A Molecularly Cloned, Live-Attenuated Japanese Encephalitis Vaccine SA-14-2 Virus: A Conserved Single Amino Acid in the Hairpin of the Viral E Glycoprotein Determines Neurovirulence in Mice

1. EndyTP, NisalakA (2002) Japanese encephalitis virus: ecology and epidemiology. Curr Top Microbiol Immunol 267: 11–48.

2. MackenzieJS, BarrettAD, DeubelV (2002) The Japanese encephalitis serological group of flaviviruses: a brief introduction to the group. Curr Top Microbiol Immunol 267: 1–10.

3. MackenzieJS, GublerDJ, PetersenLR (2004) Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 10: S98–109.

4. MackenzieJS, JohansenCA, RitchieSA, van den HurkAF, HallRA (2002) Japanese encephalitis as an emerging virus: the emergence and spread of Japanese encephalitis virus in Australasia. Curr Top Microbiol Immunol 267: 49–73.

5. GublerDJ (2007) The continuing spread of West Nile virus in the western hemisphere. Clin Infect Dis 45: 1039–1046.

6. NashD, MostashariF, FineA, MillerJ, O'LearyD, et al. (2001) The outbreak of West Nile virus infection in the New York City area in 1999. N Engl J Med 344: 1807–1814.

7. WeaverSC, BarrettAD (2004) Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2: 789–801.

8. NettRJ, CampbellGL, ReisenWK (2009) Potential for the emergence of Japanese encephalitis virus in California. Vector Borne Zoonotic Dis 9: 511–517.

9. WeaverSC, ReisenWK (2010) Present and future arboviral threats. Antiviral Res 85: 328–345.

10. Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, et al.. (2011) Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ 89: : 766–774, 774A–774E.

11. MonathTP (2002) Japanese encephalitis vaccines: current vaccines and future prospects. Curr Top Microbiol Immunol 267: 105–138.

12. SolomonT, VaughnDW (2002) Pathogenesis and clinical features of Japanese encephalitis and West Nile virus infections. Curr Top Microbiol Immunol 267: 171–194.

13. SolomonT (2006) Control of Japanese encephalitis-within our grasp? N Engl J Med 355: 869–871.

14. MisraUK, KalitaJ (2010) Overview: Japanese encephalitis. Prog Neurobiol 91: 108–120.

15. DoklandT, WalshM, MackenzieJM, KhromykhAA, EeKH, et al. (2004) West Nile virus core protein: tetramer structure and ribbon formation. Structure 12: 1157–1163.

16. MaL, JonesCT, GroeschTD, KuhnRJ, PostCB (2004) Solution structure of dengue virus capsid protein reveals another fold. Proc Natl Acad Sci U S A 101: 3414–3419.

17. KuhnRJ, ZhangW, RossmannMG, PletnevSV, CorverJ, et al. (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108: 717–725.

18. MukhopadhyayS, KimBS, ChipmanPR, RossmannMG, KuhnRJ (2003) Structure of West Nile virus. Science 302: 248.

19. ZhangW, ChipmanPR, CorverJ, JohnsonPR, ZhangY, et al. (2003) Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat Struct Biol 10: 907–912.

20. ChenY, MaguireT, HilemanRE, FrommJR, EskoJD, et al. (1997) Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3: 866–871.

21. DavisCW, NguyenHY, HannaSL, SanchezMD, DomsRW, et al. (2006) West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol 80: 1290–1301.

22. Navarro-SanchezE, AltmeyerR, AmaraA, SchwartzO, FieschiF, et al. (2003) Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 4: 723–728.

23. PokidyshevaE, ZhangY, BattistiAJ, Bator-KellyCM, ChipmanPR, et al. (2006) Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124: 485–493.

24. TassaneetrithepB, BurgessTH, Granelli-PipernoA, TrumpfhellerC, FinkeJ, et al. (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197: 823–829.

25. ChuJJ, NgML (2004) Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway. J Virol 78: 10543–10555.

26. van der SchaarHM, RustMJ, WaartsBL, van der Ende-MetselaarH, KuhnRJ, et al. (2007) Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J Virol 81: 12019–12028.

27. van der SchaarHM, RustMJ, ChenC, van der Ende-MetselaarH, WilschutJ, et al. (2008) Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 4: e1000244.

