- -

Interaction network of tobacco etch potyvirus NIa protein with the host proteome during infection

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Interaction network of tobacco etch potyvirus NIa protein with the host proteome during infection

Mostrar el registro sencillo del ítem

Ficheros en el ítem

Thumbnail
Nombre: MARTINEZ;Rodrigo; ...
Tamaño: 3.025Mb
Formato: PDF
Descripción: Versión editorial
Abrir
dc.contributor.author Martinez Roberto, Fernando es_ES
dc.contributor.author Rodrigo Tarrega, Guillermo es_ES
dc.contributor.author Aragones, Verónica es_ES
dc.contributor.author Ruiz Server, Marta es_ES
dc.contributor.author Lodewijk, Iris es_ES
dc.contributor.author Fernandez, Unai es_ES
dc.contributor.author Elena Fito, Santiago Fco es_ES
dc.contributor.author Daros Arnau, Jose Antonio es_ES
dc.date.accessioned 2017-05-05T09:54:08Z
dc.date.available 2017-05-05T09:54:08Z
dc.date.issued 2016-02-01
dc.identifier.issn 1471-2164
dc.identifier.uri http://hdl.handle.net/10251/80650
dc.description.abstract Conclusions: Potyviral NIa targets many host elements during infection, establishing a network in which information is efficiently transmitted. es_ES
dc.description.abstract Background: The genomes of plant viruses have limited coding capacity, and to complete their infectious cycles, viral factors must target, direct or indirectly, many host elements. However, the interaction networks between viruses and host factors are poorly understood. The genus Potyvirus is the largest group of plus-strand RNA viruses infecting plants. Potyviral nuclear inclusion a (NIa) plays many roles during infection. NIa is a polyprotein consisting of two domains, viral protein genome-linked (VPg) and protease (NIaPro), separated by an inefficiently utilized self-proteolytic site. To gain insights about the interaction between potyviral NIa and the host cell during infection, we constructed Tobacco etch virus (TEV, genus Potyvirus) infectious clones in which the VPg or the NIaPro domains of NIa were tagged with the affinity polypeptide Twin-Strep-tag and identified the host proteins targeted by the viral proteins by affinity purification followed by mass spectrometry analysis (AP-MS). Results: We identified 232 different Arabidopsis thaliana proteins forming part of complexes in which TEV NIa products were also involved. VPg and NIaPro specifically targeted 89 and 76 of these proteins, respectively, whereas 67 proteins were targeted by both domains and considered full-length NIa targets. Taking advantage of the currently known A. thaliana interactome, we constructed a protein interaction network between TEV NIa domains and 516 host proteins. The most connected elements specifically targeted by VPg were G-box regulating factor 6 and mitochondrial ATP synthase delta subunit; those specifically targeted by NIaPro were plasma membrane aquaporin PIP2;7 and actin 7, whereas those targeted by full-length NIa were heat shock protein 70-1 and photosystem protein LHCA3. Moreover, a contextualization in the global A. thaliana interactome showed that NIa targets are not more connected with other host proteins than expected by chance, but are in a position that allows them to connect with other host proteins in shorter paths. Further analysis of NIa-targeted host proteins revealed that they are mainly involved in response to stress, metabolism, photosynthesis, and localization. Many of these proteins are connected with the phytohormone ethylene. Conclusions: Potyviral NIa targets many host elements during infection, establishing a network in which information is efficiently transmitted. es_ES
