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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, DJ204
Abdalla, FC
Abeliovich, H489
Abraham, RT
AcevedoArozena, A425
Adeli, K
Agholme, L33
Agnello, M198
Agostinis, P
AguirreGhiso, JA329
Ahn, HJ97
Osborne, TF1
Kim, HR
Kim, JS326
Kim, JH154
Kim, JC386
Kim, JK204
Swanson, MS204
Kim, PK493
Kim, SW386
Kim, YS
Bánhegyi, G
Ostrander, GK283
Kim, Y388
Kimchi, A327
Kimmelman, AC207
King, JS
Kinsella, TJ
Kirkin, V
Bursch, W370
Kirshenbaum, LA151 426
Kitamoto, K
Kitazato, K170
Bost, F248
Klein, L30
Bartholomew, CR204
Klimecki, WT344
Klucken, J83
Knecht, E256
Ko, BCB
Koch, JC280
Swanton, C
Koga, H52
Koh, JY386
Otsu, K53
Koh, YH
Koike, M321
Komatsu, M
Bassham, DC78
Kominami, E321
Kong, HJ434
Kong, WJ372
Korolchuk, VI125
Sweeney, ST477
Kotake, Y
Ou, JHJ379
Koukourakis, MI66
Kouri Flores, JB171
Kovács, AL399
Kraft, C
Krainc, D59
Bast Jr, RC409
Krämer, H445
KretzRemy, C203 143
Krichevsky, AM
Sy, LK186
Ouimet, M231
Kroemer, G363
Krüger, R400
Krut, O500
Ktistakis, NT
Kuan, CY206
Kucharczyk, R295
Kumar, A219
Batoko, H115
Kumar, R
Kumar, S292
Overholtzer, M178
Szabadkai, G13
Kundu, M469
Kung, HJ
Kurz, T33
Kwon, HJ251
La Spada, AR414 226
Lafont, F157
Lamark, T
Landry, J276
Bay, BH137
Ozpolat, B409
Lane, JD
Tabas, I
Lapaquette, P363
Laporte, JF36
László, L399
Lavandero, S445
Lavoie, JN276
Layfield, R275
Lazo, PA
Le, W
Paganetti, P245
Le Cam, L
Beau, I284
Taegtmeyer, H112
Ledbetter, DJ121
Lee, AJX
Lee, BW272
Lee, GM
Lee, J244
Lee, JH17
Lee, M496
Pagnini, U361
Lee, MS362
Lee, SH141
Leeuwenburgh, C300
Tafani, M
Béchet, DM
Legembre, P181
Legouis, R284
Lehmann, M221
Lei, HY433
Lei, QY377
Tavernarakis, N
Thorburn, A185
Leib, DA
Leiro, J199
Lemasters, JJ7
Lemoine, A284
TakácsVellai, K399
Lesniak, MS423
Begley, TJ421
Lev, D409
Levenson, VV269
Levine, B63
Pallet, N
Levy, E17
Li, F282
Li, JL355
Li, L459
Li, S274
Takano, Y410
Li, W242
Li, XJ
Behl, C
Li, YB94
Palmer, GE324
Li, YP
Liang, C379
Liang, Q356
Liao, YF360
Liberski, PP491
Lieberman, A204
Takegawa, K156
Lim, HJ364
Lim, KL137
Lim, K431
Palumbo, C188
Behrends, C101
Lin, CF433
Lin, FC189
Lin, J299
Lin, JD204 247
Lin, K
Lin, WW25
Butchar, JP179
Lin, WC40
Lin, YL
Bourquin, JP182
Linden, R
Lingor, P280
Bekri, S
LippincottSchwartz, J241
Lisanti, MP184
Liton, PB237
Liu, B
Liu, CF448
Takemura, G407
Liu, K227
Pan, T40
Liu, L323
Liu, QA
Liu, W129
Liu, YC86
Bellaire, B78
Liu, Y
Lockshin, RA228
Lok, CN186
Lonial, S459
Takeshita, F293
Panaretakis, T84
Loos, B435
LopezBerestein, G409
LópezOtín, C494
Lossi, L310
Lotze, MT
Lõw, P399
Bendall, LJ200
Lu, B332
Lu, B216
Lu, B
Pandey, UB324
Talbot, NJ
Lu, Z409
Luciano, F248
Lukacs, NW204
Lund, AH103
LynchDay, MA204
Ma, Y94
Macian, F52
Benetti, L357
MacKeigan, JP136
Papackova, Z183
Macleod, KF423
Tan, KSW137
Madeo, F290
Maiuri, L220
Maiuri, MC363
Malagoli, D92
Malicdan, MCV99
Malorni, W74
Man, N
Mandelkow, EM405
Papassideri, I67
Berliocchi, L279
Manon, S142
Tanaka, K
Manov, I
Mao, K204
Mao, X64
Mao, Z459
Marambaud, P173
Marazziti, D
Marcel, YL231
Mograbi, B248
Paris, I118
Marchbank, K53
Marchetti, P374
Bernardi, H
Tanaka, K349
Marciniak, SJ446
Marcondes, M
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Mariño, G363
Markaki, M288
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Martin, SJ54
MartinandMari, C193
Martinet, W277
Tang, D
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Masini, M374
Matarrese, P
Matsuo, S291
Bydlowski, SP
Matteoni, R
Mayer, A
Mazure, NM248
McConkey, DJ409
McConnell, MJ
Tang, D376 225
McDermott, C381
Besteiro, S193
