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

Volumn 396, Issue 2, 2010, Pages 298-304

  Tajima, Shigeru ^a   Nerome, Reiko ^a   Nukui, Yoko ^a   Kato, Fumihiro ^a   Takasaki, Tomohiko ^a   Kurane, Ichiro ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

E protein; Infections clone; Japanese encephalitis virus; Pathogenesis

Indexed keywords

ARGININE; PROTEIN E; SERINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EPIDEMIC ENCEPHALITIS; FEMALE; GENE MUTATION; GROWTH RATE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; JAPANESE ENCEPHALITIS VIRUS; MISSENSE MUTATION; MOUSE; MOUSE STRAIN; NEUROBLASTOMA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; VERO CELL; VIROGENESIS; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CULICIDAE; ENCEPHALITIS VIRUSES, JAPANESE; MEMBRANE GLYCOPROTEINS; MICE; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; NEUROBLASTOMA; PLAQUE ASSAY; SWINE; VERO CELLS; VIRAL ENVELOPE PROTEINS;

JAPANESE ENCEPHALITIS VIRUS; MUS;

EID: 70749130682     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.10.035     Document Type: Article

References (44)

1. Aihara S., Rao C.M., Yu Y.X., Lee T., Watanabe K., Komiya T., Sumiyoshi H., Hashimoto H., and Nomoto A. Identification of mutations that occurred on the genome of Japanese encephalitis virus during the attenuation process. Virus Genes 5 (1991) 95-109
2. Arroyo J., Guirakhoo F., Fenner S., Zhang Z.X., Monath T.P., and Chambers T.J. Molecular basis for attenuation of neurovirulence of a yellow fever virus/Japanese encephalitis virus chimera vaccine (ChimeriVax-JE). J. Virol. 75 (2001) 934-942
3. Burke D.S., and Monath T.P. Flaviviruses. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology. 4th ed (2001), Lippincott Willams and Wilkins, Philadelphia 1043-1125
4. Cecilia D., and Gould E.A. Nucleotide changes responsible for loss of neuroinvasiveness in Japanese encephalitis virus neutralization-resistant mutants. Virology 181 (1991) 70-77
5. Chambers T.J., Droll D.A., Jiang X., Wold W.S., and Nickells J.A. JE Nakayama/JE SA14-14-2 virus structural region intertypic viruses: biological properties in the mouse model of neuroinvasive disease. Virology 366 (2007) 51-61
6. Chen L.K., Liao C.L., Lin C.G., Lai S.C., Liu C.I., Ma S.H., Huang Y.Y., and Lin Y.L. Persistence of Japanese encephalitis virus is associated with abnormal expression of the nonstructural protein NS1 in host cells. Virology 217 (1996) 220-229
7. Chiou S.S., Liu H., Chuang C.K., Lin C.C., and Chen W.J. Fitness of Japanese encephalitis virus to Neuro-2a cells is determined by interactions of the viral envelope protein with highly sulfated glycosaminoglycans on the cell surface. J. Med. Virol. 76 (2005) 583-592
8. Hanna J.N., Ritchie S.A., Phillips D.A., Shield J., Bailey M.C., Mackenzie J.S., Poidinger M., McCall B.J., and Mills P.J. An outbreak of Japanese encephalitis in the Torres Strait, Australia, 1995. Med. J. Aust. 165 (1996) 256-260
9. Hasegawa H., Yoshida M., Shiosaka T., Fujita S., and Kobayashi Y. Mutations in the envelope protein of Japanese encephalitis virus affect entry into cultured cells and virulence in mice. Virology 191 (1992) 158-165
10. Hashimoto H., Nomoto A., Watanabe K., Mori T., Takezawa T., Aizawa C., Takegami T., and Hiramatsu K. Molecular cloning and complete nucleotide sequence of the genome of Japanese encephalitis virus Beijing-1 strain. Virus Genes 1 (1988) 305-317