28. BressanelliS, StiasnyK, AllisonSL, SturaEA, DuquerroyS, et al. (2004) Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J 23: 728–738.

29. LiaoM, Sanchez-San MartinC, ZhengA, KielianM (2010) In vitro reconstitution reveals key intermediate states of trimer formation by the dengue virus membrane fusion protein. J Virol 84: 5730–5740.

30. ModisY, OgataS, ClementsD, HarrisonSC (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427: 313–319.

31. NayakV, DessauM, KuceraK, AnthonyK, LedizetM, et al. (2009) Crystal structure of dengue virus type 1 envelope protein in the postfusion conformation and its implications for membrane fusion. J Virol 83: 4338–4344.

32. StiasnyK, KosslC, LepaultJ, ReyFA, HeinzFX (2007) Characterization of a structural intermediate of flavivirus membrane fusion. PLoS Pathog 3: e20.

33. HarrisonSC (2008) Viral membrane fusion. Nat Struct Mol Biol 15: 690–698.

34. Lindenbach BD, Thiel HJ, Rice CM (2007) Flaviviridae: the viruses and their replication. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al.., editors. Fields virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins Publishers. pp. 1101–1152.

35. BrintonMA (2002) The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu Rev Microbiol 56: 371–402.

36. ParanjapeSM, HarrisE (2010) Control of dengue virus translation and replication. Curr Top Microbiol Immunol 338: 15–34.

37. VillordoSM, GamarnikAV (2009) Genome cyclization as strategy for flavivirus RNA replication. Virus Res 139: 230–239.

38. WestawayEG, MackenzieJM, KhromykhAA (2002) Replication and gene function in Kunjin virus. Curr Top Microbiol Immunol 267: 323–351.

39. GillespieLK, HoenenA, MorganG, MackenzieJM (2010) The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J Virol 84: 10438–10447.

40. HsuNY, IlnytskaO, BelovG, SantianaM, ChenYH, et al. (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141: 799–811.

41. WelschS, MillerS, Romero-BreyI, MerzA, BleckCK, et al. (2009) Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5: 365–375.

42. LiL, LokSM, YuIM, ZhangY, KuhnRJ, et al. (2008) The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319: 1830–1834.

43. ZhangY, CorverJ, ChipmanPR, ZhangW, PletnevSV, et al. (2003) Structures of immature flavivirus particles. EMBO J 22: 2604–2613.

44. LorenzIC, AllisonSL, HeinzFX, HeleniusA (2002) Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J Virol 76: 5480–5491.

45. StadlerK, AllisonSL, SchalichJ, HeinzFX (1997) Proteolytic activation of tick-borne encephalitis virus by furin. J Virol 71: 8475–8481.

46. YuIM, ZhangW, HoldawayHA, LiL, KostyuchenkoVA, et al. (2008) Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319: 1834–1837.

47. ZhangY, ZhangW, OgataS, ClementsD, StraussJH, et al. (2004) Conformational changes of the flavivirus E glycoprotein. Structure 12: 1607–1618.

48. Gubler DJ, Kuno G, Markoff L (2007) Flaviviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al.., editors. Fields virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins Publishers. pp. 1153–1252.

49. BeasleyDW, LewthwaiteP, SolomonT (2008) Current use and development of vaccines for Japanese encephalitis. Expert Opin Biol Ther 8: 95–106.

50. Wilder-SmithA, HalsteadSB (2010) Japanese encephalitis: update on vaccines and vaccine recommendations. Curr Opin Infect Dis 23: 426–431.

51. FischerM, LindseyN, StaplesJE, HillsS (2010) Centers for Disease Control and Prevention (2010) Japanese encephalitis vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 59: 1–27.

52. PlesnerAM (2003) Allergic reactions to Japanese encephalitis vaccine. Immunol Allergy Clin North Am 23: 665–697.

53. YuY (2010) Phenotypic and genotypic characteristics of Japanese encephalitis attenuated live vaccine virus SA14-14-2 and their stabilities. Vaccine 28: 3635–3641.

54. HalsteadSB, ThomasSJ (2010) Japanese encephalitis: new options for active immunization. Clin Infect Dis 50: 1155–1164.

55. JelinekT (2009) Ixiaro: a new vaccine against Japanese encephalitis. Expert Rev Vaccines 8: 1501–1511.

56. KollaritschH, Paulke-KorinekM, Dubischar-KastnerK (2009) IC51 Japanese encephalitis vaccine. Expert Opin Biol Ther 9: 921–931.