McDonald, C
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Park, J251
McKenna, SL
McLaughlin, B
McLean, PJ59
McMaster, CR
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Meijer, AJ105
Tanida, I88
Meisler, MH204
Meléndez, A228 329
BhatiaKissova, I
Park, OK456
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Melino, G188
Mena, MA123
Menendez, JA168
MennaBarreto, RFS62
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Menzies, FM446
Tannous, BA59
Mercer, CA146
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Parys, JB
Merry, DE
Bi, X411
Meschini, S
Meyer, CG134
Meyer, TF
Miao, CY
Miao, JY117
Michels, PAM
Buzgariu, W442
Michiels, C468
Parzych, KR204
Mijaljica, D314
Milojkovic, A
Minucci, S497
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Miracco, C499
Miranti, CK136
Mitroulis, I66
Miyazawa, K
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Pattingre, S
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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
2013 Impact Factor: 11.423
2013 SCImago Journal Rankings: 3.351
 
DOIhttp://dx.doi.org/10.4161/auto.19496
 
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dc.contributor.authorKang, KB
 
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dc.contributor.authorKang, YA
 
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dc.contributor.authorSuzuki, T
 
dc.contributor.authorKim, DR
 
dc.contributor.authorKim, DH
 
dc.contributor.authorBampton, ETW
 
dc.contributor.authorKim, DH
 
dc.contributor.authorKim, EK
 
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_OA_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
2013 Impact Factor: 11.423
2013 SCImago Journal Rankings: 3.351
 
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
 
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<contributor.author>Jaakkola, PM</contributor.author>
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<contributor.author>Jackson, WT</contributor.author>
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<contributor.author>Jendrach, M</contributor.author>
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<contributor.author>Jiang, H</contributor.author>
<contributor.author>Jiang, JX</contributor.author>
<contributor.author>Jiang, M</contributor.author>
<contributor.author>Jiang, Q</contributor.author>
<contributor.author>Baiocchi, R</contributor.author>
<contributor.author>Jiang, X</contributor.author>
<contributor.author>Jim&#233;nez, A</contributor.author>
<contributor.author>Sun, J</contributor.author>
<contributor.author>Oleinick, NL</contributor.author>
<contributor.author>Jin, M</contributor.author>
<contributor.author>Jin, S</contributor.author>
<contributor.author>Joe, CO</contributor.author>
<contributor.author>Johansen, T</contributor.author>
<contributor.author>Johnson, DE</contributor.author>
<contributor.author>Johnson, GVW</contributor.author>
<contributor.author>Jones, NL</contributor.author>
<contributor.author>Joseph, B</contributor.author>
<contributor.author>Baldini, G</contributor.author>
<contributor.author>Joseph, SK</contributor.author>
<contributor.author>Oliver, FJ</contributor.author>
<contributor.author>Sun, SY</contributor.author>
<contributor.author>Joubert, AM</contributor.author>
<contributor.author>Juh&#225;sz, G</contributor.author>
<contributor.author>JuilleratJeanneret, L</contributor.author>
<contributor.author>Jung, CH</contributor.author>
<contributor.author>Jung, YK</contributor.author>
<contributor.author>Kaarniranta, K</contributor.author>
