Cited 1942 time in webofscience Cited 2020 time in scopus

Guidelines for the use and interpretation of assays for monitoring autophagy

Title
Guidelines for the use and interpretation of assays for monitoring autophagy
Authors
Klionsky, Daniel J.Abdalla, Fabio C.Abeliovich, HagaiAbraham, Robert T.Acevedo-Arozena, AbrahamAdeli, KhosrowAgholme, LottaAgnello, MariaAgostinis, PatriziaAguirre-Ghiso, Julio A.Ahn, Hyung JunAit-Mohamed, OuardiaAit-Si-Ali, SlimaneAkematsu, TakahikoAkira, ShizuoAl-Younes, Hesham M.Al-Zeer, Munir A.Albert, Matthew L.Albin, Roger L.Alegre-Abarrategui, JavierAleo, Maria FrancescaAlirezaei, MehrdadAlmasan, AlexandruAlmonte-Becerril, MaylinAmano, AtsuoAmaravadi, RaviAmarnath, ShobaAmer, Amal O.Andrieu-Abadie, NathalieAnantharam, VellareddyAnn, David K.Anoopkumar-Dukie, ShailendraAoki, HiroshiApostolova, NadezdaArancia, GiuseppeAris, John P.Asanuma, KatsuhikoAsare, Nana Y. O.Ashida, HisashiAskanas, ValerieAskew, David S.Auberger, PatrickBaba, MisuzuBackues, Steven K.Baehrecke, Eric H.Bahr, Ben A.Bai, Xue-YuanBailly, YannickBaiocchi, RobertBaldini, GiuliaBalduini, WalterBallabio, AndreaBamber, Bruce A.Bampton, Edward T. W.Banhegyi, GaborBartholomew, Clinton R.Bassham, Diane C.Bast, Robert C., Jr.Batoko, HenriBay, Boon-HuatBeau, IsabelleBechet, Daniel M.Begley, Thomas J.Behl, ChristianBehrends, ChristianBekri, SoumeyaBellaire, BryanBendall, Linda J.Benetti, LucaBerliocchi, LauraBernardi, HenriBernassola, FrancescaBesteiro, SebastienBhatia-Kissova, IngridBi, XiaoningBiard-Piechaczyk, MartineBlum, Janice S.Boise, Lawrence H.Bonaldo, PaoloBoone, David L.Bornhauser, Beat C.Bortoluci, Karina R.Bossis, IoannisBost, FredericBourquin, Jean-PierreBoya, PatriciaBoyer-Guittaut, MichaelBozhkov, Peter V.Brady, Nathan R.Brancolini, ClaudioBrech, AndreasBrenman, Jay E.Brennand, AnaBresnick, Emery H.Brest, PatrickBridges, DaveBristol, Molly L.Brookes, Paul S.Brown, Eric J.Brumell, John H.Brunetti-Pierri, NicolaBrunk, Ulf T.Bulman, Dennis E.Bultman, Scott J.Bultynck, GreetBurbulla, Lena F.Bursch, WilfriedButchar, Jonathan P.Buzgariu, WandaBydlowski, Sergio P.Cadwell, KenCahova, MonikaCai, DongshengCai, JiyangCai, QianCalabretta, BrunoCalvo-Garrido, JavierCamougrand, NadineCampanella, MichelangeloCampos-Salinas, JennyCandi, EleonoraCao, LizhiCaplan, Allan B.Carding, Simon R.Cardoso, Sandra M.Carew, Jennifer S.Carlin, Cathleen R.Carmignac, VirgineCarneiro, Leticia A. M.Carra, SerenaCaruso, Rosario A.Casari, GiorgioCasas, CatyCastino, RobertaCebollero, EduardoCecconi, FrancescoCelli, JeanChaachouay, HassanChae, Han-JungChai, Chee-YinChan, David C.Chan, Edmond Y.Chang, Raymond Chuen-ChungChe, Chi-MingChen, Ching-ChowChen, Guang-ChaoChen, Guo-QiangChen, MinChen, QuanChen, Steve S. -L.Chen, WenLiChen, XiChen, XiangmeiChen, XiequnChen, Ye-GuangChen, YingyuChen, YongqiangChen, Yu-JenChen, ZhixiangCheng, AlanCheng, Christopher H. K.Cheng, YanCheong, HeesunCheong, Jae-HoCherry, SaraChess-Williams, RussCheung, Zelda H.Chevet, EricChiang, Hui-LingChiarelli, RobertoChiba, TomokiChin, Lih-ShenChiou, Shih-HwaChisari, Francis