Replication enhancer elements within the open reading frame of tick-borne encephalitis virus and their evolution within the Flavivirus genus

Nucleic Acids Research

Volumn 39, Issue 16, 2011, Pages 7034-7048

  Tuplin, A ^a   Evans, D J ^a   Buckley, A ^b   Jones, I M ^c   Gould, E A ^d   Gritsun, T S ^c  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b CRANFIELD UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

^d Aix Marseille University IRD 190 Inserm 1207   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BASE PAIRING; CONFORMATION; CYTOPATHOGENIC EFFECT; ENHANCER REGION; FLAVIVIRUS; GENE REPLICATION; GENE STRUCTURE; MOLECULAR EVOLUTION; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; POINT MUTATION; PRIORITY JOURNAL; REPLICATION ENHANCER REGION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; THERMODYNAMICS; TICK BORNE ENCEPHALITIS FLAVIVIRUS; UPREGULATION; VIRUS ATTENUATION; VIRUS CAPSID; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; BASE SEQUENCE; CELLS, CULTURED; ENCEPHALITIS VIRUSES, TICK-BORNE; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; FLAVIVIRUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; RNA, VIRAL; VIRUS REPLICATION;

FLAVIVIRUS; IXODIDA; MIRIDAE; RODENTIA; TICK-BORNE ENCEPHALITIS VIRUS;

EID: 80052501185     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr237     Document Type: Article

References (61)

