Browse > Article

Characterization of Homologous Defective Interfering RNA during Persistent Infection of Vero Cells with Japanese Encephalitis Virus  

Yoon, Sung Wook (Department of Biology and Research Institute of Basic Sciences, Kyung Hee University)
Lee, Sang-Yong (Department of Biology and Research Institute of Basic Sciences, Kyung Hee University)
Won, Sung-Yong (Department of Biology and Research Institute of Basic Sciences, Kyung Hee University)
Park, Sun-Hee (Department of Biology and Research Institute of Basic Sciences, Kyung Hee University)
Park, Soo-Young (Department of Biology and Research Institute of Basic Sciences, Kyung Hee University)
Jeong, Yong Seok (Department of Biology and Research Institute of Basic Sciences, Kyung Hee University)
Abstract
It has been suggested that defective interfering (DI) RNA contributes to the persistence of Japanese encephalitis virus (JEV). In this study, we characterized molecular and biological aspects of the DI RNA and its relation to viral persistence. We identified a homologous DI virus intimately associated with JEV persistence in Vero cells. The production of DI RNA during undiluted serial passages of JEV coincided with the appearance of cells refractory to acute infection with JEV. We also established a Vero cell clone with a persistent JEV infection in which the DI RNA coreplicated efficiently at the expense of helper virus. The infectious virus yield of the clone fluctuated during its growth depending upon the amount of DI RNA accumulated in the previous replication cycle. Identification of the corresponding negative-sense RNA of the DI RNA indicated that the DI RNA functioned as a replication unit. Most of the DI RNA molecules retained their open reading frames despite a large deletion, encompassing most of the prM, the entire E, and the 5' half of the NS1 gene. Taken together, these observations suggest that the generation of homologous DI RNA during successive JEV acute infections in Vero cells probably participates actively in persistent JEV infection.
Keywords
Defective Interfering RNA; Japanese Encephalitis Virus; Persistent Infection;
Citations & Related Records

Times Cited By Web Of Science : 11  (Related Records In Web of Science)
연도 인용수 순위
  • Reference
1 Atkinson, T., Barrett, A. D. T., Mackenzie, A., and Dimmock, N. J. (1986) Persistence of virulent Semliki Forest virus in mouse brain following co-inoculation with defective interfering particles. J. Gen. Virol. 67, 1189-1194   DOI   ScienceOn
2 Blackwell, J. L. and Brinton, M. A. (1995) BHK cell proteins that bind to the 3′ stem-loop structure of the West Nile virus genome RNA. J. Virol. 69, 5650-5658
3 Ding, X., Wu, X., Duan, T., Siirin, M., Guzman, H., et al. (2005) Nucleotide and amino acid changes in West Nile virus strains exhibiting renal tropism in hamsters. Am. Trop. Med. Hyg. 73, 803−807
4 Kajigaya, S., Arakawa, H., Kuge, S., Koi, T., Imura, N., et al. (1985) Isolation and characterization of defective-interfering particles of poliovirus Sabin 1 strain. Virology 142, 307-316   DOI   ScienceOn
5 Park, J., Hwang, H., Shim, H., Im, K., Auh, C. K., et al. (2004) Altered cell shapes, hyperplasia, and secondary growth in Arabidopsis caused by beet curly top geminivirus infection. Mol. Cells 17, 117−124
6 Perrault, J. (1981) Origins and replication of defective interfering particles. Curr. Top. Microbiol. Immunol. 93, 151−207
7 Specter, S. and Lancz, G. (1992) Clinical Virology Manual, 2nd ed., Elsevier Science Publishing Company, New York
8 Urosevic, N., van Maanen, M., Mansfield, J. P., Mackenzie, J. S., and Shellam, G. S. (1977) Molecular characterization of virus-specific RNA produced in the brains of flavivirussusceptible and -resistant mice with Murray Valley encephalitis virus. J. Gen. Virol. 78, 23-29