V.Cho, Chi HinCho, Dong-HyungChoi, Augustine M. K.Choi, DooSeokChoi, Kyeong SookChoi, Mary E.Chouaib, SalemChoubey, DivakerChoubey, VinayChu, Charleen T.Chuang, Tsung-HsienChueh, Sheau-HueiChun, TaehoonChwae, Yong-JoonChye, Mee-LenCiarcia, RobertoCiriolo, Maria R.Clague, Michael J.Clark, Robert S. B.Clarke, Peter G. H.Clarke, RobertCodogno, PatriceColler, Hilary A.Colombo, Maria I.Comincini, SergioCondello, MariaCondorelli, FabrizioCookson, Mark R.Coppens, Graham H. Coombs IsabelleCorbalan, RamonCossart, PascaleCostelli, PaolaCostes, SafiaCoto-Montes, AnaCouve, EduardoCoxon, Fraser P.Cregg, James M.Crespo, Jose L.Cronje, Marianne J.Cuervo, Ana MariaCullen, Joseph J.Czaja, Mark J.D'Amelio, MarcelloDarfeuille-Michaud, ArletteDavids, Lester M.Davies, Faith E.De Felici, Massimode Groot, John F.de Haan, Cornelis A. M.De Martino, LuisaDe Milito, AngeloDe Tata, VincenzoDebnath, JayantaDegterev, AlexeiDehay, BenjaminDelbridge, Lea M. D.Demarchi, FrancescaDeng, Yi ZhenDengjel, JoenDent, PaulDenton, DonnaDeretic, VojoDesai, Shyamal D.Devenish, Rodney J.Di Gioacchino, MarioDi Paolo, GilbertDi Pietro, ChiaraDiaz-Araya, GuillermoDiaz-Laviada, InesDiaz-Meco, Maria T.Diaz-Nido, JavierDikic, IvanDinesh-Kumar, Savithramma P.Ding, Wen-XingDistelhorst, Clark W.Diwan, AbhinavDjavaheri-Mergny, MojganDokudovskaya, SvetlanaDong, ZhengDorsey, Frank C.Dosenko, VictorDowling, James J.Doxsey, StephenDreux, MarleneDrew, Mark E.Duan, QiuhongDuchosal, Michel A.Duff, KarenDugail, IsabelleDurbeej, MadeleineDuszenko, MichaelEdelstein, Charles L.Edinger, Aimee L.Egea, GustavoEichinger, LudwigEissa, N. TonyEkmekcioglu, SuhendanEl-Deiry, Wafik S.Elazar, ZvulunElgendy, MohamedEllerby, Lisa M.Eng, Kai ErEngelbrecht, Anna-MartEngelender, SimoneErenpreisa, JekaterinaEscalante, RicardoEsclatine, AudreyEskelinen, Eeva-LiisaEspert, LucileEspina, VirginiaFan, HuizhouFan, JiaFan, Qi-WenFan, ZhenFang, ShengyunFang, YongqiFanto, ManolisFanzani, AlessandroFarkas, ThomasFarre, Jean-ClaudeFaure, MathiasFechheimer, MarcusFeng, Carl G.Feng, JianFeng, QiliFeng, YoujiFesues, LaszloFeuer, RalphFigueiredo-Pereira, Maria E.Fimia, Gian MariaFingar, Diane C.Finkbeiner, StevenFinkel, TorenFinley, Kim D.Fiorito, FilomenaFisher, Edward A.Fisher, Paul B.Flajolet, MarcFlorez-McClure, Maria L.Florio, SalvatoreFon, Edward A.Fornai, FrancescoFortunato, FrancoFotedar, RatiFowler, Daniel H.Fox, Howard S.Franco, RodrigoFrankel, Lisa B.Fransen, MarcFuentes, Jose M.Fueyo, JuanFujii, JunFujisaki, KozoFujita, ErikoFukuda, MitsunoriFurukawa, Ruth H.Gaestel, MatthiasGailly, PhilippeGajewska, MalgorzataGalliot, BrigitteGaly, VincentGanesh, SubramaniamGanetzky, BarryGanley, Ian G.Gao, Fen-BiaoGao, George F.Gao, JinmingGarcia, LorenaGarcia-Manero, GuillermoGarcia-Marcos, MikelGarmyn, MarjanGartel, Andrei L.Gatti, EvelinaGautel, MathiasGawriluk, Thomas R.Gegg, Matthew E.Geng, JiefeiGermain, MarcGestwicki, Jason E.Gewirtz, David A.Ghavami, SaeidGhosh, PradiptaGiammarioli, Anna M.Giatromanolaki, Alexandra N.Gibson, Spencer B.Gilkerson, Robert W.Ginger, Michael