Exploration of binary protein-protein interactions between tick-borne flaviviruses and Ixodes ricinus.
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
06 Mar 2021
06 Mar 2021
Historique:
received:
11
12
2020
accepted:
18
02
2021
entrez:
7
3
2021
pubmed:
8
3
2021
medline:
4
9
2021
Statut:
epublish
Résumé
Louping ill virus (LIV) and tick-borne encephalitis virus (TBEV) are tick-borne flaviviruses that are both transmitted by the major European tick, Ixodes ricinus. Despite the importance of I. ricinus as an arthropod vector, its capacity to acquire and subsequently transmit viruses, known as vector competence, is poorly understood. At the molecular scale, vector competence is governed in part by binary interactions established between viral and cellular proteins within infected tick cells. To investigate virus-vector protein-protein interactions (PPIs), the entire set of open reading frames for LIV and TBEV was screened against an I. ricinus cDNA library established from three embryonic tick cell lines using yeast two-hybrid methodology (Y2H). PPIs revealed for each viral bait were retested in yeast by applying a gap repair (GR) strategy, and notably against the cognate protein of both viruses, to determine whether the PPIs were specific for a single virus or common to both. The interacting tick proteins were identified by automatic BLASTX, and in silico analyses were performed to expose the biological processes targeted by LIV and TBEV. For each virus, we identified 24 different PPIs involving six viral proteins and 22 unique tick proteins, with all PPIs being common to both viruses. According to our data, several viral proteins (pM, M, NS2A, NS4A, 2K and NS5) target multiple tick protein modules implicated in critical biological pathways. Of note, the NS5 and pM viral proteins establish PPI with several tumor necrosis factor (TNF) receptor-associated factor (TRAF) proteins, which are essential adaptor proteins at the nexus of multiple signal transduction pathways. We provide the first description of the TBEV/LIV-I. ricinus PPI network, and indeed of any PPI network involving a tick-borne virus and its tick vector. While further investigation will be needed to elucidate the role of each tick protein in the replication cycle of tick-borne flaviviruses, our study provides a foundation for understanding the vector competence of I. ricinus at the molecular level. Indeed, certain PPIs may represent molecular determinants of vector competence of I. ricinus for TBEV and LIV, and potentially for other tick-borne flaviviruses.
Sections du résumé
BACKGROUND
BACKGROUND
Louping ill virus (LIV) and tick-borne encephalitis virus (TBEV) are tick-borne flaviviruses that are both transmitted by the major European tick, Ixodes ricinus. Despite the importance of I. ricinus as an arthropod vector, its capacity to acquire and subsequently transmit viruses, known as vector competence, is poorly understood. At the molecular scale, vector competence is governed in part by binary interactions established between viral and cellular proteins within infected tick cells.
METHODS
METHODS
To investigate virus-vector protein-protein interactions (PPIs), the entire set of open reading frames for LIV and TBEV was screened against an I. ricinus cDNA library established from three embryonic tick cell lines using yeast two-hybrid methodology (Y2H). PPIs revealed for each viral bait were retested in yeast by applying a gap repair (GR) strategy, and notably against the cognate protein of both viruses, to determine whether the PPIs were specific for a single virus or common to both. The interacting tick proteins were identified by automatic BLASTX, and in silico analyses were performed to expose the biological processes targeted by LIV and TBEV.
RESULTS
RESULTS
For each virus, we identified 24 different PPIs involving six viral proteins and 22 unique tick proteins, with all PPIs being common to both viruses. According to our data, several viral proteins (pM, M, NS2A, NS4A, 2K and NS5) target multiple tick protein modules implicated in critical biological pathways. Of note, the NS5 and pM viral proteins establish PPI with several tumor necrosis factor (TNF) receptor-associated factor (TRAF) proteins, which are essential adaptor proteins at the nexus of multiple signal transduction pathways.
CONCLUSION
CONCLUSIONS
We provide the first description of the TBEV/LIV-I. ricinus PPI network, and indeed of any PPI network involving a tick-borne virus and its tick vector. While further investigation will be needed to elucidate the role of each tick protein in the replication cycle of tick-borne flaviviruses, our study provides a foundation for understanding the vector competence of I. ricinus at the molecular level. Indeed, certain PPIs may represent molecular determinants of vector competence of I. ricinus for TBEV and LIV, and potentially for other tick-borne flaviviruses.
