- -

A viral suppressor of RNA silencing inhibits ARGONAUTE 1 function by precluding target RNA binding to pre-assembled RISC

RiuNet: Institutional repository of the Polithecnic University of Valencia

Share/Send to

Cited by

Statistics

A viral suppressor of RNA silencing inhibits ARGONAUTE 1 function by precluding target RNA binding to pre-assembled RISC

Show simple item record

Files in this item

dc.contributor.author Kenesi, Erzsebet es_ES
dc.contributor.author CARBONELL, ALBERTO es_ES
dc.contributor.author Lozsa, Rita es_ES
dc.contributor.author Vertessy, Beata es_ES
dc.contributor.author Lakatos, Lorant es_ES
dc.date.accessioned 2021-02-13T04:31:43Z
dc.date.available 2021-02-13T04:31:43Z
dc.date.issued 2017-07-27 es_ES
dc.identifier.issn 0305-1048 es_ES
dc.identifier.uri http://hdl.handle.net/10251/161199
dc.description.abstract [EN] In most eukaryotes, RNA silencing is an adaptive immune system regulating key biological processes including antiviral defense. To evade this response, viruses of plants, worms and insects have evolved viral suppressors of RNA silencing proteins (VSRs). Various VSRs, such as P1 from Sweet potato mild mottle virus (SPMMV), inhibit the activity of RNA-induced silencing complexes (RISCs) including an ARGONAUTE (AGO) protein loaded with a small RNA. However, the specific mechanisms explaining this class of inhibition are unknown. Here, we show that SPMMV P1 interacts with AGO1 and AGO2 from Arabidopsis thaliana, but solely interferes with AGO1 function. Moreover, a mutational analysis of a newly identified zinc finger domain in P1 revealed that this domain could represent an effector domain as it is required for P1 suppressor activity but not for AGO1 binding. Finally, a comparative analysis of the target RNA binding capacity of AGO1 in the presence of wild-type or suppressor-defective P1 forms revealed that P1 blocks target RNA binding to AGO1. Our results describe the negative regulation of RISC, the small RNA containing molecular machine. es_ES
dc.description.sponsorship Hungarian Scientific Research Fund (OTKA) [K91042, NN107787, NN11024 to L.L.]; European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska Curie [655841 to A.C.]. Funding for open access charge: OTKA [NN11024] es_ES
dc.language Inglés es_ES
dc.publisher Oxford University Press es_ES
dc.relation.ispartof Nucleic Acids Research es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject RNA silencing es_ES
dc.subject Plant virus, siRNA es_ES
dc.subject AGO es_ES
dc.subject Immunoprecipitation es_ES
dc.subject Silencing suppressor es_ES
dc.title A viral suppressor of RNA silencing inhibits ARGONAUTE 1 function by precluding target RNA binding to pre-assembled RISC es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1093/nar/gkx379 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/655841/EU/Genome-wide analysis of RNA and protein interacting profiles during a plant virus infection/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/OTKA//K91042/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/OTKA//NN107787/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/OTKA//NN11024/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Kenesi, E.; Carbonell, A.; Lozsa, R.; Vertessy, B.; Lakatos, L. (2017). A viral suppressor of RNA silencing inhibits ARGONAUTE 1 function by precluding target RNA binding to pre-assembled RISC. Nucleic Acids Research. 45(13):7736-7750. https://doi.org/10.1093/nar/gkx379 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1093/nar/gkx379 es_ES
dc.description.upvformatpinicio 7736 es_ES
dc.description.upvformatpfin 7750 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 45 es_ES
dc.description.issue 13 es_ES
dc.identifier.pmid 28499009 es_ES
