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

Journal of Virology

Volumn 83, Issue 16, 2009, Pages 7909-7930

  Yun, Sang Im ^a   Choi, Yu Jeong ^a   Song, Byung Hak ^a   Lee, Young Min ^a  

^a Chungbuk National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; VIRUS RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE DUPLICATION; GENE MAPPING; HUMAN; HUMAN CELL; JAPANESE ENCEPHALITIS VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; RNA REPLICATION; SPONTANEOUS MUTATION; VIRION; VIRUS REPLICATION; 3' UNTRANSLATED REGION; AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; GENOMIC INSTABILITY; HAMSTER; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; REGULATORY SEQUENCE; VIRUS GENOME;

CRICETINAE; JAPANESE ENCEPHALITIS VIRUS;

3' UNTRANSLATED REGIONS; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; CRICETINAE; ENCEPHALITIS VIRUS, JAPANESE; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; GENOMIC INSTABILITY; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, VIRAL; SEQUENCE DELETION; VIRUS REPLICATION;

EID: 67749120705     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02541-08     Document Type: Article

References (88)

1. Ackermann, M., and R. Padmanabhan. 2001. De novo synthesis of RNA by the dengue virus RNA-dependent RNA polymerase exhibits temperature dependence at the initiation but not elongation phase. J. Biol. Chem. 276: 39926-39937.
2. Alvarez, D. E., A. L. De Lella Ezcurra, S. Fucito, and A. V. Gamarnik. 2005a. Role of RNA structures present at the 3′UTR of dengue virus on translation, RNA synthesis, and viral replication. Virology 339:200-212.
3. Alvarez, D. E., M. F. Lodeiro, S. J. Luduena, L. I. Pietrasanta, and A. V. Gamarnik. 2005b. Long-range RNA-RNA interactions circularize the dengue virus genome. J. Virol. 79:6631-6643.
4. Alvarez, D. E., C. V. Filomatori, and A. V. Gamarnik. 2008. Functional analysis of dengue virus cyclization sequences located at the 5′ and 3′UTRs. Virology 375:223-235.
5. Ball, L. A. 1997. Nodavirus RNA recombination. Semin. Virol. 8:95-100.
6. Blackwell, J. L., and M. A. Brinton. 1995. BHK cell proteins that bind to the 3′ stem-loop structure of the West Nile virus genome RNA. J. Virol. 69: 5650-5658.
7. Blackwell, J. L., and M. A. Brinton. 1997. Translation elongation factor-1 alpha interacts with the 3′ stem-loop region of West Nile virus genomic RNA. J. Virol. 71:6433-6444.
8. Bredenbeek, P. J., E. A. Kooi, B. Lindenbach, N. Huijkman, C. M. Rice, and W. J. Spaan. 2003. A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication. J. Gen. Virol. 84:1261-1268.
9. Brinton, M. A., A. V. Fernandez, and J. H. Dispoto. 1986. The 3′-nucleotides of flavivirus genomic RNA form a conserved secondary structure. Virology 153:113-121.
10. Brinton, M. A., and J. H. Dispoto. 1988. Sequence and secondary structure analysis of the 5′-terminal region of flavivirus genome RNA. Virology 162:290-299.
11. Calisher, C. H., and E. A. Gould. 2003. Taxonomy of the virus family Flaviviridae. Adv. Virus Res. 59:1-19.
12. Cammisa-Parks, H., L. A. Cisar, A. Kane, and V. Stollar. 1992. The complete nucleotide sequence of cell fusing agent (CFA): homology between the nonstructural proteins encoded by CFA and the nonstructural proteins encoded by arthropod-borne flaviviruses. Virology 189:511-524.
13. Chambers, T. J., C. S. Hahn, R. Galler, and C. M. Rice. 1990. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 44:649-688.
14. Corver, J., E. Lenches, K. Smith, R. A. Robison, T. Sando, E. G. Strauss, and J. H. Strauss. 2003. Fine mapping of a cis-acting sequence element in yellow fever virus RNA that is required for RNA replication and cyclization. J. Virol. 77:2265-2270.
