Uncovering viral RNA–host cell interactions on a proteome-wide scale

Trends in Biochemical Sciences - Tập 47 - Trang 23-38 - 2022
Louisa Iselin1,2, Natasha Palmalux3, Wael Kamel2,3, Peter Simmonds1, Shabaz Mohammed2,4,5, Alfredo Castello2,3
1Nuffield Department of Medicine, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, OX1 3SY, UK
2Department of Biochemistry, University of Oxford, South Parks Road, OX1 3QU Oxford, UK
3MRC-University of Glasgow Centre for Virus Research, 464 Bearsden Road, Glasgow G61 1QH, Scotland, UK
4Chemistry Research Laboratory, University of Oxford, Mansfield Road, Oxford OX1 3TA, UK
5The Rosalind Franklin Institute, Oxfordshire OX11 0FA, UK

Tài liệu tham khảo

Garcia-Moreno, 2018, Unconventional RNA-binding proteins step into the virus–host battlefront, Wiley Interdiscip. Rev. RNA, 9, 10.1002/wrna.1498 Li, 2011, Diverse roles of host RNA-binding proteins in RNA virus replication, RNA Biol., 8, 305, 10.4161/rna.8.2.15391 Nagy, 2012, The dependence of viral RNA replication on co-opted host factors, Nat. Rev. Microbiol., 10, 137, 10.1038/nrmicro2692 Girardi, 2021, Roadblocks and fast tracks: how RNA binding proteins affect the viral RNA journey in the cell, Semin. Cell Dev. Biol., 111, 86, 10.1016/j.semcdb.2020.08.006 Dicker, 2021, The importance of virion-incorporated cellular RNA-binding proteins in viral particle assembly and infectivity, Semin. Cell Dev. Biol., 111, 108, 10.1016/j.semcdb.2020.08.002 Barbalat, 2011, Nucleic acid recognition by the innate immune system, Annu. Rev. Immunol., 29, 185, 10.1146/annurev-immunol-031210-101340 Rehwinkel, 2013, Targeting the viral Achilles’ heel: recognition of 5′-triphosphate RNA in innate anti-viral defence, Curr. Opin. Microbiol., 16, 485, 10.1016/j.mib.2013.04.009 Vladimer, 2014, IFITs: emerging roles as key anti-viral proteins, Front. Immunol., 5, 94, 10.3389/fimmu.2014.00094 Castello, 2012, Insights into RNA biology from an atlas of mammalian mRNA-binding proteins, Cell, 149, 1393, 10.1016/j.cell.2012.04.031 Hentze, 2018, A brave new world of RNA-binding proteins, Nat. Rev. Mol. Cell Biol., 19, 327, 10.1038/nrm.2017.130 Queiroz, 2019, Comprehensive identification of RNA–protein interactions in any organism using orthogonal organic phase separation (OOPS), Nat. Biotechnol., 37, 169, 10.1038/s41587-018-0001-2 Trendel, 2019, The human RNA-binding proteome and its dynamics during translational arrest, Cell, 176, 391, 10.1016/j.cell.2018.11.004 Asencio, 2018, Silica-based solid-phase extraction of cross-linked nucleic acid–bound proteins, Life Sci. Alliance, 1, 10.26508/lsa.201800088 Urdaneta, 2019, Purification of cross-linked RNA-protein complexes by phenol-toluol extraction, Nat. Commun., 10, 990, 10.1038/s41467-019-08942-3 Gack, 2007, TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity, Nature, 446, 916, 10.1038/nature05732 Li, 2017, TRIM25 enhances the antiviral action of zinc-finger antiviral protein (ZAP), PLoS Pathog., 13, 10.1371/journal.ppat.1006145 Zheng, 2017, TRIM25 is required for the antiviral activity of zinc finger antiviral protein, J. Virol., 91, 10.1128/JVI.00088-17 Manokaran, 2015, Dengue subgenomic RNA binds TRIM25 to inhibit interferon expression for epidemiological fitness, Science, 350, 217, 10.1126/science.aab3369 Castello, 2016, Comprehensive identification of RNA-binding domains in human cells, Mol. Cell, 63, 696, 10.1016/j.molcel.2016.06.029 Garcia-Moreno, 2019, System-wide profiling of RNA-binding proteins uncovers key regulators of virus infection, Mol. Cell, 74, 196, 10.1016/j.molcel.2019.01.017 Kwon, 2013, The RNA-binding protein repertoire of embryonic stem cells, Nat. Struct. Mol. Biol., 20, 1122, 10.1038/nsmb.2638 Choudhury, 2017, RNA-binding activity of TRIM25 is mediated by its PRY/SPRY domain and is required for ubiquitination, BMC Biol., 15, 105, 10.1186/s12915-017-0444-9 