Article: Guidelines for the use and interpretation of assays for monitoring autophagy

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TitleGuidelines for the use and interpretation of assays for monitoring autophagy
AuthorsKlionsky, DJ
Abdalla, FC
Abeliovich, H472
Abraham, RT
AcevedoArozena, A406
Adeli, K
Agholme, L40
Agnello, M201
Agostinis, P
AguirreGhiso, JA344
Ahn, HJ100
BrunettiPierri, N470
Shi, Y
Shibuya, K454
Shidoji, Y175
Shieh, JJ
Shih, CM
Shimada, Y
Shimizu, S
Shintani, T340
Shirihai, OS232
Shore, GC
Brunk, UT40
Sibirny, AA346 383
Sidhu, SB185
Sikorska, B473
SilvaZacarin, ECM
Simmons, A
Simon, AK350
Simon, HU492
Simone, C8 112
Simonsen, A456
Sinclair, DA151
Bulman, DE484
Singh, R63
Sinha, D
Sinicrope, FA246
Sirko, A
Siu, PM408
Sivridis, E49
Skop, V204
Skulachev, VP
Slack, RS
Smaili, SS328
Bultman, SJ
Smith, DR
Soengas, MS
Soldati, T433
Song, X
Sood, AK393
Soong, TW483
Sotgia, F
Spector, SA226 396
Spies, CD444
Springer, W259
Bultynck, G
Srinivasula, SM173
Stefanis, L14
Steffan, JS461
Stendel, R444
Stenmark, H456
Stephanou, A34
Stern, ST481
Sternberg, C87
Stork, B
Strålfors, P40
Burbulla, LF386
Subauste, CS442
Sui, X195
Sulzer, D369
Sun, J294
Sun, SY415
Sun, ZJ230
Sung, JJY
Suzuki, K495
Suzuki, T285
Swanson, MS
Bursch, W421
Swanton, C440
Sweeney, ST489
Sy, LK192
Szabadkai, G34
Tabas, I188
Taegtmeyer, H118
Tafani, M
TakácsVellai, K378
Takano, Y402
Takegawa, K171
Butchar, JP168
Takemura, G390
Takeshita, F280
Talbot, NJ
Tan, KSW483
Tanaka, K447
Tanaka, K340
Tang, D
Tang, D352
Tanida, I95
Tannous, BA11
Buzgariu, W433
Tavernarakis, N
Taylor, GS364
Taylor, GA88 335
Taylor, JP464
Terada, AS6
Terman, A84
Tettamanti, G140
Thevissen, K
Thompson, CB178
Thorburn, A181
Bydlowski, SP
Thumm, M272
Tian, F13
Tian, Y417
TocchiniValentini, G
Tolkovsky, AM435
Tomino, Y462
Tönges, L272
Tooze, SA440
Tournier, C191
Tower, J238
AitMohamed, O222
Cadwell, K27
Towns, R240
Trajkovic, V377
Travassos, LH
Tsai, TF446
Tschan, MP492
Tsubata, T
Tsung, A298
Turk, B89
Turner, LS160
Tyagi, SC220
Cahová, M180
Uchiyama, Y258
Ueno, T258
Umekawa, M
UmemiyaShirafuji, R206
Unni, VK
Vaccaro, MI
Valente, EM82 166
Van Den Berghe, G
Van Der Klei, IJ311
Van Doorn, WG75
Cai, D63
Van Dyk, LF181
Van Egmond, M227
Van Grunsven, LA443
Vandenabeele, P197
Vandenberghe, WP
Vanhorebeek, I
Vaquero, EC68
Velasco, G169
Vellai, T378
Vicencio, JM34
Cai, J
Vierstra, RD273
Vila, M30 282
Vindis, C351 498
Viola, G39
Viscomi, MT
Voitsekhovskaja, OV134
Von Haefen, C444
Votruba, M372
Wada, K164
WadeMartins, R
Cai, Q69
Walker, CL315
Walsh, CM461
Walter, J46
Wan, XB326
Wang, A
Wang, C
Wang, D98
Wang, F88
Wang, F265
Wang, G423
Calabretta, B
Wang, H453
Wang, HG29 116
Wang, HD380
Wang, J67
Wang, K
Wang, M52
Wang, RC6
Wang, X442
Wang, X343
Wang, YJ427
CalvoGarrido, J3
Wang, Y440
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Wansink, DG241
Ward, DM448
Watada, H258
Waters, SL44
Webster, P
Wei, L
Camougrand, N76
Weihl, CC93
Weiss, WA31
Welford, SM442
Wen, LP254
Whitehouse, CA44
Whitton, JL264
Whitworth, AJ198
Wileman, T338
Wiley, JW240
Wilkinson, S
Campanella, M161 172
Willbold, D7
Williams, RL394
Williamson, PR407
Wouters, BG475
Wu, C213
Wu, DC
Wu, WKK
Wyttenbach, A149
Xavier, RJ11
Xi, Z
CamposSalinas, J
Xia, P185
Xiao, G352
Xie, Z292
Xie, Z
Xu, DZ326
Xu, J47
Xu, L35
Xu, X125
Yamamoto, A369
Yamamoto, A
AitSiAli, S222
Candi, E182
Yamashina, S258
Yamashita, M53
Yan, X496
Yanagida, M202
Yang, DS27
Yang, E38
Yang, JM29 116
Yang, SY34
Yang, W332
Yang, WY154
Cao, L
Yang, Z70
Yao, MC154
Yao, TP88
Yeganeh, B170
Yen, WL
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Carding, SR338
Yu, WH369
Yuan, ZM214
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Yun, CH391
Yuzaki, M303
Zabirnyk, O135
SilvaZacarin, E
David Zacks, E240
Zacksenhaus, L21
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Cardoso, SM101
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Zeh III, HJ345