Identifiants
pubmed: 33676573
doi: 10.1186/s13071-021-04651-3
pii: 10.1186/s13071-021-04651-3
pmc: PMC7937244
doi:
Substances chimiques
Arthropod Proteins
0
Viral Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
144Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P024270/1
Pays : United Kingdom
Organisme : labex IBEID
ID : ANR-10-LABX-62-IBEID
Références
Labuda M, Nuttall PA. Tick-borne viruses. Parasitology. 2004;129(Suppl):S221–45. https://doi.org/10.1017/s0031182004005220 .
doi: 10.1017/s0031182004005220
pubmed: 15938513
Calisher CH. Antigenic classification and taxonomy of flaviviruses (family Flaviviridae) emphasizing a universal system for the taxonomy of viruses causing tick-borne encephalitis. Acta Virol. 1988;32:469–78.
pubmed: 2904743
Gritsun TS, Nuttall PA, Gould EA. Tick-borne flaviviruses. Adv Virus Res. 2003;61:317–71. https://doi.org/10.1016/S0065-3527(03)61008-0 .
doi: 10.1016/S0065-3527(03)61008-0
pubmed: 14714436
Süss J. Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia—an overview. Ticks Tick Borne Dis. 2011;2:2–15. https://doi.org/10.1016/j.ttbdis.2010.10.007 .
doi: 10.1016/j.ttbdis.2010.10.007
pubmed: 21771531
Gritsun TS, Lashkevich VA, Gould EA. Tick-borne encephalitis. Antiviral Res. 2003;57:129–46.
doi: 10.1016/S0166-3542(02)00206-1
Lindquist L, Vapalahti O. Tick-borne encephalitis. Lancet. 2008;371:1861–71.
doi: 10.1016/S0140-6736(08)60800-4
Pool WA, Brownlee A, Wilson DR. The etiology of “louping-ill.” J Comp Pathol Ther. 1930;43:253–90. https://doi.org/10.1016/S0368-1742(30)80026-2 .
doi: 10.1016/S0368-1742(30)80026-2
Jeffries CL, Mansfield KL, Phipps LP, Wakeley PR, Mearns R, Schock A, et al. Louping ill virus: an endemic tick-borne disease of Great Britain. J Gen Virol. 2014;95(5):1005–14.
doi: 10.1099/vir.0.062356-0
Gilbert L. Louping ill virus in the UK: a review of the hosts, transmission and ecological consequences of control. Exp Appl Acarol. 2016;68:363–74.
doi: 10.1007/s10493-015-9952-x
Davidson MM, Williams H, Macleod JA. Louping ill in man: a forgotten disease. J Infect. 1991;23:241–9.
doi: 10.1016/0163-4453(91)92756-U
Spirin V, Mirny LA. Protein complexes and functional modules in molecular networks. Proc Natl Acad Sci USA. 2003;100:12123–8. https://doi.org/10.1073/pnas.2032324100 .
doi: 10.1073/pnas.2032324100
pubmed: 14517352
pmcid: 218723
Kovanich D, Saisawang C, Sittipaisankul P, Ramphan S, Kalpongnukul N, Somparn P, et al. Analysis of the Zika and Japanese Encephalitis virus NS5 interactomes. J Proteome Res. 2019;18:3203–18. https://doi.org/10.1021/acs.jproteome.9b00318 .
doi: 10.1021/acs.jproteome.9b00318
pubmed: 31199156
de la Fuente J, Antunes S, Bonnet S, Cabezas-Cruz A, Domingos AG, Estrada-Peña A, et al. Tick–pathogen interactions and vector competence: identification of molecular drivers for tick-borne diseases. Front Cell Infect Microbiol. 2017. https://doi.org/10.3389/fcimb.2017.00114 .
doi: 10.3389/fcimb.2017.00114
pubmed: 29085806
pmcid: 5649210
Grabowski JM, Hill CA. A roadmap for tick-borne flavivirus research in the “Omics” era. Front Cell Infect Microbiol. 2017;7:519. https://doi.org/10.3389/fcimb.2017.00519 .
doi: 10.3389/fcimb.2017.00519
pubmed: 29312896
pmcid: 5744076
Lindenbach BD, Thiel H-J, Rice CM. Flaviviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields virology. 5th ed. Lippincott-Raven Publishers: Philadelphia; 2007. p. 1101–52.
