Flavivirus RNA methylation

Journal of General Virology

Volumn 95, Issue PART 4, 2014, Pages 763-778

  Dong, Hongping ^a   Fink, Katja ^b   Züst, Roland ^b   Lim, Siew Pheng ^a   Qin, Cheng Feng ^c   Shi, Pei Yong ^a  

^a NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

^c BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; GUANOSINE TRIPHOSPHATE; LIVE VACCINE; MESSENGER RNA; METHYLTRANSFERASE; NEUTRALIZING ANTIBODY; VIRUS RNA;

ANTIVIRAL ACTIVITY; CATALYSIS; DENGUE VIRUS; DRUG TARGETING; ENZYME ACTIVITY; FLAVIVIRUS; IMMUNE RESPONSE; INNATE IMMUNITY; JAPANESE ENCEPHALITIS VIRUS; MOLECULE; PRIORITY JOURNAL; REVIEW; RNA CAPPING; RNA METHYLATION; RNA STRUCTURE; RNA SYNTHESIS; TRANSLATION INITIATION; VIRUS MORPHOLOGY; VIRUS MUTANT; VIRUS VIRULENCE;

FLAVIVIRUS; IMMUNE EVASION; METHYLATION; PROTEIN BIOSYNTHESIS; RNA CAP ANALOGS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, VIRAL; TRNA METHYLTRANSFERASES;

EID: 84897053354     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.062208-0     Document Type: Review

References (102)

1. Ahola, T. & Kaariainen, L. (1995). Reaction in alphavirus mRNA capping: formation of a covalent complex of nonstructural protein nsP1 with 7-methyl-GMP. Proc Natl Acad Sci U S A 92, 507-511.
2. Ahola, T., Laakkonen, P., Vihinen, H. & Kaariainen, L. (1997). Critical residues of Semliki Forest virus RNA capping enzyme involved in methyltransferase and guanylyltransferase-like activities. J Virol 71, 392-397.
3. Assenberg, R., Ren, J., Verma, A., Walter, T. S., Alderton, D., Hurrelbrink, R. J., Fuller, S. D., Bressanelli, S., Owens, R. J. & other authors (2007). Crystal structure of the Murray Valley encephalitis virus NS5 methyltransferase domain in complex with cap analogues. J Gen Virol 88, 2228-2236.
4. Banerjee, A. K. (1980). 59-terminal cap structure in eucaryotic messenger ribonucleic acids. Microbiol Rev 44, 175-205.
5. Benarroch, D., Egloff, M. P., Mulard, L., Guerreiro, C., Romette, J. L. & Canard, B. (2004). A structural basis for the inhibition of the NS5 dengue virus mRNA 29-O-methyltransferase domain by ribavirin 59-triphosphate. J Biol Chem 279, 35638-35643.
6. Bollati, M., Milani, M., Mastrangelo, E., Ricagno, S., Tedeschi, G., Nonnis, S., Decroly, E., Selisko, B., de Lamballerie, X. & other authors (2009). Recognition of RNA cap in the Wesselsbron virus NS5 methyltransferase domain: implications for RNA-capping mechanisms in Flavivirus. J Mol Biol 385, 140-152.
7. Bouloy, M., Plotch, S. J. & Krug, R. M. (1978). Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. Proc Natl Acad Sci U S A 75, 4886-4890.
8. Bouvet, M., Debarnot, C., Imbert, I., Selisko, B., Snijder, E. J., Canard, B. & Decroly, E. (2010). In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog 6, e1000863.
9. Brinton, M. A. & Dispoto, J. H. (1988). Sequence and secondary structure analysis of the 59-terminal region of flavivirus genome RNA. Virology 162, 290-299.
10. Bussetta, C. & Choi, K. H. (2012). Dengue virus nonstructural protein 5 adopts multiple conformations in solution. Biochemistry 51, 5921-5931.
11. Chen, Y., Cai, H., Pan, J., Xiang, N., Tien, P., Ahola, T. & Guo, D. (2009). Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc Natl Acad Sci U S A106,3484-3489.
12. Chen, Y., Su, C., Ke, M., Jin, X., Xu, L., Zhang, Z., Wu, A., Sun, Y., Yang, Z. & other authors (2011). Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 29-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog 7, e1002294.
