TRIMmunity: The roles of the TRIM E3-ubiquitin ligase family in innate antiviral immunity

Journal of Molecular Biology

Volumn 426, Issue 6, 2014, Pages 1265-1284

  Rajsbaum, Ricardo ^a   García Sastre, Adolfo ^a   Versteeg, Gijs A ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

antiviral response; E3 ubiquitin ligase; innate immunity; restriction factors; tripartite motif

Indexed keywords

DEUBIQUITINASE; TRIPARTITE MOTIF PROTEIN; TRIPARTITE MOTIF PROTEIN 19; TRIPARTITE MOTIF PROTEIN 21; TRIPARTITE MOTIF PROTEIN 22; TRIPARTITE MOTIF PROTEIN 24; TRIPARTITE MOTIF PROTEIN 25; TRIPARTITE MOTIF PROTEIN 33; TRIPARTITE MOTIF PROTEIN 5; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIVIRAL ACTIVITY; CELLULAR DISTRIBUTION; CHROMOSOME 11; CYTOPLASM; ENZYME ACTIVITY; HUMAN; HUMAN CHROMOSOME; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; VIRUS CAPSID; VIRUS REPLICATION;

ANTIVIRAL RESPONSE; E3-UBIQUITIN LIGASE; INNATE IMMUNITY; RESTRICTION FACTORS; TRIPARTITE MOTIF;

ANIMALS; ANTIVIRAL AGENTS; HUMANS; IMMUNITY, INNATE; UBIQUITIN-PROTEIN LIGASES; VIRUS DISEASES; VIRUS REPLICATION; VIRUSES;

EID: 84894515095     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.12.005     Document Type: Review

References (167)

1. R. Medzhitov Recognition of microorganisms and activation of the immune response Nature 449 2007 819 826
2. D. Blanco-Melo, S. Venkatesh, and P.D. Bieniasz Intrinsic cellular defenses against human immunodeficiency viruses Immunity 37 2012 399 411
3. P.D. Bieniasz Intrinsic immunity: a front-line defense against viral attack Nat Immunol 5 2004 1109 1115
4. L.C. Platanias Mechanisms of type-I- and type-II-interferon-mediated signalling Nat Rev Immunol 5 2005 375 386
5. M.R. Thompson, J.J. Kaminski, E.A. Kurt-Jones, and K.A. Fitzgerald Pattern recognition receptors and the innate immune response to viral infection Viruses 3 2011 920 940
6. T. Kawai, K. Takahashi, S. Sato, C. Coban, H. Kumar, and H. Kato et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction Nat Immunol 6 2005 981 988
7. M. Yamamoto, S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, and H. Sanjo et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway Science 301 2003 640 643
8. A.M. Pham, and B.R. Tenoever The IKK kinases: operators of antiviral signaling Viruses 2 2010 55 72
9. E. Zandi, D.M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation Cell 91 1997 243 252
10. H. Hemmi, O. Takeuchi, S. Sato, M. Yamamoto, T. Kaisho, and H. Sanjo et al. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection J Exp Med 199 2004 1641 1650
11. S. Sharma, B.R. tenOever, N. Grandvaux, G.P. Zhou, R. Lin, and J. Hiscott Triggering the interferon antiviral response through an IKK-related pathway Science 300 2003 1148 1151
12. R.E. Randall, and S. Goodbourn Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures J Gen Virol 89 2008 1 47
13. J.W. Schoggins, and C.M. Rice Interferon-stimulated genes and their antiviral effector functions Curr Opin Virol 1 2011 519 525
14. J.W. Schoggins, S.J. Wilson, M. Panis, M.Y. Murphy, C.T. Jones, and P. Bieniasz et al. A diverse range of gene products are effectors of the type I interferon antiviral response Nature 472 2011 481 485
15. B.A. Reddy, and L.D. Etkin A unique bipartite cysteine-histidine motif defines a subfamily of potential zinc-finger proteins Nucleic Acids Res 19 1991 6330
16. B.A. Reddy, L.D. Etkin, and P.S. Freemont A novel zinc finger coiled-coil domain in a family of nuclear proteins Trends Biochem Sci 17 1992 344 345
17. A.J. Saurin, K.L. Borden, M.N. Boddy, and P.S. Freemont Does this have a familiar RING? Trends Biochem Sci 21 1996 208 214
