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Volume 95, Issue 12

Characterization of a novel insect-specific flavivirus from Brazil: potential for inhibition of infection of arthropod cells with medically important flaviviruses Free

Abstract

In the past decade, there has been an upsurge in the number of newly described insect-specific flaviviruses isolated pan-globally. We recently described the isolation of a novel flavivirus (tentatively designated ‘Nhumirim virus’; NHUV) that represents an example of a unique subset of apparently insect-specific viruses that phylogenetically affiliate with dual-host mosquito-borne flaviviruses despite appearing to be limited to replication in mosquito cells. We characterized the growth potential and 3′ untranslated region (UTR) sequence homology with alternative flaviviruses, and evaluated the virus’s capacity to suppress replication of representative spp.-vectored pathogenic flaviviruses in mosquito cells. Only mosquito cell lines were found to support NHUV replication, further reinforcing the insect-specific phenotype of this virus. Analysis of the sequence and predicted RNA secondary structures of the 3′ UTR indicated NHUV to be most similar to viruses within the yellow fever serogroup and Japanese encephalitis serogroup, and viruses in the tick-borne flavivirus clade. NHUV was found to share the fewest conserved sequence elements when compared with traditional insect-specific flaviviruses. This suggests that, despite apparently being insect specific, this virus probably diverged from an ancestral mosquito-borne flavivirus. Co-infection experiments indicated that prior or concurrent infection of mosquito cells with NHUV resulted in a significant reduction in virus production of West Nile virus (WNV), St Louis encephalitis virus (SLEV) and Japanese encephalitis virus. The inhibitory effect was most effective against WNV and SLEV with over a 10-fold and 10-fold reduction in peak titres, respectively.

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© 2014 The Authors
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2014-12-01
2024-04-26
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References

  1. Akashi H. 1994; Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:927–935[PubMed]
     [Google Scholar]
  2. Aliota M. T., Jones S. A., Dupuis A. P. II, Ciota A. T., Hubalek Z., Kramer L. D. 2012; Characterization of Rabensburg virus, a flavivirus closely related to West Nile virus of the Japanese encephalitis antigenic group. PLoS ONE 7:e39387 [View Article][PubMed]
     [Google Scholar]
  3. Almirón W. R., Brewer M. M. 1995; [Host preference of Culicidae (Diptera) collected in central Argentina]. Rev Saude Publica 29:108–114 (in Spanish) [View Article][PubMed]
     [Google Scholar]
  4. Aranda C., Sánchez-Seco M. P., Cáceres F., Escosa R., Gálvez J. C., Masià M., Marqués E., Ruíz S., Alba A.other authors 2009; Detection and monitoring of mosquito flaviviruses in Spain between 2001 and 2005. Vector Borne Zoonotic Dis 9:171–178 [View Article][PubMed]
     [Google Scholar]
  5. Biacchesi S., Skiadopoulos M. H., Yang L., Murphy B. R., Collins P. L., Buchholz U. J. 2005; Rapid human metapneumovirus microneutralization assay based on green fluorescent protein expression. J Virol Methods 128:192–197 [View Article][PubMed]
     [Google Scholar]
  6. Blitvich B. J., Lin M., Dorman K. S., Soto V., Hovav E., Tucker B. J., Staley M., Platt K. B., Bartholomay L. C. 2009; Genomic sequence and phylogenetic analysis of Culex flavivirus, an insect-specific flavivirus, isolated from Culex pipiens (Diptera: Culicidae) in Iowa. J Med Entomol 46:934–941 [View Article][PubMed]