Van Ende, 2020, Single and combined methods to specifically or bulk-purify RNA–protein complexes, Biomolecules, 10, 1160, 10.3390/biom10081160 Ortín, 2015, The RNA synthesis machinery of negative-stranded RNA viruses, Virology, 479–480, 532, 10.1016/j.virol.2015.03.018 Kim, 2020, Discovery of widespread host protein interactions with the pre-replicated genome of CHIKV using VIR-CLASP, Mol. Cell, 78, 624, 10.1016/j.molcel.2020.04.013 Kamel, 2021, Global analysis of protein-RNA interactions in SARS-CoV-2-infected cells reveals key regulators of infection, Mol. Cell, 81, 2851, 10.1016/j.molcel.2021.05.023 Knoener, 2021, Identification of host proteins differentially associated with HIV-1 RNA splice variants, Elife, 10, 10.7554/eLife.62470 Pashev, 1991, Crosslinking proteins to nucleic acids by ultraviolet laser irradiation, Trends Biochem. Sci., 16, 323, 10.1016/0968-0004(91)90133-G Beckmann, 2016, The expanding universe of ribonucleoproteins: of novel RNA-binding proteins and unconventional interactions, Pflugers Arch., 468, 1029, 10.1007/s00424-016-1819-4 Kramer, 2014, Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNA-binding proteins, Nat. Methods, 11, 1064, 10.1038/nmeth.3092 Bach-Pages, 2020, Discovering the RNA-binding proteome of plant leaves with an improved RNA interactome capture method, Biomolecules, 10, 661, 10.3390/biom10040661 Favre, 1986, 4-Thiouridine photosensitized RNA-protein crosslinking in mammalian cells, Biochem. Biophys. Res. Commun., 141, 847, 10.1016/S0006-291X(86)80250-9 Baltz, 2012, The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts, Mol. Cell, 46, 674, 10.1016/j.molcel.2012.05.021 He, 2016, High-resolution mapping of RNA-binding regions in the nuclear proteome of embryonic stem cells, Mol. Cell, 64, 416, 10.1016/j.molcel.2016.09.034 Hafner, 2010, Transcriptome-wide Identification of RNA-binding protein and microRNA target sites by PAR-CLIP, Cell, 141, 129, 10.1016/j.cell.2010.03.009 Hoffman, 2015, Formaldehyde crosslinking: a tool for the study of chromatin complexes, J. Biol. Chem., 290, 26404, 10.1074/jbc.R115.651679 Sutherland, 2008, Enhanced immune system regeneration in humans following allogeneic or autologous hemopoietic stem cell transplantation by temporary sex steroid blockade, Clin. Cancer Res., 14, 1138, 10.1158/1078-0432.CCR-07-1784 Singh, 2012, The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus, Cell, 151, 750, 10.1016/j.cell.2012.10.007 Hu, 2015, Biological chromodynamics: a general method for measuring protein occupancy across the genome by calibrating ChIP-seq, Nucleic Acids Res., 43 Knoener, 2017, Elucidating the in vivo interactome of HIV-1 RNA by hybridization capture and mass spectrometry, Sci. Rep., 7, 16965, 10.1038/s41598-017-16793-5 Lee, 2021, The SARS-CoV-2 RNA interactome, Mol. Cell, 81, 2838, 10.1016/j.molcel.2021.04.022 Phillips, 2016, Identification of proteins bound to dengue viral RNA in vivo reveals new host proteins important for virus replication, mBio, 7, 10.1128/mBio.01865-15 Schmidt, 2021, The SARS-CoV-2 RNA–protein interactome in infected human cells, Nat. Microbiol., 6, 339, 10.1038/s41564-020-00846-z Ooi, 2019, An RNA-centric dissection of host complexes controlling flavivirus infection, Nat. Microbiol., 4, 2369, 10.1038/s41564-019-0518-2 Labeau, 2021, Characterization and functional interrogation of SARS-CoV-2 RNA interactome, bioRxiv Flynn, 2021, Discovery and functional interrogation of SARS-CoV- 2 RNA-host protein interactions, Cell, 184, 2394, 10.1016/j.cell.2021.03.012 Rogell, 2017, Specific RNP capture with antisense LNA/DNA mixmers, RNA, 23, 1290, 10.1261/rna.060798.117 Perez-Perri, 2018, Discovery of RNA-binding proteins and characterization of their dynamic responses by enhanced RNA interactome capture, Nat. Commun., 9, 4408, 10.1038/s41467-018-06557-8 Perez-Perri, 2021, Global analysis of