Dr Chris Boutell
- Programme Leader (Virology)
telephone:
01413308374
email:
Chris.Boutell@glasgow.ac.uk
Centre for Virus Research, Garscube Campus, 464 Bearsden Road, Glasgow, G61 1qh
https://orcid.org/0000-0002-2970-7785Research interests
Ubiquitin and ubiquitin-like modifications play a critical role in the regulation of many cellular pathways; including protein stability, the cell cycle, transcription, DNA repair and antiviral immunity. Consequently, many human viruses have evolved strategies to utilise or suppress ubiquitin and ubiquitin-like pathways during infection in order to enhance their replication.
My research aims to define how viruses engage with these modification pathways with respect to cellular antiviral immunity, both at the molecular and biochemical level, in order to develop novel avenues for future therapeutic intervention.
Current work within the laboratory focuses on two modification pathways, namely ubiquitin and SUMO (Small Ubiquitin-like MOdifier), which have been shown to play important roles in the activation and regulation of various aspects of intracellular immunity during virus infection. We study this virus host-cell interface using a number of clinically important viruses, including herpes simplex virus type-1 (HSV-1), hepatitis C virus (HCV), and influenza virus.
Publications
2024
Herder, V. et al. (2024) Correlates of disease severity in bluetongue as a model of acute arbovirus infection. PLoS Pathogens, 20(8), e1012466. (doi: 10.1371/journal.ppat.1012466) (PMID:39150989) (PMCID:PMC11357116)
Francois, A. K. et al. (2024) Single-genome analysis reveals heterogeneous association of the herpes simplex virus genome with H3K27me2 and the reader PHF20L1 following infection of human fibroblasts. mBio, (doi: 10.1128/mbio.03278-23) (PMID:32753500) (PMCID:PMC7407090) (Early Online Publication)
Herder, V. et al. (2024) A machine learning framework to identify the correlates of disease severity in acute arbovirus infection. bioRxiv, (doi: 10.1101/2024.02.23.581333)
2023
Pinto, R. M. et al. (2023) BTN3A3 evasion promotes the zoonotic potential of influenza A viruses. Nature, 619(7969), pp. 338-347. (doi: 10.1038/s41586-023-06261-8) (PMID:37380775)
Sims, A. et al. (2023) Superinfection exclusion creates spatially distinct influenza virus populations. PLoS Biology, 21(2), e3001941. (doi: 10.1371/journal.pbio.3001941) (PMID:36757937) (PMCID:PMC9910727)
2022
Mai, J., Stubbe, M., Hofmann, S., Masser, S., Dobner, T., Boutell, C. , Groitl, P. and Schreiner, S. (2022) PML alternative splice products differentially regulate HAdV productive infection. Microbiology Spectrum, 10(4), e0078522. (doi: 10.1128/spectrum.00785-22) (PMID:35699431) (PMCID:PMC9431499)
2021
Herder, V. et al. (2021) Elevated temperature inhibits SARS-CoV-2 replication in respiratory epithelium independently of IFN-mediated innate immune defences. PLoS Biology, 19(12), e3001065. (doi: 10.1371/journal.pbio.3001065) (PMID:34932557) (PMCID:PMC8765667)
Charman, M. et al. (2021) Constitutive TRIM22 expression in the respiratory tract confers a pre-existing defence against influenza A virus infection. Frontiers in Cellular and Infection Microbiology, 11, 689707. (doi: 10.3389/fcimb.2021.689707) (PMID:34621686) (PMCID:PMC8490869)
Suzich, J. B., Cuddy, S. R., Baidas, H., Dochnal, S., Ke, E., Schinlever, A. R., Babnis, A., Boutell, C. and Cliffe, A. R. (2021) PML-NB-dependent type I interferon memory results in a restricted form of HSV latency. EMBO Reports, 22(9), e52547. (doi: 10.15252/embr.202152547) (PMID:34197022)
