TRIM5α restricts poxviruses and is antagonized by CypA and the viral protein C6.
Humans
Antiviral Agents
/ metabolism
Antiviral Restriction Factors
/ metabolism
Capsid Proteins
/ metabolism
Cell Line
Cyclophilin A
/ metabolism
Poxviridae
/ metabolism
Tripartite Motif Proteins
/ metabolism
Ubiquitin-Protein Ligases
/ metabolism
Viral Proteins
/ metabolism
Proteasome Endopeptidase Complex
/ metabolism
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
22
12
2022
accepted:
04
07
2023
medline:
25
8
2023
pubmed:
10
8
2023
entrez:
9
8
2023
Statut:
ppublish
Résumé
Human tripartite motif protein 5α (TRIM5α) is a well-characterized restriction factor for some RNA viruses, including HIV
Identifiants
pubmed: 37558876
doi: 10.1038/s41586-023-06401-0
pii: 10.1038/s41586-023-06401-0
pmc: PMC10447239
doi:
Substances chimiques
Antiviral Agents
0
Antiviral Restriction Factors
0
Capsid Proteins
0
Cyclophilin A
EC 5.2.1.-
TRIM5 protein, human
EC 2.3.2.27
Tripartite Motif Proteins
0
Ubiquitin-Protein Ligases
EC 2.3.2.27
Viral Proteins
0
Proteasome Endopeptidase Complex
EC 3.4.25.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
873-880Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s).
Références
Chiramel, A. I. et al. TRIM5α restricts flavivirus replication by targeting the viral protease for proteasomal degradation. Cell Rep. 27, 3269–3283.e6 (2019).
pubmed: 31189110
pmcid: 8666140
doi: 10.1016/j.celrep.2019.05.040
Stremlau, M. et al. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427, 848–853 (2004).
pubmed: 14985764
doi: 10.1038/nature02343
Jimenez-Guardeno, J. M., Apolonia, L., Betancor, G. & Malim, M. H. Immunoproteasome activation enables human TRIM5α restriction of HIV-1. Nat. Microbiol. 4, 933–940 (2019).
pubmed: 30886358
pmcid: 6544544
doi: 10.1038/s41564-019-0402-0
Kim, K. et al. Cyclophilin A protects HIV-1 from restriction by human TRIM5α. Nat. Microbiol. 4, 2044–2051 (2019).
pubmed: 31636416
pmcid: 6879858
doi: 10.1038/s41564-019-0592-5
Selyutina, A. et al. Cyclophilin A prevents HIV-1 restriction in lymphocytes by blocking human TRIM5α binding to the viral core. Cell Rep. 30, 3766–3777.e6 (2020).
pubmed: 32187548
pmcid: 7363000
doi: 10.1016/j.celrep.2020.02.100
Huang, H. H. et al. TRIM5α promotes ubiquitination of Rta from Epstein–Barr virus to attenuate lytic progression. Front. Microbiol. 7, 2129 (2016).
pubmed: 28105027
Lin, L. T. et al. Regulation of Epstein–Barr virus minor capsid protein BORF1 by TRIM5α. Int. J. Mol. Sci. https://doi.org/10.3390/ijms232315340 (2022).
Smith, G. L. et al. Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J. Gen. Virol. 94, 2367–2392 (2013).
pubmed: 23999164
doi: 10.1099/vir.0.055921-0
Moss, B. & Smith, G. L. in Fields Virology: DNA Viruses Vol. 2 (eds Howley, P. M. & Knipe, D. M.) 573–613 (Wolters Kluwer, 2021).
Soday, L. et al. Quantitative temporal proteomic analysis of vaccinia virus infection reveals regulation of histone deacetylases by an interferon antagonist. Cell Rep. 27, 1920–1933.e7 (2019).
pubmed: 31067474
pmcid: 6518873
doi: 10.1016/j.celrep.2019.04.042
Lu, Y. et al. Histone deacetylase 4 promotes type I interferon signaling, restricts DNA viruses, and is degraded via vaccinia virus protein C6. Proc. Natl Acad. Sci. USA 116, 11997–12006 (2019).
pubmed: 31127039
pmcid: 6575207
doi: 10.1073/pnas.1816399116
Symons, J. A., Alcami, A. & Smith, G. L. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81, 551–560 (1995).
