Structural complexity of Dengue virus untranslated regions: Cis-acting RNA motifs and pseudoknot interactions modulating functionality of the viral genome

Nucleic Acids Research

Volumn 41, Issue 9, 2013, Pages 5075-5089

  Sztuba Solinska, Joanna ^a   Teramoto, Tadahisa ^b   Rausch, Jason W ^a   Shapiro, Bruce A ^a   Padmanabhan, Radhakrishnan ^b   Le Grice, Stuart F J ^a  

^a FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEAD; VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; COMPUTER MODEL; DENGUE VIRUS; GENE MUTATION; HYDROLYSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; RNA HYBRIDIZATION; RNA STRUCTURE; RNA SYNTHESIS; SITE DIRECTED MUTAGENESIS; UNTRANSLATED REGION; VIRUS GENOME; VIRUS REPLICATION;

DENGUE VIRUS; GENOME, VIRAL; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; OLIGONUCLEOTIDES, ANTISENSE; RNA, VIRAL; UNTRANSLATED REGIONS;

EID: 84877267759     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt203     Document Type: Article

References (60)

1. Miller, W.A. and White, K.A. (2006) Long-distance RNA-RNA interactions in plant virus gene expression and replication. Annu. Rev. Phytopathol., 44, 447-467.
2. Alvarez, D.E., Lodeiro, M.F., Luduena, S.J., Pietrasanta, L.I. and Gamarnik, A.V. (2005) Long-range RNA-RNA interactions circularize the dengue virus genome. J. Virol., 79, 6631-6643.
3. Song, B.H., Yun, S.I., Choi, Y.J., Kim, J.M., Lee, C.H. and Lee, Y.M. (2008) A complex RNA motif defined by three discontinuous 5-nucleotide-long strands is essential for Flavivirus RNA replication. RNA, 14, 1791-1813.
4. Wu, B., Pogany, J., Na, H., Nicholson, B.L., Nagy, P.D. and White, K.A. (2009) A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA-based regulation of viral processes. PLoS Pathog., 5, e1000323.
5. Villordo, S.M. and Gamarnik, A.V. (2009) Genome cyclization as strategy for flavivirus RNA replication. Virus Res., 139, 230-239.
6. Filomatori, C.V., Iglesias, N.G., Villordo, S.M., Alvarez, D.E. and Gamarnik, A.V. (2011) RNA sequences and structures required for the recruitment and activity of the dengue virus polymerase. J. Biol. Chem., 286, 6929-6939.
7. 0untranslated region of the dengue type 2 virus genome. Am. J. Trop. Med. Hyg., 81, 817-824.
8. Manzano, M., Reichert, E.D., Polo, S., Falgout, B., Kasprzak, W., Shapiro, B.A. and Padmanabhan, R. (2011) Identification of cis-acting elements in the 3-untranslated region of the dengue virus type 2 RNA that modulate translation and replication. J. Biol. Chem., 286, 22521-22534.
9. 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.
10. Silva, P.A., Pereira, C.F., Dalebout, T.J., Spaan, W.J. and Bredenbeek, P.J. (2010) An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J. Virol., 84, 11395-11406.
11. Friebe, P. and 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.
12. Polacek, C., Foley, J.E. and Harris, E. (2009) Conformational changes in the solution structure of the dengue virus 5 end in the presence and absence of the 3 untranslated region. J. Virol., 83, 1161-1166.
13. Olsthoorn, R.C. and Bol, J.F. (2001) Sequence comparison and secondary structure analysis of the 3 noncoding region of flavivirus genomes reveals multiple pseudoknots. RNA, 7, 1370-1377.
14. Lo, M.K., Tilgner, M., Bernard, K.A. and 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.
15. Alvarez, D.E., De Lella Ezcurra, A.L., Fucito, S. and Gamarnik, A.V. (2005) Role of RNA structures present at the 3UTR of dengue virus on translation, RNA synthesis, and viral replication. Virology, 339, 200-212.
16. Romero, T.A., Tumban, E., Jun, J., Lott, W.B. and Hanley, K.A. (2006) Secondary structure of dengue virus type 4 3 untranslated region: impact of deletion and substitution mutations. J. Gen. Virol., 87, 3291-3296.
17. Lodeiro, M.F., Filomatori, C.V. and Gamarnik, A.V. (2009) Structural and functional studies of the promoter element for dengue virus RNA replication. J. Virol., 83, 993-1008.