     [Google Scholar]
  7. Bolling B. G., Eisen L., Moore C. G., Blair C. D. 2011; Insect-specific flaviviruses from Culex mosquitoes in Colorado, with evidence of vertical transmission. Am J Trop Med Hyg 85:169–177 [View Article][PubMed]
     [Google Scholar]
  8. Bolling B. G., Olea-Popelka F. J., Eisen L., Moore C. G., Blair C. D. 2012; Transmission dynamics of an insect-specific flavivirus in a naturally infected Culex pipiens laboratory colony and effects of co-infection on vector competence for West Nile virus. Virology 427:90–97 [View Article][PubMed]
     [Google Scholar]
  9. Calzolari M., Bonilauri P., Bellini R., Caimi M., Defilippo F., Maioli G., Albieri A., Medici A., Veronesi R.other authors 2010; Arboviral survey of mosquitoes in two northern Italian regions in 2007 and 2008. Vector Borne Zoonotic Dis 10:875–884 [View Article][PubMed]
     [Google Scholar]
  10. Castle E., Leidner U., Nowak T., Wengler G., Wengler G. 1986; Primary structure of the West Nile flavivirus genome region coding for all nonstructural proteins. Virology 149:10–26 [View Article][PubMed]
     [Google Scholar]
  11. Charlier N., Leyssen P., Pleij C. W., Lemey P., Billoir F., Van Laethem K., Vandamme A. M., De Clercq E., de Lamballerie X., Neyts J. 2002; Complete genome sequence of Montana Myotis leukoencephalitis virus, phylogenetic analysis and comparative study of the 3′ untranslated region of flaviviruses with no known vector. J Gen Virol 83:1875–1885[PubMed]
     [Google Scholar]
  12. Cirimotich C. M., Ramirez J. L., Dimopoulos G. 2011; Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10:307–310 [View Article][PubMed]
     [Google Scholar]
  13. Clarke B. 1970; Darwinian evolution of proteins. Science 168:1009–1011 [View Article][PubMed]
     [Google Scholar]
  14. Cook S., Bennett S. N., Holmes E. C., De Chesse R., Moureau G., de Lamballerie X. 2006; Isolation of a new strain of the flavivirus cell fusing agent virus in a natural mosquito population from Puerto Rico. J Gen Virol 87:735–748 [View Article][PubMed]
     [Google Scholar]
  15. Cook S., Moureau G., Harbach R. E., Mukwaya L., Goodger K., Ssenfuka F., Gould E., Holmes E. C., de Lamballerie X. 2009; Isolation of a novel species of flavivirus and a new strain of Culex flavivirus (Flaviviridae) from a natural mosquito population in Uganda. J Gen Virol 90:2669–2678 [View Article][PubMed]
     [Google Scholar]
  16. Crabtree M. B., Sang R. C., Stollar V., Dunster L. M., Miller B. R. 2003; Genetic and phenotypic characterization of the newly described insect flavivirus, Kamiti River virus. Arch Virol 148:1095–1118 [View Article][PubMed]
     [Google Scholar]
  17. Crabtree M. B., Nga P. T., Miller B. R. 2009; Isolation and characterization of a new mosquito flavivirus, Quang Binh virus, from Vietnam. Arch Virol 154:857–860 [View Article][PubMed]
     [Google Scholar]
  18. Crockett R. K., Burkhalter K., Mead D., Kelly R., Brown J., Varnado W., Roy A., Horiuchi K., Biggerstaff B. J.other authors 2012; Culex flavivirus and West Nile virus in Culex quinquefasciatus populations in the southeastern United States. J Med Entomol 49:165–174 [View Article][PubMed]
     [Google Scholar]
  19. Eaton B. T. 1979; Heterologous interference in Aedes albopictus cells infected with alphaviruses. J Virol 30:45–55[PubMed]
     [Google Scholar]
  20. Eaton B. T. 1981; Viral interference and persistence in Sindbis virus infected Aedes albopictus cells. Can J Microbiol 27:563–567 [View Article][PubMed]
     [Google Scholar]
