Kissing-loop interaction between 5′ and 3′ ends of tick-borne Langat virus genome 'bridges the gap' between mosquito-and tick-borne flaviviruses in mechanisms of viral RNA cyclization: Applications for virus attenuation and vaccine development

Nucleic Acids Research

Volumn 44, Issue 7, 2016, Pages 3330-3350

  Tsetsarkin, Konstantin A ^a   Liu, Guangping ^a   Shen, Kui ^a   Pletnev, Alexander G ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; MICRORNA; VIRUS RNA; VIRUS VACCINE; CAPSID PROTEIN; LIVE VACCINE; NUCLEOTIDE; REGULATORY RNA SEQUENCE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYCLIZATION; DUPLICATED CAPSID GENE REGION; FLAVIVIRUS; GENE STRUCTURE; GENETIC STABILITY; IMMUNITY; LANGAT VIRUS; MOSQUITO BORNE FLAVIVIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA REPLICATION; RNA STRUCTURE; TICK BORNE FLAVIVIRUS; VIRUS ATTENUATION; VIRUS CAPSID; VIRUS GENOME; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; CHEMISTRY; CHLOROCEBUS AETHIOPS; DUPLICATE GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MUTATION; OPEN READING FRAME; PHYSIOLOGY; REGULATORY RNA SEQUENCE; TICK BORNE ENCEPHALITIS; TICK BORNE ENCEPHALITIS VIRUS; VERO CELL LINE; VIROLOGY; VIRUS REPLICATION;

ANIMALS; BRAIN; CAPSID PROTEINS; CERCOPITHECUS AETHIOPS; ENCEPHALITIS VIRUSES, TICK-BORNE; ENCEPHALITIS, TICK-BORNE; GENES, DUPLICATE; GENOME, VIRAL; MICE; MICRORNAS; MUTATION; NUCLEOTIDES; OPEN READING FRAMES; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA, VIRAL; VACCINES, ATTENUATED; VERO CELLS; VIRAL VACCINES; VIRUS REPLICATION;

EID: 84965121420     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw061     Document Type: Article

References (64)