Simser JA, Palmer AT, Fingerle V, Wilske B, Kurtti TJ, Munderloh UG. Rickettsia monacensis sp. nov., a spotted fever group rickettsia, from ticks (Ixodes ricinus) collected in a European city park. Appl Environ Microbiol. 2002;68:4559–66. https://doi.org/10.1128/AEM.68.9.4559-4566.2002 .
doi: 10.1128/AEM.68.9.4559-4566.2002
pubmed: 12200314
pmcid: 124077
Bell-Sakyi L, Zweygarth E, Blouin EF, Gould EA, Jongejan F. Tick cell lines: tools for tick and tick-borne disease research. Trends Parasitol. 2007;23:450–7.
doi: 10.1016/j.pt.2007.07.009
Pospíšil L, Jandásek L, Pešek J. Isolation of new strains of meningoencephalitis virus in the Brno region during the summer of 1953. Lek List. 1954;9:388–9.
pubmed: 13234616
Mansfield KL, Morales AB, Johnson N, Ayllón N, Höfle U, Alberdi P, et al. Identification and characterization of a novel tick-borne flavivirus subtype in goats (Capra hircus) in Spain. J Gen Virol. 2015;96:1676–81.
doi: 10.1099/vir.0.000096
Titz B, Thomas S, Rajagopala SV, Chiba T, Ito T, Uetz P. Transcriptional activators in yeast. Nucleic Acids Res. 2006;34:955–67. https://doi.org/10.1093/nar/gkj493 .
doi: 10.1093/nar/gkj493
pubmed: 16464826
pmcid: 1361621
Vidalain PO, Boxem M, Ge H, Li S, Vidal M. Increasing specificity in high-throughput yeast two-hybrid experiments. Methods. 2004;32:363–70.
doi: 10.1016/j.ymeth.2003.10.001
Walhout AJM, Vidal M. High-throughput yeast two-hybrid assays for large-scale protein interaction mapping. Methods. 2001;24:297–306. https://doi.org/10.1006/METH.2001.1190 .
doi: 10.1006/METH.2001.1190
pubmed: 11403578
Gulia-Nuss M, Nuss AB, Meyer JM, Sonenshine DE, Roe RM, Waterhouse RM, et al. Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun. 2016;7:10507. https://doi.org/10.1038/ncomms10507 .
doi: 10.1038/ncomms10507
pubmed: 26856261
pmcid: 4748124
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. https://doi.org/10.1101/gr.1239303 .
doi: 10.1101/gr.1239303
pubmed: 403769
pmcid: 403769
Assenov Y, Ramírez F, Schelhorn SESE, Lengauer T, Albrecht M. Computing topological parameters of biological networks. Bioinformatics. 2008;24:282–4. https://doi.org/10.1093/bioinformatics/btm554 .
doi: 10.1093/bioinformatics/btm554
pubmed: 18006545
Weisheit S, Villar M, Tykalová H, Popara M, Loecherbach J, Watson M, et al. Ixodes scapularis and Ixodes ricinus tick cell lines respond to infection with tick-borne encephalitis virus: transcriptomic and proteomic analysis. Parasites Vectors. 2015;8:1–26.
doi: 10.1186/s13071-015-1210-x
Mansfield KL, Cook C, Ellis RJ, Bell-Sakyi L, Johnson N, Alberdi P, et al. Tick-borne pathogens induce differential expression of genes promoting cell survival and host resistance in Ixodes ricinus cells. Parasites Vectors. 2017;10:1–12.
doi: 10.1186/s13071-017-2011-1
Růžek D, Bell-Sakyi L, Kopecký J, Grubhoffer L. Growth of tick-borne encephalitis virus (European subtype) in cell lines from vector and non-vector ticks. Virus Res. 2008;137:142–6. https://doi.org/10.1016/j.virusres.2008.05.013 .
doi: 10.1016/j.virusres.2008.05.013
pubmed: 18602711
Mi H, Muruganujan A, Thomas PD. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res. 2013;41:D377–86. https://doi.org/10.1038/nprot.2013.092 .
doi: 10.1038/nprot.2013.092
pubmed: 23193289
Thomas PD, Kejariwal A, Campbell MJ, Mi H, Diemer K, Guo N, et al. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification | Nucleic Acids Research | Oxford Academic. Nucleic Acids Res. 2003;31:334–41. https://doi.org/10.1093/nar/gkg115 .
doi: 10.1093/nar/gkg115
pubmed: 12520017
pmcid: 165562
Supek F, Bošnjak M, Škunca N, Šmuc T. Revigo summarizes and visualizes long lists of gene ontology terms. PLoS ONE. 2011;6:e21800.