dc.identifier.pmcid PMC5737661 es_ES
dc.relation.pasarela S\375859 es_ES
dc.contributor.funder Hungarian Scientific Research Fund es_ES
dc.contributor.funder European Commission es_ES
dc.description.references Sayed, D., & Abdellatif, M. (2011). MicroRNAs in Development and Disease. Physiological Reviews, 91(3), 827-887. doi:10.1152/physrev.00006.2010 es_ES
dc.description.references Martin, R. C., Liu, P.-P., Goloviznina, N. A., & Nonogaki, H. (2010). microRNA, seeds, and Darwin?: diverse function of miRNA in seed biology and plant responses to stress. Journal of Experimental Botany, 61(9), 2229-2234. doi:10.1093/jxb/erq063 es_ES
dc.description.references BAULCOMBE, D. (2004). Crystal structure of p19 ? a universal suppressor of RNA silencing. Trends in Biochemical Sciences, 29(6), 279-281. doi:10.1016/j.tibs.2004.04.007 es_ES
dc.description.references Matzke, M. A., & Mosher, R. A. (2014). RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature Reviews Genetics, 15(6), 394-408. doi:10.1038/nrg3683 es_ES
dc.description.references Bernstein, E., Caudy, A. A., Hammond, S. M., & Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature, 409(6818), 363-366. doi:10.1038/35053110 es_ES
dc.description.references Ender, C., & Meister, G. (2010). Argonaute proteins at a glance. Journal of Cell Science, 123(11), 1819-1823. doi:10.1242/jcs.055210 es_ES
dc.description.references Hutvágner, G., Simard, M. J., Mello, C. C., & Zamore, P. D. (2004). Sequence-Specific Inhibition of Small RNA Function. PLoS Biology, 2(4), e98. doi:10.1371/journal.pbio.0020098 es_ES
dc.description.references Meister, G. (2013). Argonaute proteins: functional insights and emerging roles. Nature Reviews Genetics, 14(7), 447-459. doi:10.1038/nrg3462 es_ES
dc.description.references Wilkins, C., Dishongh, R., Moore, S. C., Whitt, M. A., Chow, M., & Machaca, K. (2005). RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature, 436(7053), 1044-1047. doi:10.1038/nature03957 es_ES
dc.description.references Li, S., Liu, L., Zhuang, X., Yu, Y., Liu, X., Cui, X., … Chen, X. (2013). MicroRNAs Inhibit the Translation of Target mRNAs on the Endoplasmic Reticulum in Arabidopsis. Cell, 153(3), 562-574. doi:10.1016/j.cell.2013.04.005 es_ES
dc.description.references Van Rij, R. P., Saleh, M.-C., Berry, B., Foo, C., Houk, A., Antoniewski, C., & Andino, R. (2006). The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes & Development, 20(21), 2985-2995. doi:10.1101/gad.1482006 es_ES
dc.description.references Baulcombe, D. (2002). Viral suppression of systemic silencing. Trends in Microbiology, 10(7), 306-308. doi:10.1016/s0966-842x(02)02387-9 es_ES
dc.description.references Maillard, P. V., Ciaudo, C., Marchais, A., Li, Y., Jay, F., Ding, S. W., & Voinnet, O. (2013). Antiviral RNA Interference in Mammalian Cells. Science, 342(6155), 235-238. doi:10.1126/science.1241930 es_ES
dc.description.references Bronkhorst, A. W., & van Rij, R. P. (2014). The long and short of antiviral defense: small RNA-based immunity in insects. Current Opinion in Virology, 7, 19-28. doi:10.1016/j.coviro.2014.03.010 es_ES
dc.description.references Burgyán, J., & Havelda, Z. (2011). Viral suppressors of RNA silencing. Trends in Plant Science, 16(5), 265-272. doi:10.1016/j.tplants.2011.02.010 es_ES
dc.description.references Csorba, T., Kontra, L., & Burgyán, J. (2015). viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence. Virology, 479-480, 85-103. doi:10.1016/j.virol.2015.02.028 es_ES
dc.description.references Pumplin, N., & Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nature Reviews Microbiology, 11(11), 745-760. doi:10.1038/nrmicro3120 es_ES
dc.description.references Várallyay, É., & Havelda, Z. (2013). Unrelated viral suppressors of RNA silencing mediate the control of ARGONAUTE1 level. Molecular Plant Pathology, 14(6), 567-575. doi:10.1111/mpp.12029 es_ES
