TRIM5 is an innate immune sensor for the retrovirus capsid lattice
Open accessAbstract
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In dendritic cells, TRIM5α binding to the capsid lattice triggers signal transduction cascades resulting in activation of AP-1 and NF-κB.
“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]
TRIM5α-induced AP-1 and NF-κB activation is insufficient to induce IFN production alone but synergizes with other pathways to enhance IFN response.
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys
Stremlau, M. H., Owens, C. M., Perron, M. J., Kießling, M. K., Autissier, P., & Sodroski, J. (2004) · Nature · doi:10.1038/nature02343 · Cited by 1,820 · see citing works
Integration of murine leukemia virus DNA depends on mitosis.
Roe, T., Reynolds, T. C., Yu, G., & Brown, P. O. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05858.x · Cited by 921 · see citing works
Stremlau, M. H., Perron, M. J., Lee, M. N., Li, Y., Song, B., Javanbakht, H., Diaz‐Griffero, F., Anderson, D. J., Sundquist, W. I., & Sodroski, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509996103 · Cited by 740 · see citing works
Assembly and Analysis of Conical Models for the HIV-1 Core
Ganser, B. K., Li, S., Klishko, V. Y., Finch, J. T., & Sundquist, W. I. (1999) · Science · doi:10.1126/science.283.5398.80 · Cited by 671 · see citing works
Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1
Sayah, D. M., Sokolskaja, E., Berthoux, L., & Luban, J. (2004) · Nature · doi:10.1038/nature02777 · Cited by 662 · see citing works
Self-citationAn Atomic Model of the Interferon-β Enhanceosome
Panne, D., Maniatis, T., & Harrison, S. C. (2007) · Cell · doi:10.1016/j.cell.2007.05.019 · Cited by 625 · see citing works
Zeng, W., Sun, L., Jiang, X., Chen, X., Hou, F., Adhikari, A., Xu, M., & Chen, Z. J. (2010) · Cell · doi:10.1016/j.cell.2010.03.029 · Cited by 613 · see citing works
Direct activation of protein kinases by unanchored polyubiquitin chains
Xia, Z.-P., Sun, L., Chen, X., Pineda, G., Jiang, X., Adhikari, A., Zeng, W., & Chen, Z. J. (2009) · Nature · doi:10.1038/nature08247 · Cited by 570 · see citing works
X-Ray Structures of the Hexameric Building Block of the HIV Capsid
Pornillos, O., Ganser-Pornillos, B. K., Kelly, B. N., Hua, Y., Whitby, F. G., Stout, C. D., Sundquist, W. I., Hill, C. P., & Yeager, M. (2009) · Cell · doi:10.1016/j.cell.2009.04.063 · Cited by 523 · see citing works
Yan, N., Regalado-Magdos, A. D., Stiggelbout, B., Lee‐Kirsch, M. A., & Lieberman, J. (2010) · Nature Immunology · doi:10.1038/ni.1941 · Cited by 522 · see citing works
Host Innate Immune Receptors and Beyond: Making Sense of Microbial Infections
Ishii, K. J., Koyama, S., Nakagawa, A., Coban, C., & Akira, S. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.05.003 · Cited by 501 · see citing works
Atomic-level modelling of the HIV capsid
Pornillos, O., Ganser-Pornillos, B. K., & Yeager, M. (2011) · Nature · doi:10.1038/nature09640 · Cited by 372 · see citing works
TRIM5α mediates the postentry block to N-tropic murine leukemia viruses in human cells
Perron, M. J., Stremlau, M. H., Song, B., Ulm, W., Mulligan, R. C., & Sodroski, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403364101 · Cited by 290 · see citing works
