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Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)

Item Type:Review
Title:Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)
Creators Name:Klionsky, D.J. and Abdel-Aziz, A.K. and Abdelfatah, S. and Abdellatif, M. and Abdoli, A. and Abel, S. and Abeliovich, H. and Abildgaard, M.H. and Abudu, Y.P. and Acevedo-Arozena, A. and Adamopoulos, I.E. and Adeli, K. and Adolph, T.E. and Adornetto, A. and Aflaki, E. and Agam, G. and Agarwal, A. and Aggarwal, B.B. and Agnello, M. and Agostinis, P. and Agrewala, J.N. and Agrotis, A. and Aguilar, P.V. and Ahmad, S.T. and Ahmed, Z.M. and Ahumada-Castro, U. and Aits, S. and Aizawa, S. and Akkoc, Y. and Akoumianaki, T. and Akpinar, H.A. and Al-Abd, A.M. and Al-Akra, L. and Al-Gharaibeh, A. and Alaoui-Jamali, M.A. and Alberti, S. and Alcocer-Gómez, E. and Alessandri, C. and Ali, M. and Alim Al-Bari, M.A. and Aliwaini, S. and Alizadeh, J. and Almacellas, E. and Almasan, A. and Alonso, A. and Alonso, G.D. and Altan-Bonnet, N. and Altieri, D.C. and Álvarez, E.M.C. and Alves, S. and Alves da Costa, C. and Alzaharna, M.M. and Amadio, M. and Amantini, C. and Amaral, C. and Ambrosio, S. and Amer, A.O. and Ammanathan, V. and An, Z. and Andersen, S.U. and Andrabi, S.A. and Andrade-Silva, M. and Andres, A.M. and Angelini, S. and Ann, D. and Anozie, U.C. and Ansari, M.Y. and Antas, P. and Antebi, A. and Antón, Z. and Anwar, T. and Apetoh, L. and Apostolova, N. and Araki, T. and Araki, Y. and Arasaki, K. and Araújo, W.L. and Araya, J. and Arden, C. and Arévalo, M.A. and Arguelles, S. and Arias, E. and Arikkath, J. and Arimoto, H. and Ariosa, A.R. and Armstrong-James, D. and Arnauné-Pelloquin, L. and Aroca, A. and Arroyo, D.S. and Arsov, I. and Artero, R. and Asaro, D.M.L. and Aschner, M. and Ashrafizadeh, M. and Ashur-Fabian, O. and Atanasov, A.G. and Au, A.K. and Auberger, P. and Auner, H.W. and Aurelian, L. and Autelli, R. and Avagliano, L. and Ávalos, Y. and Aveic, S. and Aveleira, C.A. and Avin-Wittenberg, T. and Aydin, Y. and Ayton, S. and Ayyadevara, S. and Azzopardi, M. and Baba, M.u and Backer, J.M. and Backues, S.K. and Bae, D.H. and Bae, O.N. and Bae, S.H. and Baehrecke, E.H. and Baek, A. and Baek, S.H. and Baek, S.H. and Bagetta, G. and Bagniewska-Zadworna, A. and Bai, H. and Bai, J. and Bai, X. and Bai, Y. and Bairagi, N. and Baksi, S. and Balbi, T. and Baldari, C.T. and Balduini, W. and Ballabio, A. and Ballester, M. and Balazadeh, S. and Balzan, R. and Bandopadhyay, R. and Banerjee, S. and Banerjee, S. and Bánréti, A. and Bao, Y. and Baptista, M.S. and Baracca, A. and Barbati, C. and Bargiela, A. and Barilà, D. and Barlow, P.G. and Barmada, S.J. and Barreiro, E. and Barreto, G.E. and Bartek, J. and Bartel, B. and Bartolome, A. and Barve, G.R. and Basagoudanavar, S.H. and Bassham, D.C. and Bast, R.C. and Basu, A. and Batoko, H. and Batten, I. and Baulieu, E.E. and Baumgarner, B.L. and Bayry, J. and Beale, R. and Beau, I. and Beaumatin, F. and Bechara, L.R.G. and Beck, G.R. and Beers, M.F. and Begun, J. and Behrends, C. and