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-AbarrateguiMaria Francesca Aleo, Mehrdad Alirezaei, Alexandru Almasan, Maylin Almonte-Becerril, Atsuo Amano, Ravi 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 Bánhegyi, 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. 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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, Aleš Gregorc, Frédéric Gros, Charles Grose, Thomas W. 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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. 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2372 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)445-544
Number of pages100
JournalAutophagy
Volume8
Issue number4
DOIs
Publication statusPublished - 2012 Apr 1

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Autophagy
Guidelines
Lysosomes
Eukaryota
Research Personnel
Dictyostelium
Knowledge Bases
Vacuoles
Research
Fungi
Autophagosomes
Technology

ASJC Scopus subject areas

  • Cell Biology
  • Molecular Biology

Cite this

Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., ... Zuckerbraun, B. (2012). Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy, 8(4), 445-544. https://doi.org/10.4161/auto.19496

Guidelines for the use and interpretation of assays for monitoring autophagy. / Klionsky, Daniel J.; Abdalla, Fabio C.; Abeliovich, Hagai; Abraham, Robert T.; Acevedo-Arozena, Abraham; Adeli, Khosrow; Agholme, Lotta; Agnello, Maria; Agostinis, Patrizia; Aguirre-Ghiso, Julio A.; Ahn, Hyung Jun; Ait-Mohamed, Ouardia; Ait-Si-Ali, Slimane; Akematsu, Takahiko; Akira, Shizuo; Al-Younes, Hesham M.; Al-Zeer, Munir A.; Albert, Matthew L.; Albin, Roger L.; Alegre-Abarrategui, Javier; Aleo, Maria Francesca; Alirezaei, Mehrdad; Almasan, Alexandru; Almonte-Becerril, Maylin; Amano, Atsuo; Amaravadi, Ravi; Amarnath, Shoba; Amer, Amal O.; Andrieu-Abadie, Nathalie; Anantharam, Vellareddy; Ann, David K.; Anoopkumar-Dukie, Shailendra; Aoki, Hiroshi; Apostolova, Nadezda; Arancia, Giuseppe; Aris, John P.; Asanuma, Katsuhiko; Asare, Nana Y O; Ashida, Hisashi; Askanas, Valerie; Askew, David S.; Auberger, Patrick; Baba, Misuzu; Backues, Steven K.; Baehrecke, Eric H.; Bahr, Ben A.; Bai, Xue Yuan; Bailly, Yannick; Baiocchi, Robert; Baldini, Giulia; Balduini, Walter; Ballabio, Andrea; Bamber, Bruce A.; Bampton, Edward T W; Bánhegyi, Gábor; Bartholomew, Clinton R.; Bassham, Diane C.; Bast, Robert C.; Batoko, Henri; Bay, Boon Huat; Beau, Isabelle; Béchet, Daniel M.; Begley, Thomas J.; Behl, Christian; Behrends, Christian; Bekri, Soumeya; Bellaire, Bryan; Bendall, Linda J.; Benetti, Luca; Berliocchi, Laura; Bernardi, Henri; Bernassola, Francesca; Besteiro, Sébastien; Bhatia-Kissova, Ingrid; Bi, Xiaoning; Biard-Piechaczyk, Martine; Blum, Janice S.; Boise, Lawrence H.; Bonaldo, Paolo; Boone, David L.; Bornhauser, Beat C.; Bortoluci, Karina R.; Bossis, Ioannis; Bost, Frédéric; Bourquin, Jean Pierre; Boya, Patricia; Boyer-Guittaut, Michaël; Bozhkov, Peter V.; Brady, Nathan R.; Brancolini, Claudio; Brech, Andreas; Brenman, Jay E.; Brennand, Ana; Bresnick, Emery H.; Brest, Patrick; Bridges, Dave; Bristol, Molly L.; Brookes, Paul S.; Brown, Eric J.; Brumell, John H.; Brunetti-Pierri, Nicola; Brunk, Ulf T.; 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In: Autophagy, Vol. 8, No. 4, 01.04.2012, p. 445-544.