Kornbluth, R. S., Oh, P., Munis, J. R., Cleveland, P. H., & Richman, D. D. (1989) · The Journal of Experimental Medicine · doi:10.1084/jem.169.3.1137 · Cited by 270 · see citing works
Shi, M., Deng, W., Bi, E., Mao, K., Ji, Y., Lin, G., Wu, X., Tao, Z., Li, Z., Cai, X., et al. (2008) · Nature Immunology · doi:10.1038/ni1577 · Cited by 254 · see citing works
Hexagonal assembly of a restricting TRIM5α protein
Ganser‐Pornillos, B. K., Chandrasekaran, V., Pornillos, O., Sodroski, J., Sundquist, W. I., & Yeager, M. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013426108 · Cited by 248 · see citing works
TRIM5α selectively binds a restriction-sensitive retroviral capsid
Sebastian, S., & Luban, J. (2005) · Retrovirology · doi:10.1186/1742-4690-2-40 · Cited by 240 · see citing works
Self-citationCyclophilin A is required for TRIM5α-mediated resistance to HIV-1 in Old World monkey cells
Berthoux, L., Sebastian, S., Sokolskaja, E., & Luban, J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505659102 · Cited by 147 · see citing works
Self-citationCyclophilin A, TRIM5, and Resistance to Human Immunodeficiency Virus Type 1 Infection
Luban, J. (2007) · Journal of Virology · doi:10.1128/jvi.01519-06 · Cited by 147 · see citing works
Self-citationPotent inhibition of HIV-1 by TRIM5-cyclophilin fusion proteins engineered from human components
Neagu, M. R., Ziegler, P., Pertel, T., Strambio‐De‐Castillia, C., Grütter, C., Martinetti, G., Mazzucchelli, L., Grütter, M. G., Manz, M. G., & Luban, J. (2009) · Journal of Clinical Investigation · doi:10.1172/jci39354 · Cited by 123 · see citing works
Self-citationLangelier, C., Sandrin, V., Eckert, D. M., Christensen, D. E., Chandrasekaran, V., Alam, S. L., Aiken, C., Olsen, J. C., Kar, A. K., Sodroski, J., et al. (2008) · Journal of Virology · doi:10.1128/jvi.01562-08 · Cited by 120 · see citing works
Structural Basis for the Lack of E2 Interaction in the RING Domain of TRAF2
Yin, Q., Lamothe, B., Darnay, B. G., & Wu, H. (2009) · Biochemistry · doi:10.1021/bi901462e · Cited by 112 · see citing works
Sokolskaja, E., Berthoux, L., & Luban, J. (2006) · Journal of Virology · doi:10.1128/jvi.80.6.2855-2862.2006 · Cited by 103 · see citing works
Self-citationAs 2 O 3 Enhances Retroviral Reverse Transcription and Counteracts Ref1 Antiviral Activity
Berthoux, L., Towers, G. J., Gurer, C., Salomoni, P., Pandolfi, P. P., & Luban, J. (2003) · Journal of Virology · doi:10.1128/jvi.77.5.3167-3180.2003 · Cited by 71 · see citing works
Self-citationHuman Trim5α has additional activities that are uncoupled from retroviral capsid recognition
Tareen, S. U., & Emerman, M. (2010) · Virology · doi:10.1016/j.virol.2010.09.018 · Cited by 63 · see citing works
HIV immunology needs a new direction
Medzhitov, R. M., & Littman, D. R. (2008) · Nature · doi:10.1038/455591a · Cited by 32 · see citing works
Ulm, J. W., Perron, M. J., Sodroski, J., & Mulligan, R. C. (2007) · Virology · doi:10.1016/j.virol.2006.09.048 · Cited by 25 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
van der Harst, P., & Verweij, N. (2018) · Circulation Research · doi:10.1161/circresaha.117.312086 · Cited by 1,141 · see citing works
Interferon-Stimulated Genes: What Do They All Do?