Behrens, G.M.N. and Bei, R. and Bejarano, E. and Bel, S. and Behl, C. and Belaid, A. and Belgareh-Touzé, N. and Bellarosa, C. and Belleudi, F. and Belló Pérez, M. and Bello-Morales, R. and Beltran, J.S.O. and Beltran, S. and Benbrook, D.M. and Bendorius, M. and Benitez, B.A. and Benito-Cuesta, I. and Bensalem, J. and Berchtold, M.W. and Berezowska, S. and Bergamaschi, D. and Bergami, M. and Bergmann, A. and Berliocchi, L. and Berlioz-Torrent, C. and Bernard, A. and Berthoux, L. and Besirli, C.G. and Besteiro, S. and Betin, V.M. and Beyaert, R. and Bezbradica, J.S. and Bhaskar, K. and Bhatia-Kissova, I. and Bhattacharya, R. and Bhattacharya, S. and Bhattacharyya, S. and Bhuiyan, M.S. and Bhutia, S.K. and Bi, L. and Bi, X. and Biden, T.J. and Bijian, K. and Billes, V.A. and Binart, N. and Bincoletto, C. and Birgisdottir, A.B. and Bjorkoy, G. and Blanco, G. and Blas-Garcia, A. and Blasiak, J. and Blomgran, R. and Blomgren, K. and Blum, J.S. and Boada-Romero, E. and Boban, M. and Boesze-Battaglia, K. and Boeuf, P. and Boland, B. and Bomont, P. and Bonaldo, P. and Bonam, S.R. and Bonfili, L. and Bonifacino, J.S. and Boone, B.A. and Bootman, M.D. and Bordi, M. and Borner, C. and Bornhauser, B.C. and Borthakur, G. and Bosch, J. and Bose, S. and Botana, L.M. and Botas, J. and Boulanger, C.M. and Boulton, M.E. and Bourdenx, M. and Bourgeois, B. and Bourke, N.M. and Bousquet, G. and Boya, P. and Bozhkov, P.V. and Bozi, L.H.M. and Bozkurt, T.O. and Brackney, D.E. and Brandts, C.H. and Braun, R.J. and Braus, G.H. and Bravo-Sagua, R. and Bravo-San Pedro, J.M. and Brest, P. and Bringer, M.A. and Briones-Herrera, A. and Broaddus, V.C. and Brodersen, P. and Brodsky, J.L. and Brody, S.L. and Bronson, P.G. and Bronstein, J.M. and Brown, C.N. and Brown, R.E. and Brum, P.C. and Brumell, J.H. and Brunetti-Pierri, N. and Bruno, D. and Bryson-Richardson, R.J. and Bucci, C. and Buchrieser, C. and Bueno, M. and Buitrago-Molina, L.E. and Buraschi, S. and Buch, S. and Buchan, J.R. and Buckingham, E.M. and Budak, H. and Budini, M. and Bultynck, G. and Burada, F. and Burgoyne, J.R. and Burón, M.I. and Bustos, V. and Büttner, S. and Butturini, E. and Byrd, A. and Cabas, I. and Cabrera-Benitez, S. and Cadwell, K. and Cai, J. and Cai, L. and Cai, Q. and Cairó, M. and Calbet, J.A. and Caldwell, G.A. and Caldwell, K.A. and Call, J.A. and Calvani, R. and Calvo, A.C. and Calvo-Rubio Barrera, M. and Camara, N.O. and Camonis, J.H. and Camougrand, N. and Campanella, M. and Campbell, E.M. and Campbell-Valois, F.X. and Campello, S. and Campesi, I. and Campos, J.C. and Camuzard, O. and Cancino, J. and Candido de Almeida, D. and Canesi, L. and Caniggia, I. and Canonico, B. and Cantí, C. and Cao, B. and Caraglia, M. and Caramés, B. and Carchman, E.H. and Cardenal-Muñoz, E. and Cardenas, C. and Cardenas, L. and Cardoso, S.M. and Carew, J.S. and Carle, G.F. and Carleton, G. and Carloni, S. and Carmona-Gutierrez, D. and Carneiro, L.A. and Carnevali, O. and Carosi, J.M. and Carra, S. and Carrier, A. and Carrier, L. and Carroll, B. and Carter, A.B. and