15. Davis, W. G., J. L. Blackwell, P. Y. Shi, and M. A. Brinton. 2007. Interaction between the cellular protein eEF1A and the 3′-terminal stem-loop of West Nile virus genomic RNA facilitates viral minus-strand RNA synthesis. J. Virol. 81:10172-10187.
16. De Nova-Ocampo, M., N. Villegas-Sepúlveda, and R. M. del Angel. 2002. Translation elongation factor-1alpha, La, and PTB interact with the 3′ untranslated region of dengue 4 virus RNA. Virology 295:337-347.
17. Dong, H., B. Zhang, and P. Y. Shi. 2008. Terminal structures of West Nile virus genomic RNA and their interactions with viral NS5 protein. Virology 381:123-135.
18. Elghonemy, S., W. G. Davis, and M. A. Brinton. 2005. The majority of the nucleotides in the top loop of the genomic 3′ terminal stem loop structure are cis-acting in a West Nile virus infectious clone. Virology 331:238-246.
19. Emara, M. M., and M. A. Brinton. 2007. Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc. Natl. Acad. Sci. USA 104:9041-9046.
20. Emara, M. M., H. Liu, W. G. Davis, and M. A. Brinton. 2008. Mutation of mapped TIA-1/TIAR binding sites in the 3′ terminal stem-loop of West Nile virus minus-strand RNA in an infectious clone negatively affects genomic RNA amplification. J. Virol. 82:10657-10670.
21. Endy, T. P., and A. Nisalak. 2002. Japanese encephalitis virus: ecology and epidemiology. Curr. Top. Microbiol. Immunol. 267:11-48.
22. Filomatori, C. V., M. F. Lodeiro, D. E. Alvarez, M. M. Samsa, L. Pietrasanta, and A. V. Gamarnik. 2006. A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome. Genes Dev. 20:2238-2249.
23. Gritsun, T. S., A. Tuplin, and E. A. Gould. 2006. Origin, evolution, and function of flavivirus RNA in untranslated and coding regions: implications for virus transmission, p. 47-99. In M. Kalitzky and P. Borowski (ed.), Molecular biology of the flavivirus. Horizon Scientific Press, Norwich, United Kingdom.
24. Gritsun, T. S., and E. A. Gould. 2006a. The 3′ untranslated regions of Kamiti River virus and cell fusing agent virus originated by self-duplication. J. Gen. Virol. 87:2615-2619.
25. Gritsun, T. S., and E. A. Gould. 2006b. The 3′ untranslated region of tick-borne flaviviruses originated by the duplication of long repeat sequences within the open reading frame. Virology 354:217-223.
26. Gritsun, T. S., and E. A. Gould. 2006c. Direct repeats in the 3′ untranslated regions of mosquito-borne flaviviruses: possible implications for virus transmission. J. Gen. Virol. 87:3297-3305.
27. Gritsun, T. S., and E. A. Gould. 2007a. Direct repeats in the flavivirus 3′ untranslated region; a strategy for survival in the environment? Virology 358:258-265.
28. Gritsun, T. S., and E. A. Gould. 2007b. Origin and evolution of 3′UTR of flaviviruses: long direct repeats as a basis for the formation of secondary structures and their significance for virus transmission. Adv. Virus Res. 69:203-248.
29. Gubler, D. J., G. Kuno, and L. Markoff. 2007. Flaviviruses, p. 1153-1252. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins Publishers, Philadelphia, PA.
30. Hahn, C. S., Y. S. Hahn, C. M. Rice, E. Lee, L. Dalgarno, E. G. Strauss, and J. H. Strauss. 1987. Conserved elements in the 3′ untranslated region of flavivirus RNAs and potential cyclization sequences. J. Mol. Biol. 198:33-41.
31. Hoenninger, V. M., H. Rouha, K. K. Orlinger, L. Miorin, A. Marcello, R. M. Kofler, and C. W. Mandl. 2008. Analysis of the effects of alterations in the tick-borne encephalitis virus 3′-noncoding region on translation and RNA replication using reporter replicons. Virology 377:419-430.