dc.description.sponsorship This work was supported by grants BIO2011-26741, BIO2014-54269-R and BFU2012-30805 from Ministerio de Economia y Competitividad (Spain) and PROMETEOII/2014/021 from Generalitat Valenciana. F.M. was the recipient of a predoctoral fellowship from Universidad Politecnica de Valencia. The proteomics analysis was carried out in the SCSIE, Universitat de Valencia Proteomics Unit, member of ISCIII ProteoRed Proteomics Platform (Spain). We particularly thank Luz Valero (SCSIE, Universitat de Valencia) for excellent assistance. en_EN
dc.language Inglés es_ES
dc.publisher BioMed Central es_ES
dc.relation.ispartof BMC Genomics es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Host-virus systems biology es_ES
dc.subject Protein interaction network es_ES
dc.subject RNA virus es_ES
dc.subject Plant virus es_ES
dc.subject Potyvirus es_ES
dc.subject Nuclear inclusion a protein es_ES
dc.subject Affinity purification mass spectrometry es_ES
dc.subject Arabidopsis thaliana es_ES
dc.subject.classification LENGUAJES Y SISTEMAS INFORMATICOS es_ES
dc.title Interaction network of tobacco etch potyvirus NIa protein with the host proteome during infection es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1186/s12864-016-2394-y
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//BIO2011-26741/ES/PATOGENOS DE RNA DE PLANTAS: INTERACCION CON EL HUESPED Y DESARROLLO DE HERRAMIENTAS BIOTECNOLOGICAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BIO2014-54269-R/ES/INSTRUMENTOS BIOTECNOLOGICOS DERIVADOS DE VIRUS DE PLANTAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BFU2012-30805/ES/EVOLUTIONARY SYSTEMS VIROLOGY: EPISTASIS AND THE RUGGEDNESS OF ADAPTIVE LANDSCAPES, MUTATIONS IN REGULATORY SEQUENCES, AND THE HOST DETERMINANTS OF VIRAL FITNESS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEOII%2F2014%2F021/ES/Comparative systems biology of host-virus interactions/ 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.contributor.affiliation Universitat Politècnica de València. Departamento de Sistemas Informáticos y Computación - Departament de Sistemes Informàtics i Computació es_ES
dc.description.bibliographicCitation Martinez Roberto, F.; Rodrigo Tarrega, G.; Aragones, V.; Ruiz Server, M.; Lodewijk, I.; Fernandez, U.; Elena Fito, SF.... (2016). Interaction network of tobacco etch potyvirus NIa protein with the host proteome during infection. BMC Genomics. 17:1-13. https://doi.org/10.1186/s12864-016-2394-y es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://dx.doi.org/10.1186/s12864-016-2394-y es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 13 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 17 es_ES
dc.relation.senia 331944 es_ES
dc.identifier.pmid 26830344 en_EN
dc.identifier.pmcid PMC4735970 en_EN
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder Universitat Politècnica de València es_ES
dc.description.references Elena SF, Rodrigo G. Towards an integrated molecular model of plant-virus interactions. Curr Opin Virol. 2012;2:719–24. doi: 10.1016/j.coviro.2012.09.004 . es_ES
dc.description.references Bosque G, Folch-Fortuny A, Picó J, Ferrer A, Elena SF. Topology analysis and visualization of Potyvirus protein-protein interaction network. BMC Syst Biol. 2014;8:129. doi: 10.1186/s12918-014-0129-8 . es_ES
dc.description.references Germain MA, Chatel-Chaix L, Gagné B, Bonneil E, Thibault P, Pradezynski F, et al. Elucidating novel hepatitis C virus-host interactions using combined mass spectrometry and functional genomics approaches. Mol Cell Proteomics. 2014;13:184–203. doi: 10.1074/mcp.M113.030155 . es_ES
dc.description.references Pichlmair A, Kandasamy K, Alvisi G, Mulhern O, Sacco R, Habjan M, et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature. 2012;487:486–90. doi: 10.1038/nature11289 . es_ES
dc.description.references Dunham WH, Mullin M, Gingras AC. Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics. 2012;12:1576–90. doi: 10.1002/pmic.201100523 . es_ES
dc.description.references Gingras AC, Gstaiger M, Raught B, Aebersold R. Analysis of protein complexes using mass spectrometry. Nat Rev Mol Cell Biol. 2007;8:645–54. doi: 10.1038/nrm2208 . es_ES