Carvalho, A.N. and Casanova, M. and Casas, C. and Casas, J. and Cassioli, C. and Castillo, E.F. and Castillo, K. and Castillo-Lluva, S. and Castoldi, F. and Castori, M. and Castro, A.F. and Castro-Caldas, M. and Castro-Hernandez, J. and Castro-Obregon, S. and Catz, S.D. and Cavadas, C. and Cavaliere, F. and Cavallini, G. and Cavinato, M. and Cayuela, M.L. and Cebollada Rica, P. and Cecarini, V. and Cecconi, F. and Cechowska-Pasko, M. and Cenci, S. and Ceperuelo-Mallafré, V. and Cerqueira, J.J. and Cerutti, J.M. and Cervia, D. and Cetintas, V.B. and Cetrullo, S. and Chae, H.J. and Chagin, A.S. and Chai, C.Y. and Chakrabarti, G. and Chakrabarti, O. and Chakraborty, T. and Chakraborty, T. and Chami, M. and Chamilos, G. and Chan, D.W. and Chan, E.Y.W. and Chan, E.D. and Chan, H.Y.E. and Chan, H.H. and Chan, H. and Chan, M.T.V. and Chan, Y.S. and Chandra, P.K. and Chang, C.P. and Chang, C. and Chang, H.C. and Chang, K. and Chao, J. and Chapman, T. and Charlet-Berguerand, N. and Chatterjee, S. and Chaube, S.K. and Chaudhary, A. and Chauhan, S. and Chaum, E. and Checler, F. and Cheetham, M.E. and Chen, C.S. and Chen, G.C. and Chen, J.F. and Chen, L.L. and Chen, L. and Chen, L. and Chen, M. and Chen, M.K. and Chen, N. and Chen, Q. and Chen, R.H. and Chen, S. and Chen, W. and Chen, W. and Chen, X.M. and Chen, X.W. and Chen, X. and Chen, Y. and Chen, Y.G. and Chen, Y. and Chen, Y. and Chen, Y.J. and Chen, Y.Q. and Chen, Z.S. and Chen, Z. and Chen, Z.H. and Chen, Z.J. and Chen, Z. and Cheng, H. and Cheng, J. and Cheng, S.Y. and Cheng, W. and Cheng, X. and Cheng, X.T. and Cheng, Y. and Cheng, Z. and Chen, Z. and Cheong, H. and Cheong, J.K. and Chernyak, B.V. and Cherry, S. and Cheung, C.F.R. and Cheung, C.H.A. and Cheung, K.H. and Chevet, E. and Chi, R.J. and Chiang, A.K.S. and Chiaradonna, F. and Chiarelli, R. and Chiariello, M. and Chica, N. and Chiocca, S. and Chiong, M. and Chiou, S.H. and Chiramel, A.I. and Chiurchiù, V. and Cho, D.H. and Choe, S.K. and Choi, A.M.K. and Choi, M.E. and Choudhury, K.R. and Chow, N.S. and Chu, C.T. and Chua, J.P. and Chua, J.J.E. and Chung, H. and Chung, K.P. and Chung, S. and Chung, S.H. and Chung, Y.L. and Cianfanelli, V. and Ciechomska, I.A. and Cifuentes, M. and Cinque, L. and Cirak, S. and Cirone, M. and Clague, M.J. and Clarke, R. and Clementi, E. and Coccia, E.M. and Codogno, P. and Cohen, E. and Cohen, M.M and Colasanti, T. and Colasuonno, F. and Colbert, R.A. and Colell, A. and Čolić, M. and Coll, N.S. and Collins, M.O. and Colombo, M.I. and Colón-Ramos, D.A. and Combaret, L. and Comincini, S. and Cominetti, M.R. and Consiglio, A. and Conte, A. and Conti, F. and Contu, V.R. and Cookson, M.R. and Coombs, K.M. and Coppens, I. and Corasaniti, M.T. and Corkery, D.P. and Cordes, N. and Cortese, K. and Costa, M.D.C. and Costantino, S. and Costelli, P. and Coto-Montes, A. and Crack, P.J. and Crespo, J.L. and Criollo, A. and Crippa, V. and Cristofani, R. and Csizmadia, T. and Cuadrado, A. and Cui, B. and Cui, J. and Cui, Y. and Cui, Y. and Culetto, E. and Cumino, A.C. and Cybulsky, A.V. and