57. Centers for Disease Control and Prevention (2011) Recommendations for use of a booster dose of inactivated vero cell culture-derived Japanese encephalitis vaccine: advisory committee on immunization practices, 2011. MMWR Morb Mortal Wkly Rep 60: 661–663.

58. Centers for Disease Control and Prevention (2011) Update on Japanese encephalitis vaccine for children: United States, May 2011. MMWR Morb Mortal Wkly Rep 60: 664–665.

59. ChambersTJ, NestorowiczA, MasonPW, RiceCM (1999) Yellow fever/Japanese encephalitis chimeric viruses: construction and biological properties. J Virol 73: 3095–3101.

60. MonathTP, LevenbookI, SoikeK, ZhangZX, RatterreeM, et al. (2000) Chimeric yellow fever virus 17D-Japanese encephalitis virus vaccine: dose-response effectiveness and extended safety testing in rhesus monkeys. J Virol 74: 1742–1751.

61. HalsteadSB, ThomasSJ (2011) New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines 10: 355–364.

62. AppaiahgariMB, VratiS (2012) Clinical development of IMOJEV (R)-a recombinant Japanese encephalitis chimeric vaccine (JE-CV). Expert Opin Biol Ther 12: 1251–1263.

63. AiharaS, RaoCM, YuYX, LeeT, WatanabeK, et al. (1991) Identification of mutations that occurred on the genome of Japanese encephalitis virus during the attenuation process. Virus Genes 5: 95–109.

64. NiH, ChangGJ, XieH, TrentDW, BarrettAD (1995) Molecular basis of attenuation of neurovirulence of wild-type Japanese encephalitis virus strain SA14. J Gen Virol 76: 409–413.

65. NitayaphanS, GrantJA, ChangGJ, TrentDW (1990) Nucleotide sequence of the virulent SA-14 strain of Japanese encephalitis virus and its attenuated vaccine derivative, SA-14-14-2. Virology 177: 541–552.

66. CeciliaD, GouldEA (1991) Nucleotide changes responsible for loss of neuroinvasiveness in Japanese encephalitis virus neutralization-resistant mutants. Virology 181: 70–77.

67. ChambersTJ, DrollDA, JiangX, WoldWS, NickellsJA (2007) JE Nakayama/JE SA14-14-2 virus structural region intertypic viruses: biological properties in the mouse model of neuroinvasive disease. Virology 366: 51–61.

68. HasegawaH, YoshidaM, ShiosakaT, FujitaS, KobayashiY (1992) Mutations in the envelope protein of Japanese encephalitis virus affect entry into cultured cells and virulence in mice. Virology 191: 158–165.

69. LeeE, HallRA, LobigsM (2004) Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J Virol 78: 8271–8280.

70. NiH, BarrettAD (1996) Molecular differences between wild-type Japanese encephalitis virus strains of high and low mouse neuroinvasiveness. J Gen Virol 77: 1449–1455.

71. NiH, BarrettAD (1998) Attenuation of Japanese encephalitis virus by selection of its mouse brain membrane receptor preparation escape variants. Virology 241: 30–36.

72. ShahPS, TanakaM, KhanAH, MathengeEG, FukeI, et al. (2006) Molecular characterization of attenuated Japanese encephalitis live vaccine strain ML-17. Vaccine 24: 402–411.

73. SumiyoshiH, TignorGH, ShopeRE (1995) Characterization of a highly attenuated Japanese encephalitis virus generated from molecularly cloned cDNA. J Infect Dis 171: 1144–1151.

74. WuSC, LinCW, LeeSC, LianWC (2003) Phenotypic and genotypic characterization of the neurovirulence and neuroinvasiveness of a large-plaque attenuated Japanese encephalitis virus isolate. Microbes Infect 5: 475–480.

75. KimJM, YunSI, SongBH, HahnYS, LeeCH, et al. (2008) A single N-linked glycosylation site in the Japanese encephalitis virus prM protein is critical for cell type-specific prM protein biogenesis, virus particle release, and pathogenicity in mice. J Virol 82: 7846–7862.

76. YunSI, ChoiYJ, SongBH, LeeYM (2009) 3' cis-acting elements that contribute to the competence and efficiency of Japanese encephalitis virus genome replication: functional importance of sequence duplications, deletions, and substitutions. J Virol 83: 7909–7930.

