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Guidelines for the use and interpretation of assays for monitoring autophagy

DJ Klionsky, FC Abdalla, H Abeliovich, RT Abraham, A Acevedo-Arozena, K Adeli, L Agholme, M Agnello, P Agostinis and JA Aguirre-Ghiso, et al. (2012) 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 elements (e.g., autophagosomes or autolysosomes) at any stage of the autophagic process vs. those that measure flux through the autophagy pathway (i.e., the complete process); thus, a block in macroautophagy that results in autophagosome accumulation needs to be differentiated from stimuli that result in increased autophagic activity, defined as increased autophagy induction coupled with increased delivery to, and degradation within, lysosomes (in most higher eukaryotes and some protists such as Dictyostelium) or the vacuole (in plants and fungi). In other words, it is especially important that investigators new to the field understand that the appearance of more autophagosomes does not necessarily equate with more autophagy. In fact, in many cases, autophagosomes accumulate because of a block in trafficking to lysosomes without a concomitant change in autophagosome biogenesis, whereas an increase in autolysosomes may reflect a reduction in degradative activity. Here, we present a set of guidelines for the selection and interpretation of methods for use by investigators who aim to examine macroautophagy and related processes, as well as for reviewers who need to provide realistic and reasonable critiques of papers that are focused on these processes. These guidelines are not meant to be a formulaic set of rules, because the appropriate assays depend in part on the question being asked and the system being used. In addition, we emphasize that no individual assay is guaranteed to be the most appropriate one in every situation, and we strongly recommend the use of multiple assays to monitor autophagy. In these guidelines, we consider these various methods of assessing autophagy and what information can, or cannot, be obtained from them. Finally, by discussing the merits and limits of particular autophagy assays, we hope to encourage technical innovation in the field.
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author
organization
year
type
journalArticle (review)
publication status
published
subject
keyword
STARVATION-INDUCED AUTOPHAGY, VACUOLE TARGETING PATHWAY, ISOLATED RAT HEPATOCYTES, PROGRAMMED CELL-DEATH, CHAPERONE-MEDIATED AUTOPHAGY, ACTIVATED PROTEIN-KINASE, vacuole, stress, phagophore, lysosome, LC3, flux, autophagosome, autolysosome, GLUCAGON-INDUCED AUTOPHAGY, BREAST-CANCER CELLS, BETAINE HOMOCYSTEINE METHYLTRANSFERASE, ENDOPLASMIC-RETICULUM STRESS
journal title
AUTOPHAGY
Autophagy
volume
8
issue
4
pages
445 - 544
Web of Science type
Review
Web of Science id
000305403400002
JCR category
CELL BIOLOGY
JCR impact factor
12.042 (2012)
JCR rank
12/181 (2012)
JCR quartile
1 (2012)
ISSN
1554-8627
DOI
10.4161/auto.19496
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
3040526
handle
http://hdl.handle.net/1854/LU-3040526
date created
2012-11-05 09:27:28
date last changed
2012-11-05 10:56:23
@article{3040526,