dc.description.references Ivanov KI, Eskelin K, Lõhmus A, Mäkinen K. Molecular and cellular mechanisms underlying potyvirus infection. J Gen Virol. 2014;95:1415–29. doi: 10.1099/vir.0.064220-0 . es_ES
dc.description.references Puustinen P, Mäkinen K. Uridylylation of the potyvirus VPg by viral replicase NIb correlates with the nucleotide binding capacity of VPg. J Biol Chem. 2004;279:38103–10. doi: 10.1074/jbc.M402910200 . es_ES
dc.description.references Eskelin K, Hafrén A, Rantalainen KI, Mäkinen K. Potyviral VPg enhances viral RNA Translation and inhibits reporter mRNA translation in planta. J Virol. 2011;85:9210–21. doi: 10.1128/JVI.00052-11 . es_ES
dc.description.references Schaad MC, Lellis AD, Carrington JC. VPg of tobacco etch potyvirus is a host genotype-specific determinant for long-distance movement. J Virol. 1997;71:8624–31. es_ES
dc.description.references Murphy JF, Klein PG, Hunt AG, Shaw JG. Replacement of the tyrosine residue that links a potyviral VPg to the viral RNA is lethal. Virology. 1996;220:535–8. doi: 10.1006/viro.1996.0344 . es_ES
dc.description.references Robaglia C, Caranta C. Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci. 2006;11:40–5. doi: 10.1016/j.tplants.2005.11.004 . es_ES
dc.description.references Carrington JC, Dougherty WG. Small nuclear inclusion protein encoded by a plant potyvirus genome is a protease. J Virol. 1987;61:2540–8. es_ES
dc.description.references Daròs JA, Carrington JC. RNA binding activity of Nla proteinase of tobacco etch potyvirus. Virology. 1997;237:327–36. es_ES
dc.description.references Daròs JA, Schaad MC, Carrington JC. Functional analysis of the interaction between VPg-proteinase (NIa) and RNA polymerase (NIb) of tobacco etch potyvirus, using conditional and suppressor mutants. J Virol. 1999;73:8732–40. es_ES
dc.description.references Schaad MC, Haldeman-Cahill R, Cronin S, Carrington JC. Analysis of the VPg-proteinase (NIa) encoded by tobacco etch potyvirus: effects of mutations on subcellular transport, proteolytic processing, and genome amplification. J Virol. 1996;70:7039–48. es_ES
dc.description.references Kim DH, Park YS, Kim SS, Lew J, Nam HG, Choi KY. Expression, purification, and identification of a novel self-cleavage site of the Nla C-terminal 27-kDa protease of turnip mosaic potyvirus C5. Virology. 1995;213:517–25. es_ES
dc.description.references Parks TD, Howard ED, Wolpert TJ, Arp DJ, Dougherty WG. Expression and purification of a recombinant tobacco etch virus NIa proteinase: biochemical analyses of the full-length and a naturally occurring truncated proteinase form. Virology. 1995;210:194–201. doi: 10.1006/viro.1995.1331 . es_ES
dc.description.references Schmidt TG, Batz L, Bonet L, Carl U, Holzapfel G, Kiem K, et al. Development of the Twin-Strep-tag(R) and its application for purification of recombinant proteins from cell culture supernatants. Protein Expr Purif. 2013;92:54–61. doi: 10.1016/j.pep.2013.08.021 . es_ES
dc.description.references Martínez F, Daròs JA. Tobacco etch virus protein P1 traffics to the nucleolus and associates with the host 60S ribosomal subunits during infection. J Virol. 2014;88:10725–37. doi: 10.1128/JVI.00928-14 . es_ES
dc.description.references Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics. 2005;4:1265–72. doi: 10.1074/mcp.M500061-MCP200 . es_ES
dc.description.references de Chassey B, Navratil V, Tafforeau L, Hiet MS, Aublin-Gex A, Agaugue S, et al. Hepatitis C virus infection protein network. Mol Syst Biol. 2008;4:230. doi: 10.1038/msb.2008.66 . es_ES
dc.description.references Barabási AL, Oltvai ZN. Network biology: understanding the cell’s functional organization. Nat Rev Genet. 2004;5:101–13. doi: 10.1038/nrg1272 . es_ES
dc.description.references Menche J, Sharma A, Kitsak M, Ghiassian SD, Vidal M, Loscalzo J, et al. Uncovering disease-disease relationships through the incomplete interactome. Science. 2015;347:1257601. doi: 10.1126/science.1257601 . es_ES