18. P.S. Freemont The RING finger. A novel protein sequence motif related to the zinc finger Ann N Y Acad Sci 684 1993 174 192
19. K. Ozato, D.M. Shin, T.H. Chang, and H.C. Morse TRIM family proteins and their emerging roles in innate immunity Nat Rev Immunol 8 2008 849 860
20. D.A. Rhodes, B. de Bono, and J. Trowsdale Relationship between SPRY and B30.2 protein domains. Evolution of a component of immune defence? Immunology 116 2005 411 417
21. K. Han, D.I. Lou, and S.L. Sawyer Identification of a genomic reservoir for new TRIM genes in primate genomes PLoS Genet 7 2011 e1002388
22. P. Boudinot, L.M. van der Aa, L. Jouneau, L. Du Pasquier, P. Pontarotti, and V. Briolat et al. Origin and evolution of TRIM proteins: new insights from the complete TRIM repertoire of zebrafish and pufferfish PLoS One 6 2011 e22022
23. M. Sardiello, S. Cairo, B. Fontanella, A. Ballabio, and G. Meroni Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties BMC Evol Biol 8 2008 225
24. L.M. van der Aa, J.P. Levraud, M. Yahmi, E. Lauret, V. Briolat, and P. Herbomel et al. A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish BMC Biol 7 2009 7
25. S. Nisole, J.P. Stoye, and A. Saib TRIM family proteins: retroviral restriction and antiviral defence Nat Rev Microbiol 3 2005 799 808
26. J.H. Rombout, H.B. Huttenhuis, S. Picchietti, and G. Scapigliati Phylogeny and ontogeny of fish leucocytes Fish Shellfish Immunol 19 2005 441 455
27. T. Kawai, and S. Akira Regulation of innate immune signalling pathways by the tripartite motif (TRIM) family proteins EMBO Mol Med 3 2011 513 527
28. P.D. Uchil, A. Hinz, S. Siegel, A. Coenen-Stass, T. Pertel, and J. Luban et al. TRIM protein-mediated regulation of inflammatory and innate immune signaling and its association with antiretroviral activity J Virol 87 2013 257 272
29. G.A. Versteeg, R. Rajsbaum, M.T. Sanchez-Aparicio, A.M. Maestre, J. Valdiviezo, and M. Shi et al. The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors Immunity 38 2013 384 398
30. G. Meroni, and G. Diez-Roux TRIM/RBCC, a novel class of "single protein RING finger" E3 ubiquitin ligases BioEssays 27 2005 1147 1157
31. C. Wu, I. Macleod, and A.I. Su BioGPS and MyGene.info: organizing online, gene-centric information Nucleic Acids Res 41 2013 D561 D565
32. C. Wu, C. Orozco, J. Boyer, M. Leglise, J. Goodale, and S. Batalov et al. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources Genome Biol 10 2009 R130
33. J.F. Trempe Reading the ubiquitin postal code Curr Opin Struct Biol 21 2011 792 801
34. D. Komander, and M. Rape The ubiquitin code Annu Rev Biochem 81 2012 203 229
35. J. Chen, and Z.J. Chen Regulation of NF-kappaB by ubiquitination Curr Opin Immunol 25 2013 4 12
36. W. Zeng, L. Sun, X. Jiang, X. Chen, F. Hou, and A. Adhikari et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity Cell 141 2010 315 330
37. L.M. Napolitano, E.G. Jaffray, R.T. Hay, and G. Meroni Functional interactions between ubiquitin E2 enzymes and TRIM proteins Biochem J 434 2011 309 319
38. T. Pertel, S. Hausmann, D. Morger, S. Zuger, J. Guerra, and J. Lascano et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice Nature 472 2011 361 365
39. W. Zou, and D.E. Zhang The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase J Biol Chem 281 2006 3989 3994
40. Q. Liang, H. Deng, X. Li, X. Wu, Q. Tang, and T.H. Chang et al. Tripartite motif-containing protein 28 is a small ubiquitin-related modifier E3 ligase and negative regulator of IFN regulatory factor 7 J Immunol 187 2011 4754 4763
41. P.S. Freemont RING for destruction? Curr Biol 10 2000 R84 R87
42. A. Kentsis, and K.L. Borden Construction of macromolecular assemblages in eukaryotic processes and their role in human disease: linking RINGs together Curr Protein Pept Sci 1 2000 49 73