  21. Edgar R. C. 2004; muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  22. Evangelista J., Cruz C., Guevara C., Astete H., Carey C., Kochel T. J., Morrison A. C., Williams M., Halsey E. S., Forshey B. M. 2013; Characterization of a novel flavivirus isolated from Culex (Melanoconion) ocossa mosquitoes from Iquitos, Peru. J Gen Virol 94:1266–1272 [View Article][PubMed]
     [Google Scholar]
  23. Farfan-Ale J. A., Loroño-Pino M. A., Garcia-Rejon J. E., Hovav E., Powers A. M., Lin M., Dorman K. S., Platt K. B., Bartholomay L. C.other authors 2009; Detection of RNA from a novel West Nile-like virus and high prevalence of an insect-specific flavivirus in mosquitoes in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 80:85–95[PubMed]
     [Google Scholar]
  24. Farfan-Ale J. A., Loroño-Pino M. A., Garcia-Rejon J. E., Soto V., Lin M., Staley M., Dorman K. S., Bartholomay L. C., Hovav E., Blitvich B. J. 2010; Detection of flaviviruses and orthobunyaviruses in mosquitoes in the Yucatan Peninsula of Mexico in 2008. Vector Borne Zoonotic Dis 10:777–783 [View Article][PubMed]
     [Google Scholar]
  25. Gentry M. K., Henchal E. A., McCown J. M., Brandt W. E., Dalrymple J. M. 1982; Identification of distinct antigenic determinants on dengue-2 virus using monoclonal antibodies. Am J Trop Med Hyg 31:548–555[PubMed]
     [Google Scholar]
  26. Gould E. A., de Lamballerie X., Zanotto P. M., Holmes E. C. 2003; Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59:277–314 [View Article][PubMed]
     [Google Scholar]
  27. Grard G., Moureau G., Charrel R. N., Lemasson J. J., Gonzalez J. P., Gallian P., Gritsun T. S., Holmes E. C., Gould E. A., de Lamballerie X. 2007; Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology 361:80–92 [View Article][PubMed]
     [Google Scholar]
  28. Gritsun T. S., Gould E. A. 2006a; The 3′ untranslated region of tick-borne flaviviruses originated by the duplication of long repeat sequences within the open reading frame. Virology 354:217–223 [View Article][PubMed]
     [Google Scholar]
  29. Gritsun T. S., Gould E. A. 2006b; The 3′ untranslated regions of Kamiti River virus and Cell fusing agent virus originated by self-duplication. J Gen Virol 87:2615–2619 [View Article][PubMed]
     [Google Scholar]
  30. Gritsun T. S., Gould E. A. 2006c; Direct repeats in the 3′ untranslated regions of mosquito-borne flaviviruses: possible implications for virus transmission. J Gen Virol 87:3297–3305 [View Article][PubMed]
     [Google Scholar]
  31. Gritsun T. S., Gould E. A. 2007a; Direct repeats in the flavivirus 3′ untranslated region; a strategy for survival in the environment?. Virology 358:258–265 [View Article][PubMed]
     [Google Scholar]
  32. Gritsun T. S., Gould E. A. 2007b; Origin and evolution of 3′UTR of flaviviruses: long direct repeats as a basis for the formation of secondary structures and their significance for virus transmission. Adv Virus Res 69:203–248 [View Article][PubMed]
     [Google Scholar]
  33. Gritsun T. S., Venugopal K., Zanotto P. M., Mikhailov M. V., Sall A. A., Holmes E. C., Polkinghorne I., Frolova T. V., Pogodina V. V.other authors 1997; Complete sequence of two tick-borne flaviviruses isolated from Siberia and the UK: analysis and significance of the 5′ and 3′-UTRs. Virus Res 49:27–39 [View Article][PubMed]
     [Google Scholar]
  34. Gritsun D. J., Jones I. M., Gould E. A., Gritsun T. S. 2014; Molecular archaeology of Flaviviridae untranslated regions: duplicated RNA structures in the replication enhancer of flaviviruses and pestiviruses emerged via convergent evolution. PLoS ONE 9:e92056 [View Article][PubMed]
