1887

Abstract

Duck Tembusu virus (DTMUV), a newly identified flavivirus, has rapidly spread to China, Malaysia and Thailand. The potential threats to public health have been well-highlighted; however its virulence and pathogenesis remain largely unknown. Here, by using reverse genetics, a recombinant chimeric DTMUV based on Japanese encephalitis live vaccine strain SA14-14-2 was obtained by substituting the corresponding prM and E genes (named ChinDTMUV). characterization demonstrated that ChinDTMUV replicated efficiently in mammalian cells with small-plaque phenotype in comparison with its parental viruses. Mouse tests showed ChinDTMUV exhibited avirulent phenotype in terms of neuroinvasiveness, while it retained neurovirulence from its parental virus DTMUV. Furthermore, immunization with ChinDTMUV was evidenced to elicit robust IgG and neutralizing antibody responses in mice. Overall, we successfully developed a viable chimeric DTMUV, and these results provide a useful platform for further investigation of the pathogenesis of DTMUV and development of a live attenuated DTMUV vaccine candidate.

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2016-07-01
2021-10-16
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References

  1. Arroyo J., Guirakhoo F., Fenner S., Zhang Z. X., Monath T. P., Chambers T. J. 2001; Molecular basis for attenuation of neurovirulence of a yellow fever virus/Japanese encephalitis virus chimera vaccine (ChimeriVax-JE). J Virol 75:934–942 [View Article][PubMed]
    [Google Scholar]
  2. Avirutnan P., Fuchs A., Hauhart R. E., Somnuke P., Youn S., Diamond M. S., Atkinson J. P. 2010; Antagonism of the complement component C4 by flavivirus nonstructural protein NS1. J Exp Med 207:793–806 [View Article][PubMed]
    [Google Scholar]
  3. Best S. M., Morris K. L., Shannon J. G., Robertson S. J., Mitzel D. N., Park G. S., Boer E., Wolfinbarger J. B., Bloom M. E. 2005; Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J Virol 79:12828–12839 [View Article][PubMed]
    [Google Scholar]
  4. Bhatt T. R., Crabtree M. B., Guirakhoo F., Monath T. P., Miller B. R. 2000; Growth characteristics of the chimeric Japanese encephalitis virus vaccine candidate, ChimeriVax-JE (YF/JE SA14-14-2), in Culex tritaeniorhynchus, Aedes albopictus, and Aedes aegypti mosquitoes. Am J Trop Med Hyg 62:480–484[PubMed]
    [Google Scholar]
  5. Bista M. B., Banerjee M. K., Shin S. H., Tandan J. B., Kim M. H., Sohn Y. M., Ohrr H. C., Tang J. L., Halstead S. B. 2001; Efficacy of single-dose SA 14-14-2 vaccine against Japanese encephalitis: a case control study. Lancet 358:791–795[PubMed] [CrossRef]
    [Google Scholar]
  6. Brandler S., Brown N., Ermak T. H., Mitchell F., Parsons M., Zhang Z., Lang J., Monath T. P., Guirakhoo F. 2005; Replication of chimeric yellow fever virus-dengue serotype 1–4 virus vaccine strains in dendritic and hepatic cells. Am J Trop Med Hyg 72:74–81[PubMed]
    [Google Scholar]
  7. Chambers T. J., Nestorowicz A., Mason P. W., Rice C. M. 1999; Yellow fever/Japanese encephalitis chimeric viruses: construction and biological properties. J Virol 73:3095–3101[PubMed]
    [Google Scholar]
  8. Chen L. K., Lin Y. L., Liao C. L., Lin C. G., Huang Y. L., Yeh C. T., Lai S. C., Jan J. T., Chin C. 1996; Generation and characterization of organ-tropism mutants of Japanese encephalitis virus in vivo and in vitro . Virology 223:79–88 [View Article][PubMed]
    [Google Scholar]
  9. Chen P., Liu J., Jiang Y., Zhao Y., Li Q., Wu L., He X., Chen H. 2014a; The vaccine efficacy of recombinant duck enteritis virus expressing secreted E with or without PrM proteins of duck tembusu virus. Vaccine 32:5271–5277 [View Article][PubMed]
    [Google Scholar]