43. K.L. Borden RING fingers and B-boxes: zinc-binding protein-protein interaction domains Biochem Cell Biol 76 1998 351 358
44. W.A. McEwan, J.C. Tam, R.E. Watkinson, S.R. Bidgood, D.L. Mallery, and L.C. James Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21 Nat Immunol 14 2013 327 336
45. T. Tsuchida, J. Zou, T. Saitoh, H. Kumar, T. Abe, and Y. Matsuura et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA Immunity 33 2012 765 776
46. M.U. Gack, Y.C. Shin, C.H. Joo, T. Urano, C. Liang, and L. Sun et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity Nature 446 2007 916 920
47. K. Arimoto, K. Funami, Y. Saeki, K. Tanaka, K. Okawa, and O. Takeuchi et al. Polyubiquitin conjugation to NEMO by triparite motif protein 23 (TRIM23) is critical in antiviral defense Proc Natl Acad Sci U S A 107 2010 15856 15861
48. K.L. Borden, S.R. Martin, N.J. O'Reilly, J.M. Lally, B.A. Reddy, and L.D. Etkin et al. Characterisation of a novel cysteine/histidine-rich metal binding domain from Xenopus nuclear factor XNF7 FEBS Lett 335 1993 255 260
49. M.A. Massiah, J.A. Matts, K.M. Short, B.N. Simmons, S. Singireddy, and Z. Yi et al. Solution structure of the MID1 B-box2 CHC(D/C)C(2)H(2) zinc-binding domain: insights into an evolutionarily conserved RING fold J Mol Biol 369 2007 1 10
50. M.A. Massiah, B.N. Simmons, K.M. Short, and T.C. Cox Solution structure of the RBCC/TRIM B-box1 domain of human MID1: B-box with a RING J Mol Biol 358 2006 532 545
51. J.L. Bell, A. Malyukova, J.K. Holien, J. Koach, M.W. Parker, and M. Kavallaris et al. TRIM16 acts as an E3 ubiquitin ligase and can heterodimerize with other TRIM family members PLoS One 7 2012 e37470
52. T. Cao, K.L. Borden, P.S. Freemont, and L.D. Etkin Involvement of the rfp tripartite motif in protein-protein interactions and subcellular distribution J Cell Sci 110 1997 1563 1571
53. S. Cainarca, S. Messali, A. Ballabio, and G. Meroni Functional characterization of the Opitz syndrome gene product (midin): evidence for homodimerization and association with microtubules throughout the cell cycle Hum Mol Genet 8 1999 1387 1396
54. A. Reymond, G. Meroni, A. Fantozzi, G. Merla, S. Cairo, and L. Luzi et al. The tripartite motif family identifies cell compartments EMBO J 20 2001 2140 2151
55. L.M. Napolitano, and G. Meroni TRIM family: pleiotropy and diversification through homomultimer and heteromultimer formation IUBMB Life 64 2012 64 71
56. M.W. Yap, S. Nisole, and J.P. Stoye A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction Curr Biol 15 2005 73 78
57. S.L. Sawyer, L.I. Wu, M. Emerman, and H.S. Malik Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain Proc Natl Acad Sci U S A 102 2005 2832 2837
58. M. Stremlau, C.M. Owens, M.J. Perron, M. Kiessling, P. Autissier, and J. Sodroski The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys Nature 427 2004 848 853
59. S.P. Goff Host factors exploited by retroviruses Nat Rev Microbiol 5 2007 253 263
60. E. Sokolskaja, and J. Luban Cyclophilin, TRIM5, and innate immunity to HIV-1 Curr Opin Microbiol 9 2006 404 408
61. G.J. Towers, and S.P. Goff Post-entry restriction of retroviral infections AIDS Rev 5 2003 156 164
62. G.J. Towers The control of viral infection by tripartite motif proteins and cyclophilin A Retrovirology 4 2007 40
63. F. Zhang, T. Hatziioannou, D. Perez-Caballero, D. Derse, and P.D. Bieniasz Antiretroviral potential of human tripartite motif-5 and related proteins Virology 353 2006 396 409
64. W.E. Johnson Rapid adversarial co-evolution of viruses and cellular restriction factors Curr Top Microbiol Immunol 371 2013 123 151
65. M. Stremlau, M. Perron, S. Welikala, and J. Sodroski Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction J Virol 79 2005 3139 3145