1. Gritsun, T.S., Nuttall, P.A. and Gould, E.A. (2003) Tick-borne flaviviruses. Adv. Virus Res., 61, 317-371. (Pubitemid 137639390)
2. Gritsun, T.S., Lashkevich, V.A. and Gould, E.A. (2003) Tick-borne encephalitis. Antiviral Res., 57, 129-146. (Pubitemid 36254727)
3. Suss, J. (2008) Tick-borne encephalitis in Europe and beyond-the epidemiological situation as of 2007. Euro. Surveill., 13, 1-7.
4. Heinz, F.X., Collett, M.S., Purcell, R.H., Gould, E.A., Howard, C.R., Houghton, M., Moormann, R.J.M., Rice, C.M. and Thiel, H.J. (2000) Family Flaviviridae. In M.H.V., Fauquet, R., Bishop, C.M., Carstens, D.H.L., Estes, E., Lemon, M.K., Maniloff, S., Mayo, J., McGeogch, M.A., Pringle, D.C.R. et al. (eds), Virus Taxonomy. 7th International committee for the Taxonomy of Viruses. Academic Press, San Diego, pp. 859-878.
5. Crabtree, M.B., Sang, R.C., Stollar, V., Dunster, L.M. and Miller, B.R. (2003) Genetic and phenotypic characterization of the newly described insect flavivirus, Kamiti River virus. Arch. Virol., 148, 1095-1118. (Pubitemid 36720307)
6. Cammisa Parks, H., Cisar, L.A., Kane, A. and Stollar, V. (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.
7. Hoshino, K., Isawa, H., Tsuda, Y., Yano, K., Sasaki, T., Yuda, M., Takasaki, T., Kobayashi, M. and Sawabe, K. (2007) Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. Virology, 359, 405-414. (Pubitemid 46274879)
8. Gritsun, T.S. and Gould, E.A. (2008) In Mahy, B.W.J. and van Regenmortel, M.H.V. (eds), Encyclopedia of Virology, Vol. 5, 3 rd edn. Elsevier, Oxford, pp. 45-54.
9. Hahn, C.S., Hahn, Y.S., Rice, C.M., Lee, E., Dalgarno, L., Strauss, E.G. and Strauss, J.H. (1987) Conserved elements in the 30 untranslated region of flavivirus RNAs and potential cyclization sequences. J. Mol. Biol., 198, 33-41.
10. Cahour, A., Pletnev, A., Vazielle Falcoz, M., Rosen, L. and Lai, C.J. (1995) Growth-restricted dengue virus mutants containing deletions in the 50 noncoding region of the RNA genome. Virology, 207, 68-76.
11. Khromykh, A.A., Meka, H., Guyatt, K.J. and Westaway, E.G. (2001) Essential role of cyclization sequences in flavivirus RNA replication. J. Virol., 75, 6719-6728. (Pubitemid 32578194)
12. Corver, J., Lenches, E., Smith, K., Robison, R.A., Sando, T., Strauss, E.G. and Strauss, J.H. (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. (Pubitemid 36110041)
13. Filomatori, C.V., Lodeiro, M.F., Alvarez, D.E., Samsa, M.M., Pietrasanta, L. and Gamarnik, A.V. (2006) A 50 RNA element promotes dengue virus RNA synthesis on a circular genome. Gene. Dev., 20, 2238-2249.
14. Kofler, R.M., Leitner, A., O'Riordain, G., Heinz, F.X. and Mandl, C.W. (2003) Spontaneous mutations restore the viability of tick-borne encephalitis virus mutants with large deletions in protein C. J. Virol., 77, 443-451. (Pubitemid 36004984)
15. Kofler, R.M., Hoenninger, V.M., Thurner, C. and Mandl, C.W. (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.
16. Gritsun, T.S. and Gould, E.A. (2007) Origin and evolution of flavivirus 50UTRs and panhandles: trans-terminal duplications? Virology, 366, 8-15. (Pubitemid 47314395)
17. Gritsun, T.S. and Gould, E.A. (2006) The 30 untranslated region of tick-borne flaviviruses originated by the duplication of long repeat sequences within the open reading frame. Virology, 350, 269-275. (Pubitemid 43928114)
18. Gritsun, T.S. and Gould, E.A. (2007) Origin and evolution of 30UTR 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.
19. Men, R., Bray, M., Clark, D., Chanock, R.M. and Lai, C.J. (1996) Dengue type 4 virus mutants containing deletions in the 30 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.
20. Mandl, C.W., Holzmann, H., Meixner, T., Rauscher, S., Stadler, P.F., Allison, S.L. and Heinz, F.X. (1998) Spontaneous and engineered deletions in the 30 noncoding region of tick-borne encephalitis virus: construction of highly attenuated mutants of a flavivirus. J. Virol., 72, 2132-2140. (Pubitemid 28100769)
21. Bredenbeek, P.J., Kooi, E.A., Lindenbach, B., Huijkman, N., Rice, C.M. and Spaan, W.J. (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. (Pubitemid 36592619)