RNA-binding protein dynamics by comparative and enhanced RNA interactome capture, Nat. Protoc., 16, 27, 10.1038/s41596-020-00404-1 Lenarcic, 2013, Thiouracil cross-linking mass spectrometry: a cell-based method to identify host factors involved in viral amplification, J. Virol., 87, 8697, 10.1128/JVI.00950-13 Viktorovskaya, 2016, Identification of RNA binding proteins associated with dengue virus RNA in infected cells reveals temporally distinct host factor requirements, PLoS Negl. Trop. Dis., 10, 10.1371/journal.pntd.0004921 LaPointe, 2018, Identification and characterization of sindbis virus RNA-host protein interactions, J. Virol., 92, 10.1128/JVI.02171-17 Gebhart, 2020, Comparative analyses of alphaviral RNA: protein complexes reveals conserved host-pathogen interactions, PLoS One, 15, 10.1371/journal.pone.0238254 Kula, 2011, Characterization of the HIV-1 RNA associated proteome identifies Matrin 3 as a nuclear cofactor of Rev function, Retrovirology, 8, 60, 10.1186/1742-4690-8-60 Ward, 2014, Identification of dengue RNA binding proteins using RNA chromatography and quantitative mass spectrometry, Methods Mol. Biol., 1138, 253, 10.1007/978-1-4939-0348-1_16 Liao, 2018, Identification and characterization of host proteins bound to dengue virus 3′ UTR reveal an antiviral role for quaking proteins, RNA, 24, 803, 10.1261/rna.064006.117 Marchand, 2011, Identification of protein partners of the human immunodeficiency virus 1 tat/rev exon 3 leads to the discovery of a new HIV-1 splicing regulator, protein hnRNP K, RNA Biol., 8, 325, 10.4161/rna.8.2.13984 Yoon, 2012, MS2-TRAP (MS2-tagged RNA affinity purification): tagging RNA to identify associated miRNAs, Methods, 58, 81, 10.1016/j.ymeth.2012.07.004 Oberg, 2009, Statistical design of quantitative mass spectrometry-based proteomic experiments, J. Proteome Res., 8, 2144, 10.1021/pr8010099 Bantscheff, 2012, Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present, Anal. Bioanal. Chem., 404, 939, 10.1007/s00216-012-6203-4 Lunde, 2007, RNA-binding proteins: modular design for efficient function, Nat. Rev. Mol. Cell Biol., 8, 479, 10.1038/nrm2178 Onomoto, 2014, Antiviral innate immunity and stress granule responses, Trends Immunol., 35, 420, 10.1016/j.it.2014.07.006 Bidet, 2014, G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA, PLoS Pathog., 10, 10.1371/journal.ppat.1004242 Horos, 2019, The small non-coding vault RNA1-1 acts as a riboregulator of autophagy, Cell, 176, 1054, 10.1016/j.cell.2019.01.030 Lemaire, 2008, Mechanism of PKR Activation by dsRNA, J. Mol. Biol., 381, 351, 10.1016/j.jmb.2008.05.056 Gunnery, 1992, Tat-responsive region RNA of human immunodeficiency virus type 1 stimulates protein synthesis in vivo and in vitro: relationship between structure and function, Proc. Natl. Acad. Sci. U. S. A., 89, 11557, 10.1073/pnas.89.23.11557 Dickson, 2011, Strategies for viral RNA stability: live long and prosper, Trends Genet., 27, 286, 10.1016/j.tig.2011.04.003 Gao, 2002, Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein, Science, 297, 1703, 10.1126/science.1074276 Balistreri, 2014, The host nonsense-mediated mRNA decay pathway restricts mammalian RNA virus replication, Cell Host Microbe, 16, 403, 10.1016/j.chom.2014.08.007 Fischer, 2020, Structure-mediated RNA decay by UPF1 and G3BP1, Mol. Cell, 78, 70, 10.1016/j.molcel.2020.01.021 West, 2004, Human 5′ → 3′ exonuclease Xm2 promotes transcription termination at co-transcriptional cleavage sites, Nature, 432, 522, 10.1038/nature03035 Miki, 2013, The multifunctional RNase XRN2, Biochem. Soc. Trans., 41, 825, 10.1042/BST20130001 Sedano, 2014, Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2, Cell Host Microbe, 16, 257, 10.1016/j.chom.2014.07.006 Abernathy, 2015, Emerging roles for RNA degradation in viral replication and antiviral defense, Virology, 479–480, 600, 10.1016/j.virol.2015.02.007 