18. You, S. and Padmanabhan, R. (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.
19. Mitra, S., Shcherbakova, I.V., Altman, R.B., Brenowitz, M. and Laederach, A. (2008) High-throughput single-nucleotide structural mapping by capillary automated footprinting analysis. Nucleic Acids Res., 36, e63.
20. Badorrek, C.S. and Weeks, K.M. (2006) Architecture of a gamma retroviral genomic RNA dimer. Biochemistry, 45, 12664-12672.
21. Wilkinson, K.A., Gorelick, R.J., Vasa, S.M., Guex, N., Rein, A., Mathews, D.H., Giddings, M.C. and Weeks, K.M. (2008) High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol., 6, e96.
22. Deigan, K.E., Li, T.W., Mathews, D.H. and Weeks, K.M. (2009) Accurate SHAPE-directed RNA structure determination. Proc. Natl Acad. Sci. USA, 106, 97-102.
23. Ciesiolka, J., Michalowski, D., Wrzesinski, J., Krajewski, J. and Krzyzosiak, W.J. (1998) Patterns of cleavages induced by lead ions in defined RNA secondary structure motifs. J. Mol. Biol., 275, 211-220.
24. Chen, V.B., Arendall, W.B. 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr., 66, 12-21.
25. Chiu, W.W., Kinney, R.M. and Dreher, T.W. (2005) Control of translation by the 5-and 3-terminal regions of the dengue virus genome. J. Virol., 79, 8303-8315.
26. Clyde, K. and Harris, E. (2006) RNA secondary structure in the coding region of dengue virus type 2 directs translation start codon selection and is required for viral replication. J. Virol., 80, 2170-2182.
27. Ackermann, M. and Padmanabhan, R. (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.
28. Nomaguchi, M., Ackermann, M., Yon, C., You, S. and Padmanabhan, R. (2003) De novo synthesis of negative-strand RNA by Dengue virus RNA-dependent RNA polymerase in vitro: nucleotide, primer, and template parameters. J. Virol., 77, 8831-8842.
29. Shapiro, B.A., Bengali, D., Kasprzak, W. and Wu, J.C. (2001) RNA folding pathway functional intermediates: their prediction and analysis. J. Mol. Biol., 312, 27-44.
30. Alvarez, D.E., Filomatori, C.V. and Gamarnik, A.V. (2008) Functional analysis of dengue virus cyclization sequences located at the 5 and 3UTRs. Virology, 375, 223-235.
31. Gutell, R.R., Cannone, J.J., Konings, D. and Gautheret, D. (2000) Predicting U-turns in ribosomal RNA with comparative sequence analysis. J. Mol. Biol., 300, 791-803.
32. Byun, Y. and Han, K. (2009) PseudoViewer3: generating planar drawings of large-scale RNA structures with pseudoknots. Bioinformatics, 25, 1435-1437.
33. Shurtleff, A.C., Beasley, D.W., Chen, J.J., Ni, H., Suderman, M.T., Wang, H., Xu, R., Wang, E., Weaver, S.C., Watts, D.M. et al. (2001) Genetic variation in the 3 non-coding region of dengue viruses. Virology, 281, 75-87.
34. Nissen, P., Ippolito, J.A., Ban, N., Moore, P.B. and Steitz, T.A. (2001) RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc. Natl Acad. Sci. USA, 98, 4899-4903.
35. Isaksson, J., Acharya, S., Barman, J., Cheruku, P. and Chattopadhyaya, J. (2004) Single-stranded adenine-rich DNA and RNA retain structural characteristics of their respective double-stranded conformations and show directional differences in stacking pattern. Biochemistry, 43, 15996-16010.
36. Cheong, C., Varani, G. and Tinoco, I. Jr (1990) Solution structure of an unusually stable RNA hairpin, 5GGAC(UUCG)GUCC. Nature, 346, 680-682.
37. Legiewicz, M., Badorrek, C.S., Turner, K.B., Fabris, D., Hamm, T.E., Rekosh, D., Hammarskjold, M.L. and Le Grice, S.F. (2008) Resistance to RevM10 inhibition reflects a conformational switch in the HIV-1 Rev response element. Proc. Natl Acad. Sci. USA, 105, 14365-14370.
38. Abramovitz, D.L. and Pyle, A.M. (1997) Remarkable morphological variability of a common RNA folding motif: the GNRA tetraloop-receptor interaction. J. Mol. Biol., 266, 493-506.
39. 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.