Kim, E. T., Dybas, J. M., Kulej, K., Reyes, E. D., Price, A. M., Akhtar, L. N., Orr, A., Garcia, B. A., Boutell, C. and Weitzman, M. D. (2021) Comparative proteomics identifies Schlafen 5 (SLFN5) as a herpes simplex virus restriction factor that suppresses viral transcription. Nature Microbiology, 6, pp. 234-245. (doi: 10.1038/s41564-020-00826-3) (PMID:33432153) (PMCID:PMC7856100)
2020
Cuddy, S. R. et al. (2020) Neuronal hyperexcitability is a DLK-dependent trigger of Herpes Simplex Virus reactivation that can be induced by IL-1. eLife, 9, e58037. (doi: 10.7554/eLife.58037) (PMID:33350386) (PMCID:PMC7773336)
Stokes, S., Almire, F., Tatham, M. H., McFarlane, S., Mertens, P., Pondeville, E. and Boutell, C. (2020) The SUMOylation pathway suppresses arbovirus replication in Aedes aegypti cells. PLoS Pathogens, 16(12), e1009134. (doi: 10.1371/journal.ppat.1009134) (PMID:33351855) (PMCID:PMC7802965)
Collados Rodríguez, M. , Dybas, J. M., Hughes, J. , Weitzman, M. D. and Boutell, C. (2020) The HSV-1 ubiquitin ligase ICP0: modifying the cellular proteome to promote infection. Virus Research, 285, 198015. (doi: 10.1016/j.virusres.2020.198015) (PMID:32416261)
2019
McFarlane, S. et al. (2019) The histone chaperone HIRA promotes the induction of host innate immune defences in response to HSV-1 infection. PLoS Pathogens, 15(3), e1007667. (doi: 10.1371/journal.ppat.1007667) (PMID:30901352) (PMCID:PMC6472835)
2018
Alandijany, T., Roberts, A. P.E., Conn, K. L., Loney, C. , McFarlane, S., Orr, A. and Boutell, C. (2018) Distinct temporal roles for the promyelocytic leukaemia (PML) protein in the sequential regulation of intracellular host immunity to HSV-1 infection. PLoS Pathogens, 14(1), e1006769. (doi: 10.1371/journal.ppat.1006769) (PMID:29309427) (PMCID:PMC5757968)
2016
Brown, J. R., Conn, K. L., Wasson, P., Charman, M., Tong, L., Grant, K., McFarlane, S. and Boutell, C. (2016) The SUMO Ligase Protein Inhibitor of Activated STAT 1 (PIAS1) is a constituent PML-NB protein that contributes to the intrinsic antiviral immune response to herpes simplex virus 1 (HSV-1). Journal of Virology, 90, 13. (doi: 10.1128/JVI.00426-16) (PMID:27099310) (PMCID:PMC4907222)
Conn, K. L., Wasson, P., McFarlane, S., Tong, L., Brown, J. R., Grant, K. G., Domingues, P. and Boutell, C. (2016) A novel role for Protein Inhibitor of Activated STAT 4 (PIAS4) in the restriction of herpes simplex virus 1 (HSV-1) by the cellular intrinsic antiviral immune response. Journal of Virology, 90(9), pp. 4807-4826. (doi: 10.1128/JVI.03055-15) (PMID:26937035)
2015
Boutell, C. and Davido, D. J. (2015) A quantitative assay to monitor HSV-1 ICP0 ubiquitin ligase activity in vitro. Methods, 90, pp. 3-7. (doi: 10.1016/j.ymeth.2015.04.004) (PMID:25862948) (PMCID:PMC4655872)
Domingues, P., Bamford, C. G.G., Boutell, C. and McLauchlan, J. (2015) Inhibition of hepatitis C virus RNA replication by ISG15 does not require its conjugation to protein substrates by the HERC5 E3 ligase. Journal of General Virology, 96(11), pp. 3236-3242. (doi: 10.1099/jgv.0.000283) (PMID:26361997) (PMCID:PMC4806579)
Brennan, B. et al. (2015) In memoriam – Richard M. Elliott (1954–2015). Journal of General Virology, 96(8), pp. 1975-1978. (doi: 10.1099/jgv.0.000241) (PMID:26315040)
2014
Busnadiego, I. et al. (2014) Host and viral determinants of Mx2 antiretroviral activity. Journal of Virology, 88(14), pp. 7738-7752. (doi: 10.1128/JVI.00214-14) (PMID:24760893) (PMCID:PMC4097781)
Everett, R.D., Boutell, C. , Pheasant, K., Cuchet-Lourenco, D. and Orr, A. (2014) Sequences related to SUMO interaction motifs in herpes simplex virus 1 protein ICP0 act cooperatively to stimulate virus infection. Journal of Virology, 88(5), pp. 2763-2774. (doi: 10.1128/JVI.03417-13) (PMID:24352468) (PMCID:PMC3958091)
2013