dc.description.references Várallyay, É., Válóczi, A., Ágyi, Á., Burgyán, J., & Havelda, Z. (2010). Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. The EMBO Journal, 29(20), 3507-3519. doi:10.1038/emboj.2010.215 es_ES
dc.description.references Baumberger, N., Tsai, C.-H., Lie, M., Havecker, E., & Baulcombe, D. C. (2007). The Polerovirus Silencing Suppressor P0 Targets ARGONAUTE Proteins for Degradation. Current Biology, 17(18), 1609-1614. doi:10.1016/j.cub.2007.08.039 es_ES
dc.description.references Csorba, T., Lózsa, R., Hutvágner, G., & Burgyán, J. (2010). Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. The Plant Journal, 62(3), 463-472. doi:10.1111/j.1365-313x.2010.04163.x es_ES
dc.description.references Karran, R. A., & Sanfaçon, H. (2014). Tomato ringspot virus Coat Protein Binds to ARGONAUTE 1 and Suppresses the Translation Repression of a Reporter Gene. Molecular Plant-Microbe Interactions®, 27(9), 933-943. doi:10.1094/mpmi-04-14-0099-r es_ES
dc.description.references Pazhouhandeh, M., Dieterle, M., Marrocco, K., Lechner, E., Berry, B., Brault, V. r., … Ziegler-Graff, V. r. (2006). F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proceedings of the National Academy of Sciences, 103(6), 1994-1999. doi:10.1073/pnas.0510784103 es_ES
dc.description.references Derrien, B., Baumberger, N., Schepetilnikov, M., Viotti, C., De Cillia, J., Ziegler-Graff, V., … Genschik, P. (2012). Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proceedings of the National Academy of Sciences, 109(39), 15942-15946. doi:10.1073/pnas.1209487109 es_ES
dc.description.references Nayak, A., Berry, B., Tassetto, M., Kunitomi, M., Acevedo, A., Deng, C., … Andino, R. (2010). Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nature Structural & Molecular Biology, 17(5), 547-554. doi:10.1038/nsmb.1810 es_ES
dc.description.references Van Mierlo, J. T., Bronkhorst, A. W., Overheul, G. J., Sadanandan, S. A., Ekström, J.-O., Heestermans, M., … van Rij, R. P. (2012). Convergent Evolution of Argonaute-2 Slicer Antagonism in Two Distinct Insect RNA Viruses. PLoS Pathogens, 8(8), e1002872. doi:10.1371/journal.ppat.1002872 es_ES
dc.description.references Mann, K. S., Johnson, K. N., Carroll, B. J., & Dietzgen, R. G. (2016). Cytorhabdovirus P protein suppresses RISC-mediated cleavage and RNA silencing amplification in planta. Virology, 490, 27-40. doi:10.1016/j.virol.2016.01.003 es_ES
dc.description.references Giner, A., Lakatos, L., García-Chapa, M., López-Moya, J. J., & Burgyán, J. (2010). Viral Protein Inhibits RISC Activity by Argonaute Binding through Conserved WG/GW Motifs. PLoS Pathogens, 6(7), e1000996. doi:10.1371/journal.ppat.1000996 es_ES
dc.description.references Vaucheret, H. (2008). Plant ARGONAUTES. Trends in Plant Science, 13(7), 350-358. doi:10.1016/j.tplants.2008.04.007 es_ES
dc.description.references Mallory, A., & Vaucheret, H. (2010). Form, Function, and Regulation of ARGONAUTE Proteins. The Plant Cell, 22(12), 3879-3889. doi:10.1105/tpc.110.080671 es_ES
dc.description.references Carbonell, A., & Carrington, J. C. (2015). Antiviral roles of plant ARGONAUTES. Current Opinion in Plant Biology, 27, 111-117. doi:10.1016/j.pbi.2015.06.013 es_ES
dc.description.references Kertész, S., Kerényi, Z., Mérai, Z., Bartos, I., Pálfy, T., Barta, E., & Silhavy, D. (2006). Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Research, 34(21), 6147-6157. doi:10.1093/nar/gkl737 es_ES
dc.description.references Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Gilbert, K. B., Montgomery, T. A., Nguyen, T., … Carrington, J. C. (2012). Functional Analysis of Three Arabidopsis ARGONAUTES Using Slicer-Defective Mutants  . The Plant Cell, 24(9), 3613-3629. doi:10.1105/tpc.112.099945 es_ES