doi: 10.1371/journal.pone.0021800
Riesgo-Escovar JR, Hafen E. Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev. 1997;11:1717–27. https://doi.org/10.1101/gad.11.13.1717 .
doi: 10.1101/gad.11.13.1717
pubmed: 9224720
Kockel L, Zeitlinger J, Staszewski LM, Mlodzik M, Bohmann D. Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev. 1997;11:1748–58. https://doi.org/10.1101/gad.11.13.1748 .
doi: 10.1101/gad.11.13.1748
pubmed: 9224723
Franciscovich AL, Vrailas Mortimer AD, Freeman AA, Gu J, Sanyal S. Overexpression screen in drosophila identifies neuronal roles of GSK-3β/shaggy as a regulator of AP-1-dependent developmental plasticity. Genetics. 2008;180:2057–71. https://doi.org/10.1534/genetics.107.085555 .
doi: 10.1534/genetics.107.085555
pubmed: 18832361
pmcid: 2600941
Bishop GA, Abdul-Sater AA, Watts TH. Editorial: TRAF proteins in health and disease. Front Immunol. 2019;10:326. https://doi.org/10.3389/fimmu.2019.00326 .
doi: 10.3389/fimmu.2019.00326
pubmed: 30863413
pmcid: 6400096
Xie P. TRAF molecules in cell signaling and in human diseases. J Mol Signal. 2013. https://doi.org/10.1186/1750-2187-8-7 .
doi: 10.1186/1750-2187-8-7
pubmed: 23758787
pmcid: 3697994
Yin H, Shi Z, Jiao S, Chen C, Wang W, Greene MI, et al. Germinal center kinases in immune regulation. Cell Mol Immunol. 2012;9:439–45. https://doi.org/10.1038/cmi.2012.30 .
doi: 10.1038/cmi.2012.30
pubmed: 22960604
pmcid: 4002213
Preisinger C, Short B, De Corte V, Bruyneel E, Haas A, Kopajtich R, et al. YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14–3-3ζ. J Cell Biol. 2004;164:1009–20. https://doi.org/10.1083/jcb.200310061 .
doi: 10.1083/jcb.200310061
pubmed: 15037601
pmcid: 2172068
Lin JL, Chen HC, Fang HI, Robinson D, Kung HJ, Shih HM. MST4, a new Ste20-related kinase that mediates cell growth and transformation via modulating ERK pathway. Oncogene. 2001;20:6559–69. https://doi.org/10.1038/sj.onc.1204818 .
doi: 10.1038/sj.onc.1204818
pubmed: 11641781
Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell. 2000;101:199–210. https://doi.org/10.1016/S0092-8674(00)80830-2 .
doi: 10.1016/S0092-8674(00)80830-2
pubmed: 10786835
Uytterhoeven V, Lauwers E, Maes I, Miskiewicz K, Melo MN, Swerts J, et al. Hsc70-4 deforms membranes to promote synaptic protein turnover by endosomal microautophagy. Neuron. 2015;88:735–48.
doi: 10.1016/j.neuron.2015.10.012
Tobaben S, Thakur P, Fernández-Chacón R, Südhof TC, Rettig J, Stahl B. A trimeric protein complex functions as a synaptic chaperone machine. Neuron. 2001;31:987–99.
doi: 10.1016/S0896-6273(01)00427-5
Leznicki P, High S. SGTA antagonizes BAG6-mediated protein triage. Proc Natl Acad Sci USA. 2012;109:19214–9. https://doi.org/10.1073/pnas.1209997109 .
doi: 10.1073/pnas.1209997109
pubmed: 23129660
pmcid: 3511132
Krysztofinska EM, Martínez-Lumbreras S, Thapaliya A, Evans NJ, High S, Isaacson RL. Structural and functional insights into the E3 ligase, RNF126. Sci Rep. 2016. https://doi.org/10.1038/srep26433 .
doi: 10.1038/srep26433
pubmed: 27827410
pmcid: 5101480
Asante D, Stevenson NL, Stephens DJ. Subunit composition of the human cytoplasmic dynein-2 complex. J Cell Sci. 2014;127:4774–87. https://doi.org/10.1242/jcs.159038 .