Everett, R.D., Boutell, C. and Hale, B.G. (2013) Interplay between viruses and host sumoylation pathways. Nature Reviews Microbiology, 11(6), pp. 400-411. (doi: 10.1038/nrmicro3015) (PMID:23624814)
Boutell, C. and Everett, R. (2013) Regulation of alphaherpesvirus infections by the ICP0 family of proteins. Journal of General Virology, 94(3), pp. 465-481. (doi: 10.1099/vir.0.048900-0) (PMID:23239572)
Griffiths, S.J. et al. (2013) A systematic analysis of host factors reveals a Med23-interferon-λ regulatory axis against herpes simplex virus type 1 replication. PLoS Pathogens, 9(8), e1003514. (doi: 10.1371/journal.ppat.1003514) (PMID:23950709) (PMCID:PMC3738494)
2012
Chaurushiya, M.S. et al. (2012) Viral E3 ubiquitin ligase-mediated degradation of a cellular E3: viral mimicry of a cellular phosphorylation mark targets the RNF8 FHA domain. Molecular Cell, 46(1), pp. 79-90. (doi: 10.1016/j.molcel.2012.02.004) (PMID:22405594) (PMCID:PMC3648639)
Grant, K., Grant, L., Tong, L. and Boutell, C. (2012) Depletion of intracellular zinc inhibits the ubiquitin ligase activity of viral regulatory protein ICP0 and restricts herpes simplex virus 1 replication in cell culture. Journal of Virology, 86(7), pp. 4029-4033. (doi: 10.1128/jvi.06962-11) (PMID:22278229) (PMCID:PMC3302540)
Vanni, E., Gatherer, D., Tong, L., Everett, R.D. and Boutell, C. (2012) Functional characterization of residues required for the herpes simplex virus 1 E3 ubiquitin ligase ICP0 to interact with the cellular E2 ubiquitin-conjugating enzyme UBE2D1 (UbcH5a). Journal of Virology, 86(11), pp. 6323-6333. (doi: 10.1128/jvi.07210-11) (PMID:22438555) (PMCID:PMC3372195)
2011
Boutell, C. , Cuchet, D., Vanni, E., Orr, A., Glass, M., McFarlane, S. and Everett, R.D. (2011) A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathogens, 7(9), e1002245. (doi: 10.1371/journal.ppat.1002245) (PMID:21949651) (PMCID:PMC3174244)
Cuchet-Lourenço, D., Boutell, C. , Lukashchuk, V., Grant, K., Sykes, A. , Murray, J., Orr, A. and Everett, R.D. (2011) SUMO pathway dependent recruitment of cellular repressors to herpes simplex virus type 1 genomes. PLoS Pathogens, 7(7), e1002123. (doi: 10.1371/journal.ppat.1002123) (PMID:21779164) (PMCID:PMC3136452)
Lilley, C.E., Chaurushiya, M.S., Boutell, C. , Everett, R.D. and Weitzman, M.D. (2011) The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathogens, 7(6), e1002084. (doi: 10.1371/journal.ppat.1002084) (PMID:20075863) (PMCID:PMC2837166)
Smith, M.C., Boutell, C. and Davido, D.J. (2011) HSV-1 ICP0: paving the way for viral replication. Future Virology, 6(4), pp. 421-429. (doi: 10.2217/FVL.11.24) (PMID:21765858) (PMCID:PMC313393)
2010
Everett, R.D., Boutell, C., McNair, C., Grant, L. and Orr, A. (2010) Comparison of the biological and biochemical activities of several members of the alphaherpesvirus ICP0 family of proteins. Journal of Virology, 84(7), pp. 3476-3487. (doi: 10.1128/JVI.02544-09) (PMID:20106921) (PMCID:PMC2838103)
Lilley, C.E., Chaurushiya, M.S., Boutell, C. , Landry, S., Suh, J., Panier, S., Everett, R.D., Stewart, G.S., Durocher, D. and Weitzman, M.D. (2010) A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO Journal, 29(5), pp. 943-955. (doi: 10.1038/emboj.2009.400) (PMID:22405594) (PMCID:PMC3648639)
2009
Antrobus, R., Grant, K., Gangadharan, B., Chittenden, D., Everett, R.D., Zitzmann, N. and Boutell, C. (2009) Proteomic analysis of cells in the early stages of herpes simplex virus type-1 infection reveals widespread changes in the host cell proteome. Proteomics, 9(15), pp. 3913-3927. (doi: 10.1002/pmic.200900207) (PMID:19670248)
Morris, J. R. et al. (2009) The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature, 462(7275), pp. 886-890. (doi: 10.1038/nature08593) (PMID:20016594)
2008
