Construction of an infectious molecular clone of Japanese encephalitis virus genotype V and its derivative subgenomic replicon capable of expressing a foreign gene

Virus Research

Volumn 195, Issue , 2015, Pages 153-161

  Ishikawa, Tomohiro ^a   Abe, Makoto ^a   Masuda, Michiaki ^a  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Flavivirus; Infectious clone; Japanese encephalitis virus; Subgenomic replicon

Indexed keywords

COMPLEMENTARY DNA; FIREFLY LUCIFERASE; LUCIFERASE; RNA POLYMERASE; STRUCTURAL PROTEIN; VIRUS RNA; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CLONE; CONTROLLED STUDY; ELECTROPORATION; FOREIGN GENE; GENE; GENE EXPRESSION; GENOME; GENOTYPE; IN VITRO STUDY; JAPANESE ENCEPHALITIS VIRUS; JAPANESE ENCEPHALITIS VIRUS GENOTYPE V; MAMMAL CELL; MOSQUITO; NONHUMAN; PLASMID; PROGENY; REPLICON; VIRUS STRAIN; ANIMAL; BIOSYNTHESIS; CELL LINE; GENETIC RECOMBINATION; GENETICS; MAMMAL; MOLECULAR CLONING; PHYSIOLOGY; VIRUS REPLICATION;

FLAVIVIRUS; JAPANESE ENCEPHALITIS VIRUS; MAMMALIA;

ANIMALS; CELL LINE; CLONING, MOLECULAR; CULICIDAE; ENCEPHALITIS VIRUS, JAPANESE; GENE EXPRESSION; LUCIFERASES, FIREFLY; MAMMALS; PLASMIDS; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC; REPLICON; VIRUS REPLICATION;

EID: 84919340015     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.10.010     Document Type: Article

References (62)