<contributor.author>Kaasik, A</contributor.author>
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<contributor.author>Kadowaki, M</contributor.author>
<contributor.author>Olsen, LJ</contributor.author>
<contributor.author>Balduini, W</contributor.author>
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<contributor.author>Kamada, Y</contributor.author>
<contributor.author>Kaminskyy, VO</contributor.author>
<contributor.author>Kampinga, HH</contributor.author>
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<contributor.author>Ballabio, A</contributor.author>
<contributor.author>Kanki, T</contributor.author>
<contributor.author>Kanneganti, TD</contributor.author>
<contributor.author>Kanno, H</contributor.author>
<contributor.author>Kanthasamy, AG</contributor.author>
<contributor.author>Kanthasamy, A</contributor.author>
<contributor.author>Karantza, V</contributor.author>
<contributor.author>Opota, O</contributor.author>
<contributor.author>Kaushal, GP</contributor.author>
<contributor.author>Kaushik, S</contributor.author>
<contributor.author>Kawazoe, Y</contributor.author>
<contributor.author>Suzuki, K</contributor.author>
<contributor.author>Ke, PY</contributor.author>
<contributor.author>Bamber, BA</contributor.author>
<contributor.author>Kehrl, JH</contributor.author>
<contributor.author>Kelekar, A</contributor.author>
<contributor.author>Kerkhoff, C</contributor.author>
<contributor.author>Kessel, DH</contributor.author>
<contributor.author>Thompson, CB</contributor.author>
<contributor.author>Khalil, H</contributor.author>
<contributor.author>Kiel, JAKW</contributor.author>
<contributor.author>Kiger, AA</contributor.author>
<contributor.author>Kihara, A</contributor.author>
<contributor.author>Suzuki, T</contributor.author>
<contributor.author>Kim, DR</contributor.author>
<contributor.author>Kim, DH</contributor.author>
<contributor.author>Bampton, ETW</contributor.author>
<contributor.author>Kim, DH</contributor.author>
<contributor.author>Kim, EK</contributor.author>
<date.accessioned>2012-10-08T03:23:42Z</date.accessioned>
<date.available>2012-10-08T03:23:42Z</date.available>
<date.issued>2012</date.issued>
<identifier.citation>Autophagy, 2012, v. 8 n. 4, p. 445-544</identifier.citation>
<identifier.issn>1554-8627</identifier.issn>
<identifier.uri>http://hdl.handle.net/10722/168634</identifier.uri>
<description.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. &#169; 2012 Landes Bioscience.</description.abstract>
<language>eng</language>
<relation.ispartof>Autophagy</relation.ispartof>
<subject>Autolysosome</subject>
<subject>Autophagosome</subject>
<subject>Flux</subject>
<subject>LC3</subject>
<subject>Lysosome</subject>
<subject>Phagophore</subject>
<subject>Stress</subject>
<subject>Vacuole</subject>
<title>Guidelines for the use and interpretation of assays for monitoring autophagy</title>
<type>Article</type>
<description.nature>link_to_OA_fulltext</description.nature>
<identifier.doi>10.4161/auto.19496</identifier.doi>
<identifier.scopus>eid_2-s2.0-84862295360</identifier.scopus>
<identifier.hkuros>203531</identifier.hkuros>
<relation.references>http://www.scopus.com/mlt/select.url?eid=2-s2.0-84862295360&amp;selection=ref&amp;src=s&amp;origin=recordpage</relation.references>
<identifier.volume>8</identifier.volume>
<identifier.issue>4</identifier.issue>
<identifier.spage>445</identifier.spage>
<identifier.epage>544</identifier.epage>
<bitstream.url>http://hub.hku.hk/bitstream/10722/168634/1/re01.htm</bitstream.url>