  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, DJ and Abdalla, FC and Abeliovich, H and Abraham, RT and Acevedo-Arozena, A and Adeli, K and Agholme, L and Agnello, M and Agostinis, P and Aguirre-Ghiso, JA and Ahn, HJ and Ait-Mohamed, O and Ait-Si-Ali, S and Akematsu, T and Akira, S and Al-Younes, HM and Al-Zeer, MA and Albert, ML and Albin, RL and Alegre-Abarrategui, J and Aleo, MF and Alirezaei, M and Almasan, A and Almonte-Becerril, M and Amano, A and Amaravadi, R and Amarnath, S and Amer, AO and Andrieu-Abadie, N and Anantharam, V and Ann, DK and Anoopkumar-Dukie, S and Aoki, H and Apostolova, N and Arancia, G and Aris, JP and Asanuma, K and Asare, NYO and Ashida, H and Askanas, V and Askew, DS and Auberger, P and Baba, M and Backues, SK and Baehrecke, EH and Bahr, BA and Bai, XY and Bailly, Y and Baiocchi, R and Baldini, G and Balduini, W and Ballabio, A and Bamber, BA and Bampton, ETW and B{\'a}nhegyi, G and Bartholomew, CR and Bassham, DC and Bast, RC and Batoko, H and Bay, BH and Beau, I and B{\'e}chet, DM and Begley, TJ and Behl, C and Behrends, C and Bekri, S and Bellaire, B and Bendall, LJ and Benetti, L and Berliocchi, L and Bernardi, H and Bernassola, F and Besteiro, S and Bhatia-Kissova, I and Bi, XN and Biard-Piechaczyk, M and Blum, JS and Boise, LH and Bonaldo, P and Boone, DL and Bornhauser, BC and Bortoluci, KR and Bossis, I and Bost, F and Bourquin, JP and Boya, P and Boyer-Guittaut, M and Bozhkov, PV and Brady, NR and Brancolini, C and Brech, A and Brenman, JE and Brennand, A and Bresnick, EH and Brest, P and Bridges, D and Bristol, ML and Brookes, PS and Brown, EJ and Brumell, JH and Brunetti-Pierri, N and Brunk, UT and Bulman, DE and Bultman, SJ and Bultynck, G and Burbulla, LF and Bursch, W and Butchar, JP and Buzgariu, W and Bydlowski, SP and Cadwell, K and Cahov{\'a}, M and Cai, DS and Cai, JY and Cai, Q and Calabretta, B and Calvo-Garrido, J and Camougrand, N and Campanella, M and Campos-Salinas, J and Candi, E and Cao, LZ and Caplan, AB and Carding, SR and Cardoso, SM and Carew, JS and Carlin, CR and Carmignac, V and Carneiro, LAM and Carra, S and Caruso, RA and Casari, G and Casas, C and Castino, R and Cebollero, E and Cecconi, F and Celli, J and Chaachouay, H and Chae, HJ and Chai, CY and Chan, DC and Chan, EY and Chang, RCC and Che, CM and Chen, CC and Chen, GC and Chen, GQ and Chen, M and Chen, Q and Chen, SSL and Chen, WL and Chen, X and Chen, XM and Chen, XQ and Chen, YG and Chen, YY and Chen, YQ and Chen, YJ and Chen, ZX and Cheng, A and Cheng, CHK and Cheng, Y and Cheong, H and Cheong, JH and Cherry, S and Chess-Williams, R and Cheung, ZH and Chevet, E and Chiang, HL and Chiarelli, R and Chiba, T and Chin, LS and Chiou, SH and Chisari, FV and Cho, CH and Cho, DH and Choi, AMK and Choi, D and Choi, KS and Choi, ME and Chouaib, S and Choubey, D and Choubey, V and Chu, CT and Chuang, TH and Chueh, SH and Chun, T and Chwae, YJ and Chye, ML and Ciarcia, R and Ciriolo, MR and Clague, MJ and Clark, RSB and Clarke, PGH and Clarke, R 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Ichihara, A and Ilkhanizadeh, S and Inoki, K and Into, T and Iovane, V and Iovanna, JL and Ip, NY and Isaka, Y and Ishida, H and Isidoro, C and Isobe, K and