11. Kim J.M., Yun S.I., Song B.H., Hahn Y.S., Lee C.H., Oh H.W., and Lee Y.M. 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 (2008) 7846-7862
12. Kolaskar A.S., and Kulkarni-Kale U. Prediction of three-dimensional structure and mapping of conformational epitopes of envelope glycoprotein of Japanese encephalitis virus. Virology 261 (1999) 31-42
13. Lee E., Hall R.A., and Lobigs M. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J. Virol. 78 (2004) 8271-8280
14. Liang J.J., Liao C.L., Liao J.T., Lee Y.L., and Lin Y.L. A Japanese encephalitis virus vaccine candidate strain is attenuated by decreasing its interferon antagonistic ability. Vaccine 27 (2009) 2746-2754
15. Lindenbach B.D., and Rice C.M. Flaviviridae: the viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology. 4th ed (2001), Lippincott Willams and Wilkins, Philadelphia 991-1041
16. Ma S.P., Yoshida Y., Makino Y., Tadano M., Ono T., and Ogawa M. Short report: a major genotype of Japanese encephalitis virus currently circulating in Japan. Am. J. Trop. Med. Hyg. 69 (2003) 151-154
17. Mishin V.P., Cominelli F., and Yamshchikov V.F. A 'minimal' approach in design of flavivirus infectious DNA. Virus. Res. 81 (2001) 113-123
18. Monath T.P., Arroyo J., Levenbook I., Zhang Z.X., Catalan J., Draper K., and Guirakhoo F. 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 (2002) 1932-1943
19. Mori Y., Okabayashi T., Yamashita T., Zhao Z., Wakita T., Yasui K., Hasebe F., Tadano M., Konishi E., Moriishi K., and Matsuura Y. Nuclear localization of Japanese encephalitis virus core protein enhances viral replication. J. Virol. 79 (2005) 3448-3458
20. Nam J.H., Chung Y.J., Ban S.J., Kim E.J., Park Y.K., and Cho H.W. Envelope gene sequence variation among Japanese encephalitis viruses isolated in Korea. Acta Virol. 40 (1996) 303-309
21. Nerome R., Tajima S., Takasaki T., Yoshida T., Kotaki A., Lim C.K., Ito M., Sugiyama A., Yamauchi A., Yano T., Kameyama T., Morishita I., Kuwayama M., Ogawa T., Sahara K., Ikegaya A., Kanda M., Hosoya Y., Itokazu K., Onishi H., Chiya S., Yoshida Y., Tabei Y., Katsuki K., Tabata K., Harada S., and Kurane I. Molecular epidemiological analyses of Japanese encephalitis virus isolates from swine in Japan from 2002 to 2004. J. Gen. Virol. 88 (2007) 2762-2768
22. Nga P.T., del Carmen Parquet M., Cuong V.D., Ma S.P., Hasebe F., Inoue S., Makino Y., Takagi M., Nam V.S., and Morita K. Shift in Japanese encephalitis virus (JEV) genotype circulating in northern Vietnam: implications for frequent introductions of JEV from Southeast Asia to East Asia. J. Gen. Virol. 85 (2004) 1625-1631
23. Ni H., and Barrett A.D. Molecular differences between wild-type Japanese encephalitis virus strains of high and low mouse neuroinvasiveness. J. Gen. Virol. 77 (1996) 1449-1455
24. Ni H., and Barrett A.D. Attenuation of Japanese encephalitis virus by selection of its mouse brain membrane receptor preparation escape variants. Virology 241 (1998) 30-36
25. Nitatpattana N., Dubot-Peres A., Gouilh M.A., Souris M., Barbazan P., Yoksan S., de Lamballerie X., and Gonzalez J.P. Change in Japanese encephalitis virus distribution. Thailand Emerg. Infect. Dis. 14 (2008) 1762-1765
