access
Type Review
Web of Science ID WOS:000305403400002
URI http://repositorio.unifesp.br/handle/11600/34737

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