Schoggins, J. W. (2019) · Annual Review of Virology · doi:10.1146/annurev-virology-092818-015756 · Cited by 1,036 · see citing works
TRIM Family Proteins: Roles in Autophagy, Immunity, and Carcinogenesis
Hatakeyama, S. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.01.002 · Cited by 955 · see citing works
Ni, Y., Lempp, F. A., Mehrle, S., Nkongolo, S., Kaufman, C., Fälth, M., Stindt, J., Königer, C., Nassal, M., Kubitz, R., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.12.024 · Cited by 774 · see citing works
CEACAM1 regulates TIM-3-mediated tolerance and exhaustion
Huang, Y.-H., Zhu, C., Kondo, Y., Anderson, A. C., Gandhi, A., Russell, A., Dougan, S. K., Petersen, B.-S., Melum, E., Pertel, T., et al. (2015) · Nature · doi:10.1038/nature13848 · Cited by 717 · see citing works
Self-citationHuman MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection
Goujon, C., Moncorgé, O., Bauby, H., Doyle, T., Ward, C. C., Schaller, T., Hué, S., Barclay, W., Schulz, R., & Malim, M. H. (2013) · Nature · doi:10.1038/nature12542 · Cited by 587 · see citing works
Interferon-inducible effector mechanisms in cell-autonomous immunity
MacMicking, J. D. (2012) · Nature reviews. Immunology · doi:10.1038/nri3210 · Cited by 564 · see citing works
Yan, N., & Chen, Z. J. (2012) · Nature Immunology · doi:10.1038/ni.2229 · Cited by 535 · see citing works
The structural biology of HIV-1: mechanistic and therapeutic insights
Engelman, A., & Cherepanov, P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2747 · Cited by 426 · see citing works
Ubiquitination in signaling to and activation of IKK
Chen, Z. J. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01108.x · Cited by 419 · see citing works
IFITM3 Inhibits Influenza A Virus Infection by Preventing Cytosolic Entry
Feeley, E. M., Sims, J. S., John, S. P., Chin, C. R., Pertel, T., Chen, L.-M., Gaiha, G. D., Ryan, B. J., Donis, R. O., Elledge, S. J., et al. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002337 · Cited by 387 · see citing works
Self-citationTargeting of TAK1 in inflammatory disorders and cancer
Sakurai, H. (2012) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2012.06.007 · Cited by 377 · see citing works
Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21
McEwan, W. A., Tam, J. C. H., Watkinson, R. E., Bidgood, S. R., Mallery, D. L., & James, L. C. (2013) · Nature Immunology · doi:10.1038/ni.2548 · Cited by 374 · see citing works
Evolutionary conflicts between viruses and restriction factors shape immunity
Duggal, N. K., & Emerman, M. (2012) · Nature reviews. Immunology · doi:10.1038/nri3295 · Cited by 369 · see citing works
Epithelia Use Butyrophilin-like Molecules to Shape Organ-Specific γδ T Cell Compartments
Barros, R. D. M., Roberts, N. A., Dart, R., Vantourout, P., Jandke, A., Nussbaumer, O., Deban, L., Cipolat, S., Hart, R., Iannitto, M. L., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.030 · Cited by 363 · see citing works
The role of ubiquitylation in immune defence and pathogen evasion
Jiang, X., & Chen, Z. J. (2011) · Nature reviews. Immunology · doi:10.1038/nri3111 · Cited by 350 · see citing works
TRIMmunity: The Roles of the TRIM E3-Ubiquitin Ligase Family in Innate Antiviral Immunity
Rajsbaum, R., García‐Sastre, A., & Versteeg, G. A. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.12.005 · Cited by 345 · see citing works
Studies of endogenous retroviruses reveal a continuing evolutionary saga
Stoye, J. P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2783 · Cited by 350 · see citing works
TRIM Proteins and Their Roles in Antiviral Host Defenses
van Gent, M., Sparrer, K. M. J., & Gack, M. U. (2018) · Annual Review of Virology · doi:10.1146/annurev-virology-092917-043323 · Cited by 325 · see citing works
TRIM Proteins Regulate Autophagy and Can Target Autophagic Substrates by Direct Recognition
Mandell, M. A., Jain, A., Arko‐Mensah, J., Chauhan, S., Kimura, T., Dinkins, C., Silvestri, G., Münch, J., Kirchhoff, F., Simonsen, A., et al. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.06.013 · Cited by 327 · see citing works
Versteeg, G. A., Rajsbaum, R., Sánchez-Aparicio, M. T., Maestre, A. M., Valdiviezo, J., Shi, M., Inn, K., Fernández-Sesma, A., Jung, J. U., & García‐Sastre, A. (2013) · Immunity · doi:10.1016/j.immuni.2012.11.013 · Cited by 320 · see citing works
HIV-1 and interferons: who's interfering with whom?