1. Alvarez D.E., De Lella Ezcurra A.L., Fucito S., Gamarnik A.V. Role of RNA structures present at the 3'UTR of dengue virus on translation, RNA synthesis, and viral replication. Virology 2005, 339:200-212.
2. Arias A., Urena L., Thorne L., Yunus M.A., Goodfellow I. Reverse genetics mediated recovery of infectious murine norovirus. J. Vis. Exp. 2012, 64:e4145.
3. Beasley D.W., Li L., Suderman M.T., Guirakhoo F., Trent D.W., Monath T.P., Shope R.E., Barrett A.D. Protection against Japanese encephalitis virus strains representing four genotypes by passive transfer of sera raised against ChimeriVax-JE experimental vaccine. Vaccine 2004, 22:3722-3726.
4. Campbell G.L., Hills S.L., Fischer M., Jacobson J.A., Hoke C.H., Hombach J.M., Marfin A.A., Solomon T., Tsai T.F., Tsu V.D., Ginsburg A.S. Estimated global incidence of Japanese encephalitis: a systematic review. Bull. World Health Organ. 2011, 89:766-774. 774A-774E.
5. Chen Y.Y., Fan Y.C., Tu W.C., Chang R.Y., Shih C.C., Lu I.H., Chien M.S., Lee W.C., Chen T.H., Chang G.J., Chiou S.S. Japanese encephalitis virus genotype replacement, Taiwan, 2009-2010. Emerg. Infect. Dis. 2011, 17:2354-2356.
6. Corver J., Lenches E., Smith K., Robison R.A., Sando T., Strauss E.G., Strauss J.H. Fine mapping of a cis-acting sequence element in yellow fever virus RNA that is required for RNA replication and cyclization. J. Virol. 2003, 77:2265-2270.
7. Davis C.W., Nguyen H.Y., Hanna S.L., Sanchez M.D., Doms R.W., Pierson T.C. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J. Virol. 2006, 80:1290-1301.
8. Erra E.O., Askling H.H., Yoksan S., Rombo L., Riutta J., Vene S., Lindquist L., Vapalahti O., Kantele A. Cross-protective capacity of Japanese encephalitis (JE) vaccines against circulating heterologous JE virus genotypes. Clin. Infect. Dis. 2013, 56:267-270.
9. Fulmali P.V., Sapkal G.N., Athawale S., Gore M.M., Mishra A.C., Bondre V.P. Introduction of Japanese encephalitis virus genotype I, India. Emerg. Infect. Dis. 2011, 17:319-321.
10. Gehrke R., Ecker M., Aberle S.W., Allison S.L., Heinz F.X., Mandl C.W. Incorporation of tick-borne encephalitis virus replicons into virus-like particles by a packaging cell line. J. Virol. 2003, 77:8924-8933.
11. Habjan M., Penski N., Spiegel M., Weber F. T7 RNA polymerase-dependent and -independent systems for cDNA-based rescue of Rift Valley fever virus. J. Gen. Virol. 2008, 89:2157-2166.
12. Hasegawa H., Yoshida M., Fujita S., Kobayashi Y. Comparison of structural proteins among antigenically different Japanese encephalitis virus strains. Vaccine 1994, 12:841-844.
13. Hasegawa H., Yoshida M., Kobayashi Y., Fujita S. Antigenic analysis of Japanese encephalitis viruses in Asia by using monoclonal antibodies. Vaccine 1995, 13:1713-1721.
14. Hoenninger V.M., Rouha H., Orlinger K.K., Miorin L., Marcello A., Kofler R.M., Mandl C.W. Analysis of the effects of alterations in the tick-borne encephalitis virus 3'-noncoding region on translation and RNA replication using reporter replicons. Virology 2008, 377:419-430.
15. Huang J.H., Lin T.H., Teng H.J., Su C.L., Tsai K.H., Lu L.C., Lin C., Yang C.F., Chang S.F., Liao T.L., Yu S.K., Cheng C.H., Chang M.C., Hu H.C., Shu P.Y. Molecular epidemiology of Japanese encephalitis virus, Taiwan. Emerg. Infect. Dis. 2010, 16:876-878.
16. Ishikawa T., Konishi E. Mosquito cells infected with Japanese encephalitis virus release slowly-sedimenting hemagglutinin particles in association with intracellular formation of smooth membrane structures. Microbiol. Immunol. 2006, 50:211-223.
17. Ishikawa T., Widman D.G., Bourne N., Konishi E., Mason P.W. Construction and evaluation of a chimeric pseudoinfectious virus vaccine to prevent Japanese encephalitis. Vaccine 2008, 26:2772-2781.
18. Ishikawa T., Konishi E. Combating Japanese encephalitis: Vero-cell derived inactivated vaccines and the situation in Japan. Future Virol. 2010, 5:785-799.
19. Ishikawa T., Wang G., Widman D.G., Infante E., Winkelmann E.R., Bourne N., Mason P.W. Enhancing the utility of a prM/E-expressing chimeric vaccine for Japanese encephalitis by addition of the JEV NS1 gene. Vaccine 2011, 29:7444-7455.
20. Ishikawa T., Yamanaka A., Konishi E. A review of successful flavivirus vaccines and the problems with those flaviviruses for which vaccines are not yet available. Vaccine 2014, 32:1326-1337.
21. Jeong H.S., Shin J.H., Park Y.N., Choi J.Y., Kim Y.L., Kim B.G., Ryu S.R., Baek S.Y., Lee S.H., Park S.N. Development of real-time RT-PCR for evaluation of JEV clearance during purification of HPV type 16 L1 virus-like particles. Biologicals 2003, 31:223-229.
22. Khromykh A.A., Westaway E.G. Subgenomic replicons of the flavivirus Kunjin: construction and applications. J. Virol. 1997, 71:1497-1505.
23. Kitai Y., Shoda M., Kondo T., Konishi E. Epitope-blocking enzyme-linked immunosorbent assay to differentiate west nile virus from Japanese encephalitis virus infections in equine sera. Clin. Vaccine Immunol. 2007, 14:1024-1031.
24. Konishi E., Suzuki T. Ratios of subclinical to clinical Japanese encephalitis (JE) virus infections in vaccinated populations: evaluation of an inactivated JE vaccine by comparing the ratios with those in unvaccinated populations. Vaccine 2002, 21:98-107.
25. Konishi E., Yagawa K., Yamanaka A. Vero cells infected with vaccinia viruses expressing Japanese encephalitis virus envelope protein induce polykaryocyte formation under neutral conditions. Jpn. J. Infect. Dis. 2008, 61:410-411.
26. Konishi E., Konishi M. Nonstructural protein 1 antibody-based epitope-blocking enzyme-linked immunosorbent assay to differentiate Japanese encephalitis virus from dengue virus infections in humans. Jpn. J. Infect. Dis. 2011, 64:284-291.
27. Lan S., McLay Schelde L., Wang J., Kumar N., Ly H., Liang Y. Development of infectious clones for virulent and avirulent pichinde viruses: a model virus to study arenavirus-induced hemorrhagic fevers. J. Virol. 2009, 83:6357-6362.
28. Li M.H., Fu S.H., Chen W.X., Wang H.Y., Guo Y.H., Liu Q.Y., Li Y.X., Luo H.M., Da W., Duo Ji D.Z., Ye X.M., Liang G.D. Genotype v Japanese encephalitis virus is emerging. PLoS Negl. Trop. Dis. 2011, 5:e1231.
29. Li M.H., Fu S.H., Chen W.X., Wang H.Y., Cao Y.X., Liang G.D. Molecular characterization of full-length genome of japanese encephalitis virus genotype V isolated from Tibet, China. Biomed. Environ. Sci. 2014, 27:231-239.
30. Li S.H., Li X.F., Zhao H., Deng Y.Q., Yu X.D., Zhu S.Y., Jiang T., Ye Q., Qin E.D., Qin C.F. Development and characterization of the replicon system of Japanese encephalitis live vaccine virus SA14-14-2. Virol. J. 2013, 10:64.
31. Li X.D., Li X.F., Ye H.Q., Deng C.L., Ye Q., Shan C., Shang B.D., Xu L.L., Li S.H., Cao S.B., Yuan Z.M., Shi P.Y., Qin C.F., Zhang B. Recovery of a chemically synthesized Japanese encephalitis virus reveals two critical adaptive mutations in NS2B and NS4A. J. Gen. Virol. 2014, 95:806-815.
32. Liu X., Yu Y., Li M., Liang G., Wang H., Jia L., Dong G. Study on the protective efficacy of SA14-14-2 attenuated Japanese encephalitis against different JE virus isolates circulating in China. Vaccine 2011, 29:2127-2130.
33. Lo M.K., Tilgner M., Bernard K.A., Shi P.Y. Functional analysis of mosquito-borne flavivirus conserved sequence elements within 3' untranslated region of West Nile virus by use of a reporting replicon that differentiates between viral translation and RNA replication. J. Virol. 2003, 77:10004-10014.
34. Mason P.W. Maturation of Japanese encephalitis virus glycoproteins produced by infected mammalian and mosquito cells. Virology 1989, 169:354-364.
35. Mishin V.P., Cominelli F., Yamshchikov V.F. A 'minimal' approach in design of flavivirus infectious DNA. Virus Res. 2001, 81:113-123.
36. Mohammed M.A., Galbraith S.E., Radford A.D., Dove W., Takasaki T., Kurane I., Solomon T. Molecular phylogenetic and evolutionary analyses of Muar strain of Japanese encephalitis virus reveal it is the missing fifth genotype. Infect. Genet. Evol. 2011, 11:855-862.
37. Pan X.L., Liu H., Wang H.Y., Fu S.H., Liu H.Z., Zhang H.L., Li M.H., Gao X.Y., Wang J.L., Sun X.H., Lu X.J., Zhai Y.G., Meng W.S., He Y., Wang H.Q., Han N., Wei B., Wu Y.G., Feng Y., Yang D.J., Wang L.H., Tang Q., Xia G., Kurane I., Rayner S., Liang G.D. Emergence of genotype I of Japanese encephalitis virus as the dominant genotype in Asia. J. Virol. 2011, 85:9847-9853.
38. Pierson T.C., Diamond M.S. Flaviviruses. Fields Virology 2013, 747-794. Lippincott Williams & Wilkins, Philadelphia, PA. sixth ed. D.M. Knipe, P.M. Howley (Eds.).
39. Pu S.Y., Wu R.H., Yang C.C., Jao T.M., Tsai M.H., Wang J.C., Lin H.M., Chao Y.S., Yueh A. Successful propagation of flavivirus infectious cDNAs by a novel method to reduce the cryptic bacterial promoter activity of virus genomes. J. Virol. 2011, 85:2927-2941.
40. Pyke A.T., Williams D.T., Nisbet D.J., van den Hurk A.F., Taylor C.T., Johansen C.A., Macdonald J., Hall R.A., Simmons R.J., Mason R.J., Lee J.M., Ritchie S.A., Smith G.A., Mackenzie J.S. The appearance of a second genotype of Japanese encephalitis virus in the Australasian region. Am. J. Trop. Med. Hyg. 2001, 65:747-753.