     [Google Scholar]
  35. Gubler D. J. 2002; The global emergence/resurgence of arboviral diseases as public health problems. Arch Med Res 33:330–342 [View Article][PubMed]
     [Google Scholar]
  36. Hahn C. S., Hahn Y. S., Rice C. M., Lee E., Dalgarno L., Strauss E. G., Strauss J. H. 1987; Conserved elements in the 3′ untranslated region of flavivirus RNAs and potential cyclization sequences. J Mol Biol 198:33–41 [View Article][PubMed]
     [Google Scholar]
  37. Hobson-Peters J., Yam A. W., Lu J. W., Setoh Y. X., May F. J., Kurucz N., Walsh S., Prow N. A., Davis S. S.other authors 2013; A new insect-specific flavivirus from northern Australia suppresses replication of West Nile virus and Murray Valley encephalitis virus in co-infected mosquito cells. PLoS ONE 8:e56534 [View Article][PubMed]
     [Google Scholar]
  38. Hoshino K., Isawa H., Tsuda Y., Sawabe K., Kobayashi M. 2009; Isolation and characterization of a new insect flavivirus from Aedes albopictus and Aedes flavopictus mosquitoes in Japan. Virology 391:119–129 [View Article][PubMed]
     [Google Scholar]
  39. Huhtamo E., Putkuri N., Kurkela S., Manni T., Vaheri A., Vapalahti O., Uzcátegui N. Y. 2009; Characterization of a novel flavivirus from mosquitoes in northern Europe that is related to mosquito-borne flaviviruses of the tropics. J Virol 83:9532–9540 [View Article][PubMed]
     [Google Scholar]
  40. Ikemura T. 1981; Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol 151:389–409 [View Article][PubMed]
     [Google Scholar]
  41. Johnston R. E., Wan K., Bose H. R. 1974; Homologous interference induced by Sindbis virus. J Virol 14:1076–1082[PubMed]
     [Google Scholar]
  42. Junglen S., Kopp A., Kurth A., Pauli G., Ellerbrok H., Leendertz F. H. 2009; A new flavivirus and a new vector: characterization of a novel flavivirus isolated from uranotaenia mosquitoes from a tropical rain forest. J Virol 83:4462–4468 [View Article][PubMed]
     [Google Scholar]
  43. Karpf A. R., Lenches E., Strauss E. G., Strauss J. H., Brown D. T. 1997; Superinfection exclusion of alphaviruses in three mosquito cell lines persistently infected with Sindbis virus. J Virol 71:7119–7123[PubMed]
     [Google Scholar]
  44. Kent R. J., Crabtree M. B., Miller B. R. 2010a; Transmission of West Nile virus by Culex quinquefasciatus Say infected with Culex Flavivirus Izabal. PLoS Negl Trop Dis 4:e671 [View Article][PubMed]
     [Google Scholar]
  45. Kent R. J., Deus S., Williams M., Savage H. M. 2010b; Development of a multiplexed polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) assay to identify common members of the subgenera Culex (Culex) and Culex (Phenacomyia) in Guatemala. Am J Trop Med Hyg 83:285–291 [View Article][PubMed]
     [Google Scholar]
  46. Kim D. Y., Guzman H., Bueno R. Jr, Dennett J. A., Auguste A. J., Carrington C. V., Popov V. L., Weaver S. C., Beasley D. W., Tesh R. B. 2009; Characterization of Culex Flavivirus (Flaviviridae) strains isolated from mosquitoes in the United States and Trinidad. Virology 386:154–159 [View Article][PubMed]
     [Google Scholar]
  47. Kinney R. M., Huang C. Y., Whiteman M. C., Bowen R. A., Langevin S. A., Miller B. R., Brault A. C. 2006; Avian virulence and thermostable replication of the North American strain of West Nile virus. J Gen Virol 87:3611–3622 [View Article][PubMed]
     [Google Scholar]
  48. Kolodziejek J., Pachler K., Bin H., Mendelson E., Shulman L., Orshan L., Nowotny N. 2013; Barkedji virus, a novel mosquito-borne flavivirus identified in Culex perexiguus mosquitoes, Israel, 2011. J Gen Virol 94:2449–2457 [View Article][PubMed]