dc.description.references Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., … Carrington, J. C. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Structural & Molecular Biology, 17(8), 997-1003. doi:10.1038/nsmb.1866 es_ES
dc.description.references Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D., Hansen, J. E., Alexander, A. L., … Carrington, J. C. (2008). Specificity of ARGONAUTE7-miR390 Interaction and Dual Functionality in TAS3 Trans-Acting siRNA Formation. Cell, 133(1), 128-141. doi:10.1016/j.cell.2008.02.033 es_ES
dc.description.references Carbonell, A., Takeda, A., Fahlgren, N., Johnson, S. C., Cuperus, J. T., & Carrington, J. C. (2014). New Generation of Artificial MicroRNA and Synthetic Trans-Acting Small Interfering RNA Vectors for Efficient Gene Silencing in Arabidopsis. Plant Physiology, 165(1), 15-29. doi:10.1104/pp.113.234989 es_ES
dc.description.references Terzi, L. C., & Simpson, G. G. (2009). Arabidopsis RNA immunoprecipitation. The Plant Journal, 59(1), 163-168. doi:10.1111/j.1365-313x.2009.03859.x es_ES
dc.description.references Li, F., Xu, D., Abad, J., & Li, R. (2012). Phylogenetic relationships of closely related potyviruses infecting sweet potato determined by genomic characterization of Sweet potato virus G and Sweet potato virus 2. Virus Genes, 45(1), 118-125. doi:10.1007/s11262-012-0749-2 es_ES
dc.description.references Harvey, J. J. W., Lewsey, M. G., Patel, K., Westwood, J., Heimstädt, S., Carr, J. P., & Baulcombe, D. C. (2011). An Antiviral Defense Role of AGO2 in Plants. PLoS ONE, 6(1), e14639. doi:10.1371/journal.pone.0014639 es_ES
dc.description.references Till, S., Lejeune, E., Thermann, R., Bortfeld, M., Hothorn, M., Enderle, D., … Ladurner, A. G. (2007). A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nature Structural & Molecular Biology, 14(10), 897-903. doi:10.1038/nsmb1302 es_ES
dc.description.references Schirle, N. T., & MacRae, I. J. (2012). The Crystal Structure of Human Argonaute2. Science, 336(6084), 1037-1040. doi:10.1126/science.1221551 es_ES
dc.description.references Elkayam, E., Kuhn, C.-D., Tocilj, A., Haase, A. D., Greene, E. M., Hannon, G. J., & Joshua-Tor, L. (2012). The Structure of Human Argonaute-2 in Complex with miR-20a. Cell, 150(1), 100-110. doi:10.1016/j.cell.2012.05.017 es_ES
dc.description.references Hutvagner, G., & Simard, M. J. (2008). Argonaute proteins: key players in RNA silencing. Nature Reviews Molecular Cell Biology, 9(1), 22-32. doi:10.1038/nrm2321 es_ES
dc.description.references Brown, K. M., Chu, C., & Rana, T. M. (2005). Target accessibility dictates the potency of human RISC. Nature Structural & Molecular Biology, 12(5), 469-470. doi:10.1038/nsmb931 es_ES
dc.description.references Webster, L. C., Zhang, K., Chance, B., Ayene, I., Culp, J. S., Huang, W. J., … Ricciardi, R. P. (1991). Conversion of the E1A Cys4 zinc finger to a nonfunctional His2,Cys2 zinc finger by a single point mutation. Proceedings of the National Academy of Sciences, 88(22), 9989-9993. doi:10.1073/pnas.88.22.9989 es_ES
dc.description.references Trinks, D., Rajeswaran, R., Shivaprasad, P. V., Akbergenov, R., Oakeley, E. J., Veluthambi, K., … Pooggin, M. M. (2005). Suppression of RNA Silencing by a Geminivirus Nuclear Protein, AC2, Correlates with Transactivation of Host Genes. Journal of Virology, 79(4), 2517-2527. doi:10.1128/jvi.79.4.2517-2527.2005 es_ES
dc.description.references Chiba, S., Hleibieh, K., Delbianco, A., Klein, E., Ratti, C., Ziegler-Graff, V., … Gilmer, D. (2013). The Benyvirus RNA Silencing Suppressor Is Essential for Long-Distance Movement, Requires Both Zinc-Finger and NoLS Basic Residues but Not a Nucleolar Localization for Its Silencing-Suppression Activity. Molecular Plant-Microbe Interactions®, 26(2), 168-181. doi:10.1094/mpmi-06-12-0142-r es_ES