66. G. Towers, M. Bock, S. Martin, Y. Takeuchi, J.P. Stoye, and O. Danos A conserved mechanism of retrovirus restriction in mammals Proc Natl Acad Sci U S A 97 2000 12295 12299
67. T. Hatziioannou, D. Perez-Caballero, A. Yang, S. Cowan, and P.D. Bieniasz Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha Proc Natl Acad Sci U S A 101 2004 10774 10779
68. Z. Keckesova, L.M. Ylinen, and G.J. Towers The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities Proc Natl Acad Sci U S A 101 2004 10780 10785
69. M.J. Perron, M. Stremlau, B. Song, W. Ulm, R.C. Mulligan, and J. Sodroski TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells Proc Natl Acad Sci U S A 101 2004 11827 11832
70. M.W. Yap, S. Nisole, C. Lynch, and J.P. Stoye Trim5alpha protein restricts both HIV-1 and murine leukemia virus Proc Natl Acad Sci U S A 101 2004 10786 10791
71. D.M. Sayah, E. Sokolskaja, L. Berthoux, and J. Luban Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1 Nature 430 2004 569 573
72. C. Munk, S.M. Brandt, G. Lucero, and N.R. Landau A dominant block to HIV-1 replication at reverse transcription in simian cells Proc Natl Acad Sci U S A 99 2002 13843 13848
73. F. Diaz-Griffero Caging the beast: TRIM5alpha binding to the HIV-1 core Viruses 3 2011 423 428
74. B.K. Ganser-Pornillos, V. Chandrasekaran, O. Pornillos, J.G. Sodroski, W.I. Sundquist, and M. Yeager Hexagonal assembly of a restricting TRIM5alpha protein Proc Natl Acad Sci U S A 108 2011 534 539
75. M.G. Grutter, and J. Luban TRIM5 structure, HIV-1 capsid recognition, and innate immune signaling Curr Opin Virol 2 2013 142 150
76. F. Diaz-Griffero, X. Li, H. Javanbakht, B. Song, S. Welikala, and M. Stremlau et al. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5 Virology 349 2006 300 315
77. L. Xu, L. Yang, P.K. Moitra, K. Hashimoto, P. Rallabhandi, and S. Kaul et al. BTBD1 and BTBD2 colocalize to cytoplasmic bodies with the RBCC/tripartite motif protein, TRIM5delta Exp Cell Res 288 2003 84 93
78. C.J. Rold, and C. Aiken Proteasomal degradation of TRIM5alpha during retrovirus restriction PLoS Pathog 4 2008 e1000074
79. Z. Lukic, S. Hausmann, S. Sebastian, J. Rucci, J. Sastri, and S.L. Robia et al. TRIM5alpha associates with proteasomal subunits in cells while in complex with HIV-1 virions Retrovirology 8 2011 93
80. M. Stremlau, M. Perron, M. Lee, Y. Li, B. Song, and H. Javanbakht et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor Proc Natl Acad Sci U S A 103 2006 5514 5519
81. A. Roa, F. Hayashi, Y. Yang, M. Lienlaf, J. Zhou, and J. Shi et al. RING domain mutations uncouple TRIM5alpha restriction of HIV-1 from inhibition of reverse transcription and acceleration of uncoating J Virol 86 2012 1717 1727
82. S.B. Kutluay, D. Perez-Caballero, and P.D. Bieniasz Fates of retroviral core components during unrestricted and TRIM5-restricted infection PLoS Pathog 9 2013 e1003214
83. Z. Si, N. Vandegraaff, C. O'Huigin, B. Song, W. Yuan, and C. Xu et al. Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection Proc Natl Acad Sci U S A 103 2006 7454 7459
84. S.U. Tareen, S.L. Sawyer, H.S. Malik, and M. Emerman An expanded clade of rodent Trim5 genes Virology 385 2009 473 483
85. R. Rajsbaum, J.P. Stoye, and A. O'Garra Type I interferon-dependent and -independent expression of tripartite motif proteins in immune cells Eur J Immunol 38 2008 619 630
86. S.L. Sawyer, M. Emerman, and H.S. Malik Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals PLoS Pathog 3 2007 e197
87. R.M. Newman, L. Hall, A. Kirmaier, L.A. Pozzi, E. Pery, and M. Farzan et al. Evolution of a TRIM5-CypA splice isoform in old world monkeys PLoS Pathog 4 2008 e1000003