Doyle, T., Goujon, C., & Malim, M. H. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3449 · Cited by 280 · see citing works
Matreyek, K. A., Yücel, S. S., Li, X., & Engelman, A. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003693 · Cited by 280 · see citing works
HIV-Specific Cytolytic CD4 T Cell Responses During Acute HIV Infection Predict Disease Outcome
Soghoian, D. Z., Jessen, H. K., Flanders, M., Sierra-Davidson, K., Cutler, S., Pertel, T., Ranasinghe, S., Lindqvist, M., Davis, I., Lane, K., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003165 · Cited by 277 · see citing works
Self-citationThe Developmental Control of Transposable Elements and the Evolution of Higher Species
Friedli, M., & Trono, D. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125514 · Cited by 258 · see citing works
Innate Sensing of HIV-1 Assembly by Tetherin Induces NFκB-Dependent Proinflammatory Responses
Galão, R. P., Tortorec, A. L., Pickering, S., Kueck, T., & Neil, S. J. D. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.10.007 · Cited by 268 · see citing works
Identification of Interferon-Stimulated Genes with Antiretroviral Activity
Kane, M., Zang, T. M., Rihn, S. J., Zhang, F., Kueck, T., Alim, M., Schoggins, J. W., Rice, C. M., Wilson, S. J., & Bieniasz, P. D. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.08.005 · Cited by 250 · see citing works
Regulation of NF-κB by ubiquitination
Chen, J., & Chen, Z. J. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2012.12.005 · Cited by 258 · see citing works
Reactivation of Latent HIV-1 by Inhibition of BRD4
Zhu, J. K., Gaiha, G. D., John, S. P., Pertel, T., Chin, C. R., Gao, G., Qu, H., Walker, B. D., Elledge, S. J., & Brass, A. L. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.008 · Cited by 246 · see citing works
Self-citationOpen conformers of HLA-F are high-affinity ligands of the activating NK-cell receptor KIR3DS1
García-Beltrán, W. F., Hölzemer, A., Martrus, G., Chung, A. W., Pacheco, Y., Simoneau, C. R., Ručević, M., Lamothe, P. A., Pertel, T., Kim, T., et al. (2016) · Nature Immunology · doi:10.1038/ni.3513 · Cited by 245 · see citing works
Self-citationCoupling viruses to dynein and kinesin‐1
Dodding, M. P., & Way, M. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.283 · Cited by 231 · see citing works
Regulation of innate immune signalling pathways by the tripartite motif (TRIM) family proteins
Kawai, T., & Akira, S. (2011) · EMBO Molecular Medicine · doi:10.1002/emmm.201100160 · Cited by 231 · see citing works
Structural Basis for Target-Directed MicroRNA Degradation
Sheu-Gruttadauria, J., Pawlica, P., Klum, S. M., Wang, S., Yario, T. A., Schirle Oakdale, N. T., Steitz, J. A., & MacRae, I. J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.06.019 · Cited by 246 · see citing works
Cell-Cell Transmission Enables HIV-1 to Evade Inhibition by Potent CD4bs Directed Antibodies
Abela, I. A., Berlinger, L., Schanz, M. M., Reynell, L., Günthard, H. F., Rusert, P., & Trkola, A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002634 · Cited by 229 · see citing works
Wang, F., Huang, S., Gao, R., Zhou, Y., Lai, C., Li, Z., Xian, W., Qian, X., Li, Z., Huang, Y., et al. (2020) · Cell Discovery · doi:10.1038/s41421-020-00231-4 · Cited by 222 · see citing works
Wu, Y., Liu, Q., Zhou, J., Xie, W., Chen, C., Wang, Z., Yang, H., & Cui, J. (2017) · Cell Discovery · doi:10.1038/celldisc.2017.6 · Cited by 219 · see citing works