Antrobus, R. and Boutell, C. (2008) Identification of a novel higher molecular weight isoform of USP7/HAUSP that interacts with the Herpes simplex virus type-1 immediate early protein ICP0. Virus Research, 137(1), pp. 64-71. (doi: 10.1016/j.virusres.2008.05.017)
Boutell, C., Everett, R.D., Hilliard, J., Schaffer, P., Orr, A. and Davido, D. (2008) Herpes simplex virus type 1 ICP0 phosphorylation mutants impair the E3 ubiquitin ligase activity of ICP0 in a cell type-dependent manner. Journal of Virology, 82(21), pp. 10647-10656. (doi: 10.1128/JVI.01063-08)
2007
Kummer, M., Turza, N.M., Muhl-Zurbes, P., Lechmann, M., Boutell, C. , Coffin, R.S., Everett, R.D., Steinkasserer, A. and Prechtel, A.T. (2007) Herpes simplex virus type 1 induces CD83 degradation in mature dendritic cells with immediate-early kinetics via the cellular proteasome. Journal of Virology, 81(12), pp. 6326-6338. (doi: 10.1128/jvi.02327-06)
2006
Morris, J.R., Pangon, L., Boutell, C. , Katagiri, T., Keep, N.H. and Solomon, E. (2006) Genetic analysis of BRCA1 ubiquitin ligase activity and its relationship to breast cancer susceptibility. Human Molecular Genetics, 15(4), pp. 599-606. (doi: 10.1093/hmg/ddi476)
2005
Boutell, C. , Canning, M., Orr, A. and Everett, R.D. (2005) Reciprocal activities between herpes simplex virus type 1 regulatory protein ICP0, a ubiquitin E3 ligase, and ubiquitin-specific protease USP7. Journal of Virology, 79(19), pp. 12342-12354. (doi: 10.1128/jvi.79.19.12342-12354.2005)
Meulmeester, E., Maurice, M., Boutell, C. , Teunisse, A., Ovaa, H., Abraham, T., Dirks, R. and Jochemsen, A. (2005) Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Molecular Cell, 18(5), pp. 565-576. (doi: 10.1016/j.molcel.2005.04.024)
2004
Boutell, C. and Everett, R.D. (2004) Herpes simplex virus type 1 infection induces the stabilization of p53 in a USP7- and ATM-independent manner. Journal of Virology, 78(15), pp. 8068-8077. (doi: 10.1128/jvi.78.15.8068-8077.2004)
Everett, R.D., Boutell, C. and Orr, A. (2004) Phenotype of a herpes simplex virus type 1 mutant that fails to express immediate-early regulatory protein ICP0. Journal of Virology, 78(4), pp. 1763-1774. (doi: 10.1128/jvi.78.4.1763-1774.2004)
Canning, M., Boutell, C.J. , Parkinson, J. and Everett, R.D. (2004) A RING finger ubiquitin ligase is protected from autocatalyzed ubiquitination and degradation by binding to ubiquitin-specific protease USP7. Journal of Biological Chemistry, 279(37), pp. 38160-38168. (doi: 10.1074/jbc.M402885200)
2003
Boutell, C. and Everett, R.D. (2003) The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and ubiquitinates p53. Journal of Biological Chemistry, 278(38), pp. 36596-36602. (doi: 10.1074/jbc.M300776200)
Boutell, C.J. , Orr, A. and Everett, R.D. (2003) PML residue lysine 160 is required for the degradation of PML induced by herpes simplex virus type 1 regulatory protein ICP0. Journal of Virology, 77(16), pp. 8686-8694. (doi: 10.1128/jvi.77.16.8686-8694.2003)
Engelhardt, O.G., Boutell, C.J. , Orr, A., Ullrich, E., Haller, O. and Everett, R.D. (2003) The homeodomain-interacting kinase PKM (HIPK-2) modifies ND10 through both its kinase domain and a SUMO-1 interaction motif and alters the posttranslational modification of PML. Experimental Cell Research, 283(1), pp. 36-50. (doi: 10.1016/s0014-4827(02)00025-3)
2002
Boutell, C. , Sadis, S. and Everett, R.D. (2002) Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases In vitro. Journal of Virology, 76(2), pp. 841-850. (doi: 10.1128/jvi.76.2.841-850.2002)
1998
Kirkitadze, M.D., Barlow, P.N., Price, N.C., Kelly, S.M. , Boutell, C.J. , Rixon, F.J. and McClelland, D.A. (1998) The herpes simplex virus triplex protein, VP23, exists as a molten globule. Journal of Virology, 72(12), pp. 10066-10072.