L.Ginsberg, Henry N.Golab, JakubGoligorsky, Michael S.Golstein, PierreGomez-Manzano, CandelariaGoncu, EbruGongora, CelineGonzalez, Claudio D.Gonzalez, RamonGonzalez-Estevez, CristinaGonzalez-Polo, Rosa AnaGonzalez-Rey, ElenaGorbunov, Nikolai V.Gorski, SharonGoruppi, SandroGottlieb, Roberta A.Gozuacik, DevrimGranato, Giovanna ElviraGrant, Gary D.Green, Kim N.Gregorc, AlesGros, FredericGrose, CharlesGrunt, Thomas W.Gual, PhilippeGuan, Jun-LinGuan, Kun-LiangGuichard, Sylvie M.Gukovskaya, Anna S.Gukovsky, IlyaGunst, JanGustafsson, Asa B.Halayko, Andrew J.Hale, Amber N.Halonen, Sandra K.Hamasaki, MahoHan, FengHan, TingHancock, Michael K.Hansen, MaleneHarada, HisashiHarada, MasaruHardt, Stefan E.Harper, J. WadeHarris, Adrian L.Harris, JamesHarris, Steven D.Hashimoto, MakotoHaspel, Jeffrey A.Hayashi, Shin-ichiroHazelhurst, Lori A.He, CongcongHe, You-WenHebert, Marie-JoseeHeidenreich, Kim A.Helfrich, Miep H.Helgason, Gudmundur V.Henske, Elizabeth P.Herman, BrianHerman, Paul K.Hetz, ClaudioHilfiker, SabineHill, Joseph A.Hocking, Lynne J.Hofman, PaulHofmann, Thomas G.Hoehfeld, JoergHolyoake, Tessa L.Hong, Ming-HuangHood, David A.Hotamisligil, Goekhan S.Houwerzijl, Ewout J.Hoyer-Hansen, MariaHu, BingrenHu, Chien-An A.Hu, Hong-MingHua, YaHuang, CanhuaHuang, JuHuang, ShengbingHuang, Wei-PangHuber, Tobias B.Huh, Won-KiHung, Tai-HoHupp, Ted R.Hur, Gang MinHurley, James B.Hussain, Sabah N. A.Hussey, Patrick J.Hwang, Jung JinHwang, SeungminIchihara, AtsuhiroIlkhanizadeh, ShirinInoki, KenInto, TakeshiIovane, ValentineIovanna, Juan L.Ip, Nancy Y.Isaka, YoshitakaIshida, HiroyukiIsidoro, CiroIsobe, Ken-ichiIwasaki, AkikoIzquierdo, MartaIzumi, YotaroJaakkola, Panu M.Jaattela, MarjaJackson, George R.Jackson, William T.Janji, BassamJendrach, MarinaJeon, Ju-HongJeung, Eui-BaeJiang, HongJiang, HongchiJiang, Jean X.Jiang, MingJiang, QingJiang, XuejunJiang, XuejunJimenez, AlbertoJin, MeiyanJin, ShengkanJoe, Cheol O.Johansen, TerjeJohnson, Daniel E.Johnson, Gail V. W.Jones, Nicola L.Joseph, BertrandJoseph, Suresh K.Joubert, Annie M.Juhasz, GaborJuillerat-Jeanneret, LucienneJung, Chang HwaJung, Yong-KeunKaarniranta, KaiKaasik, AllenKabuta, TomohiroKadowaki, MotoniKagedal, KatarinaKamada, YoshiakiKaminskyy, Vitaliy O.Kampinga, Harm H.Kanamori, HiromitsuKang, ChanheeKang, Khong BeeKang, Kwang IlKang, RuiKang, Yoon-AKanki, TomotakeKanneganti, Thirumala-DeviKanno, HaruoKanthasamy, Anumantha G.Kanthasamy, ArthiKarantza, VassilikiKaushal, Gur P.Kaushik, SusmitaKawazoe, YoshinoriKe, Po-YuanKehrl, John H.Kelekar, AmeetaKerkhoff, ClausKessel, David H.Khalil, HanyKiel, Jan A. K. W.Kiger, Amy A.Kihara, AkioKim, Deok RyongKim, Do-HyungKim, Dong-HouKim, Eun-KyoungKim, Hyung-RyongKim, Jae-SungKim, Jeong HunKim, Jin CheonKim, John K.Kim, Peter K.Kim, Seong WhoKim, Yong-SunKim, YonghyunKimchi, AdiKimmelman, Alec C.King, Jason S.Kinsella, Timothy J.Kirkin, VladimirKirshenbaum, Lorrie A.Kitamoto, KatsuhikoKitazato, KaioKlein, LudgerKlimecki, Walter T.Klucken, JochenKnecht, ErwinKo, Ben C. B.Koch, Jan C.Koga, HiroshiKoh, Jae-YoungKoh, Young