Iwasaki, A and Izquierdo, M and Izumi, Y and Jaakkola, PM and J{\"a}{\"a}ttel{\"a}, M and Jackson, GR and Jackson, WT and Janji, B and Jendrach, M and Jeon, JH and Jeung, EB and Jiang, H and Jiang, HC and Jiang, JX and Jiang, M and Jiang, Q and Jiang, XJ and Jiang, XJ and Jim{\'e}nez, A and Jin, MY and Jin, SK and Joe, CO and Johansen, T and Johnson, DE and Johnson, GVW and Jones, NL and Joseph, B and Joseph, SK and Joubert, AM and Juh{\'a}sz, G and Juillerat-Jeanneret, L and Jung, CH and Jung, YK and Kaarniranta, K and Kaasik, A and Kabuta, T and Kadowaki, M and Kagedal, K and Kamada, Y and Kaminskyy, VO and Kampinga, HH and Kanamori, H and Kang, C and Kang, KB and Kang, KI and Kang, R and Kang, YA and Kanki, T and Kanneganti, TD and Kanno, H and Kanthasamy, AG and Kanthasamy, A and Karantza, V and Kaushal, GP and Kaushik, S and 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McQuibban, GA and Meijer, AJ and Meisler, MH and Mel{\'e}ndez, A and Melia, TJ and Melino, G and Mena, MA and Menendez, JA and Menna-Barreto, RFS and Menon, MB and Menzies, FM and Mercer, CA and Merighi, A and Merry, DE and Meschini, S and Meyer, CG and Meyer, TF and Miao, CY and Miao, JY and Michels, PAM and Michiels, C and Mijaljica, D and Milojkovic, A and Minucci, S and Miracco, C and Miranti, CK and Mitroulis, I and Miyazawa, K and Mizushima, N and Mograbi, B and Mohseni, S and Molero, X and Mollereau, B and Mollinedo, F and Momoi, T and Monastyrska, I and Monick, MM and Monteiro, MJ and Moore, MN and Mora, R and Moreau, K and Moreira, PI and Moriyasu, Y and Moscat, J and Mostowy, S and Mottram, JC and Motyl, T and Moussa, CEH and M{\"u}ller, S and Munger, K and Munz, C and Murphy, LO and Murphy, ME and Musar{\`o}, A and Mysorekar, I and Nagata, E and Nagata, K and Nahimana, A and Nair, U and Nakagawa, T and Nakahira, K and Nakano, H and Nakataogawa, H and Nanjundan, M and Naqvi, 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Pervaiz, S and Peter, M and Peters, GJ and Petersen, M and Petrovski, G and Phang, JM and Piacentini, M and Pierre, P and Pierrefite-Carle, V and Pierron, G and Pinkas-Kramarski, R and Piras, A and Piri, N and Platanias, LC and P{\"o}ggeler, S and Poirot, M and Poletti, A and Po{\"u}s, C and Pozuelo-Rubio, M and Pr{\ae}torius-Ibba, M and Prasad, A and Prescott, M and Priault, M and Produit-Zengaffinen, N and Progulske-Fox, A and Proikas-Cezanne, T and Przedborski, S and Przyklenk, K and Puertollano, R and Puyal, J and Qian, SB and Qin, L and Qin, ZH and Quaggin, SE and Raben, N and Rabinowich, H and Rabkin, SW and Rahman, I and Rami, A and Ramm, G and Randall, G and Randow, F and Rao, VA and Rathmell, JC and Ravikumar, B and Ray, SK and Reed, BH and Reed, JC and Reggiori, F and R{\'e}gnier-Vigouroux, A and Reichert, AS and Reiners, JJ and Reiter, RJ and Ren, J and Revuelta, JL and Rhodes, CJ and Ritis, K and Rizzo, E and Robbins, J and Roberge, M and Roca, H and Roccheri, MC and Rocchi, S and Rodemann, HP and Rodr{\'i}guez de C{\'o}rdoba, S and Rohrer, B and Roninson, IB and Rosen, K and Rost-Roszkowska, MM and Rouis, M and Rouschop, KMA and Rovetta, F and Rubin, BP and Rubinsztein, DC and Ruckdeschel, K and Rucker, EB and Rudich, A and Rudolf, E and