13. Chen, C., Wang, Y., Shan, C., Sun, Y., Xu, P., Zhou, H., Yang, C., Shi, P. Y., Rao, Z. & other authors (2013a). Crystal structure of enterovirus 71 RNA-dependent RNA polymerase complexed with its protein primer VPg: implication for a trans mechanism of VPg uridylylation. J Virol 87, 5755-5768.
14. Chen, H., Liu, L., Jones, S. A., Banavali, N., Kass, J., Li, Z., Zhang, J., Kramer, L. D., Ghosh, A. K. & Li, H. (2013b). Selective inhibition of the West Nile virus methyltransferase by nucleoside analogs. Antiviral Res 97, 232-239.
15. Cho, E. J., Takagi, T., Moore, C. R. & Buratowski, S. (1997). mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev 11, 3319-3326.
16. Chung, K. Y., Dong, H., Chao, A. T., Shi, P. Y., Lescar, J. & Lim, S. P. (2010). Higher catalytic efficiency of N-7-methylation is responsible for processive N-7 and 29-O methyltransferase activity in dengue virus. Virology 402, 52-60.
17. Daffis, S., Szretter, K. J., Schriewer, J., Li, J., Youn, S., Errett, J., Lin, T. Y., Schneller, S., Zust, R. & other authors (2010). 29-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468, 452-456.
18. Decroly, E., Debarnot, C., Ferron, F., Bouvet, M., Coutard, B., Imbert, I., Gluais, L., Papageorgiou, N., Sharff, A. & other authors (2011). Crystal structure and functional analysis of the SARS-coronavirus RNA cap 29-O-methyltransferase nsp10/nsp16 complex. PLoS Pathog 7, e1002059.
19. Decroly, E., Ferron, F., Lescar, J. & Canard, B. (2012). Conventional and unconventional mechanisms for capping viral mRNA. Nat Rev Microbiol 10, 51-65.
20. Dias, A., Bouvier, D., Crépin, T., McCarthy, A. A., Hart, D. J., Baudin, F., Cusack, S. & Ruigrok, R. W. (2009). The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458, 914-918.
21. Dong, H., Ray, D., Ren, S., Zhang, B., Puig-Basagoiti, F., Takagi, Y., Ho, C. K., Li, H. & Shi, P. Y. (2007). Distinct RNA elements confer specificity to flavivirus RNA cap methylation events. J Virol 81, 4412-4421.
22. Dong, H., Ren, S., Li, H. & Shi, P. Y. (2008a). Separate molecules of West Nile virus methyltransferase can independently catalyze the N7 and 29-O methylations of viral RNA cap. Virology 377, 1-6.
23. Dong, H., Ren, S., Zhang, B., Zhou, Y., Puig-Basagoiti, F., Li, H. & Shi, P. Y. (2008b). West Nile virus methyltransferase catalyzes two methylations of the viral RNA cap through a substrate-repositioning mechanism. J Virol 82, 4295-4307.
24. Dong, H., Zhang, B. & Shi, P. Y. (2008c). Flavivirus methyltransferase: a novel antiviral target. Antiviral Res 80, 1-10.
25. Dong, H., Zhang, B. & Shi, P. Y. (2008d). Terminal structures of West Nile virus genomic RNA and their interactions with viral NS5 protein. Virology 381, 123-135.
26. Dong, H., Chang, D. C., Xie, X., Toh, Y. X., Chung, K. Y., Zou, G., Lescar, J., Lim, S. P. & Shi, P. Y. (2010a). Biochemical and genetic characterization of dengue virus methyltransferase. Virology 405, 568-578.
27. Dong, H., Liu, L., Zou, G., Zhao, Y., Li, Z., Lim, S. P., Shi, P. Y. & Li, H. (2010b). Structural and functional analyses of a conserved hydro-phobic pocket of flavivirus methyltransferase. J Biol Chem 285, 32586-32595.
28. Dong, H., Chang, D. C., Hua, M. H., Lim, S. P., Chionh, Y. H., Hia, F., Lee, Y. H., Kukkaro, P., Lok, S. M. & other authors (2012). 29-O methylation of internal adenosine by flavivirus NS5 methyltransferase. PLoS Pathog 8, e1002642.
29. Duangchinda, T., Dejnirattisai, W., Vasanawathana, S., Limpitikul, W., Tangthawornchaikul, N., Malasit, P., Mongkolsapaya, J. & Screaton, G. (2010). Immunodominant T-cell responses to dengue virus NS3 are associated with DHF. Proc Natl Acad Sci U S A 107, 16922-16927.