Research output: Contribution to journalArticle

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In: Autophagy. 2012 ; Vol. 8, No. 4. pp. 445-544.
@article{b8b7453f4d6642598758a1f1c485d978,
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 Bai, {Xue Yuan} 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 G{\'a}bor B{\'a}nhegyi and Bartholomew, {Clinton R.} and Bassham, {Diane C.} and Bast, {Robert C.} and Henri Batoko and Bay, {Boon Huat} and Isabelle Beau and B{\'e}chet, {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 S{\'e}bastien 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 Fr{\'e}d{\'e}ric Bost and Bourquin, {Jean Pierre} and Patricia Boya and Micha{\"e}l 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 Geert Bultynck and Burbulla, {Lena F.} and Wilfried Bursch and Butchar, {Jonathan P.} and Wanda Buzgariu and Bydlowski, {Sergio P.} and Ken Cadwell and Monika Cahov{\'a} 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 Chae, {Han Jung} and Chai, {Chee Yin} and Chan, {David C.} and Chan, {Edmond Y.} and Chang, {Raymond Chuen Chung} and Che, {Chi Ming} and Chen, {Ching Chow} and Chen, {Guang Chao} and Chen, {Guo Qiang} and Min Chen and Quan Chen and Chen, {Steve S L} and WenLi Chen and Xi Chen and Xiangmei Chen and Xiequn Chen and Chen, {Ye Guang} and Yingyu Chen and Yongqiang Chen and Chen, {Yu Jen} and Zhixiang Chen and Alan Cheng and Cheng, {Christopher H K} and Yan Cheng and Heesun Cheong and Cheong, {Jae Ho} and Sara Cherry and Russ Chess-Williams and Cheung, {Zelda H.} and Eric Chevet and Chiang, {Hui Ling} and Roberto Chiarelli and Tomoki Chiba and Chin, {Lih Shen} and Chiou, {Shih Hwa} and Chisari, {Francis V.} and Cho, {Chi Hin} and Cho, {Dong Hyung} 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 Chuang, {Tsung Hsien} and Chueh, {Sheau Huei} and Taehoon Chun and Chwae, {Yong Joon} and Chye, {Mee Len} 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, {Mar{\'i}a I.} and Sergio Comincini and Maria Condello and Fabrizio Condorelli and Cookson, {Mark R.} and Coombs, {Graham H.} and Isabelle Coppens 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, {Jos{\'e} L.} and Cronj{\'e}, {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 J{\"o}rn 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 D{\'i}az-Araya and In{\'e}s D{\'i}az-Laviada and Diaz-Meco, {Maria T.} and Javier Diaz-Nido and Ivan Dikic and Dinesh-Kumar, {Savithramma P.} and Ding, {Wen Xing} 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 Marl{\`e}ne Dreux and Drew, {Mark E.} and Qiuhong Duan and Duchosal, {Michel A.} and Karen Duff and Isabelle Dugail and Madeleine Durbeej 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 {Er Eng}, Kai and Engelbrecht, {Anna Mart} and Simone Engelender and Jekaterina Erenpreisa and Ricardo Escalante and Audrey Esclatine and Eskelinen, {Eeva Liisa} and Lucile Espert and Virginia Espina and Huizhou Fan and Jia Fan and Fan, {Qi Wen} and Zhen Fan and Shengyun Fang and Yongqi Fang and Manolis Fanto and Alessandro Fanzani and Thomas Farkas and Farr{\'e}, {Jean Claude} and Mathias Faure and Marcus Fechheimer and Feng, {Carl G.} and Jian Feng and Qili Feng and Youji Feng and L{\'a}szl{\'o} F{\'e}s{\"u}s 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, {Jos{\'e} 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 Gao, {Fen Biao} 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 C{\'e}line Gongora and Gonzalez, {Claudio D.