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PMID: 22966490 Published · ppublish English Guideline Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Guidelines for the use and interpretation of assays for monitoring autophagy.

Autophagy ·Vol. 8 ·No. 4 ·2012-04-00 ·Pages 445-544

Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, Aleo MF, Alirezaei M, Almasan A, Almonte-Becerril M, Amano A, Amaravadi R, Amarnath S, Amer AO, Andrieu-Abadie N, Anantharam V, Ann DK, Anoopkumar-Dukie S, Aoki H, Apostolova N, Arancia G, Aris JP, Asanuma K, Asare NY, Ashida H, Askanas V, Askew DS, Auberger P, Baba M, Backues SK, Baehrecke EH, Bahr BA, Bai XY, Bailly Y, Baiocchi R, Baldini G, Balduini W, Ballabio A, Bamber BA, Bampton ET, Bánhegyi G, Bartholomew CR, Bassham DC, Bast RC, Batoko H, Bay BH, Beau I, Béchet DM, Begley TJ, Behl C, Behrends C, Bekri S, Bellaire B, Bendall LJ, Benetti L, Berliocchi L, Bernardi H, Bernassola F, Besteiro S, Bhatia-Kissova I, Bi X, Biard-Piechaczyk M, Blum JS, Boise LH, Bonaldo P, Boone DL, Bornhauser BC, Bortoluci KR, Bossis I, Bost F, Bourquin JP, Boya P, Boyer-Guittaut M, Bozhkov PV, Brady NR, Brancolini C, Brech A, Brenman JE, Brennand A, Bresnick EH, Brest P, Bridges D, Bristol ML, Brookes PS, Brown EJ, Brumell JH, Brunetti-Pierri N, Brunk UT, Bulman DE, Bultman SJ, Bultynck G, Burbulla LF, Bursch W, Butchar JP, Buzgariu W, Bydlowski SP, Cadwell K, Cahová M, Cai D, Cai J, Cai Q, Calabretta B, Calvo-Garrido J, Camougrand N, Campanella M, Campos-Salinas J, Candi E, Cao L, Caplan AB, Carding SR, Cardoso SM, Carew JS, Carlin CR, Carmignac V, Carneiro LA, Carra S, Caruso RA, Casari G, Casas C, Castino R, Cebollero E, Cecconi F, Celli J, Chaachouay H, Chae HJ, Chai CY, Chan DC, Chan EY, Chang RC, Che CM, Chen CC, Chen GC, Chen GQ, Chen M, Chen Q, Chen SS, Chen W, Chen X, Chen X, Chen X, Chen YG, Chen Y, Chen Y, Chen YJ, Chen Z, Cheng A, Cheng CH, Cheng Y, Cheong H, Cheong JH, Cherry S, Chess-Williams R, Cheung ZH, Chevet E, Chiang HL, Chiarelli R, Chiba T, Chin LS, Chiou SH, Chisari FV, Cho CH, Cho DH, Choi AM, Choi D, Choi KS, Choi ME, Chouaib S, Choubey D, Choubey V, Chu CT, Chuang TH, Chueh SH, Chun T, Chwae YJ, Chye ML, Ciarcia R, Ciriolo MR, Clague MJ, Clark RS, Clarke PG, Clarke R, Codogno P, Coller HA, Colombo MI, Comincini S, Condello M, Condorelli F, Cookson MR, Coombs GH, Coppens I, Corbalan R, Cossart P, Costelli P, Costes S, Coto-Montes A, Couve E, Coxon FP, Cregg JM, Crespo JL, Cronjé MJ, Cuervo AM, Cullen JJ, Czaja MJ, D'Amelio M, Darfeuille-Michaud A, Davids LM, Davies FE, De Felici M, de Groot JF, de Haan CA, De Martino L, De Milito A, De Tata V, Debnath J, Degterev A, Dehay B, Delbridge LM, Demarchi F, Deng YZ, Dengjel J, Dent P, Denton D, Deretic V, Desai SD, Devenish RJ, Di Gioacchino M, Di Paolo G, Di Pietro C, Díaz-Araya G, Díaz-Laviada I, Diaz-Meco MT, Diaz-Nido J, Dikic I, Dinesh-Kumar SP, Ding WX, Distelhorst CW, Diwan A, Djavaheri-Mergny M, Dokudovskaya S, Dong Z, Dorsey FC, Dosenko V, Dowling JJ, Doxsey S, Dreux M, Drew ME, Duan Q, Duchosal MA, Duff K, Dugail I, Durbeej M, 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TH, Hupp TR, Hur GM, Hurley JB, Hussain SN, Hussey PJ, Hwang JJ, Hwang S, Ichihara A, Ilkhanizadeh S, Inoki K, Into T, Iovane V, Iovanna JL, Ip NY, Isaka Y, Ishida H, Isidoro C, Isobe K, Iwasaki A, Izquierdo M, Izumi Y, Jaakkola PM, Jäättelä M, Jackson GR, Jackson WT, Janji B, Jendrach M, Jeon JH, Jeung EB, Jiang H, Jiang H, Jiang JX, Jiang M, Jiang Q, Jiang X, Jiang X, Jiménez A, Jin M, Jin S, Joe CO, Johansen T, Johnson DE, Johnson GV, Jones NL, Joseph B, Joseph SK, Joubert AM, Juhász G, Juillerat-Jeanneret L, Jung CH, Jung YK, Kaarniranta K, Kaasik A, Kabuta T, Kadowaki M, Kagedal K, Kamada Y, Kaminskyy VO, Kampinga HH, Kanamori H, Kang C, Kang KB, Kang KI, Kang R, Kang YA, Kanki T, Kanneganti TD, Kanno H, Kanthasamy AG, Kanthasamy A, Karantza V, Kaushal GP, Kaushik S, Kawazoe Y, Ke PY, Kehrl JH, Kelekar A, Kerkhoff C, Kessel DH, Khalil H, Kiel JA, Kiger AA, Kihara A, Kim DR, Kim DH, Kim DH, Kim EK, Kim HR, Kim JS, Kim JH, Kim JC, Kim JK, Kim PK, Kim SW, Kim YS, Kim Y, Kimchi A, 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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.