Ruiz-Opazo, N and Russo, R and Rusten, TE and Ryan, KM and Ryter, SW and Sabatini, DM and Sadoshima, J and Saha, T and Saitoh, T and Sakagami, H and Sakai, Y and Salekdeh, GH and Salomoni, P and Salvaterra, PM and Salvesen, G and Salvioli, R and Sanchez, AMJ and S{\'a}nchez-Alc{\'a}zar, JA and S{\'a}nchez-Prieto, R and Sandri, M and Sankar, U and Sansanwal, P and Santambrogio, L and Saran, S and Sarkar, S and Sarwal, M and Sasakawa, C and Sasnauskiene, A and Sato, MSK and Sato, K and Sato, M and Schapira, AHV and Scharl, M and Sch{\"a}tzl, HM and Scheper, W and Schiaffino, S and Schneider, C and Schneider, ME and Schneider-Stock, R and Schoenlein, PV and Schorderet, DF and Sch{\"u}ller, C and Schwartz, GK and Scorrano, L and Sealy, L and Seglen, PO and Segura-Aguilar, J and Seiliez, I and Seleverstov, O and Sell, C and Seo, JB and Separovic, D and Setaluri, V and Setoguchi, T and Settembre, C and Shacka, JJ and Shanmugam, M and Shapiro, IM and Shaulian, E and Shaw, RJ and Shelhamer, JH and Shen, HM and Shen, WC and Sheng, ZH and Shi, Y and Shibuya, K and Shidoji, Y and Shieh, JJ and Shih, CM and Shimada, Y and Shimizu, S and Shintani, T and Shirihai, OS and Shore, GC and Sibirny, AA and Sidhu, SB and Sikorska, B and Silva-Zacarin, ECM and Simmons, A and Simon, AK and Simon, HU and Simone, C and Simonsen, A and Sinclair, DA and Singh, R and Sinha, D and Sinicrope, FA and Sirko, A and Siu, PM and Sivridis, E and Skop, V and Skulachev, VP and Slack, RS and Smaili, SS and Smith, DR and Soengas, MS and Soldati, T and Song, XQ and Sood, AK and Soong, TW and Sotgia, F and Spector, SA and Spies, CD and Springer, W and Srinivasula, SM and Stefanis, L and Steffan, JS and Stendel, R and Stenmark, H and Stephanou, A and Stern, ST and Sternberg, C and Stork, B and Str{\aa}lfors, P and Subauste, CS and Sui, XB and Sulzer, D and Sun, JR and Sun, SY and Sun, ZJ and Sung, JJY and Suzuki, K and Suzuki, T and Swanson, MS and Swanton, C and Sweeney, ST and Sy, LK and Szabadkai, G and Tabas, I and Taegtmeyer, H and Tafani, M and Tak{\'a}cs-Vellai, K and Takano, Y and Takegawa, K and Takemura, G and Takeshita, F and Talbot, NJ and Tan, KSW and Tanaka, K and Tanaka, K and Tang, DL and Tang, DZ and Tanida, I and Tannous, BA and Tavernarakis, N and Taylor, GS and Taylor, GA and Taylor, JP and Terada, LS and Terman, A and Tettamanti, G and Thevissen, K and Thompson, CB and Thorburn, A and Thumm, M and Tian, FF and Tian, Y and Tocchini-Valentini, G and Tolkovsky, AM and Tomino, Y and T{\"o}nges, L and Tooze, SA and Tournier, C and Tower, J and Towns, R and Trajkovic, V and Travassos, LH and Tsai, TF and Tschan, MP and Tsubata, T and Tsung, A and Turk, B and Turner, LS and Tyagi, SC and Uchiyama, Y and Ueno, T and Umekawa, M and Umemiya-Shirafuji, R and Unni, VK and Vaccaro, MI and Valente, EM and Van den Berghe, G and van der Klei, IJ and van Doorn, WG and van Dyk, LF and van Egmond, M and van Grunsven, LA and Vandenabeele, Peter and Vandenberghe, WP and Vanhorebeek, I and Vaquero, EC and Velasco, G and Vellai, T and Vicencio, JM and Vierstra, RD and Vila, M and Vindis, C and Viola, G and Viscomi, MT and Voitsekhovskaja, OV and von Haefen, C and Votruba, M and Wada, K and Wade-Martins, R and