32. Khromykh, A. A., and E. G. Westaway. 1994. Completion of Kunjin virus RNA sequence and recovery of an infectious RNA transcribed from stably cloned full-length cDNA. J. Virol. 68:4580-4588.
33. Khromykh, A. A., and E. G. Westaway. 1997. Subgenomic replicons of the flavivirus Kunjin: construction and applications. J. Virol. 71:1497-1505.
34. Khromykh, A. A., H. Meka, K. J. Guyatt, and E. G. Westaway. 2001. Essential role of cyclization sequences in flavivirus RNA replication. J. Virol. 75:6719-6728.
35. Khromykh, A. A., N. Kondratieva, J. Y. Sgro, A. Palmenberg, and E. G. Westaway. 2003. Significance in replication of the terminal nucleotides of the flavivirus genome. J. Virol. 77:10623-10629.
36. Kim, J.-M., S.-I. Yun, B.-H. Song, Y.-S. Hahn, C.-H. Lee, H.-W. Oh, and Y.-M. Lee. 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.
37. Kofler, R. M., V. M. Hoenninger, C. Thurner, and C. W. Mandl. 2006. Functional analysis of the tick-borne encephalitis virus cyclization elements indicates major differences between mosquito-borne and tick-borne flaviviruses. J. Virol. 80:4099-4113.
38. Lai, M. M. 1992. RNA recombination in animal and plant viruses. Microbiol. Rev. 56:61-79.
39. Li, W., Y. Li, N. Kedersha, P. Anderson, M. Emara, K. M. Swiderek, G. T. Moreno, and M. A. Brinton. 2002. Cell proteins TIA-1 and TIAR interact with the 3′ stem-loop of the West Nile virus complementary minus-strand RNA and facilitate virus replication. J. Virol. 76:11989-12000.
40. Lindenbach, B. D., and C. M. Rice. 2003. Molecular biology of flaviviruses. Adv. Virus Res. 59:23-61.
41. Lindenbach, B. D., H.-J. Thiel, and C. M. Rice. 2007. Flaviviridae: the viruses and their replication, p. 1101-1152. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins Publishers, Philadelphia, PA.
42. Lo, M. K., M. Tilgner, K. A. Bernard, and P. Y. Shi. 2003. 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. 77:10004-10014.
43. Mackenzie, J. S., C. A. Johansen, S. A. Ritchie, A. F. Van Den Hurk, and R. A. Hall. 2002. Japanese encephalitis as an emerging virus: the emergence and spread of Japanese encephalitis virus in Australasia. Curr. Top. Microbiol. Immunol. 267:49-73.
44. Mackenzie, J. S., D. J. Gubler, and L. R. Petersen. 2004. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10:S98-S109.
45. Mandl, C. W., H. Holzmann, C. Kunz, and F. X. Heinz. 1993. Complete genomic sequence of Powassan virus: evaluation of genetic elements in tick-borne versus mosquito-borne flaviviruses. Virology 194:173-184.
46. Mandl, C. W., H. Holzmann, T. Meixner, S. Rauscher, P. F. Stadler, S. L. Allison, and F. X. Heinz. 1998. Spontaneous and engineered deletions in the 3′ noncoding region of tick-borne encephalitis virus: construction of highly attenuated mutants of a flavivirus. J. Virol. 72:2132-2140.
47. Markoff, L. 2003. 5′- And 3′-noncoding regions in flavivirus RNA. Adv. Virus Res. 59:177-228.
48. Mathews, D. H., J. Sabina, M. Zuker, and D. H. Turner. 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288:911-940.
49. Men, R., M. Bray, D. Clark, R. M. Chanock, and C. J. Lai. 1996. Dengue type 4 virus mutants containing deletions in the 3′ noncoding region of the RNA genome: analysis of growth restriction in cell culture and altered viremia pattern and immunogenicity in rhesus monkeys. J. Virol. 70:3930-3937.
50. Mohan, P. M., and R. Padmanabhan. 1991. Detection of stable secondary structure at the 3′ terminus of dengue virus type 2 RNA. Gene 108:185-191.