dc.description.references Missiuro PV, Liu K, Zou L, Ross BC, Zhao G, Liu JS, et al. Information flow analysis of interactome networks. PLoS Comput Biol. 2009;5, e1000350. doi: 10.1371/journal.pcbi.1000350 . es_ES
dc.description.references Yang X, Wang W, Coleman M, Orgil U, Feng J, Ma X, et al. Arabidopsis 14-3-3 lambda is a positive regulator of RPW8-mediated disease resistance. Plant J. 2009;60:539–50. doi: 10.1111/j.1365-313X.2009.03978.x . es_ES
dc.description.references Aoki H, Hayashi J, Moriyama M, Arakawa Y, Hino O. Hepatitis C virus core protein interacts with 14-3-3 protein and activates the kinase Raf-1. J Virol. 2000;74:1736–41. es_ES
dc.description.references Jang JY, Kim DG, Kim YO, Kim JS, Kang H. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol. 2004;54:713–25. doi: 10.1023/B:PLAN.0000040900.61345.a6 . es_ES
dc.description.references Hartl FU, Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 2002;295:1852–8. doi: 10.1126/science.1068408 . es_ES
dc.description.references Kampinga HH, Craig EA. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol. 2010;11:579–92. doi: 10.1038/nrm2941 . es_ES
dc.description.references Verchot J. Cellular chaperones and folding enzymes are vital contributors to membrane bound replication and movement complexes during plant RNA virus infection. Front Plant Sci. 2012;3:275. doi: 10.3389/fpls.2012.00275 . es_ES
dc.description.references Hafrén A, Hofius D, Rönnholm G, Sonnewald U, Mäkinen K. HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant Cell. 2010;22:523–35. doi: 10.1105/tpc.109.072413 . es_ES
dc.description.references Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, et al. Acquired resistance in Arabidopsis. Plant Cell. 1992;4:645–56. doi: 10.1105/tpc.4.6.645 . es_ES
dc.description.references Dufresne PJ, Ubalijoro E, Fortin MG, Laliberté JF. Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of turnip mosaic virus. J Gen Virol. 2008;89:2339–48. doi: 10.1099/vir.0.2008/002139-0 . es_ES
dc.description.references Léonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberté JF. Interaction of VPg-Pro of Turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J Gen Virol. 2004;85:1055–63. doi: 10.1099/vir.0.19706-0 . es_ES
dc.description.references Beauchemin C, Laliberté JF. The poly(A) binding protein is internalized in virus-induced vesicles or redistributed to the nucleolus during Turnip mosaic virus infection. J Virol. 2007;81:10905–13. doi: 10.1128/JVI.01243-07 . es_ES
dc.description.references Thivierge K, Cotton S, Dufresne PJ, Mathieu I, Beauchemin C, Ide C, et al. Eukaryotic elongation factor 1A interacts with Turnip mosaic virus RNA-dependent RNA polymerase and VPg-Pro in virus-induced vesicles. Virology. 2008;377:216–25. doi: 10.1016/j.virol.2008.04.015 . es_ES
dc.description.references Gao L, Shen W, Yan P, Tuo D, Li X, Zhou P. NIa-pro of Papaya ringspot virus interacts with papaya methionine sulfoxide reductase B1. Virology. 2012;434:78–87. doi: 10.1016/j.virol.2012.09.007 . es_ES
dc.description.references Lellis AD, Kasschau KD, Whitham SA, Carrington JC. Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol. 2002;12:1046–51. es_ES
dc.description.references Wittmann S, Chatel H, Fortin MG, Laliberté JF. Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology. 1997;234:84–92. doi: 10.1006/viro.1997.8634 . es_ES
dc.description.references Charron C, Nicolai M, Gallois JL, Robaglia C, Moury B, Palloix A, et al. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J. 2008;54:56–68. doi: 10.1111/j.1365-313X.2008.03407.x . es_ES
dc.description.references Huang TS, Wei T, Laliberté JF, Wang A. A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection. Plant Physiol. 2010;152:255–66. doi: 10.1104/pp.109.147983 . es_ES
dc.description.references Rajamäki ML, Valkonen JP. Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana species. Plant Cell. 2009;21:2485–502. doi: 10.1105/tpc.108.064147 . es_ES