HoKoike, MasatoKomatsu, MasaakiKominami, EikiKong, Hee JeongKong, Wei-JiaKorolchuk, Viktor I.Kotake, YaichiroKoukourakis, Michael I.Flores, Juan B. KouriKovacs, Attila L.Kraft, ClaudineKrainc, DimitriKraemer, HelmutKretz-Remy, CaroleKrichevsky, Anna M.Kroemer, GuidoKrueger, RejkoKrut, OlegKtistakis, Nicholas T.Kuan, Chia-YiKucharczyk, RozaKumar, AshokKumar, RajKumar, SharadKundu, MondiraKung, Hsing-JienKurz, TinoKwon, Ho JeongLa Spada, Albert R.Lafont, FrankLamark, TrondLandry, JacquesLane, Jon D.Lapaquette, PierreLaporte, Jocelyn F.Laszlo, LajosLavandero, SergioLavoie, Josee N.Layfield, RobertLazo, Pedro A.Le, WeidongLe Cam, LaurentLedbetter, Daniel J.Lee, Alvin J. X.Lee, Byung-WanLee, Gyun MinLee, JongdaeLee, Ju-HyunLee, MichaelLee, Myung-ShikLee, Sug HyungLeeuwenburgh, ChristiaanLegembre, PatrickLegouis, RenaudLehmann, MichaelLei, Huan-YaoLei, Qun-YingLeib, David A.Leiro, JoseLemasters, John J.Lemoine, AntoinetteLesniak, Maciej S.Lev, DinaLevenson, Victor V.Levine, BethLevy, EfratLi, FaqiangLi, Jun-LinLi, LianLi, ShengLi, WeijieLi, Xue-JunLi, Yan-boLi, Yi-PingLiang, ChengyuLiang, QiangrongLiao, Yung-FengLiberski, Pawel P.Lieberman, AndrewLim, Hyunjung J.Lim, Kah-LeongLim, KyuLin, Chiou-FengLin, Fu-ChengLin, JianLin, Jiandie D.Lin, KuiLin, Wan-WanLin, Weei-ChinLin, Yi-LingLinden, RafaelLingor, PaulLippincott-Schwartz, JenniferLisanti, Michael P.Liton, Paloma B.Liu, BoLiu, Chun-FengLiu, KaiyuLiu, LeyuanLiu, Qiong A.Liu, WeiLiu, Young-ChauLiu, YuleLockshin, Richard A.Lok, Chun-NamLonial, SagarLoos, BenjaminLopez-Berestein, GabrielLopez-Otin, CarlosLossi, LauraLotze, Michael T.Low, PeterLu, BinfengLu, BingweiLu, BoLu, ZhenLuciano, FredericLukacs, Nicholas W.Lund, Anders H.Lynch-Day, Melinda A.Ma, YongMacian, FernandoMacKeigan, Jeff P.Macleod, Kay F.Madeo, FrankMaiuri, LuigiMaiuri, Maria ChiaraMalagoli, DavideMalicdan, May Christine V.Malorni, WalterMan, NaMandelkow, Eva-MariaManon, StephenManov, IrenaMao, KaiMao, XiangMao, ZixuMarambaud, PhilippeMarazziti, DanielaMarcel, Yves L.Marchbank, KatieMarchetti, PieroMarciniak, Stefan J.Marcondes, MateusMardi, MohsenMarfe, GabriellaMarino, GuillermoMarkaki, MariaMarten, Mark R.Martin, Seamus J.Martinand-Mari, CamilleMartinet, WimMartinez-Vicente, MartaMasini, MatildeMatarrese, PaolaMatsuo, SaburoMatteoni, RaffaeleMayer, AndreasMazure, Nathalie M.McConkey, David J.McConnell, Melanie J.McDermott, CatherineMcDonald, ChristineMcInerney, Gerald M.McKenna, Sharon L.McLaughlin, BethAnnMcLean, Pamela J.McMaster, Christopher R.McQuibban, G. AngusMeijer, Alfred J.Meisler, Miriam H.Melendez, AliciaMelia, Thomas J.Melino, GerryMena, Maria A.Menendez, Javier A.Menna-Barreto, Rubem F. S.Menon, Manoj B.Menzies, Fiona M.Mercer, Carol A.Merighi, AdalbertoMerry, Diane E.Meschini, StefaniaMeyer, Christian G.Meyer, Thomas F.Miao, Chao-YuMiao, Jun-YingMichels, Paul A. M.Michiels, CarineMijaljica, DaliborMilojkovic, AnaMinucci, SaverioMiracco, CleliaMiranti, Cindy K.Mitroulis, IoannisMiyazawa, KeisukeMizushima, NoboruMograbi, BahariaMohseni, SiminMolero, XavierMollereau, BertrandMollinedo, FaustinoMomoi, TakashiMonastyrska, IrynaMonick, Martha