pubmed: 7758109
doi: 10.1016/0092-8674(95)90076-4
Kotwal, G. J. & Moss, B. Analysis of a large cluster of nonessential genes deleted from a vaccinia virus terminal transposition mutant. Virology 167, 524–537 (1988).
pubmed: 2849238
Graham, S. C. et al. Vaccinia virus proteins A52 and B14 share a Bcl-2-like fold but have evolved to inhibit NF-κB rather than apoptosis. PLoS Pathog. 4, e1000128 (2008).
pubmed: 18704168
pmcid: 2494871
doi: 10.1371/journal.ppat.1000128
Stuart, J. H., Sumner, R. P., Lu, Y., Snowden, J. S. & Smith, G. L. Vaccinia virus protein C6 inhibits type I IFN signalling in the nucleus and binds to the transactivation domain of STAT2. PLoS Pathog. 12, e1005955 (2016).
pubmed: 27907166
pmcid: 5131898
doi: 10.1371/journal.ppat.1005955
Unterholzner, L. et al. Vaccinia virus protein C6 is a virulence factor that binds TBK-1 adaptor proteins and inhibits activation of IRF3 and IRF7. PLoS Pathog. 7, e1002247 (2011).
pubmed: 21931555
pmcid: 3169548
doi: 10.1371/journal.ppat.1002247
Diaz-Griffero, F. et al. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5. Virology 349, 300–315 (2006).
pubmed: 16472833
doi: 10.1016/j.virol.2005.12.040
Fletcher, A. J. et al. Trivalent RING assembly on retroviral capsids activates TRIM5 ubiquitination and innate immune signaling. Cell Host Microbe 24, 761–775.e6 (2018).
pubmed: 30503508
pmcid: 6299210
doi: 10.1016/j.chom.2018.10.007
Yamauchi, K., Wada, K., Tanji, K., Tanaka, M. & Kamitani, T. Ubiquitination of E3 ubiquitin ligase TRIM5α and its potential role. FEBS J. 275, 1540–1555 (2008).
pubmed: 18312418
doi: 10.1111/j.1742-4658.2008.06313.x
Cooray, S. et al. Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. J. Gen. Virol. 88, 1656–1666 (2007).
pubmed: 17485524
pmcid: 2885619
doi: 10.1099/vir.0.82772-0
Chen, R. A., Ryzhakov, G., Cooray, S., Randow, F. & Smith, G. L. Inhibition of IκB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4, e22 (2008).
pubmed: 18266467
pmcid: 2233672
doi: 10.1371/journal.ppat.0040022
Carter, G. C. et al. Vaccinia virus cores are transported on microtubules. J. Gen. Virol. 84, 2443–2458 (2003).
pubmed: 12917466
doi: 10.1099/vir.0.19271-0
Battivelli, E. et al. Modulation of TRIM5α activity in human cells by alternatively spliced TRIM5 isoforms. J. Virol. 85, 7828–7835 (2011).
pubmed: 21632761
pmcid: 3147942
doi: 10.1128/JVI.00648-11
Li, X. & Sodroski, J. The TRIM5α B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J. Virol. 82, 11495–11502 (2008).
pubmed: 18799578
pmcid: 2583650
doi: 10.1128/JVI.01548-08
Yap, M. W., Nisole, S. & Stoye, J. P. A single amino acid change in the SPRY domain of human Trim5α leads to HIV-1 restriction. Curr. Biol. 15, 73–78 (2005).
pubmed: 15649369
doi: 10.1016/j.cub.2004.12.042
Castro, A. P., Carvalho, T. M., Moussatche, N. & Damaso, C. R. Redistribution of cyclophilin A to viral factories during vaccinia virus infection and its incorporation into mature particles. J. Virol. 77, 9052–9068 (2003).
pubmed: 12885921
pmcid: 167230
doi: 10.1128/JVI.77.16.9052-9068.2003
Damaso, C. R. & Keller, S. J. Cyclosporin A inhibits vaccinia virus replication in vitro. Arch. Virol. 134, 303–319 (1994).
pubmed: 8129618
doi: 10.1007/BF01310569
Damaso, C. R. & Moussatche, N. Inhibition of vaccinia virus replication by cyclosporin A analogues correlates with their affinity for cellular cyclophilins. J. Gen. Virol. 79, 339–346 (1998).
