BUD23-TRMT112 interacts with the L protein of Borna disease virus and mediates the chromosomal tethering of viral ribonucleoproteins.
RNA methyltransferase
bornavirus
bud23
chromosomal tethering
host-viral interaction
proximity-dependent biotinylation
Journal
Microbiology and immunology
ISSN: 1348-0421
Titre abrégé: Microbiol Immunol
Pays: Australia
ID NLM: 7703966
Informations de publication
Date de publication:
Nov 2021
Nov 2021
Historique:
revised:
05
07
2021
received:
27
05
2021
accepted:
17
07
2021
pubmed:
30
7
2021
medline:
16
11
2021
entrez:
29
7
2021
Statut:
ppublish
Résumé
Persistent intranuclear infection is an uncommon infection strategy among RNA viruses. However, Borna disease virus 1 (BoDV-1), a nonsegmented, negative-strand RNA virus, maintains viral infection in the cell nucleus by forming structured aggregates of viral ribonucleoproteins (vRNPs), and by tethering these vRNPs onto the host chromosomes. To better understand the nuclear infection strategy of BoDV-1, we determined the host protein interactors of the BoDV-1 large (L) protein. By proximity-dependent biotinylation, we identified several nuclear host proteins interacting with BoDV-1 L, one of which is TRMT112, a partner of several methyltransferases (MTases). TRMT112 binds with BoDV-1 L at the RNA-dependent RNA polymerase domain, together with BUD23, an 18S ribosomal RNA MTase and 40S ribosomal maturation factor. We then discovered that BUD23-TRMT112 mediates the chromosomal tethering of BoDV-1 vRNPs, and that the MTase activity is necessary in the tethering process. These findings provide us a better understanding on how nuclear host proteins assist the chromosomal tethering of BoDV-1, as well as new prospects of host-viral interactions for intranuclear infection strategy of orthobornaviruses.
Identifiants
pubmed: 34324219
doi: 10.1111/1348-0421.12934
doi:
Substances chimiques
Ribonucleoproteins
0
Viral Proteins
0
Methyltransferases
EC 2.1.1.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
492-504Subventions
Organisme : Ministry of Education, Culture, Sports, Science and Technology (MEXT) KAKENHI
ID : 16H06429
Organisme : Ministry of Education, Culture, Sports, Science and Technology (MEXT) KAKENHI
ID : 16K21723
Organisme : Ministry of Education, Culture, Sports, Science and Technology (MEXT) KAKENHI
ID : 16H06430
Organisme : Japan Society for the Promotion of Science (JSPS) KAKENHI
ID : 19K22530
Organisme : Japan Society for the Promotion of Science (JSPS) KAKENHI
ID : 20H05682
Organisme : JSPS Core-to-Core Program
Organisme : Joint Usage/Research Center Program on inFront, Kyoto University
Informations de copyright
© 2021 The Societies and John Wiley & Sons Australia, Ltd.
Références
Maes P, Amarasinghe GK, Ayllón MA, et al. Taxonomy of the order Mononegavirales: second update 2018. Arch Virol. 2019;164:1233-44.
Briese T, De La Torre JC, Lewis A, Ludwig H, Lipkin WI. Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proc Natl Acad Sci USA. 1992;89:11486-9.
Niller HH, Angstwurm K, Rubbenstroth D, et al. 2020) Zoonotic spillover infections with Borna disease virus 1 leading to fatal human encephalitis, 1999-2019: an epidemiological investigation. Lancet Infect Dis. 2020 Apr;20:467-77.
Kistler AL, Gancz A, Clubb S, et al. Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virol J. 2008;5:88.
Hyndman TH, Shilton CM, Stenglein MD, Wellehan JFX Jr. Divergent bornaviruses from Australian carpet pythons with neurological disease date the origin of extant Bornaviridae prior to the end-Cretaceous extinction. PLoS Pathog. 2018;14:e1006881.
Matsumoto Y, Hayashi Y, Omori H, et al. Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. Cell Host Microbe. 2012;11:492-503.