Czaja, M.J. and Czuczwar, S.J. and D'Adamo, S. and D'Amelio, M. and D'Arcangelo, D. and D'Lugos, A.C. and D'Orazi, G. and da Silva, J.A. and Dafsari, H.S. and Dagda, R.K. and Dagdas, Y. and Daglia, M. and Dai, X. and Dai, Y. and Dai, Y. and Dal Col, J. and Dalhaimer, P. and Dalla Valle, L. and Dallenga, T. and Dalmasso, G. and Damme, M. and Dando, I. and Dantuma, N.P. and Darling, A.L. and Das, H. and Dasarathy, S. and Dasari, S.K. and Dash, S. and Daumke, O. and Dauphinee, A.N. and Davies, J.S. and Dávila, V.A. and Davis, R.J. and Davis, T. and Dayalan Naidu, S. and De Amicis, F. and De Bosscher, K. and De Felice, F. and De Franceschi, L. and De Leonibus, C. and de Mattos Barbosa, M.G. and De Meyer, G.R.Y. and De Milito, A. and De Nunzio, C. and De Palma, C. and De Santi, M. and De Virgilio, C. and De Zio, D. and Debnath, J. and DeBosch, B.J. and Decuypere, J.P. and Deehan, M.A. and Deflorian, G. and DeGregori, J. and Dehay, B. and Del Rio, G. and Delaney, J.R. and Delbridge, L.M.D. and Delorme-Axford, E. and Delpino, M.V. and Demarchi, F. and Dembitz, V. and Demers, N.D. and Deng, H. and Deng, Z. and Dengjel, J. and Dent, P. and Denton, D. and DePamphilis, M.L. and Der, C.J. and Deretic, V. and Descoteaux, A. and Devis, L. and Devkota, S. and Devuyst, O. and Dewson, G. and Dharmasivam, M. and Dhiman, R. and di Bernardo, D. and Di Cristina, M. and Di Domenico, F. and Di Fazio, P. and Di Fonzo, A. and Di Guardo, G. and Di Guglielmo, G.M. and Di Leo, L. and Di Malta, C. and Di Nardo, A. and Di Rienzo, M. and Di Sano, F. and Diallinas, G. and Diao, J. and Diaz-Araya, G. and Díaz-Laviada, I. and Dickinson, J.M. and Diederich, M. and Dieudé, M. and Dikic, I. and Ding, S. and Ding, W.X. and Dini, L. and Dinić, J. and Dinic, M. and Dinkova-Kostova, A.T. and Dionne, M.S. and Distler, J.H.W. and Diwan, A. and Dixon, I.M.C. and Djavaheri-Mergny, M. and Dobrinski, I. and Dobrovinskaya, O. and Dobrowolski, R. and Dobson, R.C.J. and Đokić, J. and Dokmeci Emre, S. and Donadelli, M. and Dong, B. and Dong, X. and Dong, Z. and Dorn Ii, G.W. and Dotsch, V. and Dou, H. and Dou, J. and Dowaidar, M. and Dridi, S. and Drucker, L. and Du, A. and Du, C. and Du, G. and Du, H.N. and Du, L.L. and du Toit, A. and Duan, S.B. and Duan, X. and Duarte, S.P. and Dubrovska, A. and Dunlop, E.A. and Dupont, N. and Durán, R.V. and Dwarakanath, B.S. and Dyshlovoy, S.A. and Ebrahimi-Fakhari, D. and Eckhart, L. and Edelstein, C.L. and Efferth, T. and Eftekharpour, E. and Eichinger, L. and Eid, N. and Eisenberg, T. and Eissa, N.T. and Eissa, S. and Ejarque, M. and El Andaloussi, A. and El-Hage, N. and El-Naggar, S. and Eleuteri, A.M. and El-Shafey, E.S. and Elgendy, M. and Eliopoulos, A.G. and Elizalde, M.M. and Elks, P.M. and Elsasser, H.P. and Elsherbiny, E.S. and Emerling, B.M. and Emre, N.C.T. and Eng, C.H. and Engedal, N. and Engelbrecht, A.M. and Engelsen, A.S.T. and Enserink, J.M. and Escalante, R. and Esclatine, A. and Escobar-Henriques, M. and Eskelinen, E.L. and Espert, L. and Eusebio, M.O. and Fabrias, G. and Fabrizi, C. and Facchiano, A. and