1995
Kazushige, I., Clark, J.C., Shaw-White, J.R., Stahlman, M.T., Boutell, C.J. and Whitsett, J.A. (1995) Gene structure and expression of human thyroid transcription factor-1 in respiratory epithelial cells. Journal of Biological Chemistry, 270(14), pp. 8108-8114. (doi: 10.1074/jbc.270.14.8108)
Articles
Herder, V. et al. (2024) Correlates of disease severity in bluetongue as a model of acute arbovirus infection. PLoS Pathogens, 20(8), e1012466. (doi: 10.1371/journal.ppat.1012466) (PMID:39150989) (PMCID:PMC11357116)
Francois, A. K. et al. (2024) Single-genome analysis reveals heterogeneous association of the herpes simplex virus genome with H3K27me2 and the reader PHF20L1 following infection of human fibroblasts. mBio, (doi: 10.1128/mbio.03278-23) (PMID:32753500) (PMCID:PMC7407090) (Early Online Publication)
Herder, V. et al. (2024) A machine learning framework to identify the correlates of disease severity in acute arbovirus infection. bioRxiv, (doi: 10.1101/2024.02.23.581333)
Pinto, R. M. et al. (2023) BTN3A3 evasion promotes the zoonotic potential of influenza A viruses. Nature, 619(7969), pp. 338-347. (doi: 10.1038/s41586-023-06261-8) (PMID:37380775)
Sims, A. et al. (2023) Superinfection exclusion creates spatially distinct influenza virus populations. PLoS Biology, 21(2), e3001941. (doi: 10.1371/journal.pbio.3001941) (PMID:36757937) (PMCID:PMC9910727)
Mai, J., Stubbe, M., Hofmann, S., Masser, S., Dobner, T., Boutell, C. , Groitl, P. and Schreiner, S. (2022) PML alternative splice products differentially regulate HAdV productive infection. Microbiology Spectrum, 10(4), e0078522. (doi: 10.1128/spectrum.00785-22) (PMID:35699431) (PMCID:PMC9431499)
Herder, V. et al. (2021) Elevated temperature inhibits SARS-CoV-2 replication in respiratory epithelium independently of IFN-mediated innate immune defences. PLoS Biology, 19(12), e3001065. (doi: 10.1371/journal.pbio.3001065) (PMID:34932557) (PMCID:PMC8765667)
Charman, M. et al. (2021) Constitutive TRIM22 expression in the respiratory tract confers a pre-existing defence against influenza A virus infection. Frontiers in Cellular and Infection Microbiology, 11, 689707. (doi: 10.3389/fcimb.2021.689707) (PMID:34621686) (PMCID:PMC8490869)
Suzich, J. B., Cuddy, S. R., Baidas, H., Dochnal, S., Ke, E., Schinlever, A. R., Babnis, A., Boutell, C. and Cliffe, A. R. (2021) PML-NB-dependent type I interferon memory results in a restricted form of HSV latency. EMBO Reports, 22(9), e52547. (doi: 10.15252/embr.202152547) (PMID:34197022)
Kim, E. T., Dybas, J. M., Kulej, K., Reyes, E. D., Price, A. M., Akhtar, L. N., Orr, A., Garcia, B. A., Boutell, C. and Weitzman, M. D. (2021) Comparative proteomics identifies Schlafen 5 (SLFN5) as a herpes simplex virus restriction factor that suppresses viral transcription. Nature Microbiology, 6, pp. 234-245. (doi: 10.1038/s41564-020-00826-3) (PMID:33432153) (PMCID:PMC7856100)
Cuddy, S. R. et al. (2020) Neuronal hyperexcitability is a DLK-dependent trigger of Herpes Simplex Virus reactivation that can be induced by IL-1. eLife, 9, e58037. (doi: 10.7554/eLife.58037) (PMID:33350386) (PMCID:PMC7773336)
Stokes, S., Almire, F., Tatham, M. H., McFarlane, S., Mertens, P., Pondeville, E. and Boutell, C. (2020) The SUMOylation pathway suppresses arbovirus replication in Aedes aegypti cells. PLoS Pathogens, 16(12), e1009134. (doi: 10.1371/journal.ppat.1009134) (PMID:33351855) (PMCID:PMC7802965)
Collados Rodríguez, M. , Dybas, J. M., Hughes, J. , Weitzman, M. D. and Boutell, C. (2020) The HSV-1 ubiquitin ligase ICP0: modifying the cellular proteome to promote infection. Virus Research, 285, 198015. (doi: 10.1016/j.virusres.2020.198015) (PMID:32416261)