77. SongBH, YunGN, KimJK, YunSI, LeeYM (2012) Biological and genetic properties of SA14-14-2, a live-attenuated Japanese encephalitis vaccine that is currently available for humans. J Microbiol 50: 698–706.

78. YunSI, KimSY, RiceCM, LeeYM (2003) Development and application of a reverse genetics system for Japanese encephalitis virus. J Virol 77: 6450–6465.

79. NybakkenGE, NelsonCA, ChenBR, DiamondMS, FremontDH (2006) Crystal structure of the West Nile virus envelope glycoprotein. J Virol 80: 11467–11474.

80. LucaVC, AbiMansourJ, NelsonCA, FremontDH (2012) Crystal structure of the Japanese encephalitis virus envelope protein. J Virol 86: 2337–2346.

81. NiH, BurnsNJ, ChangGJ, ZhangMJ, WillsMR, et al. (1994) Comparison of nucleotide and deduced amino acid sequence of the 5' non-coding region and structural protein genes of the wild-type Japanese encephalitis virus strain SA14 and its attenuated vaccine derivatives. J Gen Virol 75: 1505–1510.

82. World Health Organization (2005) Global advisory committee on vaccine safety, 9–10 June 2005. Wkly Epidemiol Rec 80: 242–247.

83. MukhopadhyayS, KuhnRJ, RossmannMG (2005) A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3: 13–22.

84. StiasnyK, HeinzFX (2006) Flavivirus membrane fusion. J Gen Virol 87: 2755–2766.

85. ReyFA, HeinzFX, MandlC, KunzC, HarrisonSC (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375: 291–298.

86. AllisonSL, SchalichJ, StiasnyK, MandlCW, HeinzFX (2001) Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J Virol 75: 4268–4275.

87. LeeE, LobigsM (2002) Mechanism of virulence attenuation of glycosaminoglycan-binding variants of Japanese encephalitis virus and Murray Valley encephalitis virus. J Virol 76: 4901–4911.

88. LeeJW, ChuJJ, NgML (2006) Quantifying the specific binding between West Nile virus envelope domain III protein and the cellular receptor αVβ3 integrin. J Biol Chem 281: 1352–1360.

89. BeasleyDW, BarrettAD (2002) Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J Virol 76: 13097–13100.

90. CrillWD, RoehrigJT (2001) Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J Virol 75: 7769–7773.

91. KaufmannB, NybakkenGE, ChipmanPR, ZhangW, DiamondMS, et al. (2006) West Nile virus in complex with the Fab fragment of a neutralizing monoclonal antibody. Proc Natl Acad Sci U S A 103: 12400–12404.

92. WuKP, WuCW, TsaoYP, KuoTW, LouYC, et al. (2003) Structural basis of a flavivirus recognized by its neutralizing antibody: solution structure of the domain III of the Japanese encephalitis virus envelope protein. J Biol Chem 278: 46007–46013.

93. StiasnyK, BressanelliS, LepaultJ, ReyFA, HeinzFX (2004) Characterization of a membrane-associated trimeric low-pH-induced form of the class II viral fusion protein E from tick-borne encephalitis virus and its crystallization. J Virol 78: 3178–3183.

94. ReyFA (2003) Dengue virus envelope glycoprotein structure: new insight into its interactions during viral entry. Proc Natl Acad Sci U S A 100: 6899–6901.

95. KaufmannB, ChipmanPR, HoldawayHA, JohnsonS, FremontDH, et al. (2009) Capturing a flavivirus pre-fusion intermediate. PLoS Pathog 5: e1000672.

96. LinSR, ZouG, HsiehSC, QingM, TsaiWY, et al. (2011) The helical domains of the stem region of dengue virus envelope protein are involved in both virus assembly and entry. J Virol 85: 5159–5171.

97. PangerlK, HeinzFX, StiasnyK (2011) Mutational analysis of the zippering reaction during flavivirus membrane fusion. J Virol 85: 8495–8501.

98. SchmidtAG, YangPL, HarrisonSC (2010) Peptide inhibitors of dengue virus entry target a late-stage fusion intermediate. PLoS Pathog 6: e1000851.

99. ChuJJ, NgML (2004) Interaction of West Nile virus with αvβ3 integrin mediates virus entry into cells. J Biol Chem 279: 54533–54541.