pubmed: 9472618
doi: 10.1099/0022-1317-79-2-339
Clipstone, N. A. & Crabtree, G. R. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357, 695–697 (1992).
pubmed: 1377362
doi: 10.1038/357695a0
Fruman, D. A., Klee, C. B., Bierer, B. E. & Burakoff, S. J. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A. Proc. Natl Acad. Sci. USA 89, 3686–3690 (1992).
pubmed: 1373887
pmcid: 525555
doi: 10.1073/pnas.89.9.3686
Liu, J. et al. Calcineurin is a common target of cyclophilin–cyclosporin A and FKBP–FK506 complexes. Cell 66, 807–815 (1991).
pubmed: 1715244
doi: 10.1016/0092-8674(91)90124-H
Ohkura, S., Yap, M. W., Sheldon, T. & Stoye, J. P. All three variable regions of the TRIM5α B30.2 domain can contribute to the specificity of retrovirus restriction. J. Virol. 80, 8554–8565 (2006).
pubmed: 16912305
pmcid: 1563890
doi: 10.1128/JVI.00688-06
Stremlau, M. et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5α restriction factor. Proc. Natl Acad. Sci. USA 103, 5514–5519 (2006).
pubmed: 16540544
pmcid: 1459386
doi: 10.1073/pnas.0509996103
Stremlau, M., Perron, M., Welikala, S. & Sodroski, J. Species-specific variation in the B30.2(SPRY) domain of TRIM5α determines the potency of human immunodeficiency virus restriction. J. Virol. 79, 3139–3145 (2005).
pubmed: 15709033
pmcid: 548447
doi: 10.1128/JVI.79.5.3139-3145.2005
Resch, W. & Moss, B. The conserved poxvirus L3 virion protein is required for transcription of vaccinia virus early genes. J. Virol. 79, 14719–14729 (2005).
pubmed: 16282472
pmcid: 1287552
doi: 10.1128/JVI.79.23.14719-14729.2005
Li, X., Yeung, D. F., Fiegen, A. M. & Sodroski, J. Determinants of the higher order association of the restriction factor TRIM5α and other tripartite motif (TRIM) proteins. J. Biol. Chem. 286, 27959–27970 (2011).
pubmed: 21680743
pmcid: 3151041
doi: 10.1074/jbc.M111.260406
Li, Y. L. et al. Primate TRIM5 proteins form hexagonal nets on HIV-1 capsids. eLife https://doi.org/10.7554/eLife.16269 (2016).
Wagner, J. M. et al. Mechanism of B-box 2 domain-mediated higher-order assembly of the retroviral restriction factor TRIM5α. eLife https://doi.org/10.7554/eLife.16309 (2016).
Pertel, T. et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472, 361–365 (2011).
pubmed: 21512573
pmcid: 3081621
doi: 10.1038/nature09976
Tareen, S. U. & Emerman, M. Human Trim5α has additional activities that are uncoupled from retroviral capsid recognition. Virology 409, 113–120 (2011).
pubmed: 21035162
doi: 10.1016/j.virol.2010.09.018
Zydowsky, L. D. et al. Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci. 1, 1092–1099 (1992).
pubmed: 1338979
pmcid: 2142182
doi: 10.1002/pro.5560010903
Sumner, R. P., Ren, H., Ferguson, B. J. & Smith, G. L. Increased attenuation but decreased immunogenicity by deletion of multiple vaccinia virus immunomodulators. Vaccine 34, 4827–4834 (2016).
pubmed: 27544585
pmcid: 5022402
doi: 10.1016/j.vaccine.2016.08.002
Sumner, R. P., Ren, H. & Smith, G. L. Deletion of immunomodulator C6 from vaccinia virus strain Western Reserve enhances virus immunogenicity and vaccine efficacy. J. Gen. Virol. 94, 1121–1126 (2013).
pubmed: 23288427
pmcid: 3709586
doi: 10.1099/vir.0.049700-0
Lawitz, E. et al. Safety, pharmacokinetics, and antiviral activity of the cyclophilin inhibitor NIM811 alone or in combination with pegylated interferon in HCV-infected patients receiving 14 days of therapy. Antiviral Res. 89, 238–245 (2011).
pubmed: 21255610
doi: 10.1016/j.antiviral.2011.01.003
Zeuzem, S. et al. Randomised clinical trial: alisporivir combined with peginterferon and ribavirin in treatment-naive patients with chronic HCV genotype 1 infection (ESSENTIAL II). Aliment. Pharmacol. Ther. 42, 829–844 (2015).