Facchiano, F. and Fadeel, B. and Fader, C. and Faesen, A.C. and Fairlie, W.D. and Falcó, A. and Falkenburger, B.H. and Fan, D. and Fan, J. and Fan, Y. and Fang, E.F. and Fang, Y. and Fang, Y. and Fanto, M. and Farfel-Becker, T. and Faure, M. and Fazeli, G. and Fedele, A.O. and Feldman, A.M. and Feng, D. and Feng, J. and Feng, L. and Feng, Y. and Feng, Y. and Feng, W. and Fenz Araujo, T. and Ferguson, T.A. and Fernández, A.F. and Fernandez-Checa, J.C. and Fernández-Veledo, S. and Fernie, A.R. and Ferrante, A.W. and Ferraresi, A. and Ferrari, M.F. and Ferreira, J.C.B. and Ferro-Novick, S. and Figueras, A. and Filadi, R. and Filigheddu, N. and Filippi-Chiela, E. and Filomeni, G. and Fimia, G.M. and Fineschi, V. and Finetti, F. and Finkbeiner, S. and Fisher, E.A. and Fisher, P.B. and Flamigni, F. and Fliesler, S.J. and Flo, T.H. and Florance, I. and Florey, O. and Florio, T. and Fodor, E. and Follo, C. and Fon, E.A. and Forlino, A. and Fornai, F. and Fortini, P. and Fracassi, A. and Fraldi, A. and Franco, B. and Franco, R. and Franconi, F. and Frankel, L.B. and Friedman, S.L. and Fröhlich, L.F. and Frühbeck, G. and Fuentes, J.M. and Fujiki, Y. and Fujita, N. and Fujiwara, Y. and Fukuda, M. and Fulda, S. and Furic, L. and Furuya, N. and Fusco, C. and Gack, M.U. and Gaffke, L. and Galadari, S. and Galasso, A. and Galindo, M.F. and Gallolu Kankanamalage, S. and Galluzzi, L. and Galy, V. and Gammoh, N. and Gan, B. and Ganley, I.G. and Gao, F. and Gao, H. and Gao, M. and Gao, P. and Gao, S.J. and Gao, W. and Gao, X. and Garcera, A. and Garcia, M.N. and Garcia, V.E. and García-Del Portillo, F. and Garcia-Escudero, V. and Garcia-Garcia, A. and Garcia-Macia, M. and García-Moreno, D. and Garcia-Ruiz, C. and García-Sanz, P. and Garg, A.D. and Gargini, R. and Garofalo, T. and Garry, R.F. and Gassen, N.C. and Gatica, D. and Ge, L. and Ge, W. and Geiss-Friedlander, R. and Gelfi, C. and Genschik, P. and Gentle, I.E. and Gerbino, V. and Gerhardt, C. and Germain, K. and Germain, M. and Gewirtz, D.A. and Ghasemipour Afshar, E. and Ghavami, S. and Ghigo, A. and Ghosh, M. and Giamas, G. and Giampietri, C. and Giatromanolaki, A. and Gibson, G.E. and Gibson, S.B. and Ginet, V. and Giniger, E. and Giorgi, C. and Girao, H. and Girardin, S.E. and Giridharan, M. and Giuliano, S. and Giulivi, C. and Giuriato, S. and Giustiniani, J. and Gluschko, A. and Goder, V. and Goginashvili, A. and Golab, J. and Goldstone, D.C. and Golebiewska, A. and Gomes, L.R. and Gomez, R. and Gómez-Sánchez, R. and Gomez-Puerto, M.C. and Gomez-Sintes, R. and Gong, Q. and Goni, F.M. and González-Gallego, J. and Gonzalez-Hernandez, T. and Gonzalez-Polo, R.A. and Gonzalez-Reyes, J.A. and González-Rodríguez, P. and Goping, I.S. and Gorbatyuk, M.S. and Gorbunov, N.V. and Görgülü, K. and Gorojod, R.M. and Gorski, S.M. and Goruppi, S. and Gotor, C. and Gottlieb, R.A. and Gozes, I. and Gozuacik, D. and Graef, M. and Gräler, M.H. and Granatiero, V. and Grasso, D. and Gray, J.P. and Green, D.R. and Greenhough, A. and Gregory, S.L. and Griffin, E.F. and Grinstaff, M.W. and