doi: 10.1242/jcs.159038
pubmed: 25205765
pmcid: 4215718
Roberts AJ, Kon T, Knight PJ, Sutoh K, Burgess SA. Functions and mechanics of dynein motor proteins. Nat Rev Mol Cell Biol. 2013;14:713–26. https://doi.org/10.1038/nrm3667 .
doi: 10.1038/nrm3667
pubmed: 24064538
pmcid: 3972880
Kreko-Pierce T, Eaton BA. The Drosophila LC8 homolog cut up specifies the axonal transport of proteasomes. J Cell Sci. 2017;130:3388–98. https://doi.org/10.1242/jcs.207027 .
doi: 10.1242/jcs.207027
pubmed: 28808087
pmcid: 5665441
Callebaut I, De Gunzburg J, Goud B, Mornon JP. RUN domains: a new family of domains involved in Ras-like GTPase signaling. Trends Biochem Sci. 2001;26:79–83. https://doi.org/10.1016/S0968-0004(00)01730-8 .
doi: 10.1016/S0968-0004(00)01730-8
pubmed: 11166556
Mari M, Macia E, Le Marchand-Brustel Y, Cormont M. Role of the FYVE finger and the RUN domain for the subcellular localization of Rabip4. J Biol Chem. 2001;276:42501–8. https://doi.org/10.1074/jbc.M104885200 .
doi: 10.1074/jbc.M104885200
pubmed: 11509568
Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129:S3-14. https://doi.org/10.1017/S0031182004005967 .
doi: 10.1017/S0031182004005967
pubmed: 15938502
Le Breton M, Meyniel-Schicklin L, Deloire A, Coutard B, Canard B, de Lamballerie X, et al. Flavivirus NS3 and NS5 proteins interaction network: a high-throughput yeast two-hybrid screen. BMC Microbiol. 2011;11:234. https://doi.org/10.1186/1471-2180-11-234 .
doi: 10.1186/1471-2180-11-234
pubmed: 22014111
pmcid: 3215679
Tham HW, Balasubramaniam VRMT, Chew MF, Ahmad H, Hassan SS. Protein–protein interactions between A. aegypti midgut and dengue virus 2: two-hybrid screens using the midgut cDNA library. J Infect Dev Ctries. 2015;9:1338–49. https://doi.org/10.3855/jidc.6422 .
doi: 10.3855/jidc.6422
pubmed: 26719940
Guo X, Xu Y, Bian G, Pike AD, Xie Y, Xi Z. Response of the mosquito protein interaction network to dengue infection. BMC Genom. 2010. https://doi.org/10.1186/1471-2164-11-380 .
doi: 10.1186/1471-2164-11-380
Mairiang D, Zhang H, Sodja A, Murali T, Suriyaphol P, Malasit P, et al. Identification of new protein interactions between dengue fever virus and its hosts, human and mosquito. PLoS ONE. 2013;8:e53535. https://doi.org/10.1371/journal.pone.0053535 .
doi: 10.1371/journal.pone.0053535
pubmed: 23326450
pmcid: 3543448
Mansfield KL, Jizhou L, Phipps LP, Johnson N. Emerging tick-borne viruses in the twenty-first century. Front Cell Infect Microbiol. 2017. https://doi.org/10.3389/fcimb.2017.00298 .
doi: 10.3389/fcimb.2017.00298
pubmed: 28744449
pmcid: 5504652
Jia N, Wang J, Shi W, Du L, Sun Y, Zhan W, et al. Large-scale comparative analyses of tick genomes elucidate their genetic diversity and vector capacities. Cell. 2020;182(1328–1340):e13. https://doi.org/10.1016/j.cell.2020.07.023 .
doi: 10.1016/j.cell.2020.07.023
Cramaro WJ, Revets D, Hunewald OE, Sinner R, Reye AL, Muller CP. Integration of Ixodes ricinus genome sequencing with transcriptome and proteome annotation of the naïve midgut. BMC Genom. 2015;16:871. https://doi.org/10.1186/s12864-015-1981-7 .
doi: 10.1186/s12864-015-1981-7
Cramaro WJ, Hunewald OE, Bell-Sakyi L, Muller CP. Genome scaffolding and annotation for the pathogen vector Ixodes ricinus by ultra-long single molecule sequencing. Parasites Vectors. 2017. https://doi.org/10.1186/s13071-017-2008-9 .
doi: 10.1186/s13071-017-2008-9
pubmed: 28179027
pmcid: 5299676
Li S, Armstrong CM, Bertin N, Ge H, Milstein S, Boxem M, et al. A map of the interactome network of the metazoan C. elegans. Science. 2004;303:540–3. https://doi.org/10.1126/science.1091403 .
