TRIM5α Restricts Flavivirus Replication by Targeting the Viral Protease for Proteasomal Degradation
Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this curre...
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| Published in | Cell reports (Cambridge) Vol. 27; no. 11; pp. 3269 - 3283.e6 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier
11.06.2019
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| Abstract | Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this current understanding, we show that both human and rhesus macaque TRIM5α suppress replication of specific flaviviruses. Multiple viruses in the tick-borne encephalitis complex are sensitive to TRIM5α-dependent restriction, but mosquito-borne flaviviruses, including yellow fever, dengue, and Zika viruses, are resistant. TRIM5α suppresses replication by binding to the viral protease NS2B/3 to promote its K48-linked ubiquitination and proteasomal degradation. Importantly, TRIM5α contributes to the antiviral function of IFN-I against sensitive flaviviruses in human cells. Thus, TRIM5α possesses remarkable plasticity in the recognition of diverse virus families, with the potential to influence human susceptibility to emerging flaviviruses of global concern. |
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| AbstractList | Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this current understanding, we show that both human and rhesus macaque TRIM5α suppress replication of specific flaviviruses. Multiple viruses in the tick-borne encephalitis complex are sensitive to TRIM5α-dependent restriction, but mosquito-borne flaviviruses, including yellow fever, dengue, and Zika viruses, are resistant. TRIM5α suppresses replication by binding to the viral protease NS2B/3 to promote its K48-linked ubiquitination and proteasomal degradation. Importantly, TRIM5α contributes to the antiviral function of IFN-I against sensitive flaviviruses in human cells. Thus, TRIM5α possesses remarkable plasticity in the recognition of diverse virus families, with the potential to influence human susceptibility to emerging flaviviruses of global concern. Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this current understanding, we show that both human and rhesus macaque TRIM5α suppress replication of specific flaviviruses. Multiple viruses in the tick-borne encephalitis complex are sensitive to TRIM5α-dependent restriction, but mosquito-borne flaviviruses, including yellow fever, dengue, and Zika viruses, are resistant. TRIM5α suppresses replication by binding to the viral protease NS2B/3 to promote its K48-linked ubiquitination and proteasomal degradation. Importantly, TRIM5α contributes to the antiviral function of IFN-I against sensitive flaviviruses in human cells. Thus, TRIM5α possesses remarkable plasticity in the recognition of diverse virus families, with the potential to influence human susceptibility to emerging flaviviruses of global concern.Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this current understanding, we show that both human and rhesus macaque TRIM5α suppress replication of specific flaviviruses. Multiple viruses in the tick-borne encephalitis complex are sensitive to TRIM5α-dependent restriction, but mosquito-borne flaviviruses, including yellow fever, dengue, and Zika viruses, are resistant. TRIM5α suppresses replication by binding to the viral protease NS2B/3 to promote its K48-linked ubiquitination and proteasomal degradation. Importantly, TRIM5α contributes to the antiviral function of IFN-I against sensitive flaviviruses in human cells. Thus, TRIM5α possesses remarkable plasticity in the recognition of diverse virus families, with the potential to influence human susceptibility to emerging flaviviruses of global concern. Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this current understanding, we show that both human and rhesus macaque TRIM5α suppress replication of specific flaviviruses. Multiple viruses in the tick-borne encephalitis complex are sensitive to TRIM5α-dependent restriction, but mosquito-borne flaviviruses, including yellow fever, dengue, and Zika viruses, are resistant. TRIM5α suppresses replication by binding to the viral protease NS2B/3 to promote its K48-linked ubiquitination and proteasomal degradation. Importantly, TRIM5α contributes to the antiviral function of IFN-I against sensitive flaviviruses in human cells. Thus, TRIM5α possesses remarkable plasticity in the recognition of diverse virus families, with the potential to influence human susceptibility to emerging flaviviruses of global concern. : The antiviral activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. Here, Chiramel et al. demonstrate that TRIM5α restricts replication of specific flaviviruses by binding and degrading the viral protease. Keywords: TRIM5α, flavivirus, retrovirus, interferon, restriction factor, retrovirus, interferon stimulated genes, tick-borne encephalitis virus Tripartite motif-containing protein 5α (TRIM5α) is a cellular antiviral restriction factor that prevents early events in retrovirus replication. The activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. In contrast to this current understanding, we show that both human and rhesus macaque TRIM5α suppress replication of specific flaviviruses. Multiple viruses in the tick-borne encephalitis complex are sensitive to TRIM5α-dependent restriction, but mosquito-borne flaviviruses, including yellow fever, dengue, and Zika viruses, are resistant. TRIM5α suppresses replication by binding to the viral protease NS2B/3 to promote its K48-linked ubiquitination and proteasomal degradation. Importantly, TRIM5α contributes to the antiviral function of IFN-I against sensitive flaviviruses in human cells. Thus, TRIM5α possesses remarkable plasticity in the recognition of diverse virus families, with the potential to influence human susceptibility to emerging flaviviruses of global concern. The antiviral activity of TRIM5α is thought to be limited to retroviruses as a result of highly specific interactions with capsid lattices. Here, Chiramel et al. demonstrate that TRIM5α restricts replication of specific flaviviruses by binding and degrading the viral protease. |
