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Construction of a replicon and an infectious cDNA clone of the Sofjin strain of the Far-Eastern subtype of tick-borne encephalitis virus

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Abstract

Tick-borne encephalitis virus (TBEV) causes severe encephalitis in humans. The Sofjin-HO strain is the prototype strain of the TBEV Far-Eastern subtype and is highly pathogenic in a mouse model. In this study, we constructed replicons and infectious cDNA clones of the Sofjin-HO strain. The replication of the replicon RNA was confirmed, and infectious viruses were recovered from the infectious cDNA clone. The recombinant viruses showed similar virulence characteristics to those of the parental virus. While characterizing the replicon and infectious cDNA, several amino acid differences derived from cell culture adaptations were analysed. The amino acids differences at E position 496 and NS4A position 58 were found to affect viral replication. The Gly- or Ala-to-Glu substitution at E position 122 was shown to increase neuroinvasiveness in mice. These replicons and infectious cDNA clones are useful in revealing the viral molecular determinants involved in the replication and pathogenicity of TBEV.

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References

  1. Allison SD, Chang B, Randolph TW, Carpenter JF (1999) Hydrogen bonding between sugar and protein is responsible for inhibition of dehydration-induced protein unfolding. Arch Biochem Biophys 365:289–298

    Article  PubMed  CAS  Google Scholar 

  2. Bakhvalova VN, Rar VA, Tkachev SE, Matveev VA, Matveev LE, Karavanov AS, Dobrotvorsky AK, Morozova OV (2000) Tick-borne encephalitis virus strains of Western Siberia. Virus Res 70:1–12

    Article  PubMed  CAS  Google Scholar 

  3. Bernard KA, Klimstra WB, Johnston RE (2000) Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276:93–103

    Article  PubMed  CAS  Google Scholar 

  4. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729–777

    Article  PubMed  CAS  Google Scholar 

  5. Blaskovic D (1970) Tick-borne encephalitis in Czechoslovakia. Arch Environ Health 21:453–461

    PubMed  CAS  Google Scholar 

  6. Bredenbeek PJ, Kooi EA, Lindenbach B, Huijkman N, Rice CM, Spaan WJ (2003) A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication. J Gen Virol 84:1261–1268

    Article  PubMed  CAS  Google Scholar 

  7. Byrnes AP, Griffin DE (2000) Large-plaque mutants of Sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J Virol 74:644–651

    Article  PubMed  CAS  Google Scholar 

  8. Campbell MS, Pletnev AG (2000) Infectious cDNA clones of Langat tick-borne flavivirus that differ from their parent in peripheral neurovirulence. Virology 269:225–237

    Article  PubMed  CAS  Google Scholar 

  9. Chambers TJ, Hahn CS, Galler R, Rice CM (1990) Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44:649–688

    Article  PubMed  CAS  Google Scholar 

  10. Chambers TJ, McCourt DW, Rice CM (1990) Production of yellow fever virus proteins in infected cells: identification of discrete polyprotein species and analysis of cleavage kinetics using region-specific polyclonal antisera. Virology 177:159–174

    Article  PubMed  CAS  Google Scholar 

  11. Chiba N, Iwasaki T, Mizutani T, Kariwa H, Kurata T, Takashima I (1999) Pathogenicity of tick-borne encephalitis virus isolated in Hokkaido, Japan in mouse model. Vaccine 17:779–787

    Article  PubMed  CAS  Google Scholar 

  12. Falgout B, Chanock R, Lai CJ (1989) Proper processing of dengue virus nonstructural glycoprotein NS1 requires the N-terminal hydrophobic signal sequence and the downstream nonstructural protein NS2a. J Virol 63:1852–1860

    PubMed  CAS  Google Scholar 

  13. Goto A, Hayasaka D, Yoshii K, Mizutani T, Kariwa H, Takashima I (2002) Genetic and biological comparison of tick-borne encephalitis viruses from Hokkaido and far-eastern Russia. Jpn J Vet Res 49:297–307