doi: 10.1126/science.1091403
pubmed: 14704431
pmcid: 1698949
Chen WY, Ho KC, Leu JH, Liu KF, Wang HC, Kou GH, et al. WSSV infection activates STAT in shrimp. Dev Comp Immunol. 2008;32:1142–50. https://doi.org/10.1016/j.dci.2008.03.003 .
doi: 10.1016/j.dci.2008.03.003
pubmed: 18460415
Braun P, Tasan M, Dreze M, Barrios-Rodiles M, Lemmens I, Yu H, et al. An experimentally derived confidence score for binary protein–protein interactions. Nat Methods. 2009;6:91–7. https://doi.org/10.1038/nmeth.1281 .
doi: 10.1038/nmeth.1281
pubmed: 19060903
Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, Chaerkady R, et al. A draft map of the human proteome. Nature. 2014;509:575–81. https://doi.org/10.1038/nature13302 .
doi: 10.1038/nature13302
pubmed: 24870542
pmcid: 4403737
Wilhelm M, Schlegl J, Hahne H, Gholami AM, Lieberenz M, Savitski MM, et al. Mass-spectrometry-based draft of the human proteome. Nature. 2014;509:582–7. https://doi.org/10.1038/nature13319 .
doi: 10.1038/nature13319
pubmed: 24870543
Jensen LJ, Bork P. Biochemistry: not comparable, but complementary. Science. 2008;322:56–7. https://doi.org/10.1126/science.1164801 .
doi: 10.1126/science.1164801
pubmed: 18832636
Khadka S, Vangeloff AD, Zhang C, Siddavatam P, Heaton NS, Wang L, et al. A physical interaction network of dengue virus and human proteins. Mol Cell Proteom. 2011. https://doi.org/10.1074/mcp.M111.012187 .
doi: 10.1074/mcp.M111.012187
Shah PS, Link N, Jang GM, Sharp PP, Zhu T, Swaney DL, et al. Comparative flavivirus-host protein interaction mapping reveals mechanisms of dengue and Zika virus pathogenesis. Cell. 2018;175(7):1931–45.
doi: 10.1016/j.cell.2018.11.028
Hafirassou ML, Meertens L, Umaña-Diaz C, Labeau A, Dejarnac O, Bonnet-Madin L, et al. A global interactome map of the dengue virus NS1 identifies virus restriction and dependency host factors. Cell Rep. 2018;22:1364. https://doi.org/10.1016/J.CELREP.2018.01.038 .
doi: 10.1016/J.CELREP.2018.01.038
pubmed: 29386121
Deddouche S, Matt N, Budd A, Mueller S, Kemp C, Galiana-Arnoux D, et al. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat Immunol. 2008;9:1425–32. https://doi.org/10.1038/ni.1664 .
doi: 10.1038/ni.1664
pubmed: 18953338
Paradkar PN, Trinidad L, Voysey R, Duchemin JB, Walker PJ. Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proc Natl Acad Sci USA. 2012;109:18915–20.
doi: 10.1073/pnas.1205231109
Paradkar PN, Duchemin J-B, Voysey R, Walker PJ. Dicer-2-dependent activation of Culex Vago occurs via the TRAF-Rel2 signaling pathway. PLoS Negl Trop Dis. 2014;8:e2823. https://doi.org/10.1371/journal.pntd.0002823 .
doi: 10.1371/journal.pntd.0002823
pubmed: 24762775
pmcid: 3998923
Souza-Neto JA, Sim S, Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA. 2009;106:17841–6.
doi: 10.1073/pnas.0905006106
Angleró-Rodríguez YI, MacLeod HJ, Kang S, Carlson JS, Jupatanakul N, Dimopoulos G. Aedes aegypti molecular responses to Zika Virus: modulation of infection by the toll and Jak/Stat immune pathways and virus host factors. Front Microbiol. 2017. https://doi.org/10.3389/fmicb.2017.02050 .
doi: 10.3389/fmicb.2017.02050
pubmed: 29109710
pmcid: 5660061
Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer. 2003;3:859–68. https://doi.org/10.1038/nrc1209 .
doi: 10.1038/nrc1209
pubmed: 14668816
Hernandez JM, Floyd DH, Weilbaecher KN, Green PL, Boris-Lawrie K. Multiple facets of junD gene expression are atypical among AP-1 family members. Oncogene. 2008;27:4757–67. https://doi.org/10.1038/onc.2008.120 .