26. Nitayaphan S., Grant J.A., Chang G.J., and Trent D.W. Nucleotide sequence of the virulent SA-14 strain of Japanese encephalitis virus and its attenuated vaccine derivative, SA-14-14-2. Virology 177 (1990) 541-552
27. Nybakken G.E., Nelson C.A., Chen B.R., Diamond M.S., and Fremont D.H. Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 80 (2006) 11467-11474
28. Rey F.A., Heinz F.X., Mandl C., Kunz C., and Harrison S.C. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375 (1995) 291-298
29. Solomon T., Ni H., Beasley D.W., Ekkelenkamp M., Cardosa M.J., and Barrett A.D. Origin and evolution of Japanese encephalitis virus in southeast Asia. J. Virol. 77 (2003) 3091-3098
30. Sumiyoshi H., Hoke C.H., and Trent D.W. Infectious Japanese encephalitis virus RNA can be synthesized from in vitro-ligated cDNA templates. J. Virol. 66 (1992) 5425-5431
31. Sumiyoshi H., Tignor G.H., and Shope R.E. Characterization of a highly attenuated Japanese encephalitis virus generated from molecularly cloned cDNA. J. Infect. Dis. 171 (1995) 1144-1151
32. Tajima S., Nukui Y., Ito M., Takasaki T., and Kurane I. Nineteen nucleotides in the variable region of 3′ non-translated region are dispensable for the replication of dengue type 1 virus in vitro. Virus Res. 116 (2006) 38-44
33. Tsai T.F. New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 13-15 October 1998. Vaccine 18 (2000) 1-25
34. Uchil P.D., and 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. 65 (2001) 242-251
35. Wang H.Y., Takasaki T., Fu S.H., Sun X.H., Zhang H.L., Wang Z.X., Hao Z.Y., Zhang J.K., Tang Q., Kotaki A., Tajima S., Liang X.F., Yang W.Z., Kurane I., and Liang G.D. Molecular epidemiological analysis of Japanese encephalitis virus in China. J. Gen. Virol. 88 (2007) 885-894
36. WHO. Japanese encephalitis vaccine. Wkly. Epidemiol. Rec. 73 (1998) 337-344
37. Wu S.C., Lin C.W., Lee S.C., and Lian W.C. Phenotypic and genotypic characterization of the neurovirulence and neuroinvasiveness of a large-plaque attenuated Japanese encephalitis virus isolate. Microbes Infect. 5 (2003) 475-480
38. Yang D.K., Kim B.H., Kweon C.H., Kwon J.H., Lim S.I., and Han H.R. Molecular characterization of full-length genome of Japanese encephalitis virus (KV1899) isolated from pigs in Korea. J. Vet. Sci. 5 (2004) 197-205
39. Yoshida Y., Tabei Y., Hasegawa M., Nagashima M., and Morozumi S. Genotypic analysis of Japanese encephalitis virus strains isolated from swine in Tokyo. Japan Jpn. J. Infect. Dis. 58 (2005) 259-261
40. Yun S.I., Kim S.Y., Rice C.M., and Lee Y.M. Development and application of a reverse genetics system for Japanese encephalitis virus. J. Virol. 77 (2003) 6450-6465
41. Zeng M., Jia L.L., Yu Y.X., Dong G.M., Liu W.X., Wang Z.W., and Li D.F. Construction of infectious Japanese encephalitis virus clone based on the cDNA template of the attenuated live vaccine production strain SA14-14-2. Zhonghua Shi Yan He Lin Chuang Bing Du Xue ZaZhi 19 (2005) 9-11
42. Zhang F., Huang Q., Ma W., Jiang S., Fan Y., and 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 96 (2001) 171-182
43. Zhang J.S., Zhao Q.M., Zhang P.H., Jia N., and Cao W.C. Genomic sequence of a Japanese encephalitis virus isolate from southern China. Arch. Virol. 154 (2009) 1177-1180
44. Zhao Z., Date T., Li Y., Kato T., Miyamoto M., Yasui K., and Wakita T. 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 (2005) 2209-2220