  10. Chen S., Wang S., Li Z., Lin F., Cheng X., Zhu X., Wang J., Chen S., Huang M. et al. 2014b; Isolation and characterization of a Chinese strain of Tembusu virus from Hy-Line Brown layers with acute egg-drop syndrome in Fujian, China. Arch Virol 159:1099–1107 [View Article][PubMed]
    [Google Scholar]
  11. Courtney S. C., Scherbik S. V., Stockman B. M., Brinton M. A. 2012; West Nile virus infections suppress early viral RNA synthesis and avoid inducing the cell stress granule response. J Virol 86:3647–3657 [View Article][PubMed]
    [Google Scholar]
  12. Crook K. R., Miller-Kittrell M., Morrison C. R., Scholle F. 2014; Modulation of innate immune signaling by the secreted form of the West Nile virus NS1 glycoprotein. Virology 458–459:172–182 [View Article][PubMed]
    [Google Scholar]
  13. Evans J. D., Seeger C. 2007; Differential effects of mutations in NS4B on West Nile virus replication and inhibition of interferon signaling. J Virol 81:11809–11816 [View Article][PubMed]
    [Google Scholar]
  14. Gualano R. C., Pryor M. J., Cauchi M. R., Wright P. J., Davidson A. D. 1998; Identification of a major determinant of mouse neurovirulence of dengue virus type 2 using stably cloned genomic-length cDNA. J Gen Virol 79:437–446 [View Article][PubMed]
    [Google Scholar]
  15. Guirakhoo F., Weltzin R., Chambers T. J., Zhang Z. X., Soike K., Ratterree M., Arroyo J., Georgakopoulos K., Catalan J. et al. 2000; Recombinant chimeric yellow fever-dengue type 2 virus is immunogenic and protective in nonhuman primates. J Virol 74:5477–5485[PubMed] [CrossRef]
    [Google Scholar]
  16. Guy B., Jackson N. 2016; Dengue vaccine: hypotheses to understand CYD-TDV-induced protection. Nat Rev Microbiol 14:45–54 [View Article][PubMed]
    [Google Scholar]
  17. Holzmann H., Heinz F. X., Mandl C. W., Guirakhoo F., Kunz C. 1990; A single amino acid substitution in envelope protein E of tick-borne encephalitis virus leads to attenuation in the mouse model. J Virol 64:5156–5159[PubMed]
    [Google Scholar]
  18. Homonnay Z. G., Kovács E. W., Bányai K., Albert M., Fehér E., Mató T., Tatár-Kis T., Palya V. 2014; Tembusu-like flavivirus (Perak virus) as the cause of neurological disease outbreaks in young Pekin ducks. Avian Pathol 43:552–560 [View Article][PubMed]
    [Google Scholar]
  19. Huang X., Han K., Zhao D., Liu Y., Zhang J., Niu H., Zhang K., Zhu J., Wu D. et al. 2013; Identification and molecular characterization of a novel flavivirus isolated from geese in China. Res Vet Sci 94:774–780 [View Article][PubMed]
    [Google Scholar]
  20. Hyde J. L., Gardner C. L., Kimura T., White J. P., Liu G., Trobaugh D. W., Huang C., Tonelli M., Paessler S. et al. 2014; A viral RNA structural element alters host recognition of nonself RNA. Science 343:783–787 [View Article][PubMed]
    [Google Scholar]
  21. Jones M., Davidson A., Hibbert L., Gruenwald P., Schlaak J., Ball S., Foster G. R., Jacobs M. 2005; Dengue virus inhibits alpha interferon signaling by reducing STAT2 expression. J Virol 79:5414–5420 [View Article][PubMed]
    [Google Scholar]
  22. Kumar R., Tripathi P., Rizvi A. 2009; Effectiveness of one dose of SA 14-14-2 vaccine against Japanese encephalitis. N Engl J Med 360:1465–1466 [View Article][PubMed]
    [Google Scholar]
  23. Lee E., Lobigs M. 2002; Mechanism of virulence attenuation of glycosaminoglycan-binding variants of Japanese encephalitis virus and Murray Valley encephalitis virus. J Virol 76:4901–4911[PubMed] [CrossRef]
    [Google Scholar]
  24. Lee E., Hall R. A., Lobigs M. 2004; Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J Virol 78:8271–8280 [View Article][PubMed]
    [Google Scholar]
  25. Li J., Bhuvanakantham R., Howe J., Ng M. L. 2006; The glycosylation site in the envelope protein of West Nile virus (Sarafend) plays an important role in replication and maturation processes. J Gen Virol 87:613–622 [View Article][PubMed]
    [Google Scholar]