30. Egloff, M. P., Benarroch, D., Selisko, B., Romette, J. L. & Canard, B. (2002a). An RNA cap (nucleoside-29-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J 21, 2757-2768.
31. Egloff, M. P., Benarroch, D., Selisko, B., Romette, J. L. & Canard, B. (2002b). An RNA cap (nucleoside-29-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J 21, 2757-2768.
32. Egloff, M. P., Decroly, E., Malet, H., Selisko, B., Benarroch, D., Ferron, F. & Canard, B. (2007a). Structural and functional analysis of methylation and 59-RNA sequence requirements of short capped RNAs by the methyltransferase domain of dengue virus NS5. J Mol Biol 372, 723-736.
33. Egloff, M. P., Decroly, E., Malet, H., Selisko, B., Benarroch, D., Ferron, F. & Canard, B. (2007b). Structural and functional analysis of methylation and 59-RNA sequence requirements of short capped RNAs by the methyltransferase domain of dengue virus NS5. J Mol Biol 372, 723-736.
34. Fechter, P., Mingay, L., Sharps, J., Chambers, A., Fodor, E. & Brownlee, G. G. (2003). Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. J Biol Chem 278, 20381-20388.
35. Ferrer-Orta, C., Arias, A., Agudo, R., Pérez-Luque, R., Escarmís, C., Domingo, E. & Verdaguer, N. (2006). The structure of a protein primer-polymerase complex in the initiation of genome replication. EMBO J 25, 880-888.
36. Fitzgerald, K. D. & Semler, B. L. (2009). Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim Biophys Acta 1789, 518-528.
37. Flanegan, J. B., Petterson, R. F., Ambros, V., Hewlett, N. J. & Baltimore, D. (1977). Covalent linkage of a protein to a defined nucleotide sequence at the 59-terminus of virion and replicative intermediate RNAs of poliovirus. Proc Natl Acad Sci U S A 74, 961-965.
38. Furuichi, Y. & Shatkin, A. J. (2000). Viral and cellular mRNA capping: past and prospects. Adv Virus Res 55, 135-184.
39. Garaigorta, U. & Chisari, F. V. (2009). Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation. Cell Host Microbe 6, 513-522.
40. Geiss, B. J., Thompson, A. A., Andrews, A. J., Sons, R. L., Gari, H. H., Keenan, S. M. & Peersen, O. B. (2009). Analysis of flavivirus NS5 methyltransferase cap binding. J Mol Biol 385, 1643-1654.
41. Geiss, B. J., Stahla-Beek, H. J., Hannah, A. M., Gari, H. H., Henderson, B. R., Saeedi, B. J. & Keenan, S. M. (2011). A highthroughput screening assay for the identification of flavivirus NS5 capping enzyme GTP-binding inhibitors: implications for antiviral drug development. J Biomol Screen 16, 852-861.
42. Ghosh, A. & Lima, C. D. (2010). Enzymology of RNA cap synthesis. Wiley Interdiscip Rev RNA 1, 152-172.
43. Goodfellow, I., Chaudhry, Y., Gioldasi, I., Gerondopoulos, A., Natoni, A., Labrie, L., Laliberté, J. F. & Roberts, L. (2005). Calicivirus translation initiation requires an interaction between VPg and eIF 4 E. EMBO Rep 6, 968-972.
44. Gruez, A., Selisko, B., Roberts, M., Bricogne, G., Bussetta, C., Jabafi, I., Coutard, B., De Palma, A. M., Neyts, J. & Canard, B. (2008). The crystal structure of coxsackievirus B3 RNA-dependent RNA polymerase in complex with its protein primer VPg confirms the existence of a second VPg binding site on Picornaviridae polymerases. J Virol 82, 9577-9590.
45. Guidotti, L. G. & Chisari, F. V. (2001). Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 19, 65-91.
46. Guilligay, D., Tarendeau, F., Resa-Infante, P., Coloma, R., Crepin, T., Sehr, P., Lewis, J., Ruigrok, R. W., Ortin, J. & other authors (2008). The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15, 500-506.
47. Gunther, V. J., Putnak, R., Eckels, K. H., Mammen, M. P., Scherer, J. M., Lyons, A., Sztein, M. B. & Sun, W. (2011). A human challenge model for dengue infection reveals a possible protective role for sustained interferon gamma levels during the acute phase of illness. Vaccine 29, 3895-3904.
48. Guy, B. & Almond, J. W. (2008). Towards a dengue vaccine: progress to date and remaining challenges. Comp Immunol Microbiol Infect Dis 31, 239-252.