40. Popenda, M., Szachniuk, M., Antczak, M., Purzycka, K.J., Lukasiak, P., Bartol, N., Blazewicz, J. and Adamiak, R.W. (2012) Automated 3D structure composition for large RNAs. Nucleic Acids Res., 40, e112.
41. De Nova-Ocampo, M., Villegas-Sepulveda, N. and del Angel, R.M. (2002) Translation elongation factor-1alpha, La, and PTB interact with the 3 untranslated region of dengue 4 virus RNA. Virology, 295, 337-347.
42. Gomila, R.C., Martin, G.W. and Gehrke, L. (2011) NF90 binds the dengue virus RNA 3 terminus and is a positive regulator of dengue virus replication. PLoS One, 6, e16687.
43. Ward, A.M., Bidet, K., Yinglin, A., Ler, S.G., Hogue, K., Blackstock, W., Gunaratne, J. and Garcia-Blanco, M.A. (2011) Quantitative mass spectrometry of DENV-2 RNA-interacting proteins reveals that the DEAD-box RNA helicase DDX6 binds the DB1 and DB2 3 UTR structures. RNA Biol., 8, 1173-1186.
44. Yocupicio-Monroy, M., Padmanabhan, R., Medina, F. and del Angel, R.M. (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.
45. Jaeger, L., Michel, F. and Westhof, E. (1994) Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J. Mol. Biol., 236, 1271-1276.
46. Afonin, K.A., Lin, Y.P., Calkins, E.R. and Jaeger, L. (2012) Attenuation of loop-receptor interactions with pseudoknot formation. Nucleic Acids Res., 40, 2168-2180.
47. Brierley, I., Pennell, S. and Gilbert, R.J. (2007) Viral RNA pseudoknots: versatile motifs in gene expression and replication. Nat. Rev. Microbiol., 5, 598-610.
48. Wang, C., Le, S.Y., Ali, N. and Siddiqui, A. (1995) An RNA pseudoknot is an essential structural element of the internal ribosome entry site located within the hepatitis C virus 5 noncoding region. RNA, 1, 526-537.
49. Wilson, J.E., Pestova, T.V., Hellen, C.U. and Sarnow, P. (2000) Initiation of protein synthesis from the A site of the ribosome. Cell, 102, 511-520.
50. Brierley, I. and Pennell, S. (2001) Structure and function of the stimulatory RNAs involved in programmed eukaryotic-1 ribosomal frameshifting. Cold Spring Harb. Symp. Quant. Biol., 66, 233-248.
51. Imbert, I., Guillemot, J.C., Bourhis, J.M., Bussetta, C., Coutard, B., Egloff, M.P., Ferron, F., Gorbalenya, A.E. and Canard, B. (2006) A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J., 25, 4933-4942.
52. Brierley, I., Gilbert, R.J. and Pennell, S. (2008) RNA pseudoknots and the regulation of protein synthesis. Biochem. Soc. Trans., 36, 684-689.
53. Zuo, X., Wang, J., Yu, P., Eyler, D., Xu, H., Starich, M.R., Tiede, D.M., Simon, A.E., Kasprzak, W., Schwieters, C.D. et al. (2010) Solution structure of the cap-independent translational enhancer and ribosome-binding element in the 3 UTR of turnip crinkle virus. Proc. Natl Acad. Sci. USA, 107, 1385-1390.
54. McCormack, J.C., Yuan, X., Yingling, Y.G., Kasprzak, W., Zamora, R.E., Shapiro, B.A. and Simon, A.E. (2008) Structural domains within the 3 untranslated region of Turnip crinkle virus. J. Virol., 82, 8706-8720.
55. Tuplin, A., Struthers, M., Simmonds, P. and Evans, D.J. (2012) A twist in the tail: SHAPE mapping of long-range interactions and structural rearrangements of RNA elements involved in HCV replication. Nucleic Acids Res., 40, 6908-6921.
56. Theimer, C.A., Blois, C.A. and Feigon, J. (2005) Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Mol. Cell, 17, 671-682.
57. 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.
58. Suzuki, R., Fayzulin, R., Frolov, I. and Mason, P.W. (2008) Identification of mutated cyclization sequences that permit efficient replication of West Nile virus genomes: use in safer propagation of a novel vaccine candidate. J. Virol., 82, 6942-6951.
59. Friebe, P., Pena, J., Pohl, M.O. and Harris, E. (2012) Composition of the sequence downstream of the dengue virus 5 cyclization sequence (dCS) affects viral RNA replication. Virology, 422, 346-356.
60. Gebhard, L.G., Kaufman, S.B. and Gamarnik, A.V. (2012) Novel ATP-independent RNA annealing activity of the dengue virus NS3 helicase. PLoS One, 7, e36244.