    PubMed  Google Scholar 

  14. Goto A, Hayasaka D, Yoshii K, Mizutani T, Kariwa H, Takashima I (2003) A BHK-21 cell culture-adapted tick-borne encephalitis virus mutant is attenuated for neuroinvasiveness. Vaccine 21:4043–4051

    Article  PubMed  CAS  Google Scholar 

  15. Gritsun TS, Gould EA (1995) Infectious transcripts of tick-borne encephalitis virus, generated in days by RT-PCR. Virology 214:611–618

    Article  PubMed  CAS  Google Scholar 

  16. Gritsun TS, Gould EA (1998) Development and analysis of a tick-borne encephalitis virus infectious clone using a novel and rapid strategy. J Virol Methods 76:109–120

    Article  PubMed  CAS  Google Scholar 

  17. Gritsun TS, Lashkevich VA, Gould EA (2003) Tick-borne encephalitis. Antiviral Res 57:129–146

    Article  PubMed  CAS  Google Scholar 

  18. Gualano RC, Pryor MJ, Cauchi MR, Wright PJ, Davidson AD (1998) Identification of a major determinant of mouse neurovirulence of dengue virus type 2 using stably cloned genomic-length cDNA. J Gen Virol 79(Pt 3):437–446

    PubMed  CAS  Google Scholar 

  19. Gustafson R (1994) Epidemiological studies of Lyme borreliosis and tick-borne encephalitis. Scand J Infect Dis Suppl 92:1–63

    PubMed  CAS  Google Scholar 

  20. Hayasaka D, Gritsun TS, Yoshii K, Ueki T, Goto A, Mizutani T, Kariwa H, Iwasaki T, Gould EA, Takashima I (2004) Amino acid changes responsible for attenuation of virus neurovirulence in an infectious cDNA clone of the Oshima strain of tick-borne encephalitis virus. J Gen Virol 85:1007–1018

    Article  PubMed  CAS  Google Scholar 

  21. Hayasaka D, Yoshii K, Ueki T, Iwasaki T, Takashima I (2004) Sub-genomic replicons of Tick-borne encephalitis virus. Arch Virol 149:1245–1256

    Article  PubMed  CAS  Google Scholar 

  22. Hayasaka D, Nagata N, Fujii Y, Hasegawa H, Sata T, Suzuki R, Gould EA, Takashima I, Koike S (2009) Mortality following peripheral infection with tick-borne encephalitis virus results from a combination of central nervous system pathology, systemic inflammatory and stress responses. Virology 390:139–150

    Article  PubMed  CAS  Google Scholar 

  23. Hurrelbrink RJ, Nestorowicz A, McMinn PC (1999) Characterization of infectious Murray Valley encephalitis virus derived from a stably cloned genome-length cDNA. J Gen Virol 80(Pt 12):3115–3125

    PubMed  CAS  Google Scholar 

  24. Khromykh AA, Westaway EG (1994) Completion of Kunjin virus RNA sequence and recovery of an infectious RNA transcribed from stably cloned full-length cDNA. J Virol 68:4580–4588

    PubMed  CAS  Google Scholar 

  25. Khromykh AA, Westaway EG (1997) Subgenomic replicons of the flavivirus Kunjin: construction and applications. J Virol 71:1497–1505

    PubMed  CAS  Google Scholar 

  26. Kim CW, Goldberger OA, Gallo RL, Bernfield M (1994) Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Mol Biol Cell 5:797–805

    PubMed  CAS  Google Scholar 

  27. Kinney RM, Butrapet S, Chang GJ, Tsuchiya KR, Roehrig JT, Bhamarapravati N, Gubler DJ (1997) Construction of infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 230:300–308