1. Lasala, P.R., Holbrook, M. (2010) Tick-borne flaviviruses. Clin. Lab. Med., 30, 221-235.
2. Gritsun, T.S., Lashkevich, V.A., Gould, E.A. (2003) Tick-borne encephalitis. Antiviral Res., 57, 129-146.
3. Smith, C.E. (1956) A virus resembling Russian spring-summer encephalitis virus from an ixodid tick in Malaya. Nature, 178, 581-582.
4. Pletnev, A.G., Men, R. (1998) Attenuation of the Langat tick-borne flavivirus by chimerization with mosquito-borne flavivirus dengue type 4. Proc. Natl. Acad. Sci. U.S.A., 95, 1746-1751.
5. Price, W.H., Thind, I.S., Teasdall, R.D., O'Leary, W. (1970) Vaccination of human volunteers against Russian spring-summer (RSS) virus complex with attenuated Langat E5 virus. Bull. World Health Organ., 42, 89-94.
6. Smorodincev, A.A., Dubov, A.V. (1986) Live vaccines against tick-borne encephalitis. In: Smorodincev, AA (ed). Tick-borne encephalitis and its vaccine prophylaxis. Meditsina, Leningrad, pp. 190-211.
7. Heiss, B.L., Maximova, O.A., Pletnev, A.G. (2011) Insertion of microRNA targets into the flavivirus genome alters its highly neurovirulent phenotype. J. Virol., 85, 1464-1472.
8. Tsetsarkin, K.A., Liu, G., Kenney, H., Bustos-Arriaga, J., Hanson, C.T., Whitehead, S.S., Pletnev, A.G. (2015) Dual miRNA targeting restricts host range and attenuates neurovirulence of flaviviruses. PLoS Pathog., 11, e1004852.
9. Teterina, N.L., Liu, G., Maximova, O.A., Pletnev, A.G. (2014) Silencing of neurotropic flavivirus replication in the central nervous system by combining multiple microRNA target insertions in two distinct viral genome regions. Virology, 456-457, 247-258.
10. Shustov, A.V., Mason, P.W., Frolov, I. (2007) Production of pseudoinfectious yellow fever virus with a two-component genome. J. Virol., 81, 11737-11748.
11. McGee, C.E., Shustov, A.V., Tsetsarkin, K., Frolov, I.V., Mason, P.W., Vanlandingham, D.L., Higgs, S. (2010) Infection, dissemination, and transmission of a West Nile virus green fluorescent protein infectious clone by Culex pipiens quinquefasciatus mosquitoes. Vector Borne Zoonotic Dis., 10, 267-274.
12. Schoggins, J.W., Dorner, M., Feulner, M., Imanaka, N., Murphy, M.Y., Ploss, A., Rice, C.M. (2012) Dengue reporter viruses reveal viral dynamics in interferon receptor-deficient mice and sensitivity to interferon effectors in vitro. Proc. Natl. Acad. Sci. U.S.A., 109, 14610-14615.
13. Groat-Carmona, A.M., Orozco, S., Friebe, P., Payne, A., Kramer, L., Harris, E. (2012) A novel coding-region RNA element modulates infectious dengue virus particle production in both mammalian and mosquito cells and regulates viral replication in Aedes aegypti mosquitoes. Virology, 432, 511-526.
14. de Borba, L., Villordo, S.M., Iglesias, N.G., Filomatori, C.V., Gebhard, L.G., Gamarnik, A.V. (2015) Overlapping local and long-range RNA-RNA interactions modulate dengue virus genome cyclization and replication. J. Virol., 89, 3430-3437.
15. Liu, Z.Y., Li, X.F., Jiang, T., Deng, Y.Q., Zhao, H., Wang, H.J., Ye, Q., Zhu, S.Y., Qiu, Y., Zhou, X. et al. (2013) Novel cis-acting element within the capsid-coding region enhances flavivirus viral-RNA replication by regulating genome cyclization. J. Virol., 87, 6804-6818.
16. Gebhard, L.G., Filomatori, C.V., Gamarnik, A.V. (2011) Functional RNA elements in the dengue virus genome. Viruses, 3, 1739-1756.
17. Kofler, R.M., Hoenninger, V.M., Thurner, C., 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.
18. Hoenninger, V.M., Rouha, H., Orlinger, K.K., Miorin, L., Marcello, A., Kofler, R.M., Mandl, C.W. (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.
19. Tuplin, A., Evans, D.J., Buckley, A., Jones, I.M., Gould, E.A., Gritsun, T.S. (2011) Replication enhancer elements within the open reading frame of tick-borne encephalitis virus and their evolution within the Flavivirus genus. Nucleic Acids Res., 39, 7034-7048.