MeSH Terms

Animals Autophagy/genetics Biological Assay/methods Humans Models, Biological

Authors & Affiliations

1270 authors, click to expand affiliations / ORCID

Klionsky Daniel J

Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA. klionsky@umich.edu

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

Bulman Dennis E

Bultman Scott J

Bultynck Geert

Burbulla Lena F

Bursch Wilfried

Butchar Jonathan P

Buzgariu Wanda

Bydlowski Sergio P

Cadwell Ken

Cahová Monika

Cai Dongsheng

Cai Jiyang

Cai Qian

Calabretta Bruno

Calvo-Garrido Javier

Camougrand Nadine

Campanella Michelangelo

Campos-Salinas Jenny

Candi Eleonora

Cao Lizhi

Caplan Allan B

Carding Simon R

Cardoso Sandra M

Carew Jennifer S

Carlin Cathleen R

Carmignac Virginie

Carneiro Leticia A M

Carra Serena

Caruso Rosario A

Casari Giorgio

Casas Caty

Castino Roberta

Cebollero Eduardo

Cecconi Francesco

Celli Jean

Chaachouay Hassan

Chae Han-Jung

Chai Chee-Yin

Chan David C

Chan Edmond Y

Chang Raymond Chuen-Chung

Che Chi-Ming

Chen Ching-Chow

Chen Guang-Chao

Chen Guo-Qiang

Chen Min

Chen Quan

Chen Steve S-L

Chen WenLi

Chen Xi

Chen Xiangmei

Chen Xiequn

Chen Ye-Guang

Chen Yingyu

Chen Yongqiang

Chen Yu-Jen

Chen Zhixiang

Cheng Alan

Cheng Christopher H K

Cheng Yan

Cheong Heesun

Cheong Jae-Ho

Cherry Sara

Chess-Williams Russ

Cheung Zelda H

Chevet Eric

Chiang Hui-Ling

Chiarelli Roberto

Chiba Tomoki

Chin Lih-Shen

Chiou Shih-Hwa

Chisari Francis V

Cho Chi Hin

Cho Dong-Hyung

Choi Augustine M K

Choi DooSeok

Choi Kyeong Sook

Choi Mary E

Chouaib Salem

Choubey Divaker

Choubey Vinay

Chu Charleen T

Chuang Tsung-Hsien

Chueh Sheau-Huei

Chun Taehoon

Chwae Yong-Joon

Chye Mee-Len

Ciarcia Roberto

Ciriolo Maria R

Clague Michael J

Clark Robert S B

Clarke Peter G H

Clarke Robert

Codogno Patrice

Coller Hilary A

Colombo María I

Comincini Sergio

Condello Maria

Condorelli Fabrizio

Cookson Mark R

Coombs Graham H

Coppens Isabelle

Corbalan Ramon

Cossart Pascale

Costelli Paola

Costes Safia

Coto-Montes Ana

Couve Eduardo

Coxon Fraser P

Cregg James M

Crespo José L

Cronjé Marianne J

Cuervo Ana Maria

Cullen Joseph J

Czaja Mark J

D'Amelio Marcello

Darfeuille-Michaud Arlette

Davids Lester M

Davies Faith E

De Felici Massimo

de Groot John F

de Haan Cornelis A M

De Martino Luisa

De Milito Angelo

De Tata Vincenzo

Debnath Jayanta

Degterev Alexei

Dehay Benjamin

Delbridge Lea M D

Demarchi Francesca

Deng Yi Zhen

Dengjel Jörn

Dent Paul

Denton Donna

Deretic Vojo

Desai Shyamal D

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Article Info

Journal

Autophagy

Abbr.

Autophagy

ISSN

1554-8635

DOI

10.4161/auto.19496

klionsky@umich.edu

Published

2012-04-00

Pages

445-544

Language

English

Region

United States

NLM ID

101265188

PMCID

PMC3404883

Subset

Grants

Parkinson's UK · G-0905 · United Kingdom

NCI NIH HHS · K05 CA142885 · United States

NIDDK NIH HHS · R01 DK082437 · United States

Medical Research Council · G0600251 · United Kingdom

NHLBI NIH HHS · R01 HL096625 · United States

NHLBI NIH HHS · R01 HL102738 · United States

NIGMS NIH HHS · R01 GM099040 · United States

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NEI NIH HHS · R01 EY019320 · United States

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NEI NIH HHS · R01 EY020491 · United States

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Parkinson's UK · J-0901 · United Kingdom

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