| Author | Montoya, Vanessa R. Youseff, Brian H. Meyerson, Nicholas R. Lubick, Kirk J. Kim, Kyusik Sturdevant, Gail L. Bosio, Catharine M. Taylor, R. Travis Bouamr, Fadila McNally, Kristin L. Luban, Jeremy Chiramel, Abhilash I. Nair, Vinod Sawyer, Sara L. Best, Sonja M. Robertson, Shelly J. Hirsch, Vanessa M. Méndez-Solís, Omayra Broeckel, Rebecca M. Ireland, Robin M. |
| AuthorAffiliation | 2 Department of Molecular, Cellular and Developmental Biology, University of Colorado Boulder, Boulder, CO 80309, USA 6 Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01655, USA 3 Research Technology Branch, RML, NIAID, NIH, Hamilton, MT 59840, USA 1 Innate Immunity and Pathogenesis Section, Laboratory of Virology, Rocky Mountain Laboratories (RML), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USA 4 Department of Medical Microbiology and Immunology, College of Medicine and Life Sciences, University of Toledo Health Science Campus, Toledo, OH 43606, USA 7 Laboratory of Molecular Microbiology, NIAID, Bethesda, MD 20892, USA 5 Immunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, RML, NIAID, NIH, Hamilton, MT 59840, USA 8 These authors contributed equally 9 Lead Contact |
| AuthorAffiliation_xml | – name: 9 Lead Contact – name: 1 Innate Immunity and Pathogenesis Section, Laboratory of Virology, Rocky Mountain Laboratories (RML), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USA – name: 8 These authors contributed equally – name: 6 Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01655, USA – name: 2 Department of Molecular, Cellular and Developmental Biology, University of Colorado Boulder, Boulder, CO 80309, USA – name: 3 Research Technology Branch, RML, NIAID, NIH, Hamilton, MT 59840, USA – name: 5 Immunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, RML, NIAID, NIH, Hamilton, MT 59840, USA – name: 4 Department of Medical Microbiology and Immunology, College of Medicine and Life Sciences, University of Toledo Health Science Campus, Toledo, OH 43606, USA – name: 7 Laboratory of Molecular Microbiology, NIAID, Bethesda, MD 20892, USA |
| Author_xml | – sequence: 1 givenname: Abhilash I. surname: Chiramel fullname: Chiramel, Abhilash I. – sequence: 2 givenname: Nicholas R. surname: Meyerson fullname: Meyerson, Nicholas R. – sequence: 3 givenname: Kristin L. surname: McNally fullname: McNally, Kristin L. – sequence: 4 givenname: Rebecca M. surname: Broeckel fullname: Broeckel, Rebecca M. – sequence: 5 givenname: Vanessa R. surname: Montoya fullname: Montoya, Vanessa R. – sequence: 6 givenname: Omayra surname: Méndez-Solís fullname: Méndez-Solís, Omayra – sequence: 7 givenname: Shelly J. surname: Robertson fullname: Robertson, Shelly J. – sequence: 8 givenname: Gail L. surname: Sturdevant fullname: Sturdevant, Gail L. – sequence: 9 givenname: Kirk J. surname: Lubick fullname: Lubick, Kirk J. – sequence: 10 givenname: Vinod surname: Nair fullname: Nair, Vinod – sequence: 11 givenname: Brian H. surname: Youseff fullname: Youseff, Brian H. – sequence: 12 givenname: Robin M. surname: Ireland fullname: Ireland, Robin M. – sequence: 13 givenname: Catharine M. surname: Bosio fullname: Bosio, Catharine M. – sequence: 14 givenname: Kyusik surname: Kim fullname: Kim, Kyusik – sequence: 15 givenname: Jeremy surname: Luban fullname: Luban, Jeremy – sequence: 16 givenname: Vanessa M. surname: Hirsch fullname: Hirsch, Vanessa M. – sequence: 17 givenname: R. Travis surname: Taylor fullname: Taylor, R. Travis – sequence: 18 givenname: Fadila surname: Bouamr fullname: Bouamr, Fadila – sequence: 19 givenname: Sara L. surname: Sawyer fullname: Sawyer, Sara L. – sequence: 20 givenname: Sonja M. surname: Best fullname: Best, Sonja M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31189110$$D View this record in MEDLINE/PubMed |
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| Keywords | TRIM5α retrovirus restriction factor interferon interferon stimulated genes flavivirus tick-borne encephalitis virus |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, A.I.C. and S.M.B.; Methodology, A.I.C., N.R.M., F.B., S.L.S., and S.M.B.; Investigation, A.I.C., N.R.M., K.L.M., R.M.B., V.R.M., O.M.-S., S.J.R., F.B., G.L.S., K.J.L., V.N., B.H.Y., R.T.T., K.K., and S.M.B.; Data Curation, A.I.C., N.R.M., F.B., S.M.B.; Writing – Original Draft, A.I.C. and S.M.B.; Writing – Review & Editing, A.I.C., N.R.M., R.T.T., F.B., S.L.S., and S.M.B.; Resources, J.L., V.M.H., R.T.T., S.L.S., and S.M.B.; Visualization, A.I.C., N.R.M., V.R.M., K.L.M., O.M.-S., S.J.R., G.L.S., K.J.L., V.N., S.L.S., and S.M.B.; Supervision, J.L., R.T.T., S.L.S., and S.M.B. |
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| Title | TRIM5α Restricts Flavivirus Replication by Targeting the Viral Protease for Proteasomal Degradation |
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