Uchil, P. D., Hinz, A., Siegel, S. J., Coenen-Stass, A. M. L., Pertel, T., Luban, J., & Mothes, W. (2012) · Journal of Virology · doi:10.1128/jvi.01804-12 · Cited by 216 · see citing works
Self-citationHoran, K., Hansen, K., Jakobsen, M. R., Holm, C. K., Søby, S., Unterholzner, L., Thompson, M., West, J. A., Iversen, M. B., Rasmussen, S. B., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202749 · Cited by 204 · see citing works
Structural determinants of TRIM protein function
Esposito, D., Koliopoulos, M. G., & Rittinger, K. (2017) · Biochemical Society Transactions · doi:10.1042/bst20160325 · Cited by 206 · see citing works
The tripartite motif coiled-coil is an elongated antiparallel hairpin dimer
Sanchez, J. G., Okreglicka, K. M., Chandrasekaran, V., Welker, J. M., Sundquist, W. I., & Pornillos, O. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318962111 · Cited by 197 · see citing works
Stimulation of NF-κB Activity by the HIV Restriction Factor BST2
Tokarev, A., Suarez, M., Kwan, W., Fitzpatrick, K., Singh, R. P., & Guatelli, J. (2012) · Journal of Virology · doi:10.1128/jvi.02272-12 · Cited by 193 · see citing works
Intracellular sensing of complement C3 activates cell autonomous immunity
Tam, J. C. H., Bidgood, S. R., McEwan, W. A., & James, L. C. (2014) · Science · doi:10.1126/science.1256070 · Cited by 189 · see citing works
TRIM family: Pleiotropy and diversification through homomultimer and heteromultimer formation
Napolitano, L. M. R., & Meroni, G. (2011) · IUBMB Life · doi:10.1002/iub.580 · Cited by 174 · see citing works
Direct activation of a bacterial innate immune system by a viral capsid protein
Zhang, T., Tamman, H., Wallant, K. C. ’., Kurata, T., LeRoux, M., Srikant, S., Brodiazhenko, T., Čepauskas, A., Talavera, A., Martens, C., et al. (2022) · Nature · doi:10.1038/s41586-022-05444-z · Cited by 174 · see citing works
Vantourout, P., Laing, A., Woodward, M. J., Zlatareva, I., Apolonia, L., Jones, A. W., Snijders, A. P., Malim, M. H., & Hayday, A. C. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701237115 · Cited by 173 · see citing works
Restriction Factors: From Intrinsic Viral Restriction to Shaping Cellular Immunity Against HIV-1
Colomer-Lluch, M., Ruiz, A., Moris, A., & Prado, J. G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02876 · Cited by 165 · see citing works
Rajsbaum, R., Versteeg, G. A., Schmid, S., Maestre, A. M., Belicha-Villanueva, A., Martínez-Romero, C., Patel, J. R., Morrison, J., Pisanelli, G., Miorin, L., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.04.018 · Cited by 168 · see citing works
Regulation of Toll‐like receptor signaling pathways in innate immune responses
Qian, C., & Cao, X. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06786.x · Cited by 168 · see citing works
Restriction of HIV-1 and other retroviruses by TRIM5
Ganser-Pornillos, B. K., & Pornillos, O. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0225-2 · Cited by 163 · see citing works
Versteeg, G. A., Benke, S., García‐Sastre, A., & Rajsbaum, R. (2014) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2014.08.001 · Cited by 156 · see citing works
Regulation of Immunity by Butyrophilins
Rhodes, D. A., Reith, W., & Trowsdale, J. (2016) · Annual Review of Immunology · doi:10.1146/annurev-immunol-041015-055435 · Cited by 155 · see citing works
Salminen, A., Kaarniranta, K., Hiltunen, M. O., & Kauppinen, A. (2014) · Journal of Molecular Medicine · doi:10.1007/s00109-014-1182-x · Cited by 146 · see citing works