McFarlane, S. et al. (2019) The histone chaperone HIRA promotes the induction of host innate immune defences in response to HSV-1 infection. PLoS Pathogens, 15(3), e1007667. (doi: 10.1371/journal.ppat.1007667) (PMID:30901352) (PMCID:PMC6472835)
Alandijany, T., Roberts, A. P.E., Conn, K. L., Loney, C. , McFarlane, S., Orr, A. and Boutell, C. (2018) Distinct temporal roles for the promyelocytic leukaemia (PML) protein in the sequential regulation of intracellular host immunity to HSV-1 infection. PLoS Pathogens, 14(1), e1006769. (doi: 10.1371/journal.ppat.1006769) (PMID:29309427) (PMCID:PMC5757968)
Brown, J. R., Conn, K. L., Wasson, P., Charman, M., Tong, L., Grant, K., McFarlane, S. and Boutell, C. (2016) The SUMO Ligase Protein Inhibitor of Activated STAT 1 (PIAS1) is a constituent PML-NB protein that contributes to the intrinsic antiviral immune response to herpes simplex virus 1 (HSV-1). Journal of Virology, 90, 13. (doi: 10.1128/JVI.00426-16) (PMID:27099310) (PMCID:PMC4907222)
Conn, K. L., Wasson, P., McFarlane, S., Tong, L., Brown, J. R., Grant, K. G., Domingues, P. and Boutell, C. (2016) A novel role for Protein Inhibitor of Activated STAT 4 (PIAS4) in the restriction of herpes simplex virus 1 (HSV-1) by the cellular intrinsic antiviral immune response. Journal of Virology, 90(9), pp. 4807-4826. (doi: 10.1128/JVI.03055-15) (PMID:26937035)
Boutell, C. and Davido, D. J. (2015) A quantitative assay to monitor HSV-1 ICP0 ubiquitin ligase activity in vitro. Methods, 90, pp. 3-7. (doi: 10.1016/j.ymeth.2015.04.004) (PMID:25862948) (PMCID:PMC4655872)
Domingues, P., Bamford, C. G.G., Boutell, C. and McLauchlan, J. (2015) Inhibition of hepatitis C virus RNA replication by ISG15 does not require its conjugation to protein substrates by the HERC5 E3 ligase. Journal of General Virology, 96(11), pp. 3236-3242. (doi: 10.1099/jgv.0.000283) (PMID:26361997) (PMCID:PMC4806579)
Brennan, B. et al. (2015) In memoriam – Richard M. Elliott (1954–2015). Journal of General Virology, 96(8), pp. 1975-1978. (doi: 10.1099/jgv.0.000241) (PMID:26315040)
Busnadiego, I. et al. (2014) Host and viral determinants of Mx2 antiretroviral activity. Journal of Virology, 88(14), pp. 7738-7752. (doi: 10.1128/JVI.00214-14) (PMID:24760893) (PMCID:PMC4097781)
Everett, R.D., Boutell, C. , Pheasant, K., Cuchet-Lourenco, D. and Orr, A. (2014) Sequences related to SUMO interaction motifs in herpes simplex virus 1 protein ICP0 act cooperatively to stimulate virus infection. Journal of Virology, 88(5), pp. 2763-2774. (doi: 10.1128/JVI.03417-13) (PMID:24352468) (PMCID:PMC3958091)
Everett, R.D., Boutell, C. and Hale, B.G. (2013) Interplay between viruses and host sumoylation pathways. Nature Reviews Microbiology, 11(6), pp. 400-411. (doi: 10.1038/nrmicro3015) (PMID:23624814)
Boutell, C. and Everett, R. (2013) Regulation of alphaherpesvirus infections by the ICP0 family of proteins. Journal of General Virology, 94(3), pp. 465-481. (doi: 10.1099/vir.0.048900-0) (PMID:23239572)
Griffiths, S.J. et al. (2013) A systematic analysis of host factors reveals a Med23-interferon-λ regulatory axis against herpes simplex virus type 1 replication. PLoS Pathogens, 9(8), e1003514. (doi: 10.1371/journal.ppat.1003514) (PMID:23950709) (PMCID:PMC3738494)
Chaurushiya, M.S. et al. (2012) Viral E3 ubiquitin ligase-mediated degradation of a cellular E3: viral mimicry of a cellular phosphorylation mark targets the RNF8 FHA domain. Molecular Cell, 46(1), pp. 79-90. (doi: 10.1016/j.molcel.2012.02.004) (PMID:22405594) (PMCID:PMC3648639)
Grant, K., Grant, L., Tong, L. and Boutell, C. (2012) Depletion of intracellular zinc inhibits the ubiquitin ligase activity of viral regulatory protein ICP0 and restricts herpes simplex virus 1 replication in cell culture. Journal of Virology, 86(7), pp. 4029-4033. (doi: 10.1128/jvi.06962-11) (PMID:22278229) (PMCID:PMC3302540)