dc.description.references Zhu M, Chen Y, Ding XS, Webb SL, Zhou T, Nelson RS, et al. Maize Elongin C interacts with the viral genome-linked protein, VPg, of Sugarcane mosaic virus and facilitates virus infection. New Phytol. 2014;203:1291–304. doi: 10.1111/nph.12890 . es_ES
dc.description.references Rajamäki ML, Streng J, Valkonen JP. Silencing suppressor protein VPg of a potyvirus interacts with the plant silencing-related protein SGS3. Mol Plant Microbe Interact. 2014;27:1199–210. doi: 10.1094/MPMI-04-14-0109-R . es_ES
dc.description.references Dunoyer P, Thomas C, Harrison S, Revers F, Maule A. A cysteine-rich plant protein potentiates Potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol. 2004;78:2301–9. es_ES
dc.description.references Revers F, García JA. Molecular biology of potyviruses. Adv Virus Res. 2015;92:101–99. doi: 10.1016/bs.aivir.2014.11.006 . es_ES
dc.description.references Mi H, Muruganujan A, Casagrande JT, Thomas PD. Large-scale gene function analysis with the PANTHER classification system. Nat Protoc. 2013;8:1551–66. doi: 10.1038/nprot.2013.092 . es_ES
dc.description.references Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010;38:W64–70. doi: 10.1093/nar/gkq310 . es_ES
dc.description.references Peng ZY, Zhou X, Li L, Yu X, Li H, Jiang Z, et al. Arabidopsis Hormone Database: a comprehensive genetic and phenotypic information database for plant hormone research in Arabidopsis. Nucleic Acids Res. 2009;37:D975–82. doi: 10.1093/nar/gkn873 . es_ES
dc.description.references Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012;28:489–521. doi: 10.1146/annurev-cellbio-092910-154055 . es_ES
dc.description.references Agudelo-Romero P, Carbonell P, Perez-Amador MA, Elena SF. Virus adaptation by manipulation of host’s gene expression. PLoS One. 2008;3, e2397. es_ES
dc.description.references Bedoya LC, Martínez F, Orzáez D, Daròs JA. Visual tracking of plant virus infection and movement using a reporter MYB transcription factor that activates anthocyanin biosynthesis. Plant Physiol. 2012;158:1130–8. doi: 10.1104/pp.111.192922 . es_ES
dc.description.references Thole V, Worland B, Snape JW, Vain P. The pCLEAN dual binary vector system for Agrobacterium-mediated plant transformation. Plant Physiol. 2007;145:1211–9. es_ES
dc.description.references Bedoya LC, Daròs JA. Stability of Tobacco etch virus infectious clones in plasmid vectors. Virus Res. 2010;149:234–40. es_ES
dc.description.references Martínez F, Elena SF, Daròs JA. Fate of artificial microRNA-mediated resistance to plant viruses in mixed infections. Phytopathology. 2013;103:870–6. doi: 10.1094/PHYTO-09-12-0233-R . es_ES
dc.description.references Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, et al. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci U S A. 1996;93:14440–5. es_ES
dc.description.references Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10. doi: 10.1016/S0022-2836(05)80360-2 . es_ES
dc.description.references Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504. doi: 10.1101/gr.1239303 . es_ES
dc.description.references Arabidopsis_Interactome_Mapping_Consortium. Evidence for network evolution in an Arabidopsis interactome map. Science. 2011;333:601–7. doi: 10.1126/science.1203877 . es_ES
dc.description.references Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science. 2011;333:596–601. doi: 10.1126/science.1203659 . es_ES
dc.description.references Chatr-Aryamontri A, Breitkreutz BJ, Oughtred R, Boucher L, Heinicke S, Chen D, et al. The BioGRID interaction update database: 2015 updated. Nucleic Acids Res. 2015;2015(43):D470–8. doi: 10.1093/nar/gku1204 . es_ES
dc.description.references Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6, e21800. doi: 10.1371/journal.pone.0021800 . es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem