- Introduction
- Materials and Methods
- Cells.
- Viruses.
- Generation of Vero-adapted JEV SA14-14-2 variants.
- Construction of rJEVmut14-14-2.
- Recovery of rJEVmut14-14-2.
- Virus replication in Vero cells.
- Type I IFN sensitivity assay.
- Mouse studies.
- Production of JEV reporter virus particles (RVPs).
- JEV RVP serum neutralization assay.
- Statistical analysis.
- Results
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Rosen L, 1986. The natural history of Japanese encephalitis virus. Annu Rev Microbiol 40: 395–414.
-
2.
Buescher EL, Scherer WF, 1959. Ecologic studies of Japanese encephalitis virus in Japan. IX. Epidemiologic correlations and conclusions. Am J Trop Med Hyg 8: 719–722.
-
3.
van den Hurk AF, Ritchie SA, Mackenzie JS, 2009. Ecology and geographical expansion of Japanese encephalitis virus. Annu Rev Entomol 54: 17–35.
-
4.
Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, Marfin AA, Solomon T, Tsai TF, Tsu VD, Ginsburg AS, 2011. Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ 89: 766–774, 774A–774E.
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5.
Chambers TJ, Hahn CS, Galler R, Rice CM, 1990. Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44: 649–688.
-
6.
Lindenbach BD, Rice CM, 2003. Molecular biology of flaviviruses. Adv Virus Res 59: 23–61.
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7.
Pierson TC, Fremont DH, Kuhn RJ, Diamond MS, 2008. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4: 229–238.
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8.
Markoff L, 2000. Points to consider in the development of a surrogate for efficacy of novel Japanese encephalitis virus vaccines. Vaccine 18 (Suppl 2): 26–32.
-
9.
Larena M, Regner M, Lee E, Lobigs M, 2011. Pivotal role of antibody and subsidiary contribution of CD8+ T cells to recovery from infection in a murine model of Japanese encephalitis. J Virol 85: 5446–5455.
-
10.
Diamond MS, 2009. Mechanisms of evasion of the type I interferon antiviral response by flaviviruses. J Interferon Cytokine Res 29: 521–530.
-
11.
Turtle L, Griffiths MJ, Solomon T, 2012. Encephalitis caused by flaviviruses. QJM 105: 219–223.
-
12.
Suthar MS, Diamond MS, Gale M Jr, 2013. West Nile virus infection and immunity. Nat Rev Microbiol 11: 115–128.
-
13.
Diamond MS, 2003. Evasion of innate and adaptive immunity by flaviviruses. Immunol Cell Biol 81: 196–206.
-
14.
Beasley DW, Lewthwaite P, Solomon T, 2008. Current use and development of vaccines for Japanese encephalitis. Expert Opin Biol Ther 8: 95–106.
-
15.
Halstead SB, Thomas SJ, 2011. New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines 10: 355–364.
-
16.
Appaiahgari MB, Vrati S, 2012. Clinical development of IMOJEV (R)–a recombinant Japanese encephalitis chimeric vaccine (JE-CV). Expert Opin Biol Ther 12: 1251–1263.
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17.
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.
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18.
WHO, 2014. WHO Expert Committee on Biological Standardization. Sixty-third report. Annex 7, Recommendations to assure the quality, safety and efficacy of Japanese encephalitis vaccines (live, attenuated) for human use. Geneva: WHO Press.
-
19.
Feroldi E, Pancharoen C, Kosalaraksa P, Chokephaibulkit K, Boaz M, Meric C, Hutagalung Y, Bouckenooghe A, 2014. Primary immunization of infants and toddlers in Thailand with Japanese encephalitis chimeric virus vaccine in comparison with SA14-14-2: a randomized study of immunogenicity and safety. Pediatr Infect Dis J 33: 643–649.
-
20.
Sohn YM, Tandan JB, Yoksan S, Ji M, Ohrr H, 2008. A 5-year follow-up of antibody response in children vaccinated with single dose of live attenuated SA14-14-2 Japanese encephalitis vaccine: immunogenicity and anamnestic responses. Vaccine 26: 1638–1643.
-
21.
Tsai TF, Yu YX, Jia LL, Putvatana R, Zhang R, Wang S, Halstead SB, 1998. Immunogenicity of live attenuated SA14-14-2 Japanese encephalitis vaccine–a comparison of 1- and 3-month immunization schedules. J Infect Dis 177: 221–223.
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22.
Tsai TF, 2000. New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 13–15 October 1998. Vaccine 18 (Suppl 2): 1–25.
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23.
Bista MB, Banerjee MK, Shin SH, Tandan JB, Kim MH, Sohn YM, Ohrr HC, Tang JL, Halstead SB, 2001. Efficacy of single-dose SA 14-14-2 vaccine against Japanese encephalitis: a case control study. Lancet 358: 791–795.
-
24.
Chotpitayasunondh T, Sohn YM, Yoksan S, Min J, Ohrr H, 2011. Immunizing children aged 9 to 15 months with live attenuated SA14-14-2 Japanese encephalitis vaccine in Thailand. J Med Assoc Thai 94 (Suppl 3): S195–S203.
-
25.
Tandan JB, Ohrr H, Sohn YM, Yoksan S, Ji M, Nam CM, Halstead SB, 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.
-
26.
Ohrr H, Tandan JB, Sohn YM, Shin SH, Pradhan DP, Halstead SB, 2005. Effect of single dose of SA 14-14-2 vaccine 1 year after immunization in Nepalese children with Japanese encephalitis: a case-control study. Lancet 366: 1375–1378.
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27.
Yu Y, 2010. Phenotypic and genotypic characteristics of Japanese encephalitis attenuated live vaccine virus SA14-14-2 and their stabilities. Vaccine 28: 3635–3641.
-
28.
Aihara S, Rao CM, Yu YX, Lee T, Watanabe K, Komiya T, Sumiyoshi H, Hashimoto H, Nomoto A, 1991. Identification of mutations that occurred on the genome of Japanese encephalitis virus during the attenuation process. Virus Genes 5: 95–109.
-
29.
Ni H, Chang GJ, Xie H, Trent DW, Barrett AD, 1995. Molecular basis of attenuation of neurovirulence of wild-type Japanese encephalitis virus strain SA14. J Gen Virol 76: 409–413.
-
30.
Nitayaphan S, Grant JA, Chang GJ, Trent DW, 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.
-
31.
Arroyo J, Guirakhoo F, Fenner S, Zhang ZX, Monath TP, Chambers TJ, 2001. Molecular basis for attenuation of neurovirulence of a yellow fever virus/Japanese encephalitis virus chimera vaccine (ChimeriVax-JE). J Virol 75: 934–942.
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32.
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.
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33.
Chen LK, Lin YL, Liao CL, Lin CG, Huang YL, Yeh CT, Lai SC, Jan JT, Chin C, 1996. Generation and characterization of organ-tropism mutants of Japanese encephalitis virus in vivo and in vitro. Virology 223: 79–88.
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34.
Sumiyoshi H, Tignor GH, Shope RE, 1995. Characterization of a highly attenuated Japanese encephalitis virus generated from molecularly cloned cDNA. J Infect Dis 171: 1144–1151.
-
35.
Yang D, Li XF, Ye Q, Wang HJ, Deng YQ, Zhu SY, Zhang Y, Li SH, Qin CF, 2014. Characterization of live-attenuated Japanese encephalitis vaccine virus SA14-14-2. Vaccine 32: 2675–2681.
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36.
Chambers TJ, Droll DA, Jiang X, Wold WS, Nickells JA, 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.
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37.
Ye Q, Li XF, Zhao H, Li SH, Deng YQ, Cao RY, Song KY, Wang HJ, Hua RH, Yu YX, Zhou X, Qin ED, Qin CF, 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.
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38.
Sooryanarain H, Sapkal GN, Gore MM, 2012. Pathogenic and vaccine strains of Japanese encephalitis virus elicit different levels of human macrophage effector functions. Arch Virol 157: 1905–1918.
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Laurent-Rolle M, Boer EF, Lubick KJ, Wolfinbarger JB, Carmody AB, Rockx B, Liu W, Ashour J, Shupert WL, Holbrook MR, Barrett AD, Mason PW, Bloom ME, Garcia-Sastre A, Khromykh AA, Best SM, 2010. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J Virol 84: 3503–3515.
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Genetic and Phenotypic Properties of Vero Cell-Adapted Japanese Encephalitis Virus SA14-14-2 Vaccine Strain Variants and a Recombinant Clone, Which Demonstrates Attenuation and Immunogenicity in Mice
Gregory D. Gromowski
Gregory D. Gromowski
Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
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Cai-Yen Firestone
Cai-Yen Firestone
Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
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José Bustos-Arriaga
José Bustos-Arriaga
Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
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Stephen S. Whitehead
Stephen S. Whitehead
Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
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The live-attenuated Japanese encephalitis virus (JEV) SA14-14-2 vaccine, produced in primary hamster kidney cells, is safe and effective. Past attempts to adapt this virus to replicate in cells that are more favorable for vaccine production resulted in mutations that significantly reduced immunogenicity. In this study, 10 genetically distinct Vero cell-adapted JEV SA14-14-2 variants were isolated and a recombinant wild-type JEV clone, modified to contain the JEV SA14-14-2 polyprotein amino acid sequence, was recovered in Vero cells. A single capsid protein mutation (S66L) was important for Vero cell-adaptation. Mutations were also identified that modulated virus sensitivity to type I interferon-stimulation in Vero cells. A subset of JEV SA14-14-2 variants and the recombinant clone were evaluated in vivo and exhibited levels of attenuation that varied significantly in suckling mice, but were avirulent and highly immunogenic in weanling mice and are promising candidates for the development of a second-generation, recombinant vaccine.
Author Notes
Financial support: This work was supported by the National Institute of Allergy and Infectious Diseases Intramural Research Program, National Institutes of Health.
Authors' addresses: Gregory D. Gromowski, Cai-Yen Firestone, José Bustos-Arriaga, and Stephen S. Whitehead, Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, E-mails: gromowskig@niaid.nih.gov, cfirestone@niaid.nih.gov, bustosarriagaj2@mail.nih.gov, and swhitehead@niaid.nih.gov.
- Introduction
- Materials and Methods
- Cells.
- Viruses.
- Generation of Vero-adapted JEV SA14-14-2 variants.
- Construction of rJEVmut14-14-2.
- Recovery of rJEVmut14-14-2.
- Virus replication in Vero cells.
- Type I IFN sensitivity assay.
- Mouse studies.
- Production of JEV reporter virus particles (RVPs).
- JEV RVP serum neutralization assay.
- Statistical analysis.
- Results
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Rosen L, 1986. The natural history of Japanese encephalitis virus. Annu Rev Microbiol 40: 395–414.
-
2.
Buescher EL, Scherer WF, 1959. Ecologic studies of Japanese encephalitis virus in Japan. IX. Epidemiologic correlations and conclusions. Am J Trop Med Hyg 8: 719–722.
-
3.
van den Hurk AF, Ritchie SA, Mackenzie JS, 2009. Ecology and geographical expansion of Japanese encephalitis virus. Annu Rev Entomol 54: 17–35.
-
4.
Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, Marfin AA, Solomon T, Tsai TF, Tsu VD, Ginsburg AS, 2011. Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ 89: 766–774, 774A–774E.
-
5.
Chambers TJ, Hahn CS, Galler R, Rice CM, 1990. Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44: 649–688.
-
6.
Lindenbach BD, Rice CM, 2003. Molecular biology of flaviviruses. Adv Virus Res 59: 23–61.
-
7.
Pierson TC, Fremont DH, Kuhn RJ, Diamond MS, 2008. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4: 229–238.
-
8.
Markoff L, 2000. Points to consider in the development of a surrogate for efficacy of novel Japanese encephalitis virus vaccines. Vaccine 18 (Suppl 2): 26–32.
-
9.
Larena M, Regner M, Lee E, Lobigs M, 2011. Pivotal role of antibody and subsidiary contribution of CD8+ T cells to recovery from infection in a murine model of Japanese encephalitis. J Virol 85: 5446–5455.
-
10.
Diamond MS, 2009. Mechanisms of evasion of the type I interferon antiviral response by flaviviruses. J Interferon Cytokine Res 29: 521–530.
-
11.
Turtle L, Griffiths MJ, Solomon T, 2012. Encephalitis caused by flaviviruses. QJM 105: 219–223.
-
12.
Suthar MS, Diamond MS, Gale M Jr, 2013. West Nile virus infection and immunity. Nat Rev Microbiol 11: 115–128.
-
13.
Diamond MS, 2003. Evasion of innate and adaptive immunity by flaviviruses. Immunol Cell Biol 81: 196–206.
-
14.
Beasley DW, Lewthwaite P, Solomon T, 2008. Current use and development of vaccines for Japanese encephalitis. Expert Opin Biol Ther 8: 95–106.
-
15.
Halstead SB, Thomas SJ, 2011. New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines 10: 355–364.
-
16.
Appaiahgari MB, Vrati S, 2012. Clinical development of IMOJEV (R)–a recombinant Japanese encephalitis chimeric vaccine (JE-CV). Expert Opin Biol Ther 12: 1251–1263.
-
17.
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.
-
18.
WHO, 2014. WHO Expert Committee on Biological Standardization. Sixty-third report. Annex 7, Recommendations to assure the quality, safety and efficacy of Japanese encephalitis vaccines (live, attenuated) for human use. Geneva: WHO Press.
-
19.
Feroldi E, Pancharoen C, Kosalaraksa P, Chokephaibulkit K, Boaz M, Meric C, Hutagalung Y, Bouckenooghe A, 2014. Primary immunization of infants and toddlers in Thailand with Japanese encephalitis chimeric virus vaccine in comparison with SA14-14-2: a randomized study of immunogenicity and safety. Pediatr Infect Dis J 33: 643–649.
-
20.
Sohn YM, Tandan JB, Yoksan S, Ji M, Ohrr H, 2008. A 5-year follow-up of antibody response in children vaccinated with single dose of live attenuated SA14-14-2 Japanese encephalitis vaccine: immunogenicity and anamnestic responses. Vaccine 26: 1638–1643.
-
21.
Tsai TF, Yu YX, Jia LL, Putvatana R, Zhang R, Wang S, Halstead SB, 1998. Immunogenicity of live attenuated SA14-14-2 Japanese encephalitis vaccine–a comparison of 1- and 3-month immunization schedules. J Infect Dis 177: 221–223.
-
22.
Tsai TF, 2000. New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 13–15 October 1998. Vaccine 18 (Suppl 2): 1–25.
-
23.
Bista MB, Banerjee MK, Shin SH, Tandan JB, Kim MH, Sohn YM, Ohrr HC, Tang JL, Halstead SB, 2001. Efficacy of single-dose SA 14-14-2 vaccine against Japanese encephalitis: a case control study. Lancet 358: 791–795.
-
24.
Chotpitayasunondh T, Sohn YM, Yoksan S, Min J, Ohrr H, 2011. Immunizing children aged 9 to 15 months with live attenuated SA14-14-2 Japanese encephalitis vaccine in Thailand. J Med Assoc Thai 94 (Suppl 3): S195–S203.
-
25.
Tandan JB, Ohrr H, Sohn YM, Yoksan S, Ji M, Nam CM, Halstead SB, 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.