Zeitlin, SO155
Zhang, H
Zhang, HL423
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Carew, JS214
Zhang, XD
Zhao, M
Zhao, YF230
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Zhao, ZJ
Zheng, X195
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Zhu, C
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Zoladek, T
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KeywordsAutolysosome
Autophagosome
Flux
LC3
Lysosome
Phagophore
Stress
Vacuole
Issue Date2012
CitationAutophagy, 2012, v. 8 n. 4, p. 445-544 [How to Cite?]
DOI: http://dx.doi.org/10.4161/auto.19496
AbstractIn 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.
ISSN1554-8627
2011 Impact Factor: 7.453
2011 SCImago Journal Rankings: 0.974
DOIhttp://dx.doi.org/10.4161/auto.19496
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dc.date.accessioned2012-10-08T03:23:42Z
dc.date.available2012-10-08T03:23:42Z
dc.date.issued2012
dc.description.abstractIn 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.
dc.description.natureLink_to_subscribed_fulltext
dc.identifier.citationAutophagy, 2012, v. 8 n. 4, p. 445-544 [How to Cite?]
DOI: http://dx.doi.org/10.4161/auto.19496
dc.identifier.doihttp://dx.doi.org/10.4161/auto.19496
dc.identifier.epage544
dc.identifier.hkuros203531
dc.identifier.issn1554-8627
2011 Impact Factor: 7.453
2011 SCImago Journal Rankings: 0.974
dc.identifier.issue4
dc.identifier.scopuseid_2-s2.0-84862295360
dc.identifier.spage445
dc.identifier.urihttp://hdl.handle.net/10722/168634
dc.identifier.volume8
dc.languageeng
dc.relation.ispartofAutophagy
dc.relation.referencesReferences in Scopus
dc.subjectAutolysosome
dc.subjectAutophagosome
dc.subjectFlux
dc.subjectLC3
dc.subjectLysosome
dc.subjectPhagophore
dc.subjectStress
dc.subjectVacuole
dc.titleGuidelines for the use and interpretation of assays for monitoring autophagy
dc.typeArticle
Author Affiliations
  1. Sanford-Burnham Medical Research Institute at Lake Nona
  2. CSIC-JA-UPO-USE - Centro Andaluz de Biologia Molecular y Medicina Regenerativa (CABIMER)
  3. Universidad Autónoma de Madrid
  4. Merck KGaA
  5. Istituto Neurologico Mediterraneo Neuromed, Pozzilli
  6. UT Southwestern Medical School
  7. Forschungszentrum Jülich (FZJ)
  8. DTP
  9. Trinity College Dublin
  10. National Cancer Institute
  11. Massachusetts General Hospital
  12. University of Athens
  13. Okayama University Medical School
  14. Academy of Athens
  15. Universidad de Valparaiso
  16. University of Medicine and Dentistry of New Jersey
  17. Uniwersytet Warszawski
  18. University of Durham
  19. Kyoto Sangyo University
  20. Medical University of South Carolina
  21. Toronto General Research Institute
  22. Chungbuk National University
  23. University of Illinois at Chicago
  24. Tokyo Women's Medical University
  25. Johns Hopkins University
  26. Universite de Franche-Comte
  27. New York University School of Medicine
  28. Università Vita-Salute San Raffaele
  29. Penn State Hershey Cancer Institute
  30. Universidad Autónoma de Barcelona
  31. University of California, San Francisco
  32. Kræftens Bekæmpelse
  33. Massachusetts Institute of Technology
  34. UCL
  35. University of Kansas
  36. Institut Claudius Regaud
  37. Ludwig-Maximilians-Universität München
  38. Vanderbilt Ingram Cancer Center
  39. Università degli Studi di Padova
  40. Linköpings universitet
  41. Institute of Microbiology Chinese Academy of Sciences
  42. Cornell University
  43. AstraZeneca
  44. King's College London
  45. Fundacao Oswaldo Cruz
  46. Universität Bonn
  47. Henan University of Technology
  48. Nanjing Agricultural University
  49. Dimokrition Panepistimion Thrakis
  50. INRA Institut National de La Recherche Agronomique
  51. The University of Hong Kong Li Ka Shing Faculty of Medicine
  52. Duke-NUS Graduate Medical School Singapore