Vanni, E., Gatherer, D., Tong, L., Everett, R.D. and Boutell, C. (2012) Functional characterization of residues required for the herpes simplex virus 1 E3 ubiquitin ligase ICP0 to interact with the cellular E2 ubiquitin-conjugating enzyme UBE2D1 (UbcH5a). Journal of Virology, 86(11), pp. 6323-6333. (doi: 10.1128/jvi.07210-11) (PMID:22438555) (PMCID:PMC3372195)
Boutell, C. , Cuchet, D., Vanni, E., Orr, A., Glass, M., McFarlane, S. and Everett, R.D. (2011) A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathogens, 7(9), e1002245. (doi: 10.1371/journal.ppat.1002245) (PMID:21949651) (PMCID:PMC3174244)
Cuchet-Lourenço, D., Boutell, C. , Lukashchuk, V., Grant, K., Sykes, A. , Murray, J., Orr, A. and Everett, R.D. (2011) SUMO pathway dependent recruitment of cellular repressors to herpes simplex virus type 1 genomes. PLoS Pathogens, 7(7), e1002123. (doi: 10.1371/journal.ppat.1002123) (PMID:21779164) (PMCID:PMC3136452)
Lilley, C.E., Chaurushiya, M.S., Boutell, C. , Everett, R.D. and Weitzman, M.D. (2011) The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathogens, 7(6), e1002084. (doi: 10.1371/journal.ppat.1002084) (PMID:20075863) (PMCID:PMC2837166)
Smith, M.C., Boutell, C. and Davido, D.J. (2011) HSV-1 ICP0: paving the way for viral replication. Future Virology, 6(4), pp. 421-429. (doi: 10.2217/FVL.11.24) (PMID:21765858) (PMCID:PMC313393)
Everett, R.D., Boutell, C., McNair, C., Grant, L. and Orr, A. (2010) Comparison of the biological and biochemical activities of several members of the alphaherpesvirus ICP0 family of proteins. Journal of Virology, 84(7), pp. 3476-3487. (doi: 10.1128/JVI.02544-09) (PMID:20106921) (PMCID:PMC2838103)
Lilley, C.E., Chaurushiya, M.S., Boutell, C. , Landry, S., Suh, J., Panier, S., Everett, R.D., Stewart, G.S., Durocher, D. and Weitzman, M.D. (2010) A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO Journal, 29(5), pp. 943-955. (doi: 10.1038/emboj.2009.400) (PMID:22405594) (PMCID:PMC3648639)
Antrobus, R., Grant, K., Gangadharan, B., Chittenden, D., Everett, R.D., Zitzmann, N. and Boutell, C. (2009) Proteomic analysis of cells in the early stages of herpes simplex virus type-1 infection reveals widespread changes in the host cell proteome. Proteomics, 9(15), pp. 3913-3927. (doi: 10.1002/pmic.200900207) (PMID:19670248)
Morris, J. R. et al. (2009) The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature, 462(7275), pp. 886-890. (doi: 10.1038/nature08593) (PMID:20016594)
Antrobus, R. and Boutell, C. (2008) Identification of a novel higher molecular weight isoform of USP7/HAUSP that interacts with the Herpes simplex virus type-1 immediate early protein ICP0. Virus Research, 137(1), pp. 64-71. (doi: 10.1016/j.virusres.2008.05.017)
Boutell, C., Everett, R.D., Hilliard, J., Schaffer, P., Orr, A. and Davido, D. (2008) Herpes simplex virus type 1 ICP0 phosphorylation mutants impair the E3 ubiquitin ligase activity of ICP0 in a cell type-dependent manner. Journal of Virology, 82(21), pp. 10647-10656. (doi: 10.1128/JVI.01063-08)
Kummer, M., Turza, N.M., Muhl-Zurbes, P., Lechmann, M., Boutell, C. , Coffin, R.S., Everett, R.D., Steinkasserer, A. and Prechtel, A.T. (2007) Herpes simplex virus type 1 induces CD83 degradation in mature dendritic cells with immediate-early kinetics via the cellular proteasome. Journal of Virology, 81(12), pp. 6326-6338. (doi: 10.1128/jvi.02327-06)
Morris, J.R., Pangon, L., Boutell, C. , Katagiri, T., Keep, N.H. and Solomon, E. (2006) Genetic analysis of BRCA1 ubiquitin ligase activity and its relationship to breast cancer susceptibility. Human Molecular Genetics, 15(4), pp. 599-606. (doi: 10.1093/hmg/ddi476)
Boutell, C. , Canning, M., Orr, A. and Everett, R.D. (2005) Reciprocal activities between herpes simplex virus type 1 regulatory protein ICP0, a ubiquitin E3 ligase, and ubiquitin-specific protease USP7. Journal of Virology, 79(19), pp. 12342-12354. (doi: 10.1128/jvi.79.19.12342-12354.2005)
