Guidelines for the use and interpretation of assays for monitoring autophagy
(2012) In Autophagy 8(4). p.445-544- 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... (More)
- 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. (Less)
Please use this url to cite or link to this publication:
https://lup.lub.lu.se/record/3188191
- author
- organization
- publishing date
- 2012
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- autolysosome, autophagosome, flux, LC3, lysosome, phagophore, stress, vacuole
- in
- Autophagy
- volume
- 8
- issue
- 4
- pages
- 445 - 544
- publisher
- Landes Bioscience
- external identifiers
-
- wos:000305403400002
- scopus:84862295360
- ISSN
- 1554-8635
- DOI
- 10.4161/auto.19496
- language
- English
- LU publication?
- yes
- id
- 1941550c-fa31-428d-9646-95702963e4f6 (old id 3188191)
- date added to LUP
- 2016-04-01 09:51:30
- date last changed
- 2022-04-27 07:45:00
@article{1941550c-fa31-428d-9646-95702963e4f6, 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.}}, author = {{Klionsky, Daniel J. and Abdalla, Fabio C. and Abeliovich, Hagai and Abraham, Robert T. and Acevedo-Arozena, Abraham and Adeli, Khosrow and Agholme, Lotta and Agnello, Maria and Agostinis, Patrizia and Aguirre-Ghiso, Julio A. and Ahn, Hyung Jun and Ait-Mohamed, Ouardia and Ait-Si-Ali, Slimane and Akematsu, Takahiko and Akira, Shizuo and Al-Younes, Hesham M. and Al-Zeer, Munir A. and Albert, Matthew L. and Albin, Roger L. and Alegre-Abarrategui, Javier and Aleo, Maria Francesca and Alirezaei, Mehrdad and Almasan, Alexandru and Almonte-Becerril, Maylin and Amano, Atsuo and Amaravadi, Ravi and Amarnath, Shoba and Amer, Amal O. and Andrieu-Abadie, Nathalie and Anantharam, Vellareddy and Ann, David K. and Anoopkumar-Dukie, Shailendra and Aoki, Hiroshi and Apostolova, Nadezda and Arancia, Giuseppe and Aris, John P. and Asanuma, Katsuhiko and Asare, Nana Y. 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Kouri and Kovacs, Attila L. and Kraft, Claudine and Krainc, Dimitri and Kraemer, Helmut and Kretz-Remy, Carole and Krichevsky, Anna M. and Kroemer, Guido and Krueger, Rejko and Krut, Oleg and Ktistakis, Nicholas T. and Kuan, Chia-Yi and Kucharczyk, Roza and Kumar, Ashok and Kumar, Raj and Kumar, Sharad and Kundu, Mondira and Kung, Hsing-Jien and Kurz, Tino and Kwon, Ho Jeong and La Spada, Albert R. and Lafont, Frank and Lamark, Trond and Landry, Jacques and Lane, Jon D. and Lapaquette, Pierre and Laporte, Jocelyn F. and Laszlo, Lajos and Lavandero, Sergio and Lavoie, Josee N. and Layfield, Robert and Lazo, Pedro A. and Le, Weidong and Le Cam, Laurent and Ledbetter, Daniel J. and Lee, Alvin J. 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Angus and Meijer, Alfred J. and Meisler, Miriam H. and Melendez, Alicia and Melia, Thomas J. and Melino, Gerry 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 Merighi, Adalberto and Merry, Diane E. and Meschini, Stefania and Meyer, Christian G. and Meyer, Thomas F. and Miao, Chao-Yu and Miao, Jun-Ying and Michels, Paul A. M. and Michiels, Carine and Mijaljica, Dalibor and Milojkovic, Ana and Minucci, Saverio and Miracco, Clelia and Miranti, Cindy K. and Mitroulis, Ioannis and Miyazawa, Keisuke and Mizushima, Noboru and Mograbi, Baharia and Mohseni, Simin and Molero, Xavier and Mollereau, Bertrand and Mollinedo, Faustino and Momoi, Takashi and Monastyrska, Iryna and Monick, Martha M. and Monteiro, Mervyn J. and Moore, Michael N. and Mora, Rodrigo and Moreau, Kevin and Moreira, Paula I. and Moriyasu, Yuji and Moscat, Jorge and