} and Ramon Gonzalez and Cristina Gonz{\'a}lez-Est{\'e}vez and Gonz{\'a}lez-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 Aleš Gregorc and Fr{\'e}d{\'e}ric Gros and Charles Grose and Grunt, {Thomas W.} and Philippe Gual and Guan, {Jun Lin} and Guan, {Kun Liang} 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 Hayashi, {Shin Ichiro} and Hazelhurst, {Lori A.} and Congcong He and He, {You Wen} and H{\'e}bert, {Marie Jos{\'e}e} 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 J{\"o}rg H{\"o}hfeld and Holyoake, {Tessa L.} and Hong, {Ming Huang} and Hood, {David A.} and Hotamisligil, {G{\"o}khan S.} and Houwerzijl, {Ewout J.} and Maria H{\o}yer-Hansen and Bingren Hu and Hu, {Chien An A} and Hu, {Hong Ming} and Ya Hua and Canhua Huang and Ju Huang and Shengbing Huang and Huang, {Wei Pang} and Huber, {Tobias B.} and Huh, {Won Ki} and Hung, {Tai Ho} 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 Valentina Iovane and Iovanna, {Juan L.} and Ip, {Nancy Y.} and Yoshitaka Isaka and Hiroyuki Ishida and Ciro Isidoro and Isobe, {Ken Ichi} and Akiko Iwasaki and Marta Izquierdo and Yotaro Izumi and Jaakkola, {Panu M.} and Marja J{\"a}{\"a}ttel{\"a} and Jackson, {George R.} and Jackson, {William T.} and Bassam Janji and Marina Jendrach and Jeon, {Ju Hong} and Jeung, {Eui Bae} and Hong Jiang and Hongchi Jiang and Jiang, {Jean X.} and Ming Jiang and Qing Jiang and Xuejun Jiang and Alberto Jim{\'e}nez 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 G{\'a}bor Juh{\'a}sz and Lucienne Juillerat-Jeanneret and Jung, {Chang Hwa} and Jung, {Yong Keun} 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 {Il Kang}, Kwang and Rui Kang and Kang, {Yoon A.} and Tomotake Kanki and Kanneganti, {Thirumala Devi} and Haruo Kanno and Kanthasamy, {Anumantha G.} and Arthi Kanthasamy and Vassiliki Karantza and Kaushal, {Gur P.} and Susmita Kaushik and Yoshinori Kawazoe and Ke, {Po Yuan} 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 Kim, {Do Hyung} and Kim, {Dong Hou} and Kim, {Eun Kyoung} and Kim, {Hyung Ryong} and Kim, {Jae Sung} and Kim, {Jeong Hun} and Kim, {Jin Cheon} and Kim, {John K.} and Kim, {Peter K.} and Kim, {Seong Who} and Kim, {Yong Sun} 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 Koh, {Jae Young} and Koh, {Young Ho} and Masato Koike and Masaaki Komatsu and Eiki Kominami and Kong, {Hee Jeong} and Kong, {Wei Jia} and Korolchuk, {Viktor I.} and Yaichiro Kotake and Koukourakis, {Michael I.} and {Kouri Flores}, {Juan B.} and Kov{\'a}cs, {Attila L.} and Claudine Kraft and Dimitri Krainc and Helmut Kr{\"a}mer and Carole Kretz-Remy and Krichevsky, {Anna M.} and Guido Kroemer and Rejko Kr{\"u}ger and Oleg Krut and Ktistakis, {Nicholas T.} and Kuan, {Chia Yi} and Roza Kucharczyk and Ashok Kumar and Raj Kumar and Sharad Kumar and Mondira Kundu and Kung, {Hsing Jien} 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 L{\'a}szl{\'o} and Sergio Lavandero and Lavoie, {Jos{\'e}e 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 Lee, {Byung Wan} and Lee, {Gyun Min} and Jongdae Lee and Lee, {Ju Hyun} and Michael Lee and Lee, {Myung Shik} and Lee, {Sug Hyung} and Christiaan Leeuwenburgh and Patrick Legembre and Renaud Legouis and Michael Lehmann and Lei, {Huan Yao} and Lei, {Qun Ying} and Leib, {David A.