51. Nomaguchi, M., T. Teramoto, L. Yu, L. Markoff, and R. Padmanabhan. 2004. Requirements for West Nile virus (-)- and (+)-strand subgenomic RNA synthesis in vitro by the viral RNA-dependent RNA polymerase expressed in Escherichia coli. J. Biol. Chem. 279:12141-12151.
52. Olsthoorn, R. C., and J. F. Bol. 2001. Sequence comparison and secondary structure analysis of the 3′ noncoding region of flavivirus genomes reveals multiple pseudoknots. RNA 7:1370-1377.
53. Paranjape, S. M., and E. Harris. 2007. Y box-binding protein-1 binds to the dengue virus 3′-untranslated region and mediates antiviral effects. J. Biol. Chem. 282:30497-30508.
54. Pletnev, A. G. 2001. Infectious cDNA clone of attenuated Langat tick-borne flavivirus (strain E5) and a 3′ deletion mutant constructed from it exhibit decreased neuroinvasiveness in immunodeficient mice. Virology 282:288-300.
55. Proutski, V., E. A. Gould, and E. C. Holmes. 1997. Secondary structure of the 3′ untranslated region of flaviviruses: similarities and differences. Nucleic Acids Res. 25:1194-1202.
56. Rauscher, S., C. Flamm, C. W. Mandl, F. X. Heinz, and P. F. Stadler. 1997. Secondary structure of the 3′-noncoding region of flavivirus genomes: comparative analysis of base pairing probabilities. RNA 3:779-791.
57. Rice, C. M., E. M. Lenches, S. R. Eddy, S. J. Shin, R. L. Sheets, and J. H. Strauss. 1985. Nucleotide sequence of yellow fever virus: implications for flavivirus gene expression and evolution. Science 229:726-733.
58. Romero, T. A., E. Tumban, J. Jun, W. B. Lott, and K. A. Hanley. 2006. Secondary structure of dengue virus type 4 3′ untranslated region: impact of deletion and substitution mutations. J. Gen. Virol. 87:3291-3296.
59. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
60. Schmittgen, T. D., B. A. Zakrajsek, A. G. Mills, V. Gorn, M. J. Singer, and M. W. Reed. 2000. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal. Biochem. 285:194-204.
61. Shi, P. Y., M. A. Brinton, J. M. Veal, Y. Y. Zhong, and W. D. Wilson. 1996. Evidence for the existence of a pseudoknot structure at the 3′ terminus of the flavivirus genomic RNA. Biochemistry 35:4222-4230.
62. Silva, P. A., R. Molenkamp, T. J. Dalebout, N. Charlier, J. H. Neyts, W. J. Spaan, and P. J. Bredenbeek. 2007. Conservation of the pentanucleotide motif at the top of the yellow fever virus 17D 3′ stem-loop structure is not required for replication. J. Gen. Virol. 88:1738-1747. (Erratum, 88:2361).
63. Solomon, T. 2003. Recent advances in Japanese encephalitis. J. Neurovirol. 9:274-283.
64. Song, B.-H., S.-I. Yun, Y.-J. Choi, J.-M. Kim, C.-H. Lee, and Y.-M. Lee. 2008. A complex RNA motif defined by three discontinuous 5-nucleotide-long strands is essential for flavivirus RNA replication. RNA 14:1791-1813.
65. Strauss, J. H., and E. G. Strauss. 1997. Recombination in alphaviruses. Semin. Virol. 8:85-94.
66. Ta, M., and S. Vrati. 2000. Mov34 protein from mouse brain interacts with the 3′ noncoding region of Japanese encephalitis virus. J. Virol. 74:5108-5115.
67. Thiel, H.-J., M. S. Collett, E. A. Gould, F. X. Heinz, M. Houghton, G. Meyers, R. H. Purcell, and C. M. Rice. 2005. Family Flaviviridae, p. 981-998. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.), Virus taxonomy: eighth report of the international committee on taxonomy of viruses. Elsevier Academic Press, San Diego, CA.
68. Thurner, C., C. Witwer, I. L. Hofacker, and P. F. Stadler. 2004. Conserved RNA secondary structures in Flaviviridae genomes. J. Gen. Virol. 85:1113-1124.
69. Tilgner, M., and P. Y. Shi. 2004. Structure and function of the 3′ terminal six nucleotides of the West Nile virus genome in viral replication. J. Virol. 78:8159-8171.