</item>
Author Affiliations
  1. Sanford-Burnham Medical Research Institute at Lake Nona
  2. Toronto General Research Institute University of Toronto
  3. York University
  4. Academy of Athens
  5. University of Durham
  6. Kyoto Sangyo University
  7. Medical University of South Carolina
  8. Massachusetts Institute of Technology
  9. Chungbuk National University
  10. Universidad de Valparaiso
  11. University of Illinois at Chicago
  12. University of Medicine and Dentistry of New Jersey
  13. UCL
  14. Tokyo Women's Medical University
  15. Johns Hopkins University
  16. Universite de Franche-Comte
  17. New York University School of Medicine
  18. The University of Hong Kong Li Ka Shing Faculty of Medicine
  19. null
  20. Università Vita-Salute San Raffaele
  21. Duke-NUS Graduate Medical School Singapore
  22. National Research Institute of Fisheries Science, FRA
  23. Vanderbilt Eye Institute
  24. Penn State Hershey Cancer Institute
  25. National Taiwan University College of Medicine
  26. Universidad Autónoma de Barcelona
  27. University of California, San Francisco
  28. Kræftens Bekæmpelse
  29. University of Debrecen Medical and Health Science Center
  30. Ludwig-Maximilians-Universität München
  31. Vanderbilt Ingram Cancer Center
  32. Institut Claudius Regaud
  33. Linköpings universitet
  34. Università degli Studi di Padova
  35. Institut Universitaire de Pathologie, Lausanne
  36. Université de Strasbourg
  37. Norwegian Institute of Public Health
  38. Forschungszentrum Jülich (FZJ)
  39. Aix Marseille Université
  40. Baylor College of Medicine
  41. Hospital Clinic Barcelona
  42. Institute of Microbiology Chinese Academy of Sciences
  43. The Wistar Institute
  44. Rutgers, The State University of New Jersey
  45. University of Dundee
  46. Safar Center for Resuscitation Research
  47. Keio University
  48. Cornell University
  49. University of Shizuoka
  50. Centre Hospitalier de L'Universite de Montreal
  51. AstraZeneca
  52. Albert Einstein College of Medicine of Yeshiva University
  53. King's College London
  54. Trinity College Dublin
  55. National Cancer Institute
  56. CSIC-JA-UPO-USE - Centro Andaluz de Biologia Molecular y Medicina Regenerativa (CABIMER)
  57. DTP
  58. Universidad Autónoma de Madrid
  59. Massachusetts General Hospital
  60. Istituto Neurologico Mediterraneo Neuromed, Pozzilli
  61. Universität Bonn
  62. Fundacao Oswaldo Cruz
  63. UT Southwestern Medical School
  64. Nanjing Agricultural University
  65. Henan University of Technology
  66. Dimokrition Panepistimion Thrakis
  67. University of Athens
  68. Okayama University Medical School
  69. INRA Institut National de La Recherche Agronomique
  70. Komarov Botanical Institute, Russian Academy of Sciences
  71. Institute for Research in Ophthalmology (IRO)
  72. EMD Serono Research Institute, Inc.
  73. Sanford-Burnham Medical Research Institute
  74. San Raffaele Institute Sulmona
  75. Xijing Hospital
  76. AgroParisTech
  77. Università degli Studi di Brescia, Facoltà di Medicina e Chirurgia
  78. Iowa State University
  79. Instituto Nacional de Cancer
  80. Duke University School of Medicine
  81. Jozef Stefan Institute
  82. University of Wyoming College of Health Sciences
  83. null
  84. Karolinska University Hospital
  85. University of Liverpool
  86. Shu-Te University
  87. Whitehead Institute for Biomedical Research
  88. National Institute of Infectious Diseases
  89. null
  90. University of Aberdeen
  91. SungKyunKwan University, School of Medicine
  92. Università degli Studi di Modena e Reggio Emilia
  93. Universidade Federal de Minas Gerais
  94. Harbin Medical University
  95. Universitat fur Bodenkultur Wien
  96. University of Coimbra, Faculty of Medicine
  97. Korea Institute of Science and Technology
  98. Peking University Health Science Center
  99. National Human Genome Research Institute
  100. Penn State College of Medicine
  101. null
  102. Indiana University School of Medicine Indianapolis
  103. Københavns Universitet