41. Ryan M.D., Drew J. Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. EMBO J. 1994, 13:928-933.
42. Schuh A.J., Ward M.J., Brown A.J., Barrett A.D. Phylogeography of Japanese encephalitis virus: genotype is associated with climate. PLoS Negl. Trop. Dis. 2013, 7:e2411.
43. Schuh A.J., Ward M.J., Leigh Brown A.J., Barrett A.D. Dynamics of the emergence and establishment of a newly dominant genotype of Japanese encephalitis virus throughout Asia. J. Virol. 2014, 88:4522-4532.
44. Shi P.Y., Tilgner M., Lo M.K. Construction and characterization of subgenomic replicons of New York strain of West Nile virus. Virology 2002, 296:219-233.
45. Solomon T., Ni H., Beasley D.W., Ekkelenkamp M., Cardosa M.J., Barrett A.D. Origin and evolution of Japanese encephalitis virus in southeast Asia. J. Virol. 2003, 77:3091-3098.
46. Sumiyoshi H., Hoke C.H., Trent D.W. Infectious Japanese encephalitis virus RNA can be synthesized from in vitro-ligated cDNA templates. J. Virol. 1992, 66:5425-5431.
47. Sumiyoshi H., Tignor G.H., Shope R.E. Characterization of a highly attenuated Japanese encephalitis virus generated from molecularly cloned cDNA. J. Infect. Dis. 1995, 171:1144-1151.
48. Suzuki R., de Borba L., Duarte dos Santos C.N., Mason P.W. Construction of an infectious cDNA clone for a Brazilian prototype strain of dengue virus type 1: characterization of a temperature-sensitive mutation in NS1. Virology 2007, 362:374-383.
49. Suzuki R., Ishikawa T., Konishi E., Matsuda M., Watashi K., Aizaki H., Takasaki T., Wakita T. Production of single-round infectious chimeric flaviviruses with DNA-based Japanese encephalitis virus replicon. J. Gen. Virol. 2014, 95:60-65.
50. Tabor S., Richardson C.C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:1074-1078.
51. Tajima S., Nerome R., Nukui Y., Kato F., Takasaki T., Kurane I. 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 2010, 396:298-304.
52. Takhampunya R., Kim H.C., Tippayachai B., Kengluecha A., Klein T.A., Lee W.J., Grieco J., Evans B.P. Emergence of Japanese encephalitis virus genotype V in the Republic of Korea. Virol. J. 2011, 8:449.
53. Uchil P.D., Satchidanandam V. Phylogenetic analysis of Japanese encephalitis virus: envelope gene based analysis reveals a fifth genotype, geographic clustering, and multiple introductions of the virus into the Indian subcontinent. Am. J. Trop. Med. Hyg. 2001, 65:242-251.
54. van den Hurk A.F., Montgomery B.L., Northill J.A., Smith I.L., Zborowski P., Ritchie S.A., Mackenzie J.S., Smith G.A. Short report: the first isolation of Japanese encephalitis virus from mosquitoes collected from mainland Australia. Am. J. Trop. Med. Hyg. 2006, 75:21-25.
55. Varnavski A.N., Khromykh A.A. Noncytopathic flavivirus replicon RNA-based system for expression and delivery of heterologous genes. Virology 1999, 255:366-375.
56. Yamshchikov V., Mishin V., Cominelli F. A new strategy in design of +RNA virus infectious clones enabling their stable propagation in E. coli. Virology 2001, 281:272-280.
57. Yang Y., Zohaib A., Chen G., Ye J., Cao S. DC-SIGN increases Japanese encephalitis virus infection. Pak. Vet. J. 2013, 33:408-412.
58. Yao X., Han Q., Song J., Liang C., Wakita T., Yang R., Chen X. Baculovirus mediated production of infectious hepatitis C virus in human hepatoma cells stably expressing T7 RNA polymerase. Mol. Biotechnol. 2008, 40:186-194.
59. Yun S.I., Kim S.Y., Rice C.M., Lee Y.M. Development and application of a reverse genetics system for Japanese encephalitis virus. J. Virol. 2003, 77:6450-6465.
60. Yun S.I., Choi Y.J., Yu X.F., Song J.Y., Shin Y.H., Ju Y.R., Kim S.Y., Lee Y.M. Engineering the Japanese encephalitis virus RNA genome for the expression of foreign genes of various sizes: implications for packaging capacity and RNA replication efficiency. J. Neurovirol. 2007, 13:522-535.
61. Zhang F., Huang Q., Ma W., Jiang S., Fan Y., Zhang H. Amplification and cloning of the full-length genome of Japanese encephalitis virus by a novel long RT-PCR protocol in a cosmid vector. J. Virol. Methods 2001, 96:171-182.
62. Zheng H., Tian H., Jin Y., Wu J., Shang Y., Yin S., Liu X., Xie Q. Development of a hamster kidney cell line expressing stably T7 RNA polymerase using retroviral gene transfer technology for efficient rescue of infectious foot-and-mouth disease virus. J. Virol. Methods 2009, 156:129-137.