70. Tilgner, M., T. S. Deas, and P. Y. Shi. 2005. The flavivirus-conserved pentanucleotide in the 3′ stem-loop of the West Nile virus genome requires a specific sequence and structure for RNA synthesis, but not for viral translation. Virology 331:375-386.
71. Weaver, S. C., and A. D. Barrett. 2004. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat. Rev. Microbiol. 2:789-801.
72. Wengler, G., and G. Wengler. 1981. Terminal sequences of the genome and replicative-from RNA of the flavivirus West Nile virus: absence of poly(A) and possible role in RNA replication. Virology 113:544-555.
73. Wengler, G., and E. Castle. 1986. Analysis of structural properties which possibly are characteristic for the 3′-terminal sequence of the genome RNA of flaviviruses. J. Gen. Virol. 67:1183-1188.
74. Westaway, E. G., J. M. Mackenzie, and A. A. Khromykh. 2003. Kunjin RNA replication and applications of Kunjin replicons. Adv. Virus Res. 59:99-140.
75. Winer, J., C. K. Jung, I. Shackel, and P. M. Williams. 1999. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270:41-49.
76. Worobey, M., and E. C. Holmes. 1999. Evolutionary aspects of recombination in RNA viruses. J. Gen. Virol. 80:2535-2543.
77. Yocupicio-Monroy, M., R. Padmanabhan, F. Medina, and R. M. del Angel. 2007. Mosquito La protein binds to the 3′ untranslated region of the positive and negative polarity dengue virus RNAs and relocates to the cytoplasm of infected cells. Virology 357:29-40.
78. You, S., and C. M. Rice. 2008. 3′ RNA elements in hepatitis C virus replication: kissing partners and long poly(U). J. Virol. 82:184-195.
79. You, S., and R. Padmanabhan. 1999. A novel in vitro replication system for Dengue virus. Initiation of RNA synthesis at the 3′ end of exogenous viral RNA templates requires 5′- and 3′-terminal complementary sequence motifs of the viral RNA. J. Biol. Chem. 274:33714-33722.
80. You, S., B. Falgout, L. Markoff, and R. Padmanabhan. 2001. In vitro RNA synthesis from exogenous dengue viral RNA templates requires long range interactions between 5′- and 3′-terminal regions that influence RNA structure. J. Biol. Chem. 276:15581-15591.
81. You, S., D. D. Stump, A. D. Branch, and C. M. Rice. 2004. A cis-acting replication element in the sequence encoding the NS5B RNA-dependent RNA polymerase is required for hepatitis C virus RNA replication. J. Virol. 78:1352-1366.
82. Yu, L., and L. Markoff. 2005. The topology of bulges in the long stem of the flavivirus 3′ stem-loop is a major determinant of RNA replication competence. J. Virol. 79:2309-2324.
83. Yun, S.-I., S.-Y. Kim, C. M. Rice, and Y.-M. Lee. 2003. Development and application of a reverse genetics system for Japanese encephalitis virus. J. Virol. 77:6450-6465.
84. Yun, S.-I., and Y.-M. Lee. 2006. Japanese encephalitis virus: molecular biology and vaccine development, p. 225-271. In M. Kalitzky and P. Borowski (ed.), Molecular biology of the flavivirus. Horizon Scientific Press, Norwich, United Kingdom.
85. Yun, S.-I., Y.-J. Choi, X.-F. Yu, J.-Y. Song, Y.-H. Shin, Y.-R. Ju, S.-Y. Kim, and Y.-M. Lee. 2007. 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. 13:522-535.
86. Zeng, L., B. Falgout, and L. Markoff. 1998. Identification of specific nucleotide sequences within the conserved 3′-SL in the dengue type 2 virus genome required for replication. J. Virol. 72:7510-7522.
87. Zhang, B., H. Dong, D. A. Stein, P. L. Iversen, and P. Y. Shi. 2008. West Nile virus genome cyclization and RNA replication require two pairs of long-distance RNA interactions. Virology 373:1-13.
88. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.