49. Habjan, M., Hubel, P., Lacerda, L., Benda, C., Holze, C., Eberl, C. H., Mann, A., Kindler, E., Gil-Cruz, C. & other authors (2013). Sequestration by IFIT1 impairs translation of 29O-unmethylated capped RNA. PLoS Pathog 9, e1003663.
50. Hanley, K. A., Manlucu, L. R., Manipon, G. G., Hanson, C. T., Whitehead, S. S., Murphy, B. R. & Blaney, J. E., Jr. (2004). Introduction of mutations into the non-structural genes or 39 untranslated region of an attenuated dengue virus type 4 vaccine candidate further decreases replication in rhesus monkeys while retaining protective immunity. Vaccine 22, 3440-3448.
51. Hellen, C. U. & Sarnow, P. (2001). Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev 15, 1593-1612.
52. Issur, M., Geiss, B. J., Bougie, I., Picard-Jean, F., Despins, S., Mayette, J., Hobdey, S. E. & Bisaillon, M. (2009). The flavivirus NS5 protein is a true RNA guanylyltransferase that catalyzes a two-step reaction to form the RNA cap structure. RNA 15, 2340-2350.
53. Ivanov, K. A. & Ziebuhr, J. (2004). Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 59-triphosphatase activities. J Virol 78, 7833-7838.
54. Ivanov, K. A., Thiel, V., Dobbe, J. C., van der Meer, Y., Snijder, E. J. & Ziebuhr, J. (2004). Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol 78, 5619-5632.
55. Jansson, A. M., Jakobsson, E., Johansson, P., Lantez, V., Coutard, B., de Lamballerie, X., Unge, T. & Jones, T. A. (2009). Structure of the methyltransferase domain from the Modoc virus, a flavivirus with no known vector. Acta Crystallogr D Biol Crystallogr 65, 796-803.
56. Kimura, T., Katoh, H., Kayama, H., Saiga, H., Okuyama, M., Okamoto, T., Umemoto, E., Matsuura, Y., Yamamoto, M. & Takeda, K. (2013). Ifit1 inhibits Japanese encephalitis virus replication through binding to 59 capped 29-O unmethylated RNA. J Virol 87, 9997-10003.
57. Kroschewski, H., Lim, S. P., Butcher, R. E., Yap, T. L., Lescar, J., Wright, P. J., Vasudevan, S. G. & Davidson, A. D. (2008). Mutagenesis of the dengue virus type 2 NS5 methyltransferase domain. J Biol Chem 283, 19410-19421.
58. Lai, M. M. & Stohlman, S. A. (1981). Comparative analysis of RNA genomes of mouse hepatitis viruses. J Virol 38, 661-670.
59. Lai, M. M., Patton, C. D. & Stohlman, S. A. (1982). Further characterization of mRNA's of mouse hepatitis virus: presence of common 59-end nucleotides. J Virol 41, 557-565.
60. Lee, Y. F., Nomoto, A., Detjen, B. M. & Wimmer, E. (1977). A protein covalently linked to poliovirus genome RNA. Proc Natl Acad Sci U S A 74, 59-63.
61. Leyssen, P., Balzarini, J., De Clercq, E. & Neyts, J. (2005). The predominant mechanism by which ribavirin exerts its antiviral activity in vitro against flaviviruses and paramyxoviruses is mediated by inhibition of IMP dehydrogenase. J Virol 79, 1943-1947.
62. Li, H., Clum, S., You, S., Ebner, K. E. & Padmanabhan, R. (1999). The serine protease and RNA-stimulated nucleoside triphosphatase and RNA helicase functional domains of dengue virus type 2 NS3 converge within a region of 20 amino acids. J Virol 73, 3108-3116.
63. Li, J., Fontaine-Rodriguez, E. C. & Whelan, S. P. (2005). Amino acid residues within conserved domain VI of the vesicular stomatitis virus large polymerase protein essential for mRNA cap methyltransferase activity. J Virol 79, 13373-13384.
64. Li, J., Wang, J. T. & Whelan, S. P. (2006). A unique strategy for mRNA cap methylation used by vesicular stomatitis virus. Proc Natl Acad Sci U S A103,8493-8498.
65. Li, S. H., Dong, H., Li, X. F., Xie, X., Zhao, H., Deng, Y. Q., Wang, X. Y., Ye, Q., Zhu, S. Y. & other authors (2013). Rational design of a flavivirus vaccine by abolishing viral RNA 29-O methylation. J Virol 87, 5812-5819.