    Article  PubMed  CAS  Google Scholar 

  28. Klimstra WB, Ryman KD, Johnston RE (1998) Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol 72:7357–7366

    PubMed  CAS  Google Scholar 

  29. Kozlovskaya LI, Osolodkin DI, Shevtsova AS, Romanova L, Rogova YV, Dzhivanian TI, Lyapustin VN, Pivanova GP, Gmyl AP, Palyulin VA, Karganova GG (2010) GAG-binding variants of tick-borne encephalitis virus. Virology 398:262–272

    Article  PubMed  CAS  Google Scholar 

  30. Labuda M, Stunzner D, Kozuch O, Sixl W, Kocianova E, Schaffler R, Vyrostekova V (1993) Tick-borne encephalitis virus activity in Styria, Austria. Acta Virol 37:187–190

    PubMed  CAS  Google Scholar 

  31. Lai CJ, Zhao BT, Hori H, Bray M (1991) Infectious RNA transcribed from stably cloned full-length cDNA of dengue type 4 virus. Proc Natl Acad Sci USA 88:5139–5143

    Article  PubMed  CAS  Google Scholar 

  32. Levkovich EN, Pogodina VV (1967) The problem of tick-borne encephalitis. Vestn Akad Med Nauk SSSR 22:53–59

    PubMed  CAS  Google Scholar 

  33. Lindenbach BD, Rice CM (1997) trans-Complementation of yellow fever virus NS1 reveals a role in early RNA replication. J Virol 71:9608–9617

    PubMed  CAS  Google Scholar 

  34. Lindenbach BD, Rice CM (1999) Genetic interaction of flavivirus nonstructural proteins NS1 and NS4A as a determinant of replicase function. J Virol 73:4611–4621

    PubMed  CAS  Google Scholar 

  35. Lindenbach BD, Rice CM (2003) Molecular biology of flaviviruses. Adv Virus Res 59:23–61

    Article  PubMed  CAS  Google Scholar 

  36. Mackenzie JM, Khromykh AA, Jones MK, Westaway EG (1998) Subcellular localization and some biochemical properties of the flavivirus Kunjin nonstructural proteins NS2A and NS4A. Virology 245:203–215

    Article  PubMed  CAS  Google Scholar 

  37. Mandl CW, Ecker M, Holzmann H, Kunz C, Heinz FX (1997) Infectious cDNA clones of tick-borne encephalitis virus European subtype prototypic strain Neudoerfl and high virulence strain Hypr. J Gen Virol 78(Pt 5):1049–1057

    PubMed  CAS  Google Scholar 

  38. Mandl CW, Kroschewski H, Allison SL, Kofler R, Holzmann H, Meixner T, Heinz FX (2001) Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo. J Virol 75:5627–5637

    Article  PubMed  CAS  Google Scholar 

  39. Mavtchoutko V, Vene S, Haglund M, Forsgren M, Duks A, Kalnina V, Horling J, Lundkvist A (2000) Characterization of tick-borne encephalitis virus from Latvia. J Med Virol 60:216–222

    Article  PubMed  CAS  Google Scholar 

  40. Muylaert IR, Chambers TJ, Galler R, Rice CM (1996) Mutagenesis of the N-linked glycosylation sites of the yellow fever virus NS1 protein: effects on virus replication and mouse neurovirulence. Virology 222:159–168

    Article  PubMed  CAS  Google Scholar 

  41. Muylaert IR, Galler R, Rice CM (1997) Genetic analysis of the yellow fever virus NS1 protein: identification of a temperature-sensitive mutation which blocks RNA accumulation. J Virol 71:291–298

    PubMed  CAS  Google Scholar 

  42. Puri B, Polo S, Hayes CG, Falgout B (2000) Construction of a full length infectious clone for dengue-1 virus Western Pacific, 74 strain. Virus Genes 20:57–63

    Article  PubMed  CAS  Google Scholar 

  43. Sa-Carvalho D, Rieder E, Baxt B, Rodarte R, Tanuri A, Mason PW (1997) Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J Virol 71:5115–5123