dc.description.references Bies‐Etheve, N., Pontier, D., Lahmy, S., Picart, C., Vega, D., Cooke, R., & Lagrange, T. (2009). RNA‐directed DNA methylation requires an AGO4‐interacting member of the SPT5 elongation factor family. EMBO reports, 10(6), 649-654. doi:10.1038/embor.2009.31 es_ES
dc.description.references Chekulaeva, M., Filipowicz, W., & Parker, R. (2009). Multiple independent domains of dGW182 function in miRNA-mediated repression in Drosophila. RNA, 15(5), 794-803. doi:10.1261/rna.1364909 es_ES
dc.description.references El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., … Lagrange, T. (2007). Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes & Development, 21(20), 2539-2544. doi:10.1101/gad.451207 es_ES
dc.description.references He, X.-J., Hsu, Y.-F., Zhu, S., Wierzbicki, A. T., Pontes, O., Pikaard, C. S., … Zhu, J.-K. (2009). An Effector of RNA-Directed DNA Methylation in Arabidopsis Is an ARGONAUTE 4- and RNA-Binding Protein. Cell, 137(3), 498-508. doi:10.1016/j.cell.2009.04.028 es_ES
dc.description.references Till, S., & Ladurner, A. G. (2007). RNA Pol IV Plays Catch with Argonaute 4. Cell, 131(4), 643-645. doi:10.1016/j.cell.2007.10.044 es_ES
dc.description.references Bednenko, J., Noto, T., DeSouza, L. V., Siu, K. W. M., Pearlman, R. E., Mochizuki, K., & Gorovsky, M. A. (2009). Two GW Repeat Proteins Interact with Tetrahymena thermophila Argonaute and Promote Genome Rearrangement. Molecular and Cellular Biology, 29(18), 5020-5030. doi:10.1128/mcb.00076-09 es_ES
dc.description.references Pontier, D., Picart, C., Roudier, F., Garcia, D., Lahmy, S., Azevedo, J., … Lagrange, T. (2012). NERD, a Plant-Specific GW Protein, Defines an Additional RNAi-Dependent Chromatin-Based Pathway in Arabidopsis. Molecular Cell, 48(1), 121-132. doi:10.1016/j.molcel.2012.07.027 es_ES
dc.description.references Schirle, N. T., Sheu-Gruttadauria, J., & MacRae, I. J. (2014). Structural basis for microRNA targeting. Science, 346(6209), 608-613. doi:10.1126/science.1258040 es_ES
dc.description.references GAMSJAEGER, R., LIEW, C., LOUGHLIN, F., CROSSLEY, M., & MACKAY, J. (2007). Sticky fingers: zinc-fingers as protein-recognition motifs. Trends in Biochemical Sciences, 32(2), 63-70. doi:10.1016/j.tibs.2006.12.007 es_ES
dc.description.references Hall, T. M. T. (2005). Multiple modes of RNA recognition by zinc finger proteins. Current Opinion in Structural Biology, 15(3), 367-373. doi:10.1016/j.sbi.2005.04.004 es_ES
dc.description.references Leung, A. K. L., Vyas, S., Rood, J. E., Bhutkar, A., Sharp, P. A., & Chang, P. (2011). Poly(ADP-Ribose) Regulates Stress Responses and MicroRNA Activity in the Cytoplasm. Molecular Cell, 42(4), 489-499. doi:10.1016/j.molcel.2011.04.015 es_ES
dc.description.references Mukasa, S. B., Rubaihayo, P. R., & Valkonen, J. P. T. (2006). Interactions between a crinivirus, an ipomovirus and a potyvirus in coinfected sweetpotato plants. Plant Pathology, 55(3), 458-467. doi:10.1111/j.1365-3059.2006.01350.x es_ES
dc.description.references Ma, X., Nicole, M.-C., Meteignier, L.-V., Hong, N., Wang, G., & Moffett, P. (2014). Different roles for RNA silencing and RNA processing components in virus recovery and virus-induced gene silencing in plants. Journal of Experimental Botany, 66(3), 919-932. doi:10.1093/jxb/eru447 es_ES
dc.description.references Garcia-Ruiz, H., Carbonell, A., Hoyer, J. S., Fahlgren, N., Gilbert, K. B., Takeda, A., … Carrington, J. C. (2015). Roles and Programming of Arabidopsis ARGONAUTE Proteins during Turnip Mosaic Virus Infection. PLOS Pathogens, 11(3), e1004755. doi:10.1371/journal.ppat.1004755 es_ES


This item appears in the following Collection(s)

Show simple item record