     [Google Scholar]
  49. Kuno G., Chang G. J., Tsuchiya K. R., Karabatsos N., Cropp C. B. 1998; Phylogeny of the genus Flavivirus. J Virol 72:73–83[PubMed]
     [Google Scholar]
  50. Langevin S. A., Bent Z. W., Solberg O. D., Curtis D. J., Lane P. D., Williams K. P., Schoeniger J. S., Sinha A., Lane T. W., Branda S. S. 2013; Peregrine: a rapid and unbiased method to produce strand-specific RNA-Seq libraries from small quantities of starting material. RNA Biol 10:502–515 [View Article][PubMed]
     [Google Scholar]
  51. Lauring A. S., Acevedo A., Cooper S. B., Andino R. 2012; Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12:623–632 [View Article][PubMed]
     [Google Scholar]
  52. Lee J. S., Grubaugh N. D., Kondig J. P., Turell M. J., Kim H. C., Klein T. A., O’Guinn M. L. 2013a; Isolation and genomic characterization of Chaoyang virus strain ROK144 from Aedes vexans nipponii from the Republic of Korea. Virology 435:220–224 [View Article][PubMed]
     [Google Scholar]
  53. Lee R. C., Hapuarachchi H. C., Chen K. C., Hussain K. M., Chen H., Low S. L., Ng L. C., Lin R., Ng M. M., Chu J. J. 2013b; Mosquito cellular factors and functions in mediating the infectious entry of Chikungunya virus. PLoS Negl Trop Dis 7:e2050 [View Article][PubMed]
     [Google Scholar]
  54. Lobo F. P., Mota B. E., Pena S. D., Azevedo V., Macedo A. M., Tauch A., Machado C. R., Franco G. R. 2009; Virus–host coevolution: common patterns of nucleotide motif usage in Flaviviridae and their hosts. PLoS ONE 4:e6282 [View Article][PubMed]
     [Google Scholar]
  55. Markoff L. 2003; 5′- and 3′-noncoding regions in flavivirus RNA. Adv Virus Res 59:177–228 [View Article][PubMed]
     [Google Scholar]
  56. Miller, M. A., Pfeiffer, W. & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, USA
  57. Morales-Betoulle M. E., Monzón Pineda M. L., Sosa S. M., Panella N., López M. R., Cordón-Rosales C., Komar N., Powers A., Johnson B. W. 2008; Culex flavivirus isolates from mosquitoes in Guatemala. J Med Entomol 45:1187–1190 [View Article][PubMed]
     [Google Scholar]
  58. Moretti S., Wilm A., Higgins D. G., Xenarios I., Notredame C. 2008; R-Coffee: a web server for accurately aligning noncoding RNA sequences. Nucleic Acids Res 36:Web Server issueW10–W13 [View Article][PubMed]
     [Google Scholar]
  59. Pabbaraju K., Ho K. C., Wong S., Fox J. D., Kaplen B., Tyler S., Drebot M., Tilley P. A. 2009; Surveillance of mosquito-borne viruses in Alberta using reverse transcription polymerase chain reaction with generic primers. J Med Entomol 46:640–648 [View Article][PubMed]
     [Google Scholar]
  60. Parreira R., Cook S., Lopes A., de Matos A. P., de Almeida A. P., Piedade J., Esteves A. 2012; Genetic characterization of an insect-specific flavivirus isolated from Culex theileri mosquitoes collected in southern Portugal. Virus Res 167:152–161 [View Article][PubMed]
     [Google Scholar]
  61. Pauvolid-Corrêa A., Kenney J. L., Couto-Lima D., Campos Z. M., Schatzmayr H. G., Nogueira R. M., Brault A. C., Komar N. 2013; Ilheus virus isolation in the Pantanal, west-central Brazil. PLoS Negl Trop Dis 7:e2318 [View Article][PubMed]
     [Google Scholar]
  62. Pauvolid-Corrêa A., Solberg O. D., Couto-Lima D., Kenney J. L., Serra-Freire N. M., Brault A. C., Nogueira J. R., Langevin S. A., Komar N. 2014; Nhumirim virus, a novel flavivirus isolated from mosquitoes from the Pantanal, Brazil. Arch Virol (in press)
    [Google Scholar]
  63. Pepin K. M., Domsic J., McKenna R. 2008; Genomic evolution in a virus under specific selection for host recognition. Infect Genet Evol 8:825–834 [View Article][PubMed]