pubmed: 26238707
doi: 10.1111/apt.13342
Albarnaz, J. D. et al. Molecular mimicry of NF-κB by vaccinia virus protein enables selective inhibition of antiviral responses. Nat. Microbiol. 7, 154–168 (2022).
pubmed: 34949827
doi: 10.1038/s41564-021-01004-9
Zhang, R. Y., Pallett, M. A., French, J., Ren, H. & Smith, G. L. Vaccinia virus BTB-Kelch proteins C2 and F3 inhibit NF-κB activation. J. Gen. Virol. https://doi.org/10.1099/jgv.0.001786 (2022).
Blasco, R. & Moss, B. Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-Dalton outer envelope protein. J. Virol. 65, 5910–5920 (1991).
pubmed: 1920620
pmcid: 250254
doi: 10.1128/jvi.65.11.5910-5920.1991
Smith, G. L., Vanderplasschen, A. & Law, M. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83, 2915–2931 (2002).
pubmed: 12466468
doi: 10.1099/0022-1317-83-12-2915
Lederman, E. R. et al. Progressive vaccinia: case description and laboratory-guided therapy with vaccinia immune globulin, ST-246, and CMX001. J. Infect. Dis. 206, 1372–1385 (2012).
pubmed: 22904336
pmcid: 3529603
doi: 10.1093/infdis/jis510
Smith, T. G. et al. Resistance to anti-orthopoxviral drug tecovirimat (TPOXX®) during the 2022 mpox outbreak in the US. Preprint at medRxiv https://doi.org/10.1101/2023.05.16.23289856 (2023).
Fassbender, P. et al. Generalized cowpox virus infection in a patient with HIV, Germany, 2012. Emerg. Infect. Dis. 22, 553–555 (2016).
pubmed: 26891134
pmcid: 4766888
doi: 10.3201/eid2203.151158
McSharry, B. P., Jones, C. J., Skinner, J. W., Kipling, D. & Wilkinson, G. W. G. Human telomerase reverse transcriptase-immortalized MRC-5 and HCA2 human fibroblasts are fully permissive for human cytomegalovirus. J. Gen. Virol. 82, 855–863 (2001).
pubmed: 11257191
doi: 10.1099/0022-1317-82-4-855
Moss, B., Winters, E. & Cooper, J. A. Deletion of a 9,000-base-pair segment of the vaccinia virus genome that encodes nonessential polypeptides. J. Virol. 40, 387–395 (1981).
pubmed: 6275095
pmcid: 256639
doi: 10.1128/jvi.40.2.387-395.1981
Maluquer de Motes, C., Schiffner, T., Sumner, R. P. & Smith, G. L. Vaccinia virus virulence factor N1 can be ubiquitylated on multiple lysine residues. J. Gen. Virol. 95, 2038–2049 (2014).
pubmed: 24914067
pmcid: 4135091
doi: 10.1099/vir.0.065664-0
Alcami, A. & Smith, G. L. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J. Virol. 69, 4633–4639 (1995).
pubmed: 7609027
pmcid: 189264
doi: 10.1128/jvi.69.8.4633-4639.1995
Gloeckner, C. J., Boldt, K., Schumacher, A., Roepman, R. & Ueffing, M. A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 7, 4228–4234 (2007).
pubmed: 17979178
doi: 10.1002/pmic.200700038
Chen, R. A., Jacobs, N. & Smith, G. L. Vaccinia virus strain Western Reserve protein B14 is an intracellular virulence factor. J. Gen. Virol. 87, 1451–1458 (2006).
pubmed: 16690909
doi: 10.1099/vir.0.81736-0
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
pubmed: 27348712
doi: 10.1038/nmeth.3901
Ma, J. et al. iProX: an integrated proteome resource. Nucleic Acids Res. 47, D1211–D1217 (2019).
pubmed: 30252093
doi: 10.1093/nar/gky869
Lu, Y., Michel, H. A., Wang, P. H. & Smith, G. L. Manipulation of innate immune signaling pathways by SARS-CoV-2 non-structural proteins. Front. Microbiol. 13, 1027015 (2022).
pubmed: 36478862
pmcid: 9720297
doi: 10.3389/fmicb.2022.1027015