  104. Wayne State University
  105. Academic Medical Centre, University of Amsterdam
  106. South China Normal University
  107. Universidad Nacional de Cuyo
  108. Institute of Zoology Chinese Academy of Sciences
  109. The University of Georgia
  110. University of Tsukuba
  111. Drexel University College of Medicine
  112. University of Texas Medical School at Houston
  113. Helsingin Yliopisto
  114. University of Toledo
  115. Universite Catholique de Louvain
  116. Uniwersytet Slaski w Katowicach
  117. Shandong University
  118. Santo Tomas University
  119. National Institute of Arthritis and Musculoskeletal and Skin Diseases
  120. Dulbecco Telethon Institute
  121. University of Kentucky
  122. Università degli Studi dell'Insubria
  123. Hospital Ramon y Cajal
  124. Howard Hughes Medical Institute
  125. Newcastle University, United Kingdom
  126. Chonbuk National University
  127. University of Minnesota Twin Cities
  128. Jefferson Medical College
  129. National Cancer Institute at Frederick
  130. null
  131. Universite Pierre et Marie Curie
  132. LEO Pharma AS
  133. Cincinnati Children's Hospital Medical Center
  134. Bernhard Nocht Institut fur Tropenmedizin Hamburg
  135. Mayo Clinic
  136. Van Andel Research Institute
  137. Yong Loo Lin School of Medicine
  138. Stanford University
  139. UC Davis
  140. University of Maryland School of Medicine
  141. The Catholic University of Korea
  142. Université de Bordeaux
  143. Université de Lyon
  144. Università degli Studi del Piemonte Orientale Amedeo Avogadro
  145. Università degli Studi di Messina
  146. University of Cincinnati
  147. Children's Hospital of Iowa
  148. National Cerebral and Cardiovascular Center
  149. VAAAHS
  150. Universidad Complutense de Madrid
  151. University of Manitoba
  152. National Institutes Allergy and Infectious Diseases, Hamilton
  153. Academia Sinica Taiwan
  154. Seoul National University, College of Medical Sciences
  155. University of Virginia
  156. Kyushu University
  157. Institut Pasteur Lille
  158. Centro Europeo di Ricerca sul Cervello, Roma
  159. Turku Centre for Biotechnology
  160. Eidgenossische Technische Hochschule Zurich
  161. Gyeongsang National University (GSNU), College of Medicine
  162. National Taiwan University
  163. Columbia University in the City of New York
  164. Francis Marion University
  165. Royal Veterinary College University of London
  166. Indian Institute of Science Education and Research Thiruvananthapuram
  167. Mackay Memorial Hospital Taiwan
  168. Institute Catala Oncologia
  169. University of Iowa
  170. Nagasaki University
  171. Centro de Investigacion y de Estudios Avanzados
  172. Harvard University
  173. Feinstein Institute for Medical Research
  174. National Institute of Neuroscience, Kodaira
  175. San Diego State University
  176. IRCCS Casa Sollievo della Sofferenza
  177. Georgetown University Medical Center
  178. Memorial Sloan-Kettering Cancer Center
  179. Ohio State University
  180. University at Buffalo State University of New York
  181. Universite de Rennes 1
  182. Kinderspital Zürich
  183. Institutu Klinické a Experimentální Medicíny
  184. University of Manchester
  185. University of Colorado School of Medicine
  186. The University of Hong Kong
  187. Shanghai Jiaotong University
  188. Università degli Studi di Roma Tor Vergata
  189. Zhejiang University
  190. Vilnius University
  191. Universiteit Gent
  192. University of Sheffield
  193. Universite Montpellier 2 Sciences et Techniques
  194. Universidad de Costa Rica
  195. Università degli Studi di Udine
  196. Universidad de Extremadura
  197. University of Florida College of Dentistry
  198. Università degli Studi di Palermo
  199. Universidad de Santiago de Compostela
  200. University of Sydney
  201. University of Colorado at Boulder
  202. University of Nebraska - Lincoln
  203. null
  204. University Michigan Ann Arbor
  205. University of Southampton
  206. Cincinnati Children's Hospital Research Foundation
  207. Harvard Medical School