  53. National Research Institute of Fisheries Science, FRA
  54. University of Debrecen Medical and Health Science Center
  55. Université de Strasbourg
  56. The Wistar Institute
  57. University of Dundee
  58. Safar Center for Resuscitation Research
  59. Keio University
  60. University of Shizuoka
  61. Centre Hospitalier de L'Universite de Montreal
  62. University of Washington
  63. Albert Einstein College of Medicine of Yeshiva University
  64. Norwegian Institute of Public Health
  65. Aix Marseille Université
  66. York Universite Canada
  67. Baylor College of Medicine
  68. Hospital Clinic Barcelona
  69. Rutgers, The State University of New Jersey
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  71. San Raffaele Institute Sulmona
  72. Institute for Research in Ophthalmology (IRO)
  73. EMD Serono Research Institute, Inc.
  74. Bernhard Nocht Institut fur Tropenmedizin Hamburg
  75. UC Davis
  76. Université de Bordeaux
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  80. The Catholic University of Korea
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  91. null
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  112. null
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  116. Penn State College of Medicine
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  119. National Institute of Arthritis and Musculoskeletal and Skin Diseases
  120. Dulbecco Telethon Institute
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  122. Newcastle University, United Kingdom
  123. Chonbuk National University
  124. LEO Pharma AS
  125. Mayo Clinic
  126. Stanford University
  127. University of Toledo
  128. null
  129. Academic Medical Centre, University of Amsterdam
  130. South China Normal University
  131. Helsingin Yliopisto
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  134. Russian Academy of Sciences
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  139. Van Andel Research Institute
  140. Università degli Studi dell'Insubria
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  143. Cincinnati Children's Hospital Medical Center
  144. VAAAHS
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  146. LSU Health Sciences Center - Shreveport
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  148. null
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  153. National Institutes Allergy and Infectious Diseases, Hamilton
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  172. Centro Europeo di Ricerca sul Cervello, Roma
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  174. Mackay Memorial Hospital Taiwan
  175. Nagasaki University
  176. University at Buffalo State University of New York
  177. Centro de Investigacion y de Estudios Avanzados
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  179. Universite de Rennes 1
  180. Institutu Klinické a Experimentální Medicíny
  181. University of Colorado School of Medicine
  182. Università degli Studi di Roma Tor Vergata
  183. Universidad de Costa Rica
  184. Universidad de Santiago de Compostela
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  187. Eidgenossische Technische Hochschule Zurich
  188. Columbia University in the City of New York
  189. Harvard University
  190. Feinstein Institute for Medical Research
  191. University of Manchester
  192. The University of Hong Kong
  193. Universidad de Extremadura
  194. Shanghai Jiaotong University
  195. Zhejiang University
  196. Vilnius University
  197. Universiteit Gent
  198. University of Sheffield
  199. Universite Montpellier 2 Sciences et Techniques
  200. Università degli Studi di Udine
  201. Università degli Studi di Palermo
  202. OIST Graduate University
  203. null
  204. Vysoká škola chemicko-technologická v Praze
  205. Pontificia Universidad Católica de Chile
  206. Kagoshima University
  207. University of Glasgow