20. Campbell, M.S., Pletnev, A.G. (2000) Infectious cDNA clones of Langat tick-borne flavivirus that differ from their parent in peripheral neurovirulence. Virology, 269, 225-237.
21. Yamshchikov, V., Mishin, V., Cominelli, F. (2001) A new strategy in design of +RNA virus infectious clones enabling their stable propagation in E. coli. Virology, 281, 272-280.
22. Sambrook, J., Fritsch, E., Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory, NY.
23. Bonaldo, M.C., Mello, S.M., Trindade, G.F., Rangel, A.A., Duarte, A.S., Oliveira, P.J., Freire, M.S., Kubelka, C.F., Galler, R. (2007) Construction and characterization of recombinant flaviviruses bearing insertions between E and NS1 genes. Virol. J., 4, 1-16.
24. Engel, A.R., Rumyantsev, A.A., Maximova, O.A., Speicher, J.M., Heiss, B., Murphy, B.R., Pletnev, A.G. (2010) The neurovirulence and neuroinvasiveness of chimeric tick-borne encephalitis/dengue virus can be attenuated by introducing defined mutations into the envelope and NS5 protein genes and the 3' non-coding region of the genome. Virology, 405, 243-252.
25. Team, R.C. (2015) R: A language and environment for statistical computing, R Foundation for statistical computing Vienna.
26. Pletnev, A.G., Bray, M., Hanley, K.A., Speicher, J., Elkins, R. (2001) Tick-borne Langat/mosquito-borne dengue flavivirus chimera, a candidate live attenuated vaccine for protection against disease caused by members of the tick-borne encephalitis virus complex: evaluation in rhesus monkeys and in mosquitoes. J. Virol., 75, 8259-8267.
27. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
28. Heiss, B.L., Maximova, O.A., Thach, D.C., Speicher, J.M., Pletnev, A.G. (2012) MicroRNA targeting of neurotropic flavivirus: effective control of virus escape and reversion to neurovirulent phenotype. J. Virol., 86, 5647-5659.
29. Rouha, H., Hoenninger, V.M., Thurner, C., Mandl, C.W. (2011) Mutational analysis of three predicted 5'-proximal stem-loop structures in the genome of tick-borne encephalitis virus indicates different roles in RNA replication and translation. Virology, 417, 79-86.
30. Gritsun, D.J., Jones, I.M., Gould, E.A., Gritsun, T.S. (2014) Molecular archaeology of Flaviviridae untranslated regions: duplicated RNA structures in the replication enhancer of flaviviruses and pestiviruses emerged via convergent evolution. PLoS One, 9, e92056.
31. Elshuber, S., Allison, S.L., Heinz, F.X., Mandl, C.W. (2003) Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol., 84, 183-191.
32. Pletnev, A.G., Bray, M., Lai, C.J. (1993) Chimeric tick-borne encephalitis and dengue type 4 viruses: effects of mutations on neurovirulence in mice. J. Virol., 67, 4956-4963.
33. Bak, M., Silahtaroglu, A., Moller, M., Christensen, M., Rath, M.F., Skryabin, B., Tommerup, N., Kauppinen, S. (2008) MicroRNA expression in the adult mouse central nervous system. RNA, 14, 432-444.
34. Sempere, L.F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., Ambros, V. (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol., 5, R13.
35. 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.
36. Pham, A.M., Langlois, R.A., TenOever, B.R. (2012) Replication in cells of hematopoietic origin is necessary for Dengue virus dissemination. PLoS pathogens, 8, e1002465.
37. Alvarez, D.E., Lodeiro, M.F., Luduena, S.J., Pietrasanta, L.I., Gamarnik, A.V. (2005) Long-range RNA-RNA interactions circularize the dengue virus genome. J. Virol., 79, 6631-6643.
38. Pijlman, G.P., Funk, A., Kondratieva, N., Leung, J., Torres, S., van der Aa, L., Liu, W.J., Palmenberg, A.C., Shi, P.Y., Hall, R.A. et al. (2008) A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe, 4, 579-591.
39. Manokaran, G., Finol, E., Wang, C., Gunaratne, J., Bahl, J., Ong, E.Z., Tan, H.C., Sessions, O.M., Ward, A.M., Gubler, D.J. et al. (2015) Dengue subgenomic RNA binds TRIM25 to inhibit interferon expression for epidemiological fitness. Science, 350, 217-221.