  26. Li S. H., Li X. F., Zhao H., Deng Y. Q., Yu X. D., Zhu S. Y., Jiang T., Ye Q., Qin E. D. et al. 2013a; Development and characterization of the replicon system of Japanese encephalitis live vaccine virus SA14-14-2. Virol J 10:64 [CrossRef]
    [Google Scholar]
  27. Li X. F., Zhao W., Lin F., Ye Q., Wang H. J., Yang D., Li S. H., Zhao H., Xu Y. P. et al. 2013b; Development of chimaeric West Nile virus attenuated vaccine candidate based on the Japanese encephalitis vaccine strain SA14-14-2. J Gen Virol 94:2700–2709 [View Article][PubMed]
    [Google Scholar]
  28. Li X. F., Deng Y. Q., Yang H. Q., Zhao H., Jiang T., Yu X. D., Li S. H., Ye Q., Zhu S. Y. et al. 2013c; A chimeric dengue virus vaccine using Japanese encephalitis virus vaccine strain SA14-14-2 as backbone is immunogenic and protective against either parental virus in mice and nonhuman primates. J Virol 87:13694–13705 [View Article][PubMed]
    [Google Scholar]
  29. Li G., Gao X., Xiao Y., Liu S., Peng S., Li X., Shi Y., Zhang Y., Yu L. et al. 2014; Development of a live attenuated vaccine candidate against duck Tembusu viral disease. Virology 450–451:233–242 [View Article][PubMed]
    [Google Scholar]
  30. Liang J. J., Liao C. L., Liao J. T., Lee Y. L., Lin Y. L. 2009; A Japanese encephalitis virus vaccine candidate strain is attenuated by decreasing its interferon antagonistic ability. Vaccine 27:2746–2754 [View Article][PubMed]
    [Google Scholar]
  31. Liu M., Chen S., Chen Y., Liu C., Chen S., Yin X., Li G., Zhang Y. 2012a; Adapted Tembusu-like virus in chickens and geese in China. J Clin Microbiol 50:2807–2809 [View Article][PubMed]
    [Google Scholar]
  32. Liu P., Lu H., Li S., Moureau G., Deng Y. Q., Wang Y., Zhang L., Jiang T., de Lamballerie X. et al. 2012b; Genomic and antigenic characterization of the newly emerging Chinese duck egg-drop syndrome flavivirus: genomic comparison with Tembusu and Sitiawan viruses. J Gen Virol 93:2158–2170 [View Article][PubMed]
    [Google Scholar]
  33. Muñoz-Jordan J. L., Sánchez-Burgos G. G., Laurent-Rolle M., García-Sastre A. 2003; Inhibition of interferon signaling by dengue virus. Proc Natl Acad Sci U S A 100:14333–14338 [View Article][PubMed]
    [Google Scholar]
  34. Pletnev A. G., Bray M., Hanley K. A., Speicher J., Elkins R. 2001; Tick-borne Langat/mosquito-borne dengue flavivirus chimera, a candidate live attenuated vaccine for protection against disease caused by members of the tick-borne encephalitis virus complex: evaluation in rhesus monkeys and in mosquitoes. J Virol 75:8259–8267[PubMed] [CrossRef]
    [Google Scholar]
  35. Pletnev A. G., Putnak R., Speicher J., Wagar E. J., Vaughn D. W. 2002; West Nile virus/dengue type 4 virus chimeras that are reduced in neurovirulence and peripheral virulence without loss of immunogenicity or protective efficacy. Proc Natl Acad Sci U S A 99:3036–3041 [View Article][PubMed]
    [Google Scholar]
  36. Pletnev A. G., Claire M. S., Elkins R., Speicher J., Murphy B. R., Chanock R. M. 2003; Molecularly engineered live-attenuated chimeric West Nile/dengue virus vaccines protect rhesus monkeys from West Nile virus. Virology 314:190–195 [View Article][PubMed]
    [Google Scholar]
  37. Su J., Li S., Hu X., Yu X., Wang Y., Liu P., Lu X., Zhang G., Hu X. et al. 2011; Duck egg-drop syndrome caused by BYD virus, a new Tembusu-related flavivirus. PLoS One 6:e18106 [View Article][PubMed]
    [Google Scholar]
  38. Sumiyoshi H., Tignor G. H., Shope R. E. 1995; Characterization of a highly attenuated Japanese encephalitis virus generated from molecularly cloned cDNA. J Infect Dis 171:1144–1151[PubMed] [CrossRef]
    [Google Scholar]
  39. Sun L., Li Y., Zhang Y., Han Z., Xu Y., Kong X., Liu S. 2014; Adaptation and attenuation of duck Tembusu virus strain Du/CH/LSD/110128 following serial passage in chicken embryos. Clin Vaccine Immunol 21:1046–1053 [View Article][PubMed]