  208. CSIC-JA-UPO - Centro Andaluz de Biología del Desarrollo (CABD)
  209. Laboratorio Nazionale Consorzio Interuniversitario Biotecnologie
  210. Fraunhofer Group Extracorporeal Immune Modulation (EXIM)
  211. David Geffen School of Medicine at UCLA
  212. Yonsei University
  213. Fujian University of Traditional Chinese Medicine
  214. University of Texas Health Science Center at San Antonio
  215. Ecole Normale Supérieure de Lyon
  216. George Mason University
  217. Milton S. Hershey Medical Center
  218. Cancer Registry of Norway Institute of Population-Based Cancer Research
  219. University of Colorado at Denver
  220. null
  221. National Heart, Lung, and Blood Institute
  222. Universite Paris 7- Denis Diderot
  223. Ben-Gurion University of the Negev
  224. null
  225. Universitair Medisch Centrum Groningen
  226. Rady Children's Hospital
  227. VU University Medical Center
  228. Institut Pasteur, Paris
  229. Korea Basic Science Institute
  230. Wuhan University
  231. Yale University
  232. Tufts University School of Medicine
  233. National Cancer Centre, Singapore
  234. Stanford University School of Medicine
  235. Huazhong Normal University
  236. Queens College, City University of New York
  237. Ege Üniversitesi
  238. University of Southern California
  239. Hanshan Normal University
  240. University of Michigan Medical School
  241. Nijmegen Centre for Molecular Life Sciences - NCMLS
  242. Centro de Investigacion Principe Felipe
  243. Johannes Gutenberg Universität Mainz
  244. Osaka University
  245. University of Ottawa Heart Institute
  246. Mayo Clinic Cancer Center
  247. National Institute of Child Health and Human Development
  248. Duke University
  249. National Institute of Neurological Disorders and Stroke
  250. University of California, San Diego, School of Medicine
  251. Ecole Polytechnique Federale de Lausanne
  252. University of Alabama at Birmingham
  253. Plymouth Marine Laboratory
  254. University of Science and Technology of China
  255. Université Nice Sophia Antipolis
  256. Life Technologies
  257. Lancaster University
  258. Juntendo University School of Medicine
  259. Mayo Clinic in Jacksonville, Florida
  260. Frankfurt Institute for Molecular Life Sciences
  261. Laval Universtity Cancer Research Center
  262. CNRS UM1
  263. Monash University
  264. Scripps Research Institute
  265. Texas A and M Health Science Center
  266. Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences Chinese Academy of Sciences
  267. University of Nottingham
  268. Riken
  269. Virginia Commonwealth University
  270. Yonsei University College of Medicine
  271. Università degli studi Magna Graecia di Catanzaro
  272. Universität Göttingen
  273. University of Wisconsin Madison
  274. University of Hawaii at Manoa
  275. Universite Paris-Sud XI
  276. University of Tartu
  277. Jichi Medical University
  278. Nagoya University
  279. Osaka Prefecture University
  280. Yokohama City University School of Medicine
  281. Rush University Medical Center
  282. Hospital Vall D'hebron
  283. Universiteit Antwerpen
  284. Universität Heidelberg
  285. University of the Ryukyus
  286. Karl-Franzens-Universitat Graz
  287. Montana State University - Bozeman
  288. Mount Sinai School of Medicine
  289. University of G. d'Annunzio Chieti and Pescara
  290. Taussig Cancer Center
  291. City of Hope National Med Center
  292. Nankai University
  293. Panepistimio Kritis
  294. UT Medical Branch at Galveston
  295. University of Adelaide
  296. Agricultural Institute of Slovenia
  297. University of Florida
  298. University of Pittsburgh Medical Center
  299. Keck Graduate Institute
  300. Northwestern University Feinberg School of Medicine
  301. University of Nebraska Medical Center
  302. UniversitatsSpital Zurich
  303. Keio University School of Medicine