9 Vlaycheva, L. A. and Chambers, T. J. (2002) Neuroblastoma cell-adapted yellow fever virus: characterization of a viral variant associated with persistent infection and decreased viral spread. J. Virol. 76, 6172-6184   DOI   ScienceOn
10 Poidinger, M., Coelen, R. J., and Mackenzie, J. S. (1991) Persistent infection of Vero cells by the flavivirus Murray Valley encephalitis virus. J. Gen. Virol. 72, 573−578   DOI   ScienceOn
11 Rice, C. M. (1996) Flaviviridae: the viruses and their replication; in Virology, Fields et al. (eds.), pp. 931−959, Lippincott-Raven Publishers, Philadelphia
12 Feng, G., Takegami, T., and Zhao, G. (2002) Charaterization and E protein expression of mutant strains during persistent infection of KN73 cells with Japanese encephalitis virus. Chin. Med. J. 115, 1324−1327
13 Holland, J. J. (1990) Defective viral genomes; in Fields Virology, Fields et al. (eds.), pp. 151−165, Raven Press, New York
14 Holland, J. J., Villarreal, L. P., Welsh, R. M., Oldstone, M. B. A., Kohne, D., et al. (1976) Long-term persistent vesicular stomatitis virus and rabies virus infections of cells in vitro. J. Gen. Virol. 33, 193-211   DOI   ScienceOn
15 Cave, D. R., Hendrickson, F. M., and Huang, A. S. (1985) Defective interfering virus particles modulate virulence. J. Virol. 55, 366−373
16 Shi, P.-Y., Li, W., and Brinton, M. A. (1996) Cell proteins bind specifically to West Nile virus minus-strand 3′ stem-loop RNA. J. Virol. 70, 6278-6287
17 Burivong, P., Pattanakitsakul, S. N., Thongrungkiat, S., Malasit, P., and Flegel, T. W. (2004) Markedly reduced severity of Dengue virus infection in mosquito cell cultures persistently infected with Aedes albopictus densovirus (AalDNV). Virology 329, 261−269
18 Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
19 Sharma, S., Mathur, A., Prakash, V., Kulshreshta, R., Kumar, R., et al. (1991) Japanese encephalitis latency in peripheral blood lymphocytes and recurrence of infection in children. Clin. Exp. Immunol. 85, 85−91
20 Sumiyoshi, H., Mori, C., Fuke, I., Morita, K., Kuhara, S., et al. (1987) Complete nucleotide sequence of the Japanese encephalitis virus genome RNA. Virology 161, 497−510   DOI   ScienceOn
21 Ravi, V., Desai, A. S., Shenoy, P. K., Satishchandra, P., Chandramuki, A., et al. (1993) Persistence of Japanese encephalitis virus in the human nervous system. J. Med. Virol. 40, 326−329   DOI   ScienceOn
22 Monath, T. P. C. (1986) Pathology of flaviviruses; in The Togaviridae and Flaviviridae, Schlesinger, S. and Schlesinger, M. J. (eds.), pp. 375−440, Plenum Press, New York
23 Von Magnus (1951) Propagation of the PR8 strain of influenza virus in chick embryos. III. Properties of the incomplete virus produced in serial passages of undiluted virus. Acta Pathol. Microbiol. Scand. 29, 157−181   DOI   ScienceOn
24 White, C. L., Thomson, M., and Dimmock, N. J. (1998) Deletion analysis of a defective interfering Semliki Forest virus RNA genome defines a region in the nsP2 sequence that is required for efficient packaging of the genome into virus particles. J. Virol. 72, 4320−4326
25 Barrett, A. D. T. and Dimmock, N. J. (1984) Modulation of Semliki Forest virus-induced infection of mice by defective interfering virus. J. Infect. Dis. 150, 98-103   DOI   ScienceOn
26 Marschall, M., Meier-Ewert, H., Herrler, G., Zimmer, G., and Maassab, H. F. (1997) The cell receptor level is reduced during persistent infection with influenza C virus. Arch. Virol. 142, 1155-1164   DOI   ScienceOn
27 Nayak, D. (1980) Influenza virus defective interfering particles. Ann. Rev. Microbiol. 34, 619−644   DOI   ScienceOn
28 Weiss, B., Leveis, R., and Schlesinger, S. (1983) Evolution of virus and defective-interfering RNAs in BHK cells persistently infected with Sindbis virus. J. Virol. 48, 676-684