doi: 10.1038/onc.2008.120
pubmed: 18427548
pmcid: 2726657
Thébault S, Basbous J, Hivin P, Devaux C, Mesnard JM. HBZ interacts with JunD and stimulates its transcriptional activity. FEBS Lett. 2004;562:165–70. https://doi.org/10.1016/S0014-5793(04)00225-X .
doi: 10.1016/S0014-5793(04)00225-X
pubmed: 15044019
Larocque E, Andre-Arpin C, Borowiak M, Lemay G, Switzer WM, Duc Dodon M, et al. Human T-cell leukemia virus type 3 (HTLV-3) and HTLV-4 antisense-transcript-encoded proteins interact and transactivate Jun family-dependent transcription via their atypical bZIP motif. J Virol. 2014;88:8956–70. https://doi.org/10.1128/jvi.01094-14 .
doi: 10.1128/jvi.01094-14
pubmed: 24872589
pmcid: 4136272
Kuhlmann AS, Villaudy J, Gazzolo L, Castellazzi M, Mesnard JM, Dodon MD. HTLV-1 HBZ cooperates with JunD to enhance transcription of the human telomerase reverse transcriptase gene (hTERT). Retrovirology. 2007. https://doi.org/10.1186/1742-4690-4-92 .
doi: 10.1186/1742-4690-4-92
pubmed: 18078517
pmcid: 2235888
Jantrapirom S, Piccolo LL, Pruksakorn D, Potikanond S, Nimlamool W. Ubiquilin networking in cancers. Cancers. 2020;12:1–17. https://doi.org/10.3390/cancers12061586 .
doi: 10.3390/cancers12061586
Gao L, Tu H, Shi ST, Lee K-J, Asanaka M, Hwang SB, et al. Interaction with a ubiquitin-like protein enhances the ubiquitination and degradation of hepatitis C virus RNA-dependent RNA polymerase. J Virol. 2003;77:4149–59. https://doi.org/10.1128/jvi.77.7.4149-4159.2003 .
doi: 10.1128/jvi.77.7.4149-4159.2003
pubmed: 12634373
pmcid: 150629
Li M, Johnson JR, Truong B, Kim G, Weinbren N, Dittmar M, et al. Identification of antiviral roles for the exon–junction complex and nonsense-mediated decay in flaviviral infection. Nat Microbiol. 2019;4:985–95. https://doi.org/10.1038/s41564-019-0375-z .
doi: 10.1038/s41564-019-0375-z
pubmed: 30833725
pmcid: 6533143
Biswas N, Liu S, Ronni T, Aussenberg SE, Liu W, Fujita T, et al. The ubiquitin-like protein PLIC-1 or ubiquilin 1 inhibits TLR3-Trif signaling. PLoS ONE. 2011. https://doi.org/10.1371/journal.pone.0021153 .
doi: 10.1371/journal.pone.0021153
pubmed: 22216279
pmcid: 3247263
Rapali P, Szenes Á, Radnai L, Bakos A, Pál G, Nyitray L. DYNLL/LC8: a light chain subunit of the dynein motor complex and beyond. FEBS J. 2011;278:2980–96. https://doi.org/10.1111/j.1742-4658.2011.08254.x .
doi: 10.1111/j.1742-4658.2011.08254.x
pubmed: 21777386
Dodding MP, Way M. Coupling viruses to dynein and kinesin-1. EMBO J. 2011;30:3527–39. https://doi.org/10.1038/emboj.2011.283 .
doi: 10.1038/emboj.2011.283
pubmed: 21878994
pmcid: 3181490
Izidoro-Toledo TC, Borges AC, Araujo DD, Leitão Mazzi DPS, Junior FON, Sousa JF, et al. A myosin-Va tail fragment sequesters dynein light chains leading to apoptosis in melanoma cells. Cell Death Dis. 2013. https://doi.org/10.1038/cddis.2013.45 .
doi: 10.1038/cddis.2013.45
pubmed: 23519116
pmcid: 3613824
Fili N, Toseland CP. Unconventional myosins: how regulation meets function. Int J Mol Sci. 2020. https://doi.org/10.3390/ijms21010067 .