Walker, CL and Walsh, CM and Walter, J and Wan, XB and Wang, AM and Wang, CG and Wang, DW and Wang, F and Wang, F and Wang, GH and Wang, HC and Wang, HG and Wang, HD and Wang, J and Wang, K and Wang, M and Wang, RC and Wang, XL and Wang, XJ and Wang, YJ and Wang, YP and Wang, Z and Wang, ZC and Wang, ZN and Wansink, DG and Ward, DM and Watada, H and Waters, SL and Webster, P and Wei, LX and Weihl, CC and Weiss, WA and Welford, SM and Wen, LP and Whitehouse, CA and Whitton, JL and Whitworth, AJ and Wileman, T and Wiley, JW and Wilkinson, S and Willbold, D and Williams, RL and Williamson, PR and Wouters, BG and Wu, CH and Wu, DC and Wu, WKK and Wyttenbach, A and Xavier, RJ and Xi, ZJ and Xia, P and Xiao, GF and Xie, ZP and Xie, ZL and Xu, DZ and Xu, JZ and Xu, L and Xu, XL and Yamamoto, A and Yamamoto, A and Yamashina, S and Yamashita, M and Yan, XH and Yanagida, M and Yang, DS and Yang, E and Yang, JM and Yang, SY and Yang, WN and Yang, WY and Yang, ZF and Yao, MC and Yao, TP and Yeganeh, B and Yen, WL and Yin, JJ and Yin, XM and Yoo, OJ and Yoon, G and Yoon, SY and Yorimitsu, T and Yoshikawa, Y and Yoshimori, T and Yoshimoto, K and You, HJ and Youle, RJ and Younes, A and Yu, L and Yu, L and Yu, SW and Yu, WH and Yuan, ZM and Yue, ZY and Yun, CH and Yuzaki, M and Zabirnyk, O and Silva-Zacarin, E and Zacks, D and Zacksenhaus, E and Zaffaroni, N and Zakeri, Z and Zeh, HJ and Zeitlin, SO and Zhang, H and Zhang, HL and Zhang, JH and Zhang, JP and Zhang, L and Zhang, L and Zhang, MY and Zhang, XD and Zhao, MT and Zhao, YF and Zhao, Y and Zhao, ZZJ and Zheng, XX and Zhivotovsky, B and Zhong, Q and Zhou, CZ and Zhu, CL and Zhu, WG and Zhu, XF and Zhu, XW and Zhu, YG and Zoladek, T and Zong, WX and Zorzano, A and Zschocke, J and Zuckerbraun, B},
  issn         = {1554-8627},
  journal      = {AUTOPHAGY},
  keyword      = {STARVATION-INDUCED AUTOPHAGY,VACUOLE TARGETING PATHWAY,ISOLATED RAT HEPATOCYTES,PROGRAMMED CELL-DEATH,CHAPERONE-MEDIATED AUTOPHAGY,ACTIVATED PROTEIN-KINASE,vacuole,stress,phagophore,lysosome,LC3,flux,autophagosome,autolysosome,GLUCAGON-INDUCED AUTOPHAGY,BREAST-CANCER CELLS,BETAINE HOMOCYSTEINE METHYLTRANSFERASE,ENDOPLASMIC-RETICULUM STRESS},
  language     = {eng},
  number       = {4},
  pages        = {445--544},
  title        = {Guidelines for the use and interpretation of assays for monitoring autophagy},
  url          = {http://dx.doi.org/10.4161/auto.19496},
  volume       = {8},
  year         = {2012},
}

Chicago
Klionsky, DJ, FC Abdalla, H Abeliovich, RT Abraham, A Acevedo-Arozena, K Adeli, L Agholme, et al. 2012. “Guidelines for the Use and Interpretation of Assays for Monitoring Autophagy.” Autophagy 8 (4): 445–544.
APA
Klionsky, D., Abdalla, F., Abeliovich, H., Abraham, R., Acevedo-Arozena, A., Adeli, K., Agholme, L., et al. (2012). Guidelines for the use and interpretation of assays for monitoring autophagy. AUTOPHAGY, 8(4), 445–544.
Vancouver
1.
Klionsky D, Abdalla F, Abeliovich H, Abraham R, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. AUTOPHAGY. 2012;8(4):445–544.
MLA
Klionsky, DJ, FC Abdalla, H Abeliovich, et al. “Guidelines for the Use and Interpretation of Assays for Monitoring Autophagy.” AUTOPHAGY 8.4 (2012): 445–544. Print.