66. Lim, S. P., Sonntag, L. S., Noble, C., Nilar, S. H., Ng, R. H., Zou, G., Monaghan, P., Chung, K. Y., Dong, H. & other authors (2011). Small molecule inhibitors that selectively block dengue virus methyltransferase. J Biol Chem 286, 6233-6240.
67. López-Lastra, M., Rivas, A. & Barría, M. I. (2005). Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol Res 38, 121-146.
68. Lu, G. & Gong, P. (2013). Crystal structure of the full-length Japanese encephalitis virus NS5 reveals a conserved methyltransferase-polymerase interface. PLoS Pathog 9, e1003549.
69. Malet, H., Egloff, M. P., Selisko, B., Butcher, R. E., Wright, P. J., Roberts, M., Gruez, A., Sulzenbacher, G., Vonrhein, C. & other authors (2007). Crystal structure of the RNA polymerase domain of the West Nile virus non-structural protein 5. J Biol Chem 282, 10678-10689.
70. Mastrangelo, E., Bollati, M., Milani, M., Selisko, B., Peyrane, F., Canard, B., Grard, G., de Lamballerie, X. & Bolognesi, M. (2007). Structural bases for substrate recognition and activity in Meaban virus nucleoside-29-O-methyltransferase. Protein Sci 16, 1133-1145.
71. McCracken, S., Fong, N., Rosonina, E., Yankulov, K., Brothers, G., Siderovski, D., Hessel, A., Foster, S., Shuman, S. & Bentley, D. L. (1997). 59-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev 11, 3306-3318.
72. Niepmann, M. (2013). Hepatitis C virus RNA translation. Curr Top Microbiol Immunol 369, 143-166.
73. Ogino, T. & Banerjee, A. K. (2007). Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol Cell 25, 85-97.
74. Ogino, T. & Banerjee, A. K. (2011). An unconventional pathway of mRNA cap formation by vesiculoviruses. Virus Res 162, 100-109.
75. Ogino, T., Kobayashi, M., Iwama, M. & Mizumoto, K. (2005). Sendai virus RNA-dependent RNA polymerase L protein catalyzes cap methylation of virus-specific mRNA. J Biol Chem 280, 4429-4435.
76. Ogino, T., Yadav, S. P. & Banerjee, A. K. (2010). Histidine-mediated RNA transfer to GDP for unique mRNA capping by vesicular stomatitis virus RNA polymerase. Proc Natl Acad Sci U S A 107, 3463-3468.
77. Paul, A. V., van Boom, J. H., Filippov, D. & Wimmer, E. (1998). Protein-primed RNA synthesis by purified poliovirus RNA polymerase. Nature 393, 280-284.
78. Pichlmair, A., Schulz, O., Tan, C. P., Naslund, T. I., Liljestrom, P., Weber, F. & Reis e Sousa, C. (2006). RIG-I-mediated antiviral responses to single-stranded RNA bearing 59-phosphates. Science 314, 997-1001.
79. Rahmeh, A. A., Li, J., Kranzusch, P. J. & Whelan, S. P. (2009). Ribose 29-O methylation of the vesicular stomatitis virus mRNA cap precedes and facilitates subsequent guanine-N-7 methylation by the large polymerase protein. J Virol 83, 11043-11050.
80. Ray, D., Shah, A., Tilgner, M., Guo, Y., Zhao, Y., Dong, H., Deas, T. S., Zhou, Y., Li, H. & Shi, P.-Y. (2006). West Nile virus 59-cap structure is formed by sequential guanine N-7 and ribose 29-O methylations by nonstructural protein 5. J Virol 80, 8362-8370.
81. Reinisch, K. M., Nibert, M. L. & Harrison, S. C. (2000). Structure of the reovirus core at 3.6 A resolution. Nature 404, 960-967.
82. + T lymphocytes in dengue virus infection. J Virol 87, 2693-2706.
83. Sabchareon, A., Wallace, D., Sirivichayakul, C., Limkittikul, K., Chanthavanich, P., Suvannadabba, S., Jiwariyavej, V., Dulyachai, W., Pengsaa, K. & other authors (2012). Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380, 1559-1567.
84. Schaffer, F. L., Ehresmann, D. W., Fretz, M. K. & Soergel, M. I. (1980). A protein, VPg, covalently linked to 36S calicivirus RNA. J Gen Virol 47, 215-220.
