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TRIM5 is an innate immune sensor for the retrovirus capsid lattice
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TRIM5 is a RING domain-E3 ubiquitin ligase that restricts infection by human immunodeficiency virus (HIV)-1 and other retroviruses immediately following virus invasion of the target cell cytoplasm. Antiviral potency correlates with TRIM5 avidity for the retrovirion capsid lattice and several reports indicate that TRIM5 has a role in signal transduction, but the precise mechanism of restriction is unknown. Here we demonstrate that TRIM5 promotes innate immune signalling and that this activity is amplified by retroviral infection and interaction with the capsid lattice. Acting with the heterodimeric, ubiquitin-conjugating enzyme UBC13-UEV1A (also known as UBE2N-UBE2V1), TRIM5 catalyses the synthesis of unattached K63-linked ubiquitin chains that activate the TAK1 (also known as MAP3K7) kinase complex and stimulate AP-1 and NFκB signalling. Interaction with the HIV-1 capsid lattice greatly enhances the UBC13-UEV1A-dependent E3 activity of TRIM5 and challenge with retroviruses induces the transcription of AP-1 and NF-κB-dependent factors with a magnitude that tracks with TRIM5 avidity for the invading capsid. Finally, TAK1 and UBC13-UEV1A contribute to capsid-specific restriction by TRIM5. Thus, the retroviral restriction factor TRIM5 has two additional activities that are linked to restriction: it constitutively promotes innate immune signalling and it acts as a pattern recognition receptor specific for the retrovirus capsid lattice.
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“In DCs, TRIM5α binding to the capsid lattice also triggers signal transduction cascades resulting in the activation of the transcription factors AP-1 and NF-κB 59.”
From Are human endogenous retroviruses pathogenic? An approach to testing the hypothesis (2013) · cites this paper as [59]
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“Although this is insufficient to induce IFN production alone, these cascades synergize with other pathways, thus enhancing the IFN response 59.”
From Are human endogenous retroviruses pathogenic? An approach to testing the hypothesis (2013) · cites this paper as [59]
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Claiborne, D. T., Prince, J. L., Scully, E. P., Macharia, G. N., Micci, L., Lawson, B., Kopycinski, J. T., Deymier, M. J., Vanderford, T. H., Nganou‐Makamdop, K., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421607112 · Cited by 102
Antiviral TRIMs: friend or foe in autoimmune and autoinflammatory disease?
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Jiménez, V. C., Booiman, T., de Taeye, S. W., van Dort, K. A., Rits, M. A. N., Hamann, J., & Kootstra, N. A. (2012) · Scientific Reports · doi:10.1038/srep00763 · Cited by 102
Manocha, G. D., Mishra, R., Sharma, N., Kumawat, K. L., Basu, A., & Singh, S. K. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-24 · Cited by 99
TRIM5α requires Ube2W to anchor Lys63‐linked ubiquitin chains and restrict reverse transcription
Fletcher, A. J., Christensen, D. E., Nelson, C., Tan, C. P., Schaller, T., Lehner, P. J., Sundquist, W. I., & Towers, G. J. (2015) · The EMBO Journal · doi:10.15252/embj.201490361 · Cited by 95
HIV-1 and human genetic variation
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Whole Exome Sequencing in Females with Autism Implicates Novel and Candidate Genes
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Self-citationUbc13: the Lys63 ubiquitin chain building machine
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TRIM59 interacts with ECSIT and negatively regulates NF-κB and IRF-3/7-mediated signal pathways
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Intracellular antibody signalling is regulated by phosphorylation of the Fc receptor TRIM21
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Self-citationFates of Retroviral Core Components during Unrestricted and TRIM5-Restricted Infection
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Metadata
- Authors
- Pertel, T., Hausmann, S., Morger, D., Züger, S., Guerra, J., Lascano, J., Reinhard, C., Santoni, F. A., Uchil, P. D., Chatel, L., Bisiaux, A., Albert, M. L., Strambio-De-Castillia, C., Mothes, W., Pizzato, M., Grütter, M. G., & Luban, J.
- Affiliations
- University of Geneva (CH)
- University of Zurich (CH)
- Yale University (US)
- Light Chain Bioscience (Switzerland) (CH)
- Inserm (FR)
- Corresponding author
- Luban, Jeremy
- ORCID
- Venue
- Nature
- Published
- 2011-04
- Volume
- 472
- Issue
- 7343
- Pages
- 361-365
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3081621
- OpenAlex
- W2057040546
- Cited by
- 645
- References
- 27
- Citations by year
- 2026: 14 · 2025: 20 · 2024: 35 · 2023: 27 · 2022: 19 · 2021: 34 · 2020: 39 · 2019: 50 · 2018: 43 · 2017: 41 · 2016: 39 · 2015: 48 · 2014: 56 · 2013: 70 · 2012: 72
- FWCI
- 29.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- SERVAL (Université de Lausanne) (acceptedVersion, other-oa)
- IRIS (submittedVersion)
- HAL (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Iris (University of Trento) (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (59159, 128655, 122342, 3100A0)
- National Institutes of Health (3100A0-128655)
- National Institute of Allergy and Infectious Diseases (R01 AI59159, R01AI059159, R21AI087467)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- TRIM5, antiretroviral restriction factors, E3 ubiquitin ligase, pattern recognition receptors, innate immune signaling, K63-linked ubiquitin, TAK1, NF-κB signaling, retroviral infection
- MeSH terms
- Tripartite Motif Proteins, Antiviral Restriction Factors, MAP Kinase Kinase Kinase 7, Capsid, Carrier Proteins, Cell Line, Enzyme Activation, Humans, Immunity, Innate, Lipopolysaccharides, Protein Binding, Retroviridae, Transcription Factors, Signal Transduction, HIV-1, NF-kappa B, Transcription Factor AP-1, MAP Kinase Kinase Kinases, Ubiquitin, Ubiquitin-Conjugating Enzymes, Ubiquitin-Protein Ligases, Receptors, Pattern Recognition, HEK293 Cells
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