-
26.
Ohrr H, Tandan JB, Sohn YM, Shin SH, Pradhan DP, Halstead SB, 2005. Effect of single dose of SA 14-14-2 vaccine 1 year after immunization in Nepalese children with Japanese encephalitis: a case-control study. Lancet 366: 1375–1378.
-
27.
Yu Y, 2010. Phenotypic and genotypic characteristics of Japanese encephalitis attenuated live vaccine virus SA14-14-2 and their stabilities. Vaccine 28: 3635–3641.
-
28.
Aihara S, Rao CM, Yu YX, Lee T, Watanabe K, Komiya T, Sumiyoshi H, Hashimoto H, Nomoto A, 1991. Identification of mutations that occurred on the genome of Japanese encephalitis virus during the attenuation process. Virus Genes 5: 95–109.
-
29.
Ni H, Chang GJ, Xie H, Trent DW, Barrett AD, 1995. Molecular basis of attenuation of neurovirulence of wild-type Japanese encephalitis virus strain SA14. J Gen Virol 76: 409–413.
-
30.
Nitayaphan S, Grant JA, Chang GJ, Trent DW, 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.
-
31.
Arroyo J, Guirakhoo F, Fenner S, Zhang ZX, Monath TP, Chambers TJ, 2001. Molecular basis for attenuation of neurovirulence of a yellow fever virus/Japanese encephalitis virus chimera vaccine (ChimeriVax-JE). J Virol 75: 934–942.
-
32.
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.
-
33.
Chen LK, Lin YL, Liao CL, Lin CG, Huang YL, Yeh CT, Lai SC, Jan JT, Chin C, 1996. Generation and characterization of organ-tropism mutants of Japanese encephalitis virus in vivo and in vitro. Virology 223: 79–88.
-
34.
Sumiyoshi H, Tignor GH, Shope RE, 1995. Characterization of a highly attenuated Japanese encephalitis virus generated from molecularly cloned cDNA. J Infect Dis 171: 1144–1151.
-
35.
Yang D, Li XF, Ye Q, Wang HJ, Deng YQ, Zhu SY, Zhang Y, Li SH, Qin CF, 2014. Characterization of live-attenuated Japanese encephalitis vaccine virus SA14-14-2. Vaccine 32: 2675–2681.
-
36.
Chambers TJ, Droll DA, Jiang X, Wold WS, Nickells JA, 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.
-
37.
Ye Q, Li XF, Zhao H, Li SH, Deng YQ, Cao RY, Song KY, Wang HJ, Hua RH, Yu YX, Zhou X, Qin ED, Qin CF, 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.
-
38.
Sooryanarain H, Sapkal GN, Gore MM, 2012. Pathogenic and vaccine strains of Japanese encephalitis virus elicit different levels of human macrophage effector functions. Arch Virol 157: 1905–1918.
-
39.
Laurent-Rolle M, Boer EF, Lubick KJ, Wolfinbarger JB, Carmody AB, Rockx B, Liu W, Ashour J, Shupert WL, Holbrook MR, Barrett AD, Mason PW, Bloom ME, Garcia-Sastre A, Khromykh AA, Best SM, 2010. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J Virol 84: 3503–3515.
-
40.
Petricciani JC, Hennessen W, eds, 1987. Cells products safety. Background papers from the WHO Study Group on Biologicals. Geneva, 18–19 Nov. 1986. Dev Biol Stand 68: 1–81.
-
41.
Barrett PN, Mundt W, Kistner O, Howard MK, 2009. Vero cell platform in vaccine production: moving towards cell culture-based viral vaccines. Expert Rev Vaccines 8: 607–618.
-
42.
van Wezel AL, van Steenis G, Hannik CA, Cohen H, 1978. New approach to the production of concentrated and purified inactivated polio and rabies tissue culture vaccines. Dev Biol Stand 41: 159–168.
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