Yurkovetskiy, L., Guney, M. H., Kim, K., Goh, S. L., McCauley, S. M., Dauphin, A., Diehl, W. E., & Luban, J. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0256-x · Cited by 141 · see citing works
Self-citationCocka, L. J., & Bates, P. F. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002931 · Cited by 141 · see citing works
Endogenous retroviruses: acquisition, amplification and taming of genome invaders
Dewannieux, M., & Heidmann, T. (2013) · Current Opinion in Virology · doi:10.1016/j.coviro.2013.08.005 · Cited by 138 · see citing works
TNPO3 protects HIV-1 replication from CPSF6-mediated capsid stabilization in the host cell cytoplasm
Iaco, A. D., Santoni, F. A., Vannier, A., Guipponi, M., Antonarakis, S. E., & Luban, J. (2013) · Retrovirology · doi:10.1186/1742-4690-10-20 · Cited by 140 · see citing works
Self-citationA whole genome screen for HIV restriction factors
Liu, L., Oliveira, N. M. M., Cheney, K. M., Pade, C., Dreja, H. S., Bergin, A.-M. H., Borgdorff, V., Beach, D., Bishop, C. L., Dittmar, M. T., et al. (2011) · Retrovirology · doi:10.1186/1742-4690-8-94 · Cited by 140 · see citing works
Ubiquitin enzymes in the regulation of immune responses
Ebner, P., Versteeg, G. A., & Ikeda, F. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1325829 · Cited by 139 · see citing works
IFI16 Targets the Transcription Factor Sp1 to Suppress HIV-1 Transcription and Latency Reactivation
Hotter, D., Bosso, M., Jønsson, K. L., Krapp, C., Stürzel, C. M., Das, A. T., Littwitz-Salomon, E., Berkhout, B., Russ, A., Wittmann, S., et al. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.05.002 · Cited by 135 · see citing works
Cyclophilin A protects HIV-1 from restriction by human TRIM5α
Kim, K., Dauphin, A., Keceli, S. K., McCauley, S. M., Yurkovetskiy, L., Carbone, C., Diehl, W. E., Strambio‐De‐Castillia, C., Campbell, E. M., & Luban, J. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0592-5 · Cited by 135 · see citing works
Self-citationThe TRIMendous Role of TRIMs in Virus–Host Interactions
van Tol, S., Hage, A., Giraldo, M. I., Bharaj, P., & Rajsbaum, R. (2017) · Vaccines · doi:10.3390/vaccines5030023 · Cited by 129 · see citing works
Fletcher, A. J., Mallery, D. L., Watkinson, R. E., Dickson, C. F., & James, L. C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1507534112 · Cited by 128 · see citing works
Zhao, W., Wang, L., Zhang, M., Yuan, C., & Gao, C. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103255 · Cited by 127 · see citing works
Activation of the innate immune response by endogenous retroviruses
Hurst, T. P., & Magiorkinis, G. (2014) · Journal of General Virology · doi:10.1099/jgv.0.000017 · Cited by 139 · see citing works
Capsid-Dependent Host Factors in HIV-1 Infection
Yamashita, M., & Engelman, A. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.04.004 · Cited by 123 · see citing works
Qian, Y., Wang, Z., Lin, H., Lei, T., Zhou, Z., Huang, W., Wu, X., Zuo, L., Wu, J., Liu, Y., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00953-9 · Cited by 118 · see citing works
Structural Insight into HIV-1 Restriction by MxB
Fribourgh, J. L., Nguyen, H. C., Matreyek, K. A., Alvarez, F. J. D., Summers, B. J., Dewdney, T. G., Aiken, C., Zhang, P., Engelman, A., & Xiong, Y. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.09.021 · Cited by 120 · see citing works
Identification of a Genomic Reservoir for New TRIM Genes in Primate Genomes