22. Tilgner, M., Shi, P.Y., Lo, M.K. and Bernard, K.A. (2004) Structure and function of the 30 terminal six nucleotides of the west nile virus genome in viral replication. J. Virol., 78, 8159-8171. (Pubitemid 38944300)
23. Gritsun, T.S. and Gould, E.A. (2006) Direct repeats in the 30 untranslated regions of mosquito-borne flaviviruses: possible implications for virus transmission. J. Gen. Virol., 87, 3297-3305. (Pubitemid 44608366)
24. Romero, T.A., Tumban, E., Jun, J., Lott, W.B. and Hanley, K.A. (2006) Secondary structure of dengue virus type 4 30 untranslated region: impact of deletion and substitution mutations. J. Gen. Virol., 87, 3291-3296. (Pubitemid 44608365)
25. Blaney, J.E. Jr, Sathe, N.S., Goddard, L., Hanson, C.T., Romero, T.A., Hanley, K.A., Murphy, B.R. and Whitehead, S.S. (2008) Dengue virus type 3 vaccine candidates generated by introduction of deletions in the 30 untranslated region (30-UTR) or by exchange of the DENV-3 30-UTR with that of DENV-4. Vaccine, 26, 817-828.
26. Gritsun, T.S., Venugopal, K., Zanotto, P.M., Mikhailov, M.V., Sall, A.A., Holmes, E.C., Polkinghorne, I., Frolova, T.V., Pogodina, V.V., Lashkevich, V.A. et al. (1997) Complete sequence of two tick-borne flaviviruses isolated from Siberia and the UK: analysis and significance of the 50 and 30-UTRs. Virus Res., 49, 27-39. (Pubitemid 27240120)
27. Gritsun, T.S., Tuplin, A.K. and Gould, E.A. (2006) Origin, evolution and function of flavivirus RNA in untranslated and coding regions: implications for virus transmission. In Kalitzky, M. and Borowski, P. (eds), Flaviviridae: Pathogenesis, Molecular Biology and Genetics. Horizon Scientific Press, Norwich, UK, pp. 47-99.
28. Thurner, C., Witwer, C., Hofacker, I.L. and Stadler, P.F. (2004) Conserved RNA secondary structures in Flaviviridae genomes. J. Gen. Virol., 85, 1113-1124. (Pubitemid 38659775)
29. Thompson, J.D., Gibson, T.J., Jeanmougin, F. and Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882. (Pubitemid 28022245)
30. Simmonds, P., Tuplin, A. and Evans, D.J. (2004) Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: Implications for virus evolution and host persistence. RNA, 10, 1337-1351. (Pubitemid 39122104)
31. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415. (Pubitemid 37442169)
32. Markham, N.R. and Zuker, M. (2005) DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res., 33, W577-581. (Pubitemid 44529988)
33. Gritsun, T.S., Frolova, T.V., Pogodina, V.V., Lashkevich, V.A., Venugopal, K. and Gould, E.A. (1993) Nucleotide and deduced amino acid sequence of the envelope gene of the Vasilchenko strain of TBE virus; comparison with other flaviviruses. Virus Res., 27, 201-209. (Pubitemid 23055741)
34. Gritsun, T.S. and Gould, E.A. (1998) Development and analysis of a tick-borne encephalitis virus infectious clone using a novel and rapid strategy. J. Virol. Methods, 76, 109-120. (Pubitemid 28537846)
35. Gritsun, T.S. and Gould, E.A. (1995) Infectious transcripts of tick-borne encephalitis virus, generated in days by RT-PCR. Virology, 214, 611-618. (Pubitemid 26027787)
36. Gritsun, T.S., Desai, A. and Gould, E.A. (2001) The degree of attenuation of tick-borne encephalitis virus depends on the cumulative effects of point mutations. J. Gen. Virol., 82, 1667-1675. (Pubitemid 32611508)
37. Grard, G., Moureau, G., Charrel, R.N., Lemasson, J.J., Gonzalez, J.P., Gallian, P., Gritsun, T.S., Holmes, E.C., Gould, E.A. and de Lamballerie, X. (2007) Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology, 361, 80-92. (Pubitemid 46566451)
38. Mohan, S., Hsiao, C., Bowman, J.C., Wartell, R. and Williams, L.D. RNA tetraloop folding reveals tension between backbone restraints and molecular interactions. J. Am. Chem. Soc., 132, 12679-12689.
39. Antao, V.P. and Tinoco, I. Jr (1992) Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucleic Acids Res., 20, 819-824.
40. Tuplin, A., Evans, D.J. and Simmonds, P. (2004) Detailed mapping of RNA secondary structures in core and NS5B-encoding region sequences of hepatitis C virus by RNase cleavage and novel bioinformatic prediction methods. J. Gen. Virol., 85, 3037-3047. (Pubitemid 39360048)