29 Westaway, E. G., Mackenzie, J. M., Kenney, M. T., Jones, M. K., and Khromykh, A. A. (1997) Ultrastructure of Kunjin virus- infected cells: colocalization of NS1 and NS3 with double- stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 71, 6650-6661
30 Tonry, J. H., Xiao, S. Y., Siirin, M., Chen, H., da Rosa, A. P., et al. (2005) Persistent shedding of West Nile virus in urine of experimentally infected hamsters. Am. J. Trop. Med. Hyg. 72, 320−324
31 Schmaljohn, C. and Blair, C. D. (1979) Clonal analysis of mammalian cell cultures persistently infected with by Japanese encephalitis virus. J. Virol. 31, 816−822
32 Mathur, A., Arora, K. L., Rawat, S., and Chaturvedi, U. C. (1986) Persistence, reactivation and latency of Japanese encephalitis virus infection in mice. J. Gen. Virol. 67, 381−385   DOI   ScienceOn
33 Tesh, R. B., Siirin, M., Guzman, H., Travassos da Rosa, A. P., Wu, X., et al. (2005) Persistent West Nile virus infection in the golden hamster: studies on its mechanism and possible implications for other flavivirus infections. J. Infect. Dis. 192, 287−295   DOI   ScienceOn
34 Vlaycheva, L., Nickells, M., Droll, D. A., and Chambers, T. J. (2005) Neuroblastoma cell-adapted yellow fever virus: mutagenesis of the E protein locus involved in persistent infection and its effects on virus penetration and spread. J. Gen. Virol. 86, 413−421   DOI   ScienceOn
35 Brinton, M. A. (1982) Characterization of West Nile virus persistent infections in genetically resistant and susceptible mouse cells. I. Generation of defective non-plaquing virus particles. Virology 116, 84-98   DOI   ScienceOn
36 Liao, C. L., Lin, Y. L., Shen, S. C., Shen, J. Y., Su, H. L., et al. (1998) Antiapoptotic but not antiviral function of human bcl- 2 assists establishment of Japanese encephalitis virus persistence in cultured cells. J. Virol. 72, 9844-9854
37 Mackenzie, J. M., Jones, M. K., and Young, P. R. (1996) Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 220, 232−240   DOI   ScienceOn
38 Muylaert, I. R., Galler, R., and Rice, C. M. (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
39 Huang, A. S. and Baltimore, D. (1970) Defective viral particles and viral disease processes. Nature 226, 325−327   DOI   ScienceOn
40 Chen, L. K., Liao, C. L., Lin, C. G., Lai, S. C., Liu, C. I., et al. (1996) Persistence of Japanese encephalitis virus is associated with abnormal expression of the non-structural protein NS1 in host cell. Virology 217, 220-229   DOI   ScienceOn
41 Brinton, M. A. (1986) Replication of flaviviruses; in The Togaviridae and Flaviviridae, Schlesinger, S. and Schlesinger, M. J. (eds.), pp. 327−374, Plenum Press, New York
42 Monath, T. P. C. (1971) Neutralizing antibody responses in the major immunoglobulin classes to yellow fever 17D vaccination of humans. Am. J. Epidemiol. 93, 123−129
43 Slavin, H. B. (1943) Persistence of the virus of St. Louis encephalitis in the central nervous system of mice for over five months. J. Bacteriol. 46, 113−116
44 Schmaljohn, C. and Blair, C. D. (1977) Persistent infection of cultured mammalian cells by Japanese encephalitis virus. J. Virol. 24, 580−589
45 Chambers, T. J., Hahn, C. S., Galler, R., and Rice, C. M. (1990) Flavivirus genome organization, expression and replication. Ann. Rev. Microbiol. 44, 649−688   DOI   ScienceOn
46 Kasahara, S., Ueda, M., Okamoto, Y., Yashida, S., and Yamada, R. (1936) Experimental study on Japanese encephalitis; 1, The passage and properties of virus. Tokyo 1 shinish 2954, 2806−2811
47 Lancaster, M. U., Hodgetts, S. I., Mackenzie, J. S., and Urosevic, N. (1998) Characterization of defective viral RNA produced during persistent infection of Vero cells with Murray Valley encephalitis virus. J. Virol. 72, 2474−2482
48 Umenai, T., Krzysko, R., Betkimirov, T. A., and Assad, F. A. (1985) Japanese encephalitis: current world status. Bull. WHO 63, 625−630