Mostowy, Serge and Mottram, Jeremy C. and Motyl, Tomasz and Moussa, Charbel E. -H. and Mueller, Sylke and Muenger, Karl and Muenz, Christian and Murphy, Leon O. and Murphy, Maureen E. and Musaro, Antonio and Mysorekar, Indira and Nagata, Eiichiro and Nagata, Kazuhiro and Nahimana, Aimable and Nair, Usha and Nakagawa, Toshiyuki and Nakahira, Kiichi and Nakano, Hiroyasu and Nakataogawa, Hitoshi and Nanjundan, Meera and Naqvi, Naweed I. and Narendra, Derek P. and Narita, Masashi and Navarro, Miguel and Nawrocki, Steffan T. and Nazarko, Taras Y. and Nemchenko, Andriy and Netea, Mihai G. and Neufeld, Thomas P. and Ney, Paul A. and Nezis, Ioannis P. and Nguyen, Huu Phuc and Nie, Daotai and Nishino, Ichizo and Nislow, Corey and Nixon, Ralph A. and Noda, Takeshi and Noegel, Angelika A. and Nogalska, Anna and Noguchi, Satoru and Notterpek, Lucia and Novak, Ivana and Nozaki, Tomoyoshi and Nukina, Nobuyuki and Nuernberger, Thorsten and Nyfeler, Beat and Obara, Keisuke and Oberley, Terry D. and Oddo, Salvatore and Ogawa, Michinaga and Ohashi, Toya and Okamoto, Koji and Oleinick, Nancy L. and Oliver, F. Javier and Olsen, Laura J. and Olsson, Stefan and Opota, Onya and Osborne, Timothy F. and Ostrander, Gary K. and Otsu, Kinya and Ou, Jing-hsiung James and Ouimet, Mireille and Overholtzer, Michael and Ozpolat, Bulent and Paganetti, Paolo and Pagnini, Ugo and Pallet, Nicolas and Palmer, Glen E. and Palumbo, Camilla and Pan, Tianhong and Panaretakis, Theocharis and Pandey, Udai Bhan and Papackova, Zuzana and Papassideri, Issidora and Paris, Irmgard and Park, Junsoo and Park, Ohkmae K. and Parys, Jan B. and Parzych, Katherine R. and Patschan, Susann and Patterson, Cam and Pattingre, Sophie and Pawelek, John M. and Peng, Jianxin and Perlmutter, David H. and Perrotta, Ida and Perry, George and Pervaiz, Shazib and Peter, Matthias and Peters, Godefridus J. and Petersen, Morten and Petrovski, Goran and Phang, James M. and Piacentini, Mauro and Pierre, Philippe and Pierrefite-Carle, Valerie and Pierron, Gerard and Pinkas-Kramarski, Ronit and Piras, Antonio and Piri, Natik and Platanias, Leonidas C. and Poeggeler, Stefanie and Poirot, Marc and Poletti, Angelo and Poues, Christian and Pozuelo-Rubio, Mercedes and Praetorius-Ibba, Mette and Prasad, Anil and Prescott, Mark and Priault, Muriel and Produit-Zengaffinen, Nathalie and Progulske-Fox, Ann and Proikas-Cezanne, Tassula and Przedborski, Serge and Przyklenk, Karin and Puertollano, Rosa and Puyal, Julien and Qian, Shu-Bing and Qin, Liang and Qin, Zheng-Hong and Quaggin, Susan E. and Raben, Nina and Rabinowich, Hannah and Rabkin, Simon W. and Rahman, Irfan and Rami, Abdelhaq and Ramm, Georg and Randall, Glenn and Randow, Felix and Rao, V. Ashutosh and Rathmell, Jeffrey C. and Ravikumar, Brinda and Ray, Swapan K. and Reed, Bruce H. and Reed, John C. and Reggiori, Fulvio and Regnier-Vigouroux, Anne and Reichert, Andreas S. and Reiners, John J. and Reiter, Russel J. and Ren, Jun and Revuelta, Jose L. and Rhodes, Christopher J. and Ritis, Konstantinos and Rizzo, Elizete and Robbins, Jeffrey and Roberge, Michel and Roca, Hernan and Roccheri, Maria C. and Rocchi, Stephane and Rodemann, H. Peter and de Cordoba, Santiago Rodriguez and Rohrer, Baerbel and Roninson, Igor B. and Rosen, Kirill and Rost-Roszkowska, Magdalena M. and Rouis, Mustapha and Rouschop, Kasper M. A. and Rovetta, Francesca and Rubin, Brian P. and Rubinsztein, David C. and Ruckdeschel, Klaus and Rucker, Edmund B and Rudich, Assaf and Rudolf, Emil and Ruiz-Opazo, Nelson and Russo, Rossella and