Gros, F. and Grose, C. and Gross, A.S. and Gruber, F. and Grumati, P. and Grune, T. and Gu, X. and Guan, J.L. and Guardia, C.M. and Guda, K. and Guerra, F. and Guerri, C. and Guha, P. and Guillén, C. and Gujar, S. and Gukovskaya, A. and Gukovsky, I. and Gunst, J. and Günther, A. and Guntur, A.R. and Guo, C. and Guo, C. and Guo, H. and Guo, L.W. and Guo, M. and Gupta, P. and Gupta, S.K. and Gupta, S. and Gupta, V.B. and Gupta, V. and Gustafsson, A.B. and Gutterman, D.D. and H B, R. and Haapasalo, A. and Haber, J.E. and Hać, A. and Hadano, S. and Hafrén, A.J. and Haidar, M. and Hall, B.S. and Halldén, G. and Hamacher-Brady, A. and Hamann, A. and Hamasaki, M. and Han, W. and Hansen, M. and Hanson, P.I. and Hao, Z. and Harada, M. and Harhaji-Trajkovic, L. and Hariharan, N. and Haroon, N. and Harris, J. and Hasegawa, 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Abstract:In 2008, we published the first set of guidelines for standardizing research in autophagy. Since then, this topic has received increasing attention, and many scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Thus, it is important to formulate on a regular basis updated guidelines for monitoring autophagy in different organisms. Despite numerous reviews, there continues to be confusion regarding acceptable methods to evaluate autophagy, especially in multicellular eukaryotes. Here, we present a set of guidelines for investigators to select and interpret methods to examine autophagy and related processes, and for reviewers to provide realistic and reasonable critiques of reports that are focused on these processes. These guidelines are not meant to be a dogmatic set of rules, because the appropriateness of any assay largely depends on the question being asked and the system being used. Moreover, no individual assay is perfect for every situation, calling for the use of multiple techniques to properly monitor autophagy in each experimental setting. Finally, several core components of the autophagy machinery have been implicated in distinct autophagic processes (canonical and noncanonical autophagy), implying that genetic approaches to block autophagy should rely on targeting two or more autophagy-related genes that ideally participate in distinct steps of the pathway. Along similar lines, because multiple proteins involved in autophagy also regulate other cellular pathways including apoptosis, not all of them can be used as a specific marker for bona fide autophagic responses. Here, we critically discuss current methods of assessing autophagy and the information they can, or cannot, provide. Our ultimate goal is to encourage intellectual and technical innovation in the field.
Keywords:Autophagosome, Cancer, Flux, LC3, Lysosome, Macroautophagy, Neurodegeneration, Phagophore, Stress, Vacuole
Source:Autophagy
ISSN:1554-8627
Publisher:Taylor & Francis
Volume:17
Number:1
Page Range:1-382
Date:8 February 2021
Official Publication:https://doi.org/10.1080/15548627.2020.1797280
PubMed:View item in PubMed

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