100. HurrelbrinkRJ, McMinnPC (2001) Attenuation of Murray Valley encephalitis virus by site-directed mutagenesis of the hinge and putative receptor-binding regions of the envelope protein. J Virol 75: 7692–7702.

101. LeeE, LobigsM (2000) Substitutions at the putative receptor-binding site of an encephalitic flavivirus alter virulence and host cell tropism and reveal a role for glycosaminoglycans in entry. J Virol 74: 8867–8875.

102. GotoA, YoshiiK, ObaraM, UekiT, MizutaniT, et al. (2005) Role of the N-linked glycans of the prM and E envelope proteins in tick-borne encephalitis virus particle secretion. Vaccine 23: 3043–3052.

103. HannaSL, PiersonTC, SanchezMD, AhmedAA, MurtadhaMM, et al. (2005) N-linked glycosylation of West Nile virus envelope proteins influences particle assembly and infectivity. J Virol 79: 13262–13274.

104. LorenzIC, KartenbeckJ, MezzacasaA, AllisonSL, HeinzFX, et al. (2003) Intracellular assembly and secretion of recombinant subviral particles from tick-borne encephalitis virus. J Virol 77: 4370–4382.

105. TajimaS, NeromeR, NukuiY, KatoF, TakasakiT, et al. (2010) A single mutation in the Japanese encephalitis virus E protein (S123R) increases its growth rate in mouse neuroblastoma cells and its pathogenicity in mice. Virology 396: 298–304.

106. MonathTP, ArroyoJ, LevenbookI, ZhangZX, CatalanJ, et al. (2002) Single mutation in the flavivirus envelope protein hinge region increases neurovirulence for mice and monkeys but decreases viscerotropism for monkeys: relevance to development and safety testing of live, attenuated vaccines. J Virol 76: 1932–1943.

107. ArroyoJ, GuirakhooF, FennerS, ZhangZX, MonathTP, et al. (2001) Molecular basis for attenuation of neurovirulence of a yellow fever virus/Japanese encephalitis virus chimera vaccine (ChimeriVax-JE). J Virol 75: 934–942.

108. ChenLK, LinYL, LiaoCL, LinCG, HuangYL, et al. (1996) Generation and characterization of organ-tropism mutants of Japanese encephalitis virus in vivo and in vitro. Virology 223: 79–88.

109. ZhaoZ, DateT, LiY, KatoT, MiyamotoM, et al. (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.

110. MelianEB, HinzmanE, NagasakiT, FirthAE, WillsNM, et al. (2010) NS1' of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J Virol 84: 1641–1647.

111. FirthAE, AtkinsJF (2009) A conserved predicted pseudoknot in the NS2A-encoding sequence of West Nile and Japanese encephalitis flaviviruses suggests NS1' may derive from ribosomal frameshifting. Virol J 6: 14.

112. YeQ, LiXF, ZhaoH, LiSH, DengYQ, et al. (2012) A single nucleotide mutation in NS2A of Japanese encephalitis-live vaccine virus (SA14-14-2) ablates NS1' formation and contributes to attenuation. J Gen Virol 93: 1959–1964.

113. EckelsKH, YuYX, DuboisDR, MarchetteNJ, TrentDW, et al. (1988) Japanese encephalitis virus live-attenuated vaccine, Chinese strain SA14-14-2; adaptation to primary canine kidney cell cultures and preparation of a vaccine for human use. Vaccine 6: 513–518.

114. SigelMM (1952) Influence of age on susceptibility to virus infections with particular reference to laboratory animals. Annu Rev Microbiol 6: 247–280.

115. Monath TP (1986) Pathobiology of the flaviviruses. In: Schlesinger S, Schlesinger MJ, editors. The Togaviridae and Flaviviridae. New York, NY: Plenum. pp. 375–440.

116. ThompsonJD, GibsonTJ, PlewniakF, JeanmouginF, HigginsDG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882.

117. GoujonM, McWilliamH, LiW, ValentinF, SquizzatoS, et al. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38: W695–699.

118. KieferF, ArnoldK, KunzliM, BordoliL, SchwedeT (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37: D387–392.

119. ReedLJ, MuenchH (1938) A simple method of estimating fifty percent endpoints. Am J Hyg 27: 493–497.