88. R. Malfavon-Borja, L.I. Wu, M. Emerman, and H.S. Malik Birth, decay, and reconstruction of an ancient TRIMCyp gene fusion in primate genomes Proc Natl Acad Sci U S A 110 2013 E583 E592
89. M. Wahren, P. Tengner, I. Gunnarsson, I. Lundberg, E. Hedfors, and N.R. Ringertz et al. Ro/SS-A and La/SS-B antibody level variation in patients with Sjogren's syndrome and systemic lupus erythematosus J Autoimmun 11 1998 29 38
90. D.A. Rhodes, and J. Trowsdale TRIM21 is a trimeric protein that binds IgG Fc via the B30.2 domain Mol Immunol 44 2007 2406 2414
91. L.C. James, A.H. Keeble, Z. Khan, D.A. Rhodes, and J. Trowsdale Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function Proc Natl Acad Sci U S A 104 2007 6200 6205
92. A.H. Keeble, Z. Khan, A. Forster, and L.C. James TRIM21 is an IgG receptor that is structurally, thermodynamically, and kinetically conserved Proc Natl Acad Sci U S A 105 2008 6045 6050
93. D.L. Mallery, W.A. McEwan, S.R. Bidgood, G.J. Towers, C.M. Johnson, and L.C. James Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21) Proc Natl Acad Sci U S A 107 2010 19985 19990
94. M. Vaysburd, R.E. Watkinson, H. Cooper, M. Reed, K. O'Connell, and J. Smith et al. Intracellular antibody receptor TRIM21 prevents fatal viral infection Proc Natl Acad Sci U S A 110 2013 12397 12401
95. R. Yoshimi, T.H. Chang, H. Wang, T. Atsumi, H.C. Morse, and K. Ozato Gene disruption study reveals a nonredundant role for TRIM21/Ro52 in NF-kappaB-dependent cytokine expression in fibroblasts J Immunol 182 2009 7527 7538
96. A. Espinosa, V. Dardalhon, S. Brauner, A. Ambrosi, R. Higgs, and F.J. Quintana et al. Loss of the lupus autoantigen Ro52/Trim21 induces tissue inflammation and systemic autoimmunity by disregulating the IL-23-Th17 pathway J Exp Med 206 2009 1661 1671
97. F.W. McNab, R. Rajsbaum, J.P. Stoye, and A. O'Garra Tripartite-motif proteins and innate immune regulation Curr Opin Immunol 23 2011 46 56
98. K. Ozato, R. Yoshimi, T.H. Chang, H. Wang, T. Atsumi, and H.C. Morse Comment on "Gene disruption study reveals a nonredundant role for TRIM21/Ro52 in NF-kappa B-dependent cytokine expression in fibroblasts" J Immunol 183 2009 7619 [author reply 720-721]
99. C.J. Hattlmann, J.N. Kelly, and S.D. Barr TRIM22: a diverse and dynamic antiviral protein Mol Biol Int 2012 2012 153415
100. C. Tissot, and N. Mechti Molecular cloning of a new interferon-induced factor that represses human immunodeficiency virus type 1 long terminal repeat expression J Biol Chem 270 1995 14891 14898
101. A. Kajaste-Rudnitski, S.S. Marelli, C. Pultrone, T. Pertel, P.D. Uchil, and N. Mechti et al. TRIM22 inhibits HIV-1 transcription independently of its E3 ubiquitin ligase activity, Tat, and NF-kappaB-responsive long terminal repeat elements J Virol 85 2011 5183 5196
102. S.D. Barr, J.R. Smiley, and F.D. Bushman The interferon response inhibits HIV particle production by induction of TRIM22 PLoS Pathog 4 2008 e1000007
103. P. Eldin, L. Papon, A. Oteiza, E. Brocchi, T.G. Lawson, and N. Mechti TRIM22 E3 ubiquitin ligase activity is required to mediate antiviral activity against encephalomyocarditis virus J Gen Virol 90 2009 536 545
104. A. Di Pietro, A. Kajaste-Rudnitski, A. Oteiza, L. Nicora, G.J. Towers, and N. Mechti et al. TRIM22 inhibits influenza A virus infection by targeting the viral nucleoprotein for degradation J Virol 87 2013 4523 4533
105. N. Stuurman, A. de Graaf, A. Floore, A. Josso, B. Humbel, and L. de Jong et al. A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies J Cell Sci 101 1992 773 784
106. N. Stuurman, A. Floore, A. Colen, L. de Jong, and R. van Driel Stabilization of the nuclear matrix by disulfide bridges: identification of matrix polypeptides that form disulfides Exp Cell Res 200 1992 285 294