  304. CNRS Centre National de la Recherche Scientifique
  305. University of Pennsylvania
  306. Università degli Studi di Torino
  307. Providence Portland Medical Center
  308. CSIC - Centro de Investigaciones Biologicas (CIB)
  309. null
  310. Asahi University
  311. University of Groningen Biomolecular Sciences and Biotechnology Institute
  312. Changzheng Hospital
  313. null
  314. Third People's Hospital of Yongzhou
  315. Texas A and M Institute for Biosciences and Technology
  316. Equipe Labellisée par l'Association Pour la Recherche sur le Cancer (ARC)
  317. Keck School of Medicine of USC
  318. Kaohsiung Medical University Chung-Ho Memorial Hospital
  319. Bond University
  320. UC Berkeley
  321. California Institute of Technology
  322. University of Ulsan, College of Medicine
  323. Imperial College London
  324. University of Florida College of Medicine
  325. Weizmann Institute of Science Israel
  326. Sun Yat-Sen University
  327. LSU Health Sciences Center - New Orleans
  328. Universidade Federal de Sao Paulo
  329. Venetian Institute of Molecular Medicine
  330. Universitat de Valencia
  331. Kyung Hee University
  332. Weis Center for Research
  333. Medizinische Hochschule Hannover (MHH)
  334. Maastricht University
  335. null
  336. Latvian Biomedical Research and Study Centre
  337. University of Louisville
  338. University of East Anglia
  339. Medical University of Warsaw
  340. Tohoku University
  341. Karolinska Institutet
  342. Wayne State University School of Medicine
  343. University of South Dakota, Sanford School of Medicine
  344. New York University
  345. University of Pittsburgh
  346. National Academy of Sciences in Ukraine
  347. British Columbia Cancer Agency
  348. Max-Planck-Institut für Psychiatrie
  349. University of Texas at San Antonio
  350. Nuffield Department of Clinical Medicine
  351. Inserm
  352. Chinese Academy of Sciences
  353. Indian Institute of Technology, Kanpur
  354. Tokai University School of Medicine
  355. University of Arizona
  356. Università degli Studi di Urbino
  357. Virginia Commonwealth University Health System
  358. New York Medical College
  359. Università degli Studi di Napoli Federico II
  360. Konkuk University
  361. Hunter College
  362. Merck & Co.
  363. Genentech Incorporated
  364. University of Birmingham
  365. Novartis Institutes for Biomedical Research
  366. Samsung Medical Center, Sungkyunkwan University
  367. University of Rochester
  368. Fondazione IRCCS Istituto Nazionale dei Tumori, Milan
  369. Columbia University Medical Center
  370. University of Waterloo
  371. University College Cork
  372. Cardiff University
  373. Chinese Academy of Medical Sciences
  374. The Fourth Military Medical University
  375. Huazhong University of Science and Technology
  376. Università di Pisa
  377. University of Belgrade
  378. Eötvös Loránd Tudományegyetem
  379. INRA Centre de Clermont-Ferrand-Theix
  380. National Tsing Hua University
  381. Korea University
  382. University of Pittsburgh School of Medicine
  383. University of Rzeszów
  384. Boston University
  385. Centre Hospitalier Universitaire Vaudois
  386. Universität Tübingen
  387. Korea Food Research Institute
  388. Western University of Health Sciences
  389. Minufiya University
  390. Gifu University School of Medicine
  391. Seoul National University
  392. National Institutes of Natural Sciences - National Institute for Basic Biology
  393. University of Texas M. D. Anderson Cancer Center
  394. The Medical Research Council Laboratory of Molecular Biology
  395. Riken Brain Science Institute
  396. University of California, San Diego
  397. Southern Illinois University School of Medicine
  398. University at Albany State University of New York
  399. University of Arkansas System
  400. Bogomoletz Institute of Physiology