M.Monteiro, Mervyn J.Moore, Michael N.Mora, RodrigoMoreau, KevinMoreira, Paula I.Moriyasu, YujiMoscat, JorgeMostowy, SergeMottram, Jeremy C.Motyl, TomaszMoussa, Charbel E. -H.Mueller, SylkeMuenger, KarlMuenz, ChristianMurphy, Leon O.Murphy, Maureen E.Musaro, AntonioMysorekar, IndiraNagata, EiichiroNagata, KazuhiroNahimana, AimableNair, UshaNakagawa, ToshiyukiNakahira, KiichiNakano, HiroyasuNakataogawa, HitoshiNanjundan, MeeraNaqvi, Naweed I.Narendra, Derek P.Narita, MasashiNavarro, MiguelNawrocki, Steffan T.Nazarko, Taras Y.Nemchenko, AndriyNetea, Mihai G.Neufeld, Thomas P.Ney, Paul A.Nezis, Ioannis P.Huu Phuc NguyenNie, DaotaiNishino, IchizoNislow, CoreyNixon, Ralph A.Noda, TakeshiNoegel, Angelika A.Nogalska, AnnaNoguchi, SatoruNotterpek, LuciaNovak, IvanaNozaki, TomoyoshiNukina, NobuyukiNuernberger, ThorstenNyfeler, BeatObara, KeisukeOberley, Terry D.Oddo, SalvatoreOgawa, MichinagaOhashi, ToyaOkamoto, KojiOleinick, Nancy L.Oliver, F. JavierOlsen, Laura J.Olsson, StefanOpota, OnyaOsborne, Timothy F.Ostrander, Gary K.Otsu, KinyaOu, Jing-hsiung JamesOuimet, MireilleOverholtzer, MichaelOzpolat, BulentPaganetti, PaoloPagnini, UgoPallet, NicolasPalmer, Glen E.Palumbo, CamillaPan, TianhongPanaretakis, TheocharisPandey, Udai BhanPapackova, ZuzanaPapassideri, IssidoraParis, IrmgardPark, JunsooPark, Ohkmae K.Parys, Jan B.Parzych, Katherine R.Patschan, SusannPatterson, CamPattingre, SophiePawelek, John M.Peng, JianxinPerlmutter, David H.Perrotta, IdaPerry, GeorgePervaiz, ShazibPeter, MatthiasPeters, Godefridus J.Petersen, MortenPetrovski, GoranPhang, James M.Piacentini, MauroPierre, PhilippePierrefite-Carle, ValeriePierron, GerardPinkas-Kramarski, RonitPiras, AntonioPiri, NatikPlatanias, Leonidas C.Poeggeler, StefaniePoirot, MarcPoletti, AngeloPoues, ChristianPozuelo-Rubio, MercedesPraetorius-Ibba, MettePrasad, AnilPrescott, MarkPriault, MurielProduit-Zengaffinen, NathalieProgulske-Fox, AnnProikas-Cezanne, TassulaPrzedborski, SergePrzyklenk, KarinPuertollano, RosaPuyal, JulienQian, Shu-BingQin, LiangQin, Zheng-HongQuaggin, Susan E.Raben, NinaRabinowich, HannahRabkin, Simon W.Rahman, IrfanRami, AbdelhaqRamm, GeorgRandall, GlennRandow, FelixRao, V. 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DGIST Authors
Kim, Eun-KyoungYu, Seong Woon
Issue Date
2012-04
Citation
Autophagy, 8(4), 445-544
Type
Article
Article Type
Review
Keywords
AnimalAnimalsAutolysosomeAutophagosomeautophagyAutophagybioassayBiological Assaybiological modelFluxGneticsHumanHumansLC3LysosomeModels, BiologicalPhagophoreProceduresStressVacuole
ISSN
1554-8627
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. ⓒ 2012 Landes Bioscience.
URI
http://hdl.handle.net/20.500.11750/3372
DOI
10.4161/auto.19496
Publisher
Taylor and Francis Ltd.
Related Researcher
Files:
There are no files associated with this item.
Collection:
ETC1. Journal Articles
Brain and Cognitive SciencesLaboratory of Neuronal Cell Death1. Journal Articles


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