Rusten, Tor Erik and Ryan, Kevin M. and Ryter, Stefan W. and Sabatini, David M. and Sadoshima, Junichi and Saha, Tapas and Saitoh, Tatsuya and Sakagami, Hiroshi and Sakai, Yasuyoshi and Salekdeh, Ghasem Hoseini and Salomoni, Paolo and Salvaterra, Paul M. and Salvesen, Guy and Salvioli, Rosa and Sanchez, Anthony M. J. and Sanchez-Alcazar, Jose A. and Sanchez-Prieto, Ricardo and Sandri, Marco and Sankar, Uma and Sansanwal, Poonam and Santambrogio, Laura and Saran, Shweta and Sarkar, Sovan and Sarwal, Minnie and Sasakawa, Chihiro and Sasnauskiene, Ausra and Sass, Miklos and Sato, Ken and Sato, Miyuki and Schapira, Anthony H. V. and Scharl, Michael and Schaetzl, Hermann M. and Scheper, Wiep and Schiaffino, Stefano and Schneider, Claudio and Schneider, Marion E. and Schneider-Stock, Regine and Schoenlein, Patricia V. and Schorderet, Daniel F. and Schueller, Christoph and Schwartz, Gary K. and Scorrano, Luca and Sealy, Linda and Seglen, Per O. and Segura-Aguilar, Juan and Seiliez, Iban and Seleverstov, Oleksandr and Sell, Christian and Seo, Jong Bok and Separovic, Duska and Setaluri, Vijayasaradhi and Setoguchi, Takao and Settembre, Carmine and Shacka, John J. and Shanmugam, Mala and Shapiro, Irving M. and Shaulian, Eitan and Shaw, Reuben J. and Shelhamer, James H. and Shen, Han-Ming and Shen, Wei-Chiang and Sheng, Zu-Hang and Shi, Yang and Shibuya, Kenichi and Shidoji, Yoshihiro and Shieh, Jeng-Jer and Shih, Chwen-Ming and Shimada, Yohta and Shimizu, Shigeomi and Shintani, Takahiro and Shirihai, Orian S. and Shore, Gordon C. and Sibirny, Andriy A. and Sidhu, Stan B. and Sikorska, Beata and Silva-Zacarin, Elaine C. M. and Simmons, Alison and Simon, Anna Katharina and Simon, Hans-Uwe and Simone, Cristiano and Simonsen, Anne and Sinclair, David A. and Singh, Rajat and Sinha, Debasish and Sinicrope, Frank A. and Sirko, Agnieszka and Siu, Parco M. and Sivridis, Efthimios and Skop, Vojtech and Skulachev, Vladimir P. and Slack, Ruth S. and Smaili, Soraya S. and Smith, Duncan R. and Soengas, Maria S. and Soldati, Thierry and Song, Xueqin and Sood, Anil K. and Soong, Tuck Wah and Sotgia, Federica and Spector, Stephen A. and Spies, Claudia D. and Springer, Wolfdieter and Srinivasula, Srinivasa M. and Stefanis, Leonidas and Steffan, Joan S. and Stendel, Ruediger and Stenmark, Harald and Stephanou, Anastasis and Stern, Stephan T. and Sternberg, Cinthya and Stork, Bjoern and Stralfors, Peter and Subauste, Carlos S. and Sui, Xinbing and Sulzer, David and Sun, Jiaren and Sun, Shi-Yong and Sun, Zhi-Jun and Sung, Joseph J. Y. and Suzuki, Kuninori and Suzuki, Toshihiko and Swanson, Michele S. and Swanton, Charles and Sweeney, Sean T. and Sy, Lai-King and Szabadkai, Gyorgy and Tabas, Ira and Taegtmeyer, Heinrich and Tafani, Marco and Takacs-Vellai, Krisztina and Takano, Yoshitaka and Takegawa, Kaoru and Takemura, Genzou and Takeshita, Fumihiko and Talbot, Nicholas J. and Tan, Kevin S. W. and Tanaka, Keiji and Tanaka, Kozo and Tang, Daolin and Tang, Dingzhong and Tanida, Isei and Tannous, Bakhos A. and Tavernarakis, Nektarios and Taylor, Graham S. and Taylor, Gregory A. and Taylor, J. Paul and Terada, Lance S. and Terman, Alexei and Tettamanti, Gianluca and Thevissen, Karin and Thompson, Craig B. and Thorburn, Andrew and Thumm, Michael and Tian, FengFeng and Tian, Yuan and Tocchini-Valentini, Glauco and Tolkovsky, Aviva M. and Tomino, Yasuhiko and Toenges, Lars and Tooze, Sharon A. and Tournier, Cathy and Tower, John and Towns, Roberto and Trajkovic, Vladimir and Travassos, Leonardo H. and Tsai, Ting-Fen and