Akiyama, 2016, Zika virus produces noncoding RNAs using a multi-pseudoknot structure that confounds a cellular exonuclease, Science, 354, 1148, 10.1126/science.aah3963 Charley, 2016, Standing your ground to exoribonucleases: function of flavivirus long non-coding RNAs, Virus Res., 212, 70, 10.1016/j.virusres.2015.09.009 Molleston, 2017, Attacked from all sides: RNA decay in antiviral defense, Viruses, 9, 2, 10.3390/v9010002 Walsh, 2019, Exploitation of cytoskeletal networks during early viral infection, Trends Microbiol., 27, 39, 10.1016/j.tim.2018.06.008 Caudron-Herger, 2019, R-DeeP: proteome-wide and quantitative identification of RNA-dependent proteins by density gradient ultracentrifugation, Mol. Cell, 75, 184, 10.1016/j.molcel.2019.04.018 Doller, 2013, RNA-dependent association with myosin IIA promotes F-actin-guided trafficking of the ELAV-like protein HuR to polysomes, Nucleic Acids Res., 41, 9152, 10.1093/nar/gkt663 Guo, 2016, Porcine reproductive and respiratory syndrome virus utilizes nanotubes for intercellular spread, J. Virol., 90, 5163, 10.1128/JVI.00036-16 Shao, 2021, Non-muscle myosin heavy chain 9 is a critical factor for infectious pancreatic necrosis virus cellular entry, Aquaculture, 533, 10.1016/j.aquaculture.2020.736138 Martinez, 2016, Intercellular extensions are induced by the alphavirus structural proteins and mediate virus transmission, PLoS Pathog., 12, 10.1371/journal.ppat.1006061 Roberts, 2015, Influenza A virus uses intercellular connections to spread to neighboring cells, J. Virol., 89, 1537, 10.1128/JVI.03306-14 Kumar, 2017, Influenza virus exploits tunneling nanotubes for cell-to-cell spread, Sci. Rep., 7, 40360, 10.1038/srep40360 Schwarzl Guo, 2019, Human papillomavirus 16 oncoprotein E7 retards mitotic progression by blocking Mps1-MAP4 signaling cascade, Oncogene, 38, 5959, 10.1038/s41388-019-0851-1 Gallo, 2012, Knockdown of MAP4 and DNAL1 produces a post-fusion and pre-nuclear translocation impairment in HIV-1 replication, Virology, 422, 13, 10.1016/j.virol.2011.09.015 de Conto, 2012, Highly dynamic microtubules improve the effectiveness of early stages of human influenza A/NWS/33 virus infection in LLC-MK2 cells, PLoS One, 7, 10.1371/journal.pone.0041207 Davis, 2014, DNA-PK: a dynamic enzyme in a versatile DSB repair pathway, DNA Repair (Amst), 17, 21, 10.1016/j.dnarep.2014.02.020 Luftig, 2014, Viruses and the DNA damage response: activation and antagonism, Annu. Rev. Virol., 1, 605, 10.1146/annurev-virology-031413-085548 Ryan, 2016, Activation of the DNA damage response by RNA viruses, Biomolecules, 6, 2, 10.3390/biom6010002 Ferguson, 2012, DNA-PK is a DNA sensor for IRF-3-dependent innate immunity, Elife, 1, 10.7554/eLife.00047 Sun, 2020, DNA-PK deficiency potentiates cGAS-mediated antiviral innate immunity, Nat. Commun., 11, 6182, 10.1038/s41467-020-19941-0 Thompson, 2014, Interferon γ-inducible protein (IFI) 16 transcriptionally regulates type I interferons and other interferon-stimulated genes and controls the interferon response to both DNA and RNA viruses, J. Biol. Chem., 289, 23568, 10.1074/jbc.M114.554147 Ni, 2016, New insights into the structural basis of DNA recognition by HINa and HINb domains of IFI16, J. Mol. Cell Biol., 8, 51, 10.1093/jmcb/mjv053 Lamaa, 2016, A novel cytoprotective function for the DNA repair protein Ku in regulating p53 mRNA translation and function, EMBO Rep., 17, 508, 10.15252/embr.201541181 Silvera, 2006, Effect of Ku proteins on IRES-mediated translation, Biol. Cell., 98, 353, 10.1042/BC20050060 Rüdiger, 2019, Multiscale modeling of influenza a virus replication in cell cultures predicts infection dynamics for highly different infection conditions, PLoS Comput. Biol., 15, 10.1371/journal.pcbi.1006819 Sawicki, 1971, On the differential cytotoxicity of actinomycin D, J. Cell Biol., 50, 746, 10.1083/jcb.50.3.746