40. Funk, A., Truong, K., Nagasaki, T., Torres, S., Floden, N., Balmori Melian, E., Edmonds, J., Dong, H., Shi, P.Y., Khromykh, A.A. (2010) RNA structures required for production of subgenomic flavivirus RNA. J. Virol., 84, 11407-11417.
41. Brinton, M.A., Basu, M. (2015) Functions of the 3' and 5' genome RNA regions of members of the genus Flavivirus. Virus Res., 206, 108-119.
42. Hahn, C.S., Hahn, Y.S., Rice, C.M., Lee, E., Dalgarno, L., Strauss, E.G., Strauss, J.H. (1987) Conserved elements in the 3' untranslated region of flavivirus RNAs and potential cyclization sequences. J. Mol. Biol., 198, 33-41.
43. Khromykh, A.A., Meka, H., Guyatt, K.J., Westaway, E.G. (2001) Essential role of cyclization sequences in flavivirus RNA replication. J. Virol., 75, 6719-6728.
44. Thurner, C., Witwer, C., Hofacker, I.L., Stadler, P.F. (2004) Conserved RNA secondary structures in Flaviviridae genomes. J. Gen. Virol., 85, 1113-1124.
45. Zhang, B., Dong, H., Stein, D.A., Iversen, P.L., Shi, P.Y. (2008) West Nile virus genome cyclization and RNA replication require two pairs of long-distance RNA interactions. Virology, 373, 1-13.
46. Friebe, P., Harris, E. (2010) Interplay of RNA elements in the dengue virus 5' and 3' ends required for viral RNA replication. J. Virol., 84, 6103-6118.
47. Alvarez, D.E., De Lella Ezcurra, A.L., Fucito, S., Gamarnik, A.V. (2005) Role of RNA structures present at the 3'UTR of dengue virus on translation, RNA synthesis, and viral replication. Virology, 339, 200-212.
48. Lo, M.K., Tilgner, M., Bernard, K.A., Shi, P.Y. (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.
49. Corver, J., Lenches, E., Smith, K., Robison, R.A., Sando, T., Strauss, E.G., 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.
50. Alvarez, D.E., Filomatori, C.V., Gamarnik, A.V. (2008) Functional analysis of dengue virus cyclization sequences located at the 5' and 3'UTRs. Virology, 375, 223-235.
51. Filipowicz, W., Bhattacharyya, S.N., Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet., 9, 102-114.
52. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
53. Gu, S., Jin, L., Zhang, F., Sarnow, P., Kay, M.A. (2009) Biological basis for restriction of microRNA targets to the 3' untranslated region in mammalian mRNAs. Nat. Struct. Mol. Biol., 16, 144-150.
54. Grimson, A., Farh, K.K., Johnston, W.K., Garrett-Engele, P., Lim, L.P., Bartel, D.P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell, 27, 91-105.
55. Men, R., Bray, M., Clark, D., Chanock, R.M., Lai, C.J. (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.
56. Mandl, C.W., Holzmann, H., Meixner, T., Rauscher, S., Stadler, P.F., Allison, S.L., Heinz, F.X. (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.
57. Smirnova, L., Grafe, A., Seiler, A., Schumacher, S., Nitsch, R., Wulczyn, F.G. (2005) Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci., 21, 1469-1477.
58. Makeyev, E.V., Zhang, J., Carrasco, M.A., Maniatis, T. (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell, 27, 435-448.
59. Yao, H., Ma, R., Yang, L., Hu, G., Chen, X., Duan, M., Kook, Y., Niu, F., Liao, K., Fu, M. et al. (2014) MiR-9 promotes microglial activation by targeting MCPIP1. Nat. Commun., 5, 4386.
60. Liu, G.D., Zhang, H., Wang, L., Han, Q., Zhou, S.F., Liu, P. (2013) Molecular hydrogen regulates the expression of miR-9, miR-21 and miR-199 in LPS-activated retinal microglia cells. Int. J. Ophthalmol., 6, 280-285.
61. Saetrom, P., Snove, O. Jr (2007) Robust machine learning algorithms predict microRNA genes and targets. Methods Enzymol., 427, 25-49.
62. Monath, T.P. (2005) Yellow fever vaccine. Expert Rev. Vaccines, 4, 553-574.
63. Halstead, S.B., Jacobson, J. (2008) Japanese encephalitis virus vaccines. In: Plotkin, S, Orenstein, W and Offit, P (eds). Vaccines. Elsevier, Philadelphia, pp. 311-352.
64. Kofler, R.M., Heinz, F.X., Mandl, C.W. (2004) A novel principle of attenuation for the development of new generation live flavivirus vaccines. Arch. Virol. Suppl., 18, 191-200.