     [Google Scholar]
  64. Pesko K., Mores C. N. 2009; Effect of sequential exposure on infection and dissemination rates for West Nile and St. Louis encephalitis viruses in Culex quinquefasciatus. Vector Borne Zoonotic Dis 9:281–286 [View Article][PubMed]
     [Google Scholar]
  65. Proutski V., Gould E. A., Holmes E. C. 1997; Secondary structure of the 3′ untranslated region of flaviviruses: similarities and differences. Nucleic Acids Res 25:1194–1202 [View Article][PubMed]
     [Google Scholar]
  66. Reed M., Muench H. 1938; A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–497
     [Google Scholar]
  67. Rice C. M., Lenches E. M., Eddy S. R., Shin S. J., Sheets R. L., Strauss J. H. 1985; Nucleotide sequence of yellow fever virus: implications for flavivirus gene expression and evolution. Science 229:726–733 [View Article][PubMed]
     [Google Scholar]
  68. Roiz D., Vázquez A., Seco M. P., Tenorio A., Rizzoli A. 2009; Detection of novel insect flavivirus sequences integrated in Aedes albopictus (Diptera: Culicidae) in Northern Italy. Virol J 6:93 [View Article][PubMed]
     [Google Scholar]
  69. Sánchez-Seco M. P., Vázquez A., Collao X., Hernández L., Aranda C., Ruiz S., Escosa R., Marqués E., Bustillo M. A.other authors 2010; Surveillance of arboviruses in Spanish wetlands: detection of new flavi- and phleboviruses. Vector Borne Zoonotic Dis 10:203–206 [View Article][PubMed]
     [Google Scholar]
  70. Sang R. C., Gichogo A., Gachoya J., Dunster M. D., Ofula V., Hunt A. R., Crabtree M. B., Miller B. R., Dunster L. M. 2003; Isolation of a new flavivirus related to cell fusing agent virus (CFAV) from field-collected flood-water Aedes mosquitoes sampled from a dambo in central Kenya. Arch Virol 148:1085–1093 [View Article][PubMed]
     [Google Scholar]
  71. Stamatakis A., Hoover P., Rougemont J. 2008; A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771 [View Article][PubMed]
     [Google Scholar]
  72. Vázquez A., Sánchez-Seco M. P., Palacios G., Molero F., Reyes N., Ruiz S., Aranda C., Marqués E., Escosa R.other authors 2012; Novel flaviviruses detected in different species of mosquitoes in Spain. Vector Borne Zoonotic Dis 12:223–229 [View Article][PubMed]
     [Google Scholar]
  73. Wang Z., An S., Wang Y., Han Y., Guo J. 2009; A new virus of flavivirus: Chaoyang virus isolated in Liaoning province. China J Pub Health 25:769–772 (in Chinese)
    [Google Scholar]
  74. Weiss B., Aksoy S. 2011; Microbiome influences on insect host vector competence. Trends Parasitol 27:514–522 [View Article][PubMed]
     [Google Scholar]
  75. Wengler G., Wengler G., Gross H. J. 1978; Studies on virus-specific nucleic acids synthesized in vertebrate and mosquito cells infected with flaviviruses. Virology 89:423–437 [View Article][PubMed]
     [Google Scholar]
  76. Zhao Z., Jiang C. 2007; Methylation-dependent transition rates are dependent on local sequence lengths and genomic regions. Mol Biol Evol 24:23–25 [View Article][PubMed]
     [Google Scholar]
  77. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [View Article][PubMed]
     [Google Scholar]
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Characterization of a novel insect-specific flavivirus from Brazil: potential for inhibition of infection of arthropod cells with medically important flaviviruses
J. Gen. Virol. 95, 2796 (2014); https://doi.org/10.1099/vir.0.068031-0
/content/journal/jgv/10.1099/vir.0.068031-0
/content/journal/jgv/10.1099/vir.0.068031-0
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