Hirai Y, Hirano Y, Matsuda A, Hiraoka Y, Honda T, Tomonaga K. Borna disease virus assembles porous cage-like viral factories in the nucleus. J Biol Chem. 2016;291:25789-98.
Planz O, Pleschka S, Oesterle K, et al. Borna disease virus nucleoprotein interacts with the CDC2-cyclin B1 complex. J Virol. 2003;77:11186-92.
Hirai Y, Honda T, Makino A, Watanabe Y, Tomonaga K. X-linked RNA-binding motif protein (RBMX) is required for the maintenance of Borna disease virus nuclear viral factories. J Gen Virol. 2015;96:3198-203.
Hayashi Y, Horie M, Daito T, Honda T, Ikuta K, Tomonaga K. Heat shock cognate protein 70 controls Borna disease virus replication via interaction with the viral non-structural protein X. Microbes Infect. 2009;11:394-402.
Poch O, Blumberg BM, Bougueleret L, Tordo N. Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol. 1990;71(Pt 5):1153-62.
Liang B, Li Z, Jenni S, et al. Structure of the L protein of vesicular stomatitis virus from electron cryomicroscopy. Cell. 2015;162:314-27.
Ogino T, Banerjee AK. Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol Cell. 2007;25:85-97.
Cubitt B, Oldstone C, De La Torre JC. Sequence and genome organization of Borna disease virus. J Virol. 1994;68:1382-96.
Horie M, Kobayashi Y, Honda T, et al. An RNA-dependent RNA polymerase gene in bat genomes derived from an ancient negative-strand RNA virus. Sci Rep. 2016;6:25873.
Gillen J, Nita-Lazar A. Experimental analysis of viral-host interactions. Front Physiol. 2019;10:425.
Varnaite R, Macneill SA. Meet the neighbors: mapping local protein interactomes by proximity-dependent labeling with BioID. Proteomics. 2016;16:2503-18.
Roux KJ, Kim DI, Raida M, Burke B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol. 2012;196:801-10.
Haag S, Kretschmer J, Bohnsack MT. WBSCR22/Merm1 is required for late nuclear pre-ribosomal RNA processing and mediates N7-methylation of G1639 in human 18S rRNA. RNA. 2015;21:180-7.
White J, Li Z, Sardana R, Bujnicki JM, Marcotte EM, Johnson AW. Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol Cell Biol. 2008;28:3151-61.
Ounap K, Kasper L, Kurg A, Kurg R. The human WBSCR22 protein is involved in the biogenesis of the 40S ribosomal subunits in mammalian cells. PLoS One. 2013;8:e75686.
Cheah JS, Yamada S. A simple elution strategy for biotinylated proteins bound to streptavidin conjugated beads using excess biotin and heat. Biochem Biophys Res Commun. 2017;493:1522-7.
Pandolfini L, Barbieri I, Bannister AJ, et al. METTL1 Promotes let-7 microRNA processing via m7G methylation. Mol Cell. 2019;74(6):1278-1290.e9.
Lin S, Liu Q, Lelyveld VS, Choe J, Szostak JW, Gregory RI. Mettl1/Wdr4-mediated m(7)G tRNA methylome is required for normal mRNA translation and embryonic stem cell self-renewal and differentiation. Mol Cell. 2018;71:244-55, e5.
Szklarczyk D, Gable AL, Lyon D, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607-13.
Kim DI, Jensen SC, Noble KA, et al. An improved smaller biotin ligase for BioID proximity labeling. Mol Biol Cell. 2016;27:1188-96.
Ounap K, Leetsi L, Matsoo M, Kurg R. The stability of ribosome biogenesis factor WBSCR22 is regulated by interaction with TRMT112 via ubiquitin-proteasome pathway. PLoS One. 2015;10:e0133841.
Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20:1160-6.
Jangani M, Poolman TM, Matthews L, et al. The methyltransferase WBSCR22/Merm1 enhances glucocorticoid receptor function and is regulated in lung inflammation and cancer. J Biol Chem. 2014;289:8931-46.
Wan Q., Song D., Li H., He M.L. (2020) Stress proteins: the biological functions in virus infection, present and challenges for target-based antiviral drug development. Signal Transduct Target Ther 5: 125.