  208. Laboratorio Nazionale Consorzio Interuniversitario Biotecnologie
  209. School of Life Sciences-LifeNet
  210. OIST Graduate University
  211. Yale University
  212. Tufts University School of Medicine
  213. National Cancer Centre, Singapore
  214. Cancer Registry of Norway Institute of Population-Based Cancer Research
  215. National Heart, Lung, and Blood Institute
  216. Stanford University School of Medicine
  217. Universite Paris 7- Denis Diderot
  218. Ben-Gurion University of the Negev
  219. null
  220. null
  221. University of Arkansas - Fayetteville
  222. Universitair Medisch Centrum Groningen
  223. Universitat de Valencia, Facultad de Medicina y Odontologia
  224. CSIC-JA-UPO - Centro Andaluz de Biología del Desarrollo (CABD)
  225. Institute of Genetics and Developmental Biology Chinese Academy of Sciences
  226. Rady Children's Hospital
  227. Huazhong Normal University
  228. Queens College, City University of New York
  229. Ege Üniversitesi
  230. VU University Medical Center
  231. University of Ottawa Heart Institute
  232. Institut Pasteur, Paris
  233. Zhejiang University School of Medicine
  234. Korea Basic Science Institute
  235. University of Southern California
  236. Wuhan University
  237. Duke University
  238. CASE School of Medicine
  239. Mayo Clinic Cancer Center
  240. National Institute of Neurological Disorders and Stroke
  241. National Institute of Child Health and Human Development
  242. Hanshan Normal University
  243. Plymouth Marine Laboratory
  244. University of California, San Diego, School of Medicine
  245. Ecole Polytechnique Federale de Lausanne
  246. University of Science and Technology of China
  247. University of Michigan Medical School
  248. Université Nice Sophia Antipolis
  249. University of Alabama at Birmingham
  250. David Geffen School of Medicine at UCLA
  251. Yonsei University
  252. Nijmegen Centre for Molecular Life Sciences - NCMLS
  253. Fujian University of Traditional Chinese Medicine
  254. Vysoká škola chemicko-technologická v Praze
  255. Pontificia Universidad Católica de Chile
  256. Centro de Investigacion Principe Felipe
  257. University of Texas Health Science Center at San Antonio
  258. Kagoshima University
  259. Ecole Normale Supérieure de Lyon
  260. George Mason University
  261. Johannes Gutenberg Universität Mainz
  262. University of Glasgow
  263. Osaka University
  264. Milton S. Hershey Medical Center
  265. Manitoba Institute of Cell Biology
  266. Fraunhofer Group Extracorporeal Immune Modulation (EXIM)
  267. Life Technologies
  268. University Health Network University of Toronto
  269. Rush University Medical Center
  270. Hospital Vall D'hebron
  271. Virginia Commonwealth University
  272. Yonsei University College of Medicine
  273. University of North Carolina School of Medicine
  274. Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences Chinese Academy of Sciences
  275. University of Nottingham
  276. Laval Universtity Cancer Research Center
  277. Universiteit Antwerpen
  278. Riken
  279. Università degli studi Magna Graecia di Catanzaro
  280. Universität Göttingen
  281. Universität Heidelberg
  282. University of Wisconsin Madison
  283. University of Hawaii at Manoa
  284. Universite Paris-Sud XI
  285. University of the Ryukyus
  286. University of Tartu
  287. Jichi Medical University
  288. Panepistimio Kritis
  289. UT Medical Branch at Galveston
  290. Karl-Franzens-Universitat Graz
  291. Osaka Prefecture University
  292. University of Adelaide
  293. Yokohama City University School of Medicine
  294. University of Kansas Lawrence
  295. Institute of Biochemistry and Biophysics, Warsaw
  296. Montana State University - Bozeman
  297. University of Nebraska Medical Center
  298. Agricultural Institute of Slovenia
  299. College of Chemistry and Molecular Engineering, Peking University
  300. University of Florida
  301. UniversitatsSpital Zurich
  302. Keio University School of Medicine
  303. CNRS Centre National de la Recherche Scientifique