} and Jos{\'e} 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 Li, {Jun Lin} and Lian Li and Sheng Li and Weijie Li and Li, {Xue Jun} and Li, {Yan Bo} and Li, {Yi Ping} and Chengyu Liang and Qiangrong Liang and Liao, {Yung Feng} and Liberski, {Pawel P.} and Andrew Lieberman and Lim, {Hyunjung J.} and Lim, {Kah Leong} and Kyu Lim and Lin, {Chiou Feng} and Lin, {Fu Cheng} and Jian Lin and Lin, {Jiandie D.} and Kui Lin and Lin, {Wan Wan} and Lin, {Weei Chin} and Lin, {Yi Ling} and Rafael Linden and Paul Lingor and Jennifer Lippincott-Schwartz and Lisanti, {Michael P.} and Liton, {Paloma B.} and Bo Liu and Liu, {Chun Feng} and Kaiyu Liu and Leyuan Liu and Liu, {Qiong A.} and Wei Liu and Liu, {Young Chau} and Yule Liu and Lockshin, {Richard A.} and Lok, {Chun Nam} and Sagar Lonial and Benjamin Loos and Gabriel Lopez-Berestein and Carlos L{\'o}pez-Ot{\'i}n and Laura Lossi and Lotze, {Michael T.} and Peter L{\~o}w and Binfeng Lu and Bingwei Lu and Bo Lu and Zhen Lu and Fr{\'e}d{\'e}ric 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 Mandelkow, {Eva Maria} and St{\'e}phen 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 Mari{\~n}o 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 Mel{\'e}ndez 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 Miao, {Chao Yu} and Miao, {Jun Ying} 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 M{\"u}ller and Sylviane Muller and Karl M{\"u}nger and Christian M{\"u}nz and Murphy, {Leon O.} and Murphy, {Maureen E.} and Antonio Musar{\`o} 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 Nakatogawa 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 N{\"u}rnberger 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 Ohkmae Kim 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 Val{\'e}rie Pierrefite-Carle and G{\'e}rard Pierron and Ronit Pinkas-Kramarski and Antonio Piras and Natik Piri and Platanias, {Leonidas C.} and Stefanie P{\"o}ggeler and Marc Poirot and Angelo Poletti and Christian Po{\"u}s and Mercedes Pozuelo-Rubio and Mette Pr{\ae}torius-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 Qian, {Shu Bing} and Liang Qin and Qin, {Zheng Hong} 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 R{\'e}gnier-Vigouroux and Reichert, {Andreas S.} and Reiners, {John J.} and Reiter, {Russel J.} and Jun Ren and Revuelta, {Jos{\'e} 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 C{\'o}rdoba}, {Santiago Rodr{\'i}guez} and B{\"a}rbel 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 S{\'a}nchez-Alc{\'a}zar, {Jos{\'e} A.} and Ricardo S{\'a}nchez-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 Mikl{\'o}s Sass and Ken Sato and Miyuki Sato and Schapira, {Anthony H V} and Michael Scharl and Sch{\"a}tzl, {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 Sch{\"u}ller 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 Shen, {Han Ming} and Shen, {Wei Chiang} and Sheng, {Zu Hang} and Yang Shi and Kenichi Shibuya and Yoshihiro Shidoji and Shieh, {Jeng Jer} and Shih, {Chwen Ming} 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 Simon, {Hans Uwe} 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 Bj{\"o}rn Stork and Peter Str{\aa}lfors and Subauste, {Carlos S.} and Xinbing Sui and David Sulzer and Jiaren Sun and Sun, {Shi Yong} and Sun, {Zhi Jun} and Sung, {Joseph J Y} and Kuninori Suzuki and Toshihiko Suzuki and Swanson, {Michele S.