107. R. Bernardi, and P.P. Pandolfi Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies Nat Rev Mol Cell Biol 8 2007 1006 1016
108. R.D. Everett DNA viruses and viral proteins that interact with PML nuclear bodies Oncogene 20 2001 7266 7273
109. R.D. Everett, and M.K. Chelbi-Alix PML and PML nuclear bodies: implications in antiviral defence Biochimie 89 2007 819 830
110. M.C. Geoffroy, and M.K. Chelbi-Alix Role of promyelocytic leukemia protein in host antiviral defense J Interferon Cytokine Res 31 2011 145 158
111. M.K. Chelbi-Alix, L. Pelicano, F. Quignon, M.H. Koken, L. Venturini, and M. Stadler et al. Induction of the PML protein by interferons in normal and APL cells Leukemia 9 1995 2027 2033
112. C. Lavau, A. Marchio, M. Fagioli, J. Jansen, B. Falini, and P. Lebon et al. The acute promyelocytic leukaemia-associated PML gene is induced by interferon Oncogene 11 1995 871 876
113. M. Stadler, M.K. Chelbi-Alix, M.H. Koken, L. Venturini, C. Lee, and A. Saib et al. Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element Oncogene 11 1995 2565 2573
114. W.V. Bonilla, D.D. Pinschewer, P. Klenerman, V. Rousson, M. Gaboli, and P.P. Pandolfi et al. Effects of promyelocytic leukemia protein on virus-host balance J Virol 76 2002 3810 3818
115. J. Sewatanon, H. Liu, and P.D. Ling PML protein modulates establishment and maintenance of latent gamma-herpesvirus infection in peritoneal cells J Virol 87 2013 12151 12157
116. M. Ortiz, G. Bleiber, R. Martinez, H. Kaessmann, and A. Telenti Patterns of evolution of host proteins involved in retroviral pathogenesis Retrovirology 3 2006 11
117. J. Wang, B. Liu, N. Wang, Y.M. Lee, C. Liu, and K. Li TRIM56 is a virus- and interferon-inducible E3 ubiquitin ligase that restricts pestivirus infection J Virol 85 2011 3733 3745
118. Y. Shen, N.L. Li, J. Wang, B. Liu, S. Lester, and K. Li TRIM56 is an essential component of the TLR3 antiviral signaling pathway J Biol Chem 287 2012 36404 36413
119. R.T. Taylor, K.J. Lubick, S.J. Robertson, J.P. Broughton, M.E. Bloom, and W.A. Bresnahan et al. TRIM79alpha, an interferon-stimulated gene product, restricts tick-borne encephalitis virus replication by degrading the viral RNA polymerase Cell Host Microbe 10 2011 185 196
120. P.D. Uchil, B.D. Quinlan, W.T. Chan, J.M. Luna, and W. Mothes TRIM E3 ligases interfere with early and late stages of the retroviral life cycle PLoS Pathog 4 2008 e16
121. S. Zhang, J.T. Guo, J.Z. Wu, and G. Yang Identification and characterization of multiple TRIM proteins that inhibit hepatitis B virus transcription PLoS One 8 2013 e70001
122. L. Zeng, and M.M. Zhou Bromodomain: an acetyl-lysine binding domain FEBS Lett 513 2002 124 128
123. M.H. Dyson, S. Rose, and L.C. Mahadevan Acetyllysine-binding and function of bromodomain-containing proteins in chromatin Front Biosci 6 2001 D853 D865
124. A.L. Nielsen, J.A. Ortiz, J. You, M. Oulad-Abdelghani, R. Khechumian, and A. Gansmuller et al. Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family EMBO J 18 1999 6385 6395
125. L. Venturini, J. You, M. Stadler, R. Galien, V. Lallemand, and M.H. Koken et al. TIF1gamma, a novel member of the transcriptional intermediary factor 1 family Oncogene 18 1999 1209 1217
126. K. Khetchoumian, M. Teletin, M. Mark, T. Lerouge, M. Cervino, and M. Oulad-Abdelghani et al. TIF1delta, a novel HP1-interacting member of the transcriptional intermediary factor 1 (TIF1) family expressed by elongating spermatids J Biol Chem 279 2004 48329 48341
127. D.C. Schultz, K. Ayyanathan, D. Negorev, G.G. Maul, and F.J. Rauscher SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins Genes Dev 16 2002 919 932