41. Barr, J.N. and Fearns, R. How RNA viruses maintain their genome integrity. J. Gen. Virol., 91, 1373-1387.
42. Kofler, R.M., Heinz, F.X. and Mandl, C.W. (2002) Capsid protein C of tick-borne encephalitis virus tolerates large internal deletions and is a favorable target for attenuation of virulence. J. Virol., 76, 3534-3543. (Pubitemid 34224554)
43. Gritsun, T.S. and Gould, E.A. (2007) Direct repeats in the flavivirus 30 untranslated region; a strategy for survival in the environment? Virology, 358, 258-265. (Pubitemid 46136433)
44. Gritsun, T.S. and Gould, E.A. (2006) The 30 untranslated regions of Kamiti River virus and Cell fusing agent virus originated by self-duplication. J. Gen. Virol., 87, 2615-2619.
45. Schuppli, D., Miranda, G., Qiu, S. and Weber, H. (1998) A branched stem-loop structure in the M-site of bacteriophage Qbeta RNA is important for template recognition by Qbeta replicase holoenzyme. J. Mol. Biol., 283, 585-593. (Pubitemid 28486722)
46. Klovins, J., Berzins, V. and van Duin, J. (1998) A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 30 end is required for replication. RNA, 4, 948-957. (Pubitemid 28359765)
47. McKnight, K.L. and Lemon, S.M. (1996) Capsid coding sequence is required for efficient replication of human rhinovirus 14 RNA. J. Virol., 70, 1941-1952. (Pubitemid 26062959)
48. Kim, Y.N. and Makino, S. (1995) Characterization of a murine coronavirus defective interfering RNA internal cis-acting replication signal. J. Virol., 69, 4963-4971.
49. Goodfellow, I.G., Kerrigan, D. and Evans, D.J. (2003) Structure and function analysis of the poliovirus cis-acting replication element (CRE). RNA, 9, 124-137. (Pubitemid 36206308)
50. Gerber, K., Wimmer, E. and Paul, A.V. (2001) Biochemical and genetic studies of the initiation of human rhinovirus 2 RNA replication: identification of a cis-replicating element in the coding sequence of 2 A(pro). J. Virol., 75, 10979-10990. (Pubitemid 33031565)
51. Goodfellow, I., Chaudhry, Y., Richardson, A., Meredith, J., Almond, J.W., Barclay, W. and Evans, D.J. (2000) Identification of a cis-acting replication element within the poliovirus coding region. J. Virol., 74, 4590-4600. (Pubitemid 30237884)
52. Rieder, E., Paul, A.V., Kim, D.W., van Boom, J.H. and Wimmer, E. (2000) Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation. J. Virol., 74, 10371-10380.
53. Herold, J. and Andino, R. (2001) Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell, 7, 581-591. (Pubitemid 32706350)
54. Sullivan, M.L. and Ahlquist, P. (1999) A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1 a to dramatically stabilize RNA in vivo. J. Virol., 73, 2622-2632. (Pubitemid 29135646)
55. Gamarnik, A.V. and Andino, R. (1998) Switch from translation to RNA replication in a positive-stranded RNA virus. Gene. Dev., 12, 2293-2304. (Pubitemid 28371350)
56. Kanamori, H., Yuhashi, K., Ohnishi, S., Koike, K. and Kodama, T. (2010) RNA dependent RNA polymerase of hepatitis C virus binds to its coding region RNA stem-loop structure, 5BSL3.2, and its negative strand. J. Gen. Virol., 91, 1207-1212.
57. Villordo, S.M., Alvarez, D.E. and Gamarnik, A.V. (2010) A balance between circular and linear forms of the dengue virus genome is crucial for viral replication. RNA, 16, 2325-2335.
58. Mir, M.A. and Panganiban, A.T. (2006) The bunyavirus nucleocapsid protein is an RNA chaperone: possible roles in viral RNA panhandle formation and genome replication. RNA, 12, 272-282. (Pubitemid 43121932)
59. Gould, E.A., de Lamballerie, X., Zanotto, P.M. and Holmes, E.C. (2003) Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv. Virus Res., 59, 277-314. (Pubitemid 137639368)
60. Labuda, M., Austyn, J.M., Zuffova, E., Kozuch, O., Fuchsberger, N., Lysy, J. and Nuttall, P.A. (1996) Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology, 219, 357-366. (Pubitemid 26188386)
61. Khasnatinov, M.A., Ustanikova, K., Frolova, T.V., Pogodina, V.V., Bochkova, N.G., Levina, L.S., Slovak, M., Kazimirova, M., Labuda, M., Klempa, B. et al. (2009) Non-hemagglutinating flaviviruses: molecular mechanisms for the emergence of new strains via adaptation to European ticks. PLoS One, 4, e7295.