    PubMed  CAS  Google Scholar 

  44. Schwaiger M, Cassinotti P (2003) Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol 27:136–145

    Article  PubMed  CAS  Google Scholar 

  45. Shapoval AN (1974) Chronic forms of tick-borne encephalitis. Zh Nevropatol Psikhiatr Im S S Korsakova 74:205–209

    PubMed  CAS  Google Scholar 

  46. Shapoval AN (1976) Primary progressive forms of tick-borne encephalitis. Zh Nevropatol Psikhiatr Im S S Korsakova 76:182–188

    PubMed  CAS  Google Scholar 

  47. Shi PY, Tilgner M, Lo MK (2002) Construction and characterization of subgenomic replicons of New York strain of West Nile virus. Virology 296:219–233

    Article  PubMed  CAS  Google Scholar 

  48. Shi PY, Tilgner M, Lo MK, Kent KA, Bernard KA (2002) Infectious cDNA clone of the epidemic West Nile virus from New York City. J Virol 76:5847–5856

    Article  PubMed  CAS  Google Scholar 

  49. Tumova S, Woods A, Couchman JR (2000) Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int J Biochem Cell Biol 32:269–288

    Article  PubMed  CAS  Google Scholar 

  50. Westaway EG, Mackenzie JM, Khromykh AA (2003) Kunjin RNA replication and applications of Kunjin replicons. Adv Virus Res 59:99–140

    Article  PubMed  CAS  Google Scholar 

  51. Yamshchikov VF, Wengler G, Perelygin AA, Brinton MA, Compans RW (2001) An infectious clone of the West Nile flavivirus. Virology 281:294–304

    Article  PubMed  CAS  Google Scholar 

  52. Yoshii K, Igarashi M, Ito K, Kariwa H, Holbrook MR, Takashima I (2010) Construction of an infectious cDNA clone for Omsk Hemorrhagic fever virus; and characterization of mutations in NS2A and NS5. Virus Res

  53. Yoshii K, Holbrook MR (2009) Sub-genomic replicon and virus-like particles of Omsk hemorrhagic fever virus. Arch Virol 154:573–580

    Article  PubMed  CAS  Google Scholar 

  54. Yoshii K, Ikawa A, Chiba Y, Omori Y, Maeda J, Murata R, Kariwa H, Takashima I (2009) Establishment of a neutralization test involving reporter gene-expressing virus-like particles of tick-borne encephalitis virus. J Virol Methods 161:173–176

    Article  PubMed  CAS  Google Scholar 

  55. Yun SI, Kim SY, Rice CM, Lee YM (2003) Development and application of a reverse genetics system for Japanese encephalitis virus. J Virol 77:6450–6465

    Article  PubMed  CAS  Google Scholar 

  56. Zilber LA, Soloviev VD (1946) Far Eastern tick-borne spring-summer (spring) encephalitis. Am Rev Sov Med 5:1–80

    Google Scholar 

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Acknowledgments

This work was supported by Grants-in-Aid for Scientific Research (22780268) and the Global COE Program from the Ministry of Education, Culture, Sports, Sciences and Technology of Japan, and Health Sciences Grants for Research on Emerging and Re-emerging Infectious Disease from the Ministry of Health, Labour and Welfare of Japan.

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Authors and Affiliations

  1. Laboratory of Public Health, Graduate School of Veterinary Medicine, Hokkaido University, Kita-18 Nishi-9, Kita-ku, Sapporo, Hokkaido, 060-0818, Japan

    Ayako Takano, Kentaro Yoshii, Yuki Omori-Urabe, Kana Yokozawa, Hiroaki Kariwa & Ikuo Takashima

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  1. Ayako Takano
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  2. Kentaro Yoshii
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  3. Yuki Omori-Urabe
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Correspondence to Kentaro Yoshii.

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Takano, A., Yoshii, K., Omori-Urabe, Y. et al. Construction of a replicon and an infectious cDNA clone of the Sofjin strain of the Far-Eastern subtype of tick-borne encephalitis virus. Arch Virol 156, 1931–1941 (2011). https://doi.org/10.1007/s00705-011-1066-0

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