    [Google Scholar]
  40. Tandan J. B., Ohrr H., Sohn Y. M., Yoksan S., Ji M., Nam C. M., Halstead S. B. 2007; Single dose of SA 14-14-2 vaccine provides long-term protection against Japanese encephalitis: a case control study in Nepalese children 5 years after immunization. Vaccine 25:5041–5045 [View Article][PubMed]
    [Google Scholar]
  41. Tang Y., Gao X., Diao Y., Feng Q., Chen H., Liu X., Ge P., Yu C. 2013; Tembusu virus in human, China. Transbound Emerg Dis 60:193–196 [View Article][PubMed]
    [Google Scholar]
  42. Thontiravong A., Ninvilai P., Tunterak W., Nonthabenjawan N., Chaiyavong S., Angkabkingkaew K., Mungkundar C., Phuengpho W., Oraveerakul K. et al. 2015; Tembusu-related flavivirus in ducks, Thailand. Emerg Infect Dis 21:2164–2167 [View Article][PubMed]
    [Google Scholar]
  43. Wang H. J., Li X. F., Ye Q., Li S. H., Deng Y. Q., Zhao H., Xu Y. P., Ma J., Qin E. D. et al. 2014; Recombinant chimeric Japanese encephalitis virus/tick-borne encephalitis virus is attenuated and protective in mice. Vaccine 32:949–956 [View Article][PubMed]
    [Google Scholar]
  44. Werme K., Wigerius M., Johansson M. 2008; Tick-borne encephalitis virus NS5 associates with membrane protein scribble and impairs interferon-stimulated JAK-STAT signalling. Cell Microbiol 10:696–712 [View Article][PubMed]
    [Google Scholar]
  45. Wright P. F., Ankrah S., Henderson S. E., Durbin A. P., Speicher J., Whitehead S. S., Murphy B. R., Pletnev A. G. 2008; Evaluation of the Langat/dengue 4 chimeric virus as a live attenuated tick-borne encephalitis vaccine for safety and immunogenicity in healthy adult volunteers. Vaccine 26:882–890 [View Article][PubMed]
    [Google Scholar]
  46. Yan L., Yan P., Zhou J., Teng Q., Li Z. 2011a; Establishing a Taqman-based real-time PCR assay for the rapid detection and quantification of the newly emerged duck Tembusu virus. Virol J 8:464 [View Article][PubMed]
    [Google Scholar]
  47. Yan P., Zhao Y., Zhang X., Xu D., Dai X., Teng Q., Yan L., Zhou J., Ji X. et al. 2011b; An infectious disease of ducks caused by a newly emerged Tembusu virus strain in mainland China. Virology 417:1–8 [View Article][PubMed]
    [Google Scholar]
  48. Yoshii K., Sunden Y., Yokozawa K., Igarashi M., Kariwa H., Holbrook M. R., Takashima I. 2014; A critical determinant of neurological disease associated with highly pathogenic tick-borne flavivirus in mice. J Virol 88:5406–5420 [View Article][PubMed]
    [Google Scholar]
  49. Yu Y. 2010; Phenotypic and genotypic characteristics of Japanese encephalitis attenuated live vaccine virus SA14-14-2 and their stabilities. Vaccine 28:3635–3641 [View Article][PubMed]
    [Google Scholar]
  50. Yun T., Zhang D., Ma X., Cao Z., Chen L., Ni Z., Ye W., Yu B., Hua J. et al. 2012; Complete genome sequence of a novel flavivirus, duck tembusu virus, isolated from ducks and geese in china. J Virol 86:3406–3407 [View Article][PubMed]
    [Google Scholar]
  51. Zhang S., Li L., Woodson S. E., Huang C. Y., Kinney R. M., Barrett A. D., Beasley D. W. 2006; A mutation in the envelope protein fusion loop attenuates mouse neuroinvasiveness of the NY99 strain of West Nile virus. Virology 353:35–40 [View Article][PubMed]
    [Google Scholar]
  52. Zhao Z., Date T., Li Y., Kato T., Miyamoto M., Yasui K., Wakita T. 2005; Characterization of the E-138 (Glu/Lys) mutation in Japanese encephalitis virus by using a stable, full-length, infectious cDNA clone. J Gen Virol 86:2209–2220 [View Article][PubMed]
    [Google Scholar]
  53. Zou Z., Liu Z., Jin M. 2014; Efficient strategy to generate a vectored duck enteritis virus delivering envelope of duck Tembusu virus. Viruses 6:2428–2443 [View Article][PubMed]
    [Google Scholar]
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