Meulmeester, E., Maurice, M., Boutell, C. , Teunisse, A., Ovaa, H., Abraham, T., Dirks, R. and Jochemsen, A. (2005) Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Molecular Cell, 18(5), pp. 565-576. (doi: 10.1016/j.molcel.2005.04.024)
Boutell, C. and Everett, R.D. (2004) Herpes simplex virus type 1 infection induces the stabilization of p53 in a USP7- and ATM-independent manner. Journal of Virology, 78(15), pp. 8068-8077. (doi: 10.1128/jvi.78.15.8068-8077.2004)
Everett, R.D., Boutell, C. and Orr, A. (2004) Phenotype of a herpes simplex virus type 1 mutant that fails to express immediate-early regulatory protein ICP0. Journal of Virology, 78(4), pp. 1763-1774. (doi: 10.1128/jvi.78.4.1763-1774.2004)
Canning, M., Boutell, C.J. , Parkinson, J. and Everett, R.D. (2004) A RING finger ubiquitin ligase is protected from autocatalyzed ubiquitination and degradation by binding to ubiquitin-specific protease USP7. Journal of Biological Chemistry, 279(37), pp. 38160-38168. (doi: 10.1074/jbc.M402885200)
Boutell, C. and Everett, R.D. (2003) The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and ubiquitinates p53. Journal of Biological Chemistry, 278(38), pp. 36596-36602. (doi: 10.1074/jbc.M300776200)
Boutell, C.J. , Orr, A. and Everett, R.D. (2003) PML residue lysine 160 is required for the degradation of PML induced by herpes simplex virus type 1 regulatory protein ICP0. Journal of Virology, 77(16), pp. 8686-8694. (doi: 10.1128/jvi.77.16.8686-8694.2003)
Engelhardt, O.G., Boutell, C.J. , Orr, A., Ullrich, E., Haller, O. and Everett, R.D. (2003) The homeodomain-interacting kinase PKM (HIPK-2) modifies ND10 through both its kinase domain and a SUMO-1 interaction motif and alters the posttranslational modification of PML. Experimental Cell Research, 283(1), pp. 36-50. (doi: 10.1016/s0014-4827(02)00025-3)
Boutell, C. , Sadis, S. and Everett, R.D. (2002) Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases In vitro. Journal of Virology, 76(2), pp. 841-850. (doi: 10.1128/jvi.76.2.841-850.2002)
Kirkitadze, M.D., Barlow, P.N., Price, N.C., Kelly, S.M. , Boutell, C.J. , Rixon, F.J. and McClelland, D.A. (1998) The herpes simplex virus triplex protein, VP23, exists as a molten globule. Journal of Virology, 72(12), pp. 10066-10072.
Kazushige, I., Clark, J.C., Shaw-White, J.R., Stahlman, M.T., Boutell, C.J. and Whitsett, J.A. (1995) Gene structure and expression of human thyroid transcription factor-1 in respiratory epithelial cells. Journal of Biological Chemistry, 270(14), pp. 8108-8114. (doi: 10.1074/jbc.270.14.8108)
Grants
Grants and Awards listed are those received whilst working with the University of Glasgow.
- MonkeyPox - Rapid Response
Biotechnology and Biological Sciences Research Council
2022 - 2023
- Dissecting innate immune determinants of severity and resolution in a longitudinal study of COVID-19
UK Research and Innovation
2020 - 2022
- Quinquennial Core Funds
Medical Research Council
2016 - 2021
- The role of ubiquitin and ubiquitin-like proteins during viral infection
Medical Research Council
2013 - 2016
Research datasets
2022
Sims, A., Burgess Tornaletti, L., Jasim, S., Pirillo, C., Devlin, R., Hirst, J., Loney, C. , Wojtus, J., Sloan, E., Thorley, L., Boutell, C. , Roberts, E. and Hutchinson, E. (2022) Superinfection exclusion creates spatially distinct influenza virus populations. [Data Collection]
2020
Stokes, S., Almire, F., Tatham, M., McFarlane, S., Mertens, P., Pondeville, E. and Boutell, C. (2020) The SUMOylation pathway suppresses arbovirus replication in Aedes aegypti cells. [Data Collection]
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