} and Charles Swanton and Sweeney, {Sean T.} and Sy, {Lai King} and Gyorgy Szabadkai and Ira Tabas and Heinrich Taegtmeyer and Marco Tafani and Krisztina Tak{\'a}cs-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, {Ance 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 T{\"o}nges and Tooze, {Sharon A.} and Cathy Tournier and John Tower and Roberto Towns and Vladimir Trajkovic and Travassos, {Leonardo H.} and Tsai, {Ting Fen} 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, {Maria 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 C{\'e}cile 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 Wan, {Xiang Bo} and Aimin Wang and Chenguang Wang and Dawei Wang and Fan Wang and Fen Wang and Guanghui Wang and Haichao Wang and Wang, {Hong Gang} and Wang, {Horng Dar} and Jin Wang and Ke Wang and Mei Wang and Wang, {Richard C.} and Xinglong Wang and Xuejun Wang and Wang, {Ying Jan} 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 Wen, {Long Ping} 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 Wu, {Dao Cheng} 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 Xu, {Da Zhi} 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 Yang, {Dun Sheng} and Elizabeth Yang and Yang, {Jin Ming} and Yang, {Shi Yu} and Wannian Yang and Yang, {Wei Yuan} and Zhifen Yang and Yao, {Meng Chao} and Yao, {Tso Pang} and Behzad Yeganeh and Yen, {Wei Lien} and Yin, {Jia Jing} and Yin, {Xiao Ming} and Yoo, {Ook Joon} and Gyesoon Yoon and Yoon, {Seung Yong} 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 Yu, {Seong Woon} and Yu, {Wai Haung} and Yuan, {Zhi Min} and Zhenyu Yue and Yun, {Cheol Heui} and Michisuke Yuzaki and Olga Zabirnyk and Elaine Silva-Zacarin and {David Zacks}, E. and Ldad Zacksenhaus and Nadia Zaffaroni and Zahra Zakeri and Zeh, {Herbert J.} and Zeitlin, {Scott O.} and Hong Zhang and Zhang, {Hui Ling} and Jianhua Zhang and Zhang, {Jing Pu} and Lin Zhang and Long Zhang and Zhang, {Ming Yong} and Zhang, {Xu Dong} and Mantong Zhao and Zhao, {Yi Fang} and Ying Zhao and Zhao, {Zhizhuang J.} and Xiaoxiang Zheng and Boris Zhivotovsky and Qing Zhong and Zhou, {Cong Zhao} and Changlian Zhu and Zhu, {Wei Guo} and Zhu, {Xiao Feng} and Xiongwei Zhu and Yuangang Zhu and Teresa Zoladek and Zong, {Wei Xing} and Antonio Zorzano and J{\"u}rgen Zschocke and Brian Zuckerbraun",
year = "2012",
month = "4",
day = "1",
doi = "10.4161/auto.19496",
language = "English",
volume = "8",
pages = "445--544",
journal = "Autophagy",
issn = "1554-8627",
publisher = "Landes Bioscience",
number = "4",

}

TY - JOUR

T1 - Guidelines for the use and interpretation of assays for monitoring autophagy

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PY - 2012/4/1

Y1 - 2012/4/1

N2 - 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.

AB - 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.

KW - Autolysosome

KW - Autophagosome

KW - Flux

KW - LC3

KW - Lysosome

KW - Phagophore

KW - Stress

KW - Vacuole

UR - http://www.scopus.com/inward/record.url?scp=84862295360&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84862295360&partnerID=8YFLogxK

U2 - 10.4161/auto.19496

DO - 10.4161/auto.19496

M3 - Article

C2 - 22966490

AN - SCOPUS:84862295360

VL - 8

SP - 445

EP - 544

JO - Autophagy

JF - Autophagy

SN - 1554-8627

IS - 4

ER -