  304. Mount Sinai School of Medicine
  305. University of Pittsburgh Medical Center
  306. Keck Graduate Institute
  307. Northwestern University Feinberg School of Medicine
  308. CNRS UM1
  309. University of Pennsylvania
  310. Università degli Studi di Torino
  311. Institute of Cell Biology National Academy of Sciences of Ukraine
  312. University of G. d'Annunzio Chieti and Pescara
  313. Taussig Cancer Center
  314. Monash University
  315. City of Hope National Med Center
  316. Frankfurt Institute for Molecular Life Sciences
  317. Nankai University
  318. Lancaster University
  319. University of Southern California, School of Pharmacy
  320. Scripps Research Institute
  321. Juntendo University School of Medicine
  322. Mayo Clinic in Jacksonville, Florida
  323. Texas A and M Health Science Center
  324. LSU Health Sciences Center - New Orleans
  325. Universidade Federal de Sao Paulo
  326. University of Florida College of Medicine
  327. Weizmann Institute of Science Israel
  328. Venetian Institute of Molecular Medicine
  329. New York University
  330. Institute of Medical Science The University of Tokyo
  331. Sun Yat-Sen University
  332. University of Pittsburgh
  333. SAIC-Frederick
  334. British Columbia Cancer Agency
  335. Kyung Hee University
  336. Tokai University School of Medicine
  337. Weis Center for Research
  338. Medizinische Hochschule Hannover (MHH)
  339. Maastricht University
  340. Latvian Biomedical Research and Study Centre
  341. null
  342. Equipe Labellisée par l'Association Pour la Recherche sur le Cancer (ARC)
  343. Max-Planck-Institut für Psychiatrie
  344. University of Arizona
  345. University of Louisville
  346. Università degli Studi di Urbino
  347. University of East Anglia
  348. Medical University of Warsaw
  349. Tohoku University
  350. Virginia Commonwealth University Health System
  351. Karolinska Institutet
  352. University of Texas at San Antonio
  353. Wayne State University School of Medicine
  354. New York Medical College
  355. Third People's Hospital of Yongzhou
  356. University of South Dakota, Sanford School of Medicine
  357. Merck &amp; Co.
  358. Nuffield Department of Clinical Medicine
  359. University of Rochester Medical Center
  360. Institute of Cellular and Organismic Biology, Academia Sinica
  361. Università degli Studi di Napoli Federico II
  362. Samsung Medical Center, Sungkyunkwan University
  363. Inserm
  364. Konkuk University
  365. Fondazione IRCCS Istituto Nazionale dei Tumori, Milan
  366. Hunter College
  367. Columbia University Medical Center
  368. University of Waterloo
  369. Cardiff University
  370. Medical University of Vienna Institute of Cancer Research
  371. Chinese Academy of Medical Sciences
  372. Huazhong University of Science and Technology
  373. Genentech Incorporated
  374. Università di Pisa
  375. University of Birmingham
  376. Chinese Academy of Sciences
  377. Fudan University Shanghai Medical College
  378. Novartis Institutes for Biomedical Research
  379. Keck School of Medicine of USC
  380. UC Berkeley
  381. Bond University
  382. Kaohsiung Medical University Chung-Ho Memorial Hospital
  383. California Institute of Technology
  384. Providence Portland Medical Center
  385. CSIC - Centro de Investigaciones Biologicas (CIB)
  386. University of Ulsan, College of Medicine
  387. null
  388. University of Maryland, Baltimore
  389. Texas A and M Institute for Biosciences and Technology
  390. Asahi University
  391. University of Groningen Biomolecular Sciences and Biotechnology Institute
  392. Changzheng Hospital
  393. null
  394. UniversitätsSpital Bern
  395. Indian Institute of Technology, Kanpur
  396. UCL Institute of Neurology
  397. Washington University in St. Louis School of Medicine
  398. Imperial College London
  399. Eötvös Loránd University
  400. Universität Tübingen
  401. Bogomoletz Institute of Physiology
  402. Weatherall Institute of Molecular Medicine
  403. Minufiya University