doi: 10.3390/ijms21010067
Real-Hohn A, Provance DW, Gonçalves RB, Denani CB, de Oliveira AC, Salerno VP, et al. Impairing the function of MLCK, myosin Va or myosin Vb disrupts Rhinovirus B14 replication. Sci Rep. 2017. https://doi.org/10.1038/s41598-017-17501-z .
doi: 10.1038/s41598-017-17501-z
pubmed: 29215055
pmcid: 5719429
Roberts KL, Baines JD. Myosin Va enhances secretion of herpes simplex virus 1 virions and cell surface expression of viral glycoproteins. J Virol. 2010;84:9889–96. https://doi.org/10.1128/jvi.00732-10 .
doi: 10.1128/jvi.00732-10
pubmed: 20631136
pmcid: 2937760
Wilkie AR, Sharma M, Pesola JM, Ericsson M, Fernandez R, Coen DM. A role for myosin Va in human cytomegalovirus nuclear egress. J Virol. 2018. https://doi.org/10.1128/jvi.01849-17 .
doi: 10.1128/jvi.01849-17
pubmed: 30333173
pmcid: 6288344
Xu XF, Chen ZT, Gao N, Zhang JL, An J. Myosin Vc, a member of the actin motor family associated with Rab8, is involved in the release of DV2 from HepG2 cells. Intervirology. 2009;52:258–65. https://doi.org/10.1159/000230669 .
doi: 10.1159/000230669
pubmed: 19641326
Zhang H, Ma X, Shi T, Song Q, Zhao H, Ma D. NSA2, a novel nucleolus protein regulates cell proliferation and cell cycle. Biochem Biophys Res Commun. 2010;391:651–8. https://doi.org/10.1016/j.bbrc.2009.11.114 .
doi: 10.1016/j.bbrc.2009.11.114
pubmed: 19932687
Xing J, Nan X, Cui Q, Ma W, Zhao H. Nop-7-associated 2 (NSA2) is required for ribosome biogenesis and protein synthesis. Biochem Biophys Res Commun. 2018;505:249–54. https://doi.org/10.1016/j.bbrc.2018.09.041 .
doi: 10.1016/j.bbrc.2018.09.041
pubmed: 30243719
Sotcheff S, Routh A. Understanding flavivirus capsid protein functions: the tip of the iceberg. Pathogens. 2020. https://doi.org/10.3390/pathogens9010042 .
doi: 10.3390/pathogens9010042
pubmed: 31948047
pmcid: 7168633
Tsuda Y, Mori Y, Abe T, Yamashita T, Okamoto T, Ichimura T, et al. Nucleolar protein B23 interacts with Japanese encephalitis virus core protein and participates in viral replication. Microbiol Immunol. 2006;50:225–34. https://doi.org/10.1111/j.1348-0421.2006.tb03789.x .
doi: 10.1111/j.1348-0421.2006.tb03789.x
pubmed: 16547420
Balinsky CA, Schmeisser H, Ganesan S, Singh K, Pierson TC, Zoon KC. Nucleolin Interacts with the dengue virus capsid protein and plays a role in formation of infectious virus particles. J Virol. 2013;87:13094–106. https://doi.org/10.1128/jvi.00704-13 .
doi: 10.1128/jvi.00704-13
pubmed: 24027323
pmcid: 3838225
Taracena ML, Bottino-Rojas V, Talyuli OAC, Walter-Nuno AB, Oliveira JHM, Angleró-Rodriguez YI, et al. Regulation of midgut cell proliferation impacts Aedes aegypti susceptibility to dengue virus. PLoS Negl Trop Dis. 2018. https://doi.org/10.1371/journal.pntd.0006498 .
doi: 10.1371/journal.pntd.0006498
pubmed: 29782512
pmcid: 5983868
Ličková M, Fumačová Havlíková S, Sláviková M, Slovák M, Drexler JF, Klempa B. Dermacentor reticulatus is a vector of tick-borne encephalitis virus. Ticks Tick Borne Dis. 2020;11(4):101414.
doi: 10.1016/j.ttbdis.2020.101414
Belova OA, Litov AG, Kholodilov IS, Kozlovskaya LI, Bell-Sakyi L, Romanova LI, et al. Properties of the tick-borne encephalitis virus population during persistent infection of ixodid ticks and tick cell lines. Ticks Tick Borne Dis. 2017;8:895–906. https://doi.org/10.1016/j.ttbdis.2017.07.008 .
doi: 10.1016/j.ttbdis.2017.07.008
pubmed: 28784308