Tschan, Mario P. and Tsubata, Takeshi and Tsung, Allan and Turk, Boris and Turner, Lorianne S. and Tyagi, Suresh C. and Uchiyama, Yasuo and Ueno, Takashi and Umekawa, Midori and Umemiya-Shirafuji, Rika 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 Vandenabeele, Peter and Vandenberghe, Wim P. and Vanhorebeek, Ilse and Vaquero, Eva C. and Velasco, Guillermo and Vellai, Tibor and Vicencio, Jose Miguel and Vierstra, Richard D. and Vila, Miquel and Vindis, Cecile and Viola, Giampietro and Viscomi, Maria Teresa and Voitsekhovskaja, Olga V. and von Haefen, Clarissa and Votruba, Marcela and Wada, Keiji and Wade-Martins, Richard and Walker, Cheryl L. and Walsh, Craig M. and Walter, Jochen and Wan, Xiang-Bo and Wang, Aimin and Wang, Chenguang and Wang, Dawei and Wang, Fan and Wang, Fen and Wang, Guanghui and Wang, Haichao and Wang, Hong-Gang and Wang, Horng-Dar and Wang, Jin and Wang, Ke and Wang, Mei and Wang, Richard C. and Wang, Xinglong and Wang, Xuejun and Wang, Ying-Jan and Wang, Yipeng and Wang, Zhen and Wang, Zhigang Charles and Wang, Zhinong and Wansink, Derick G. and Ward, Diane M. and Watada, Hirotaka and Waters, Sarah L. and Webster, Paul and Wei, Lixin and Weihl, Conrad C. and Weiss, William A. and Welford, Scott M. and Wen, Long-Ping and Whitehouse, Caroline A. and Whitton, J. Lindsay and Whitworth, Alexander J. and Wileman, Tom and Wiley, John W. and Wilkinson, Simon and Willbold, Dieter and Williams, Roger L. and Williamson, Peter R. and Wouters, Bradly G. and Wu, Chenghan and Wu, Dao-Cheng and Wu, William K. K. and Wyttenbach, Andreas and Xavier, Ramnik J. and Xi, Zhijun and Xia, Pu and Xiao, Gengfu and Xie, Zhiping and Xie, Zhonglin and Xu, Da-zhi and Xu, Jianzhen and Xu, Liang and Xu, Xiaolei and Yamamoto, Ai and Yamamoto, Akitsugu and Yamashina, Shunhei and Yamashita, Michiaki and Yan, Xianghua and Yanagida, Mitsuhiro and Yang, Dun-Sheng and Yang, Elizabeth and Yang, Jin-Ming and Yang, Shi Yu and Yang, Wannian and Yang, Wei Yuan and Yang, Zhifen and Yao, Meng-Chao and Yao, Tso-Pang and Yeganeh, Behzad and Yen, Wei-Lien and Yin, Jia-jing and Yin, Xiao-Ming and Yoo, Ook-Joon and Yoon, Gyesoon and Yoon, Seung-Yong and Yorimitsu, Tomohiro and Yoshikawa, Yuko and Yoshimori, Tamotsu and Yoshimoto, Kohki and You, Ho Jin and Youle, Richard J. and Younes, Anas and Yu, Li and Yu, Long and Yu, Seong-Woon and Yu, Wai Haung and Yuan, Zhi-Min and Yue, Zhenyu and Yun, Cheol-Heui and Yuzaki, Michisuke and Zabirnyk, Olga and Silva-Zacarin, Elaine and Zacks, David and Zacksenhaus, Eldad and Zaffaroni, Nadia and Zakeri, Zahra and Zeh III, Herbert J. and Zeitlin, Scott O. and Zhang, Hong and Zhang, Hui-Ling and Zhang, Jianhua and Zhang, Jing-Pu and Zhang, Lin and Zhang, Long and Zhang, Ming-Yong and Zhang, Xu Dong and Zhao, Mantong and Zhao, Yi-Fang and Zhao, Ying and Zhao, Zhizhuang J. and Zheng, Xiaoxiang and Zhivotovsky, Boris and Zhong, Qing and Zhou, Cong-Zhao and Zhu, Changlian and Zhu, Wei-Guo and Zhu, Xiao-Feng and Zhu, Xiongwei and Zhu, Yuangang and Zoladek, Teresa and Zong, Wei-Xing and Zorzano, Antonio and Zschocke, Juergen and Zuckerbraun, Brian}}, issn = {{1554-8635}}, keywords = {{autolysosome; autophagosome; flux; LC3; lysosome; phagophore; stress; vacuole}}, language = {{eng}}, number = {{4}}, pages = {{445--544}}, publisher = {{Landes Bioscience}}, series = {{Autophagy}}, title = {{Guidelines for the use and interpretation of assays for monitoring autophagy}}, url = {{http://dx.doi.org/10.4161/auto.19496}}, doi = {{10.4161/auto.19496}}, volume = {{8}}, year = {{2012}}, }