  401. Research Center Caesar
  402. Kyoto University
  403. University of Cincinnati College of Medicine
  404. Université de la Méditerranée Aix-Marseille II
  405. Lombardi Comprehensive Cancer Center
  406. MRC Mammalian Genetics Unit
  407. National Institute of Allergy and Infectious Diseases
  408. Hong Kong Polytechnic University
  409. University of New Mexico School of Medicine
  410. Institute of Basic Medical Sciences Chinese Academy of Medical Sciences
  411. H. Lee Moffitt Cancer Center and Research Institute
  412. Griffith University
  413. Fudan University
  414. Tel Aviv University
  415. Emory University School of Medicine
  416. Saint Boniface General Hospital Research Centre
  417. Rockefeller University
  418. University of Chicago
  419. Chungnam National University
  420. Università della Calabria
  421. Medizinische Universitat Wien
  422. University of Strathclyde
  423. Soochow University
  424. National Defense Medical Center Taiwan
  425. Vanderbilt University School of Medicine
  426. Kyushu University Faculty of Medicine
  427. National Cheng Kung University
  428. Universiteit Stellenbosch
  429. National Fisheries Research and Development Institute(NFRDI), Busan
  430. Yale University School of Medicine
  431. Università degli Studi di Pavia
  432. Universiteit van Pretoria
  433. Université de Genève
  434. University of Minnesota Cancer Center
  435. University of Cambridge
  436. UT Southwestern Medical Center
  437. Utrecht University
  438. Agricultural Biotechnology Research Institute of Iran
  439. Uniformed Services University of the Health Sciences
  440. Cancer Research UK
  441. Osaka University Faculty of Medicine
  442. Case Western Reserve University
  443. Vrije Universiteit Brussel
  444. null
  445. University of South Florida Tampa
  446. National Yang-Ming University Taiwan
  447. Tokyo Metropolitan Institute of Medical Science
  448. University of Utah
  449. Max Delbruck Center for Molecular Medicine
  450. Public Research Center for Health (CRP-Santé)
  451. The Babraham Institute
  452. Itä-Suomen yliopisto
  453. North Shore University Hospital
  454. National Institute of Floricultural Science, National Agriculture and Food Research Organization
  455. The University of British Columbia
  456. Universitetet i Oslo
  457. Food and Drug Administration
  458. Radboud University Nijmegen Medical Centre
  459. University of Johannesburg
  460. University of Incheon
  461. UC Irvine
  462. Juntendo University
  463. Facultes Universitaires Notre-Dame de la Paix
  464. St. Jude Children Research Hospital
  465. Medical College of Georgia
  466. National Health Research Institutes Taiwan
  467. Buck Institute for Age Research
  468. Niigata University
  469. University of Idaho
  470. TIGEM Telethon Institute of Genetics and Medicine
  471. John Radcliffe Hospital
  472. Hebrew University of Jerusalem
  473. Uniwersytet Medyczny w Lodzi
  474. Chang Gung University
  475. University of Toronto
  476. Universitätsklinikum Hamburg-Eppendorf und Medizinische Fakultät
  477. Università degli Studi di Milano
  478. Università degli Studi di Siena
  479. Lunds Universitet
  480. IRCCS San Raffaele Pisana
  481. SAIC
  482. Sveriges lantbruksuniversitet
  483. National University of Singapore
  484. The Ottawa Hospital
  485. UMDNJ Robert Wood Johnson Medical School
  486. INRA Bordeaux-Aquitaine
  487. Hong Kong University of Science and Technology
  488. Universitätsklinikum Ulm
  489. University of York
  490. Universitat de Barcelona
  491. Tokyo Institute of Technology
  492. Universität Bern
  493. Chosun University
  494. Universität zu Köln
  495. University of Tokyo
  496. Huazhong Agricultural University
  497. Dartmouth Medical School
  498. Universite Paul Sabatier Toulouse III
  499. Universitat Wien
  500. University of Split