Han, K., Lou, D. I., & Sawyer, S. L. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002388 · Cited by 120 · see citing works
Dong, Y., Zhang, X., Xie, M., Arefnezhad, B., Wang, Z., Wang, W., Feng, S., Huang, G., Guan, R., Shen, W., et al. (2015) · BMC Genomics · doi:10.1186/s12864-015-1606-1 · Cited by 116 · see citing works
HIV cell-to-cell transmission: effects on pathogenesis and antiretroviral therapy
Agosto, L. M., Uchil, P. D., & Mothes, W. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.02.003 · Cited by 114 · see citing works
Self-citationIaco, A. D., & Luban, J. (2014) · Retrovirology · doi:10.1186/1742-4690-11-11 · Cited by 111 · see citing works
Self-citationTRIM 21: a cytosolic Fc receptor with broad antibody isotype specificity
Foss, S., Watkinson, R., Sandlie, I., James, L. C., & Andersen, J. T. (2015) · Immunological Reviews · doi:10.1111/imr.12363 · Cited by 108 · see citing works
Restriction by SAMHD1 Limits cGAS/STING-Dependent Innate and Adaptive Immune Responses to HIV-1
Maelfait, J., Bridgeman, A., Benlahrech, A., Cursi, C., & Rehwinkel, J. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.07.002 · Cited by 109 · see citing works
Swaminathan, G., Rossi, F., Sierra, L., Gupta, A. A., Navas, S., & Martín‐García, J. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002937 · Cited by 108 · see citing works
Di Rienzo, M., Antonioli, M., Fusco, C., Liu, Y., Mari, M., Orhon, I., Refolo, G., Germani, F., Corazzari, M., Romagnoli, A., et al. (2019) · Science Advances · doi:10.1126/sciadv.aau8857 · Cited by 107 · see citing works
Intrinsic Cellular Defenses against Human Immunodeficiency Viruses
Blanco-Melo, D., Venkatesh, S., & Bieniasz, P. D. (2012) · Immunity · doi:10.1016/j.immuni.2012.08.013 · Cited by 107 · see citing works
Michaud, V., Bar-Magen, T., Turgeon, J., Flockhart, D. A., Desta, Z., & Wainberg, M. A. (2012) · Pharmacological Reviews · doi:10.1124/pr.111.005553 · Cited by 106 · see citing works
Fletcher, A. J., Vaysburd, M., Maslen, S., Zeng, J., Skehel, M. J., Towers, G. J., & James, L. C. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.10.007 · Cited by 106 · see citing works
Dendritic cell dysregulation during HIV ‐1 infection
Miller, E., & Bhardwaj, N. (2013) · Immunological Reviews · doi:10.1111/imr.12082 · Cited by 105 · see citing works
Primate TRIM5 proteins form hexagonal nets on HIV-1 capsids
Li, Y.-L., Chandrasekaran, V., Carter, S. D., Woodward, C. L., Christensen, D. E., Dryden, K. A., Pornillos, O., Yeager, M. J., Ganser‐Pornillos, B. K., Jensen, G. J., et al. (2016) · eLife · doi:10.7554/elife.16269 · Cited by 105 · see citing works
Precision autophagy directed by receptor regulators – emerging examples within the TRIM family
Kimura, T., Mandell, M. A., & Deretic, V. P. (2016) · Journal of Cell Science · doi:10.1242/jcs.163758 · Cited by 104 · see citing works
TRIM21 Promotes cGAS and RIG-I Sensing of Viral Genomes during Infection by Antibody-Opsonized Virus
Watkinson, R. E., McEwan, W. A., Tam, J. C. H., Vaysburd, M., & James, L. C. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005253 · Cited by 104 · see citing works
Multiple roles of the capsid protein in the early steps of HIV-1 infection
Fassati, A. (2012) · Virus Research · doi:10.1016/j.virusres.2012.09.012 · Cited by 100 · see citing works
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 · see citing works
Antiviral TRIMs: friend or foe in autoimmune and autoinflammatory disease?