Noton SL, Deflube LR, Tremaglio CZ, Fearns R. The respiratory syncytial virus polymerase has multiple RNA synthesis activities at the promoter. PLoS Pathog. 2012;8:e1002980.
Munday DC, Wu W, Smith N, et al. Interactome analysis of the human respiratory syncytial virus RNA polymerase complex identifies protein chaperones as important cofactors that promote L-protein stability and RNA synthesis. J Virol. 2015;89:917-30.
Tchesnokov EP, Raeisimakiani P, Ngure M, Marchant D, Gotte M. Recombinant RNA-dependent RNA polymerase complex of ebola virus. Sci Rep. 2018;8:3970.
Gardino AK, Yaffe MB. 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol. 2011;22:688-95.
Hermeking H, Benzinger A. 14-3-3 proteins in cell cycle regulation. Semin Cancer Biol. 2006;16:183-92.
Kino T, Gragerov A, Valentin A, et al. Vpr protein of human immunodeficiency virus type 1 binds to 14-3-3 proteins and facilitates complex formation with Cdc25C: implications for cell cycle arrest. J Virol. 2005;79:2780-7.
Chan YK, Gack MU. A phosphomimetic-based mechanism of dengue virus to antagonize innate immunity. Nat Immunol. 2016;17:523-30.
Riedl W, Acharya D, Lee JH, et al. Zika virus NS3 mimics a cellular 14-3-3-binding motif to antagonize RIG-I- and MDA5-mediated innate immunity. Cell Host Microbe. 2019;26:493-503.e6.
Li D, Wang XZ, Ding J, Yu JP. NACA as a potential cellular target of hepatitis B virus preS1 protein. Dig Dis Sci. 2005;50:1156-60.
Banerjee A, Benjamin R, Balakrishnan K, Ghosh P, Banerjee S. Human protein Staufen-2 promotes HIV-1 proliferation by positively regulating RNA export activity of viral protein Rev. Retrovirology. 2014;11:18.
Mouland AJ, Mercier J, Luo M, Bernier L, Desgroseillers L, Cohen EA. The double-stranded RNA-binding protein Staufen is incorporated in human immunodeficiency virus type 1: evidence for a role in genomic RNA encapsidation. J Virol. 2000;74:5441-51.
Doll A, Grzeschik KH. Characterization of two novel genes, WBSCR20 and WBSCR22, deleted in Williams-Beuren syndrome. Cytogenet Cell Genet. 2001;95:20-7.
Nakazawa Y, Arai H, Fujita N. The novel metastasis promoter Merm1/Wbscr22 enhances tumor cell survival in the vasculature by suppressing Zac1/p53-dependent apoptosis. Cancer Res. 2011;71:1146-55.
Agresti A, Scaffidi P, Riva A, Caiolfa VR, Bianchi ME. (2005) GR and HMGB1 interact only within chromatin and influence each other's residence time. Mol Cell 18: 109-21.
Agris PF, Sierzputowska-Gracz H, Smith C. Transfer RNA contains sites of localized positive charge: carbon NMR studies of [13C]methyl-enriched Escherichia coli and yeast tRNAPhe. Biochemistry. 1986;25:5126-31.
Wintermeyer W, Zachau HG. Tertiary structure interactions of 7-methylguanosine in yeast tRNA Phe as studied by borohydride reduction. FEBS Lett. 1975;58:306-9.
Robertus JD, Ladner JE, Finch JT, et al. Structure of yeast phenylalanine tRNA at 3 A resolution. Nature. 1974;250:546-51.
Oliva R, Cavallo L, Tramontano A. Accurate energies of hydrogen bonded nucleic acid base pairs and triplets in tRNA tertiary interactions. Nucleic Acids Res. 2006;34:865-79.
Lu M, Xue M, Wang HT, et al. Nonsegmented negative-sense RNA viruses utilize N (6)-methyladenosine (m(6)A) as a common strategy to evade host innate immunity. J Virol. 2021;95:95. https://doi.org/10.1128/JVI.01939-20