128. J. Ellis, A. Hotta, and M. Rastegar Retrovirus silencing by an epigenetic TRIM Cell 131 2007 13 14
129. D. Wolf, and S.P. Goff TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells Cell 131 2007 46 57
130. T. Matsui, D. Leung, H. Miyashita, I.A. Maksakova, H. Miyachi, and H. Kimura et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET Nature 464 2010 927 931
131. H.M. Rowe, J. Jakobsson, D. Mesnard, J. Rougemont, S. Reynard, and T. Aktas et al. KAP1 controls endogenous retroviruses in embryonic stem cells Nature 463 2010 237 240
132. A. Allouch, C. Di Primio, E. Alpi, M. Lusic, D. Arosio, and M. Giacca et al. The TRIM family protein KAP1 inhibits HIV-1 integration Cell Host Microbe 9 2011 484 495
133. B. Herquel, K. Ouararhni, I. Martianov, S. Le Gras, T. Ye, and C. Keime et al. Trim24-repressed VL30 retrotransposons regulate gene expression by producing noncoding RNA Nat Struct Mol Biol 20 2013 339 346
134. S. Kamitani, N. Ohbayashi, O. Ikeda, S. Togi, R. Muromoto, and Y. Sekine et al. KAP1 regulates type I interferon/STAT1-mediated IRF-1 gene expression Biochem Biophys Res Commun 370 2008 366 370
135. J. Tisserand, K. Khetchoumian, C. Thibault, D. Dembele, P. Chambon, and R. Losson Tripartite motif 24 (Trim24/Tif1alpha) tumor suppressor protein is a novel negative regulator of interferon (IFN)/signal transducers and activators of transcription (STAT) signaling pathway acting through retinoic acid receptor alpha (Raralpha) inhibition J Biol Chem 286 2011 33369 33379
136. K. Jensen, C. Shiels, and P.S. Freemont PML protein isoforms and the RBCC/TRIM motif Oncogene 20 2001 7223 7233
137. S. Nisole, M.A. Maroui, X.H. Mascle, M. Aubry, and M.K. Chelbi-Alix Differential Roles of PML Isoforms Front Oncol 3 2013 125
138. M.A. Maroui, M. Pampin, and M.K. Chelbi-Alix Promyelocytic leukemia isoform IV confers resistance to encephalomyocarditis virus via the sequestration of 3D polymerase in nuclear bodies J Virol 85 2011 13164 13173
139. M. Reichelt, L. Wang, M. Sommer, J. Perrino, A.M. Nour, and N. Sen et al. Entrapment of viral capsids in nuclear PML cages is an intrinsic antiviral host defense against varicella-zoster virus PLoS Pathog 7 2011 e1001266
140. D. Blondel, S. Kheddache, X. Lahaye, L. Dianoux, and M.K. Chelbi-Alix Resistance to rabies virus infection conferred by the PMLIV isoform J Virol 84 2010 10719 10726
141. H.K. Lin, S. Bergmann, and P.P. Pandolfi Cytoplasmic PML function in TGF-beta signalling Nature 431 2004 205 211
142. B.A. McNally, J. Trgovcich, G.G. Maul, Y. Liu, and P. Zheng A role for cytoplasmic PML in cellular resistance to viral infection PLoS One 3 2008 e2277
143. L.D. Passerini, Z. Keckesova, and G.J. Towers Retroviral restriction factors Fv1 and TRIM5alpha act independently and can compete for incoming virus before reverse transcription J Virol 80 2006 2100 2105
144. E. Battivelli, J. Migraine, D. Lecossier, S. Matsuoka, D. Perez-Bercoff, and S. Saragosti et al. Modulation of TRIM5alpha activity in human cells by alternatively spliced TRIM5 isoforms J Virol 85 2011 7828 7835
145. R.H. Jacobson, A.G. Ladurner, D.S. King, and R. Tjian Structure and function of a human TAFII250 double bromodomain module Science 288 2000 1422 1425
146. K.M. Short, and T.C. Cox Subclassification of the RBCC/TRIM superfamily reveals a novel motif necessary for microtubule binding J Biol Chem 281 2006 8970 8980
147. R. Rajsbaum, and A. Garcia-Sastre Viral evasion mechanisms of early antiviral responses involving regulation of ubiquitin pathways Trends Microbiol 21 2013 421 429
148. Y. Lee, B. Song, C. Park, and K.S. Kwon TRIM11 negatively regulates IFNbeta production and antiviral activity by targeting TBK1 PLoS One 8 2013 e63255