Jefferies, C. A., Wynne, C., & Higgs, R. (2011) · Nature reviews. Immunology · doi:10.1038/nri3043 · Cited by 101 · see citing works
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 99 · see citing works
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 · see citing works
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 · see citing works
HIV-1 and human genetic variation
McLaren, P. J., & Fellay, J. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00378-0 · Cited by 97 · see citing works
Wagner, J. M., Roganowicz, M., Skorupka, K. A., Alam, S. L., Christensen, D. E., Doss, G., Wan, Y., Frank, G. A., Ganser‐Pornillos, B. K., Sundquist, W. I., et al. (2016) · eLife · doi:10.7554/elife.16309 · Cited by 97 · see citing works
Whole Exome Sequencing in Females with Autism Implicates Novel and Candidate Genes
Butler, M. G., Rafi, S. K., Hossain, W. A., Stephan, D. A., & Manzardo, A. M. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16011312 · Cited by 93 · see citing works
Host restriction factors in retroviral infection: promises in virus-host interaction
Zheng, Y., Jeang, K.-T., & Tokunaga, K. (2012) · Retrovirology · doi:10.1186/1742-4690-9-112 · Cited by 96 · see citing works
Type I Interferon: Understanding Its Role in HIV Pathogenesis and Therapy
Bosinger, S. E., & Utay, N. S. (2015) · Current HIV/AIDS Reports · doi:10.1007/s11904-014-0244-6 · Cited by 96 · see citing works
Wang, Y., Lifshitz, L. M., Gellatly, K. J., Vinton, C. L., Busman‐Sahay, K., McCauley, S. M., Vangala, P., Kim, K., Derr, A. G., Jaiswal, S., et al. (2020) · Nature Immunology · doi:10.1038/s41590-020-0593-9 · Cited by 95 · see citing works
Self-citationUbc13: the Lys63 ubiquitin chain building machine
Hodge, C. D., Spyracopoulos, L., & Glover, J. N. M. (2016) · Oncotarget · doi:10.18632/oncotarget.10948 · Cited by 93 · see citing works
TRIM59 interacts with ECSIT and negatively regulates NF-κB and IRF-3/7-mediated signal pathways
Kondo, T., Watanabe, M., & Hatakeyama, S. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.05.028 · Cited by 93 · see citing works
Intracellular antibody signalling is regulated by phosphorylation of the Fc receptor TRIM21
Dickson, C. F., Fletcher, A. J., Vaysburd, M., Yang, J., Mallery, D. L., Zeng, J., Johnson, C. M., McLaughlin, S. H., Skehel, M. J., Maslen, S., et al. (2018) · eLife · doi:10.7554/elife.32660 · Cited by 93 · see citing works
Iaco, A. D., & Luban, J. (2011) · Retrovirology · doi:10.1186/1742-4690-8-98 · Cited by 92 · see citing works
Self-citationFates of Retroviral Core Components during Unrestricted and TRIM5-Restricted Infection
Kutluay, S. B., Pérez-Caballero, D., & Bieniasz, P. D. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003214 · Cited by 92 · see citing works
TRIM15 and CYLD regulate ERK activation via lysine-63-linked polyubiquitination
Zhu, G., Herlyn, M., & Yang, X. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00732-8 · Cited by 91 · see citing works
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