85. Shuman, S. (2001). Structure, mechanism, and evolution of the mRNA capping apparatus. Prog Nucleic Acid Res Mol Biol 66, 1-40.
86. Simmons, C. P., Dong, T., Chau, N. V., Dung, N. T., Chau, T. N., Thao, le T. T., Dung, N. T., Hien, T. T., Rowland-Jones, S. & Farrar, J. (2005). Early T-cell responses to dengue virus epitopes in Vietnamese adults with secondary dengue virus infections. J Virol 79, 5665-5675.
87. Stahla-Beek, H. J., April, D. G., Saeedi, B. J., Hannah, A. M., Keenan, S. M. & Geiss, B. J. (2012). Identification of a novel antiviral inhibitor of the flavivirus guanylyltransferase enzyme. J Virol 86, 8730-8739
88. Sutton, G., Grimes, J. M., Stuart, D. I. & Roy, P. (2007). Bluetongue virus VP4 is an RNA-capping assembly line. Nat Struct Mol Biol 14, 449-451.
89. Szretter, K. J., Daniels, B. P., Cho, H., Gainey, M. D., Yokoyama, W. M., Gale, M., Jr, Virgin, H. W., Klein, R. S., Sen, G. C. & Diamond, M. S. (2012). 29-O methylation of the viral mRNA cap by West Nile virus evades ifit1-dependent and -independent mechanisms of host restriction in vivo. PLoS Pathog 8, e1002698.
90. van Duijn, L. P., Kasperaitis, M., Ameling, C. & Voorma, H. O. (1986). Additional methylation at the N(2)-position of the cap of 26S Semliki Forest virus late mRNA and initiation of translation. Virus Res 5, 61-66.
91. Vasiljeva, L., Merits, A., Auvinen, P. & Kaariainen, L. (2000). Identification of a novel function of the alphavirus capping apparatus. RNA 59-triphosphatase activity of Nsp2. J Biol Chem 275, 17281-17287.
92. Wengler, G. & Wengler, G. (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.
93. Wengler, G. & Wengler, G. (1991). The carboxy-terminal part of the NS 3 protein of the West Nile flavivirus can be isolated as a soluble protein after proteolytic cleavage and represents an RNA-stimulated NTPase. Virology 184, 707-715.
94. Yap, L. J., Luo, D., Chung, K. Y., Lim, S. P., Bodenreider, C., Noble, C., Shi, P. Y. & Lescar, J. (2010). Crystal structure of the dengue virus methyltransferase bound to a 59-capped octameric RNA. PLoS ONE 5, e12836.
95. + T cells. J Immunol 182, 4865-4873.
96. + T cell or antibody responses but contribute to protection after vaccination. J Immunol 185, 5405-5416.
97. Yuan, P., Bartlam, M., Lou, Z., Chen, S., Zhou, J., He, X., Lv, Z., Ge, R., Li, X. & other authors (2009). Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458, 909-913.
98. Yue, Z., Maldonado, E., Pillutla, R., Cho, H., Reinberg, D. & Shatkin, A. J. (1997). Mammalian capping enzyme complements mutant Saccharomyces cerevisiae lacking mRNA guanylyltransferase and selectively binds the elongating form of RNA polymerase II. Proc Natl Acad Sci U S A 94, 12898-12903.
99. Zhang, B., Dong, H., Zhou, Y. & Shi, P. Y. (2008). Genetic interactions among the West Nile virus methyltransferase, the RNA-dependent RNA polymerase, and the 59 stem-loop of genomic RNA. J Virol 82, 7047-7058.
100. Zhou, Y., Ray, D., Zhao, Y., Dong, H., Ren, S., Li, Z., Guo, Y., Bernard, K. A., Shi, P.-Y. & Li, H. (2007). Structure and function of flavivirus NS5 methyltransferase. J Virol 81, 3891-3903.
101. Zust, R., Cervantes-Barragan, L., Habjan, M., Maier, R., Neuman, B. W., Ziebuhr, J., Szretter, K. J., Baker, S. C., Barchet, W. & other authors (2011). Ribose 29-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat Immunol 12, 137-143.
102. Zust, R., Dong, H., Li, X. F., Chang, D. C., Zhang, B., Balakrishnan, T., Toh, Y. X., Jiang, T., Li, S. H. & other authors (2013). Rational design of a live attenuated dengue vaccine: 29-O-methyltransferase mutants are highly attenuated and immunogenic in mice and macaques. PLoS Pathog 9, e1003521.