149. R. Higgs, J. Ni Gabhann, N. Ben Larbi, E.P. Breen, K.A. Fitzgerald, and C.A. Jefferies The E3 ubiquitin ligase Ro52 negatively regulates IFN-beta production post-pathogen recognition by polyubiquitin-mediated degradation of IRF3 J Immunol 181 2008 1780 1786
150. J.A. Young, D. Sermwittayawong, H.J. Kim, S. Nandu, N. An, and H. Erdjument-Bromage et al. Fas-associated death domain (FADD) and the E3 ubiquitin-protein ligase TRIM21 interact to negatively regulate virus-induced interferon production J Biol Chem 286 2011 6521 6531
151. Z. Zhang, M. Bao, N. Lu, L. Weng, B. Yuan, and Y.J. Liu The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA Nat Immunol 14 2013 172 178
152. K. Wada, M. Niida, M. Tanaka, and T. Kamitani Ro52-mediated monoubiquitination of IKKβ down-regulates NF-κB signalling J Biochem 146 2009 821 832
153. H.J. Kong, D.E. Anderson, C.H. Lee, M.K. Jang, T. Tamura, and P. Tailor et al. Cutting edge: autoantigen Ro52 is an interferon inducible E3 ligase that ubiquitinates IRF-8 and enhances cytokine expression in macrophages J Immunol 179 2007 26 30
154. M. Shi, W. Deng, E. Bi, K. Mao, Y. Ji, and G. Lin et al. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation Nat Immunol 9 2008 369 377
155. T. Kondo, M. Watanabe, and S. Hatakeyama TRIM59 interacts with ECSIT and negatively regulates NF-kappaB and IRF-3/7-mediated signal pathways Biochem Biophys Res Commun 422 2012 501 507
156. Q. Xue, Z. Zhou, X. Lei, X. Liu, B. He, and J. Wang et al. TRIM38 negatively regulates TLR3-mediated IFN-beta signaling by targeting TRIF for degradation PLoS One 7 2012 e46825
157. W. Zhao, L. Wang, M. Zhang, P. Wang, C. Yuan, and J. Qi et al. Tripartite motif-containing protein 38 negatively regulates TLR3/4- and RIG-I-mediated IFN-beta production and antiviral response by targeting NAP1 J Immunol 188 2012 5311 5318
158. W. Zhao, L. Wang, M. Zhang, C. Yuan, and C. Gao E3 ubiquitin ligase tripartite motif 38 negatively regulates TLR-mediated immune responses by proteasomal degradation of TNF receptor-associated factor 6 in macrophages J Immunol 188 2012 2567 2574
159. J. Zha, K.J. Han, L.G. Xu, W. He, Q. Zhou, and D. Chen et al. The Ret finger protein inhibits signaling mediated by the noncanonical and canonical IkappaB kinase family members J Immunol 176 2006 1072 1080
160. M.U. Gack, R.A. Albrecht, T. Urano, K.S. Inn, I.C. Huang, and E. Carnero et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I Cell Host Microbe 5 2009 439 449
161. R. Rajsbaum, R.A. Albrecht, M.K. Wang, N.P. Maharaj, G.A. Versteeg, and E. Nistal-Villan et al. Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein PLoS Pathog 8 2012 e1003059
162. Q. Li, J. Yan, A.P. Mao, C. Li, Y. Ran, and H.B. Shu et al. Tripartite motif 8 (TRIM8) modulates TNFalpha- and IL-1beta-triggered NF-kappaB activation by targeting TAK1 for K63-linked polyubiquitination Proc Natl Acad Sci U S A 108 2011 19341 19346
163. J. Zhang, M.M. Hu, Y.Y. Wang, and H.B. Shu TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination J Biol Chem 287 2012 28646 28655
164. B. Yang, J. Wang, Y. Wang, H. Zhou, X. Wu, and Z. Tian et al. Novel function of Trim44 promotes an antiviral response by stabilizing VISA J Immunol 190 2013 3613 3619
165. S.J. Wilson, B.L. Webb, C. Maplanka, R.M. Newman, E.J. Verschoor, and J.L. Heeney et al. Rhesus macaque TRIM5 alleles have divergent antiretroviral specificities J Virol 82 2008 7243 7247
166. A. Kirmaier, F. Wu, R.M. Newman, L.R. Hall, J.S. Morgan, and S. O'Connor et al. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species PLoS Biol 8 2010
167. F. Wu, A. Kirmaier, R. Goeken, I. Ourmanov, L. Hall, and J.S. Morgan et al. TRIM5 alpha drives SIVsmm evolution in rhesus macaques PLoS Pathog 9 2013 e1003577