  404. Korea Food Research Institute
  405. Research Center Caesar
  406. Seoul National University
  407. Gifu University School of Medicine
  408. National Institutes of Natural Sciences - National Institute for Basic Biology
  409. University of Texas M. D. Anderson Cancer Center
  410. Kyoto University
  411. Western University of Health Sciences
  412. The Medical Research Council Laboratory of Molecular Biology
  413. Riken Brain Science Institute
  414. University of California, San Diego
  415. Rockefeller University
  416. University of Cincinnati College of Medicine
  417. Université de la Méditerranée Aix-Marseille II
  418. Southern Illinois University School of Medicine
  419. Lombardi Comprehensive Cancer Center
  420. National Institute of Allergy and Infectious Diseases
  421. University at Albany State University of New York
  422. Hong Kong Polytechnic University
  423. University of Chicago
  424. Nagoya University School of Medicine
  425. MRC Mammalian Genetics Unit
  426. Saint Boniface General Hospital Research Centre
  427. University Hospital Zurich Institute of Experimental Immunology
  428. University of New Mexico School of Medicine
  429. University of Strathclyde
  430. UCSD Medical Center, Moores Cancer Center
  431. Chungnam National University
  432. Università della Calabria
  433. National Cheng Kung University
  434. National Fisheries Research and Development Institute(NFRDI), Busan
  435. Universiteit Stellenbosch
  436. H. Lee Moffitt Cancer Center and Research Institute
  437. Institute of Basic Medical Sciences Chinese Academy of Medical Sciences
  438. Yale University School of Medicine
  439. Università degli Studi di Pavia
  440. Universiteit van Pretoria
  441. Griffith University
  442. Université de Genève
  443. University of Minnesota Cancer Center
  444. University of Cambridge
  445. UT Southwestern Medical Center
  446. Cambridge Institute for Medical Research
  447. Utrecht University
  448. Soochow University
  449. National Defense Medical Center Taiwan
  450. INRA Centre de Clermont-Ferrand-Theix
  451. National Tsing Hua University
  452. Vanderbilt University School of Medicine
  453. Kyushu University Faculty of Medicine
  454. Fudan University
  455. University of Rzeszów
  456. Korea University
  457. Tel Aviv University
  458. Boston University
  459. Emory University School of Medicine
  460. Centre Hospitalier Universitaire Vaudois
  461. University of Pittsburgh School of Medicine
  462. Agricultural Biotechnology Research Institute of Iran
  463. Public Research Center for Health (CRP-Santé)
  464. Itä-Suomen yliopisto
  465. Juntendo University
  466. North Shore University Hospital
  467. National Institute of Floricultural Science, National Agriculture and Food Research Organization
  468. Facultes Universitaires Notre-Dame de la Paix
  469. St. Jude Children Research Hospital
  470. Medical College of Georgia
  471. The University of British Columbia
  472. National Health Research Institutes Taiwan
  473. Buck Institute for Age Research
  474. Hong Kong University of Science and Technology
  475. Universitetet i Oslo
  476. Universitätsklinikum Ulm
  477. University of York
  478. Niigata University
  479. Xiangya Hospital of Central-south University
  480. University of Idaho
  481. Food and Drug Administration
  482. TIGEM Telethon Institute of Genetics and Medicine
  483. Radboud University Nijmegen Medical Centre
  484. Universitat de Barcelona
  485. University of Johannesburg
  486. John Radcliffe Hospital
  487. Tokyo Institute of Technology
  488. Universität Bern
  489. Hebrew University of Jerusalem
  490. Chang Gung University
  491. Uniwersytet Medyczny w Lodzi
  492. Universitätsklinikum Hamburg-Eppendorf und Medizinische Fakultät
  493. University of Toronto
  494. Instituto Universitario de Oncologia del Principado de Asturias
  495. Chosun University
  496. University of Incheon
  497. Università degli Studi di Milano
  498. UC Irvine
  499. Università degli Studi di Siena
  500. Universität zu Köln