Rational design of a flavivirus vaccine by abolishing viral RNA 2′-O methylation

Journal of Virology

Volumn 87, Issue 10, 2013, Pages 5812-5819

  Li, Shi Hua ^a   Dong, Hongping ^b   Li, Xiao Feng ^a   Xie, Xuping ^b   Zhao, Hui ^a   Deng, Yong Qiang ^a   Wang, Xiao Yu ^a,c   Ye, Qing ^a   Zhu, Shun Ya ^a   Wang, Hong Jiang ^a   Zhang, Bo ^d   Leng, Qi Bin ^e   Zuest, Roland ^f   Qin, E De ^a   Qin, Cheng Feng ^a   Shi, Pei Yong ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b Novartis Institute for Tropical Diseases   (Singapore)

^c ZHEJIANG UNIVERSITY   (China)

^d WUHAN INSTITUTE OF VIROLOGY   (China)

^e INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^f AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; JAPANESE ENCEPHALITIS 2' O METHYLTRANSFERASE MUTANT VACCINE; JAPANESE ENCEPHALITIS VACCINE; NEUTRALIZING ANTIBODY; NUCLEASE; NUCLEASE P1; PROTEIN; PROTEIN IFIT 1; PROTEIN IFIT 2; PROTEIN IFIT 3; PROTEIN IFIT 5; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG DESIGN; FEASIBILITY STUDY; FEMALE; GENOTYPE; HUMORAL IMMUNITY; IMMUNE EVASION; IMMUNOGENICITY; IMMUNOPROPHYLAXIS; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; JAPANESE ENCEPHALITIS; JAPANESE ENCEPHALITIS VIRUS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA METHYLATION; SINGLE DRUG DOSE; VACCINE PRODUCTION; VIRUS ATTENUATION; VIRUS MUTATION;

ANIMALS; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; ENCEPHALITIS VIRUS, JAPANESE; ENCEPHALITIS, JAPANESE; FEMALE; JAPANESE ENCEPHALITIS VACCINES; LEUKOCYTES, MONONUCLEAR; METHYLATION; MICE; MICE, INBRED BALB C; RNA, VIRAL; SURVIVAL ANALYSIS; TRNA METHYLTRANSFERASES; VACCINES, ATTENUATED;

EID: 84877315512     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02806-12     Document Type: Article

References (34)

1. Talon J, Salvatore M, O'Neill RE, Nakaya Y, Zheng H, Muster T, Garcia-Sastre A, Palese P. 2000. Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach. Proc. Natl. Acad. Sci. U. S. A. 97:4309-4314.
2. Furuichi Y, Shatkin AJ. 2000. Viral and cellular mRNA capping: past and prospects. Adv. Virus Res. 55:135-184.
3. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin TY, Schneller S, Zust R, Dong H, Thiel V, Sen GC, Fensterl V, Klimstra WB, Pierson TC, Buller RM, Gale M, Jr, Shi PY, Diamond MS. 2010. 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468:452- 456.
4. Zust R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V. 2011. Ribose 2′-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.
5. Egloff MP, Benarroch D, Selisko B, Romette JL, Canard B. 2002. An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J. 21:2757-2768.
6. Ray D, Shah A, Tilgner M, Guo Y, Zhao Y, Dong H, Deas TS, Zhou Y, Li H, Shi PY. 2006. West Nile virus 5′-cap structure is formed by sequential guanine N-7 and ribose 2′-O methylations by nonstructural protein 5. J. Virol. 80:8362- 8370.
7. Zhou Y, Ray D, Zhao Y, Dong H, Ren S, Li Z, Guo Y, Bernard KA, Shi PY, Li H. 2007. Structure and function of flavivirus NS5 methyltransferase. J. Virol. 81:3891-3903.
8. Dong H, Chang DC, Hua MH, Lim SP, Chionh YH, Hia F, Lee YH, Kukkaro P, Lok SM, Dedon PC, Shi PY. 2012. 2′-O methylation of internal adenosine by flavivirus NS5 methyltransferase. PLoS Pathog. 8:e1002642. doi:10.1371/journal.ppat.1002642.
9. Chung KY, Dong H, Chao AT, Shi PY, Lescar J, Lim SP. 2010. Higher catalytic efficiency of N-7-methylation is responsible for processive N-7 and 2′-O methyltransferase activity in dengue virus. Virology 402:52- 60.
10. Dong H, Chang DC, Xie X, Toh YX, Chung KY, Zou G, Lescar J, Lim SP, Shi PY. 2010. Biochemical and genetic characterization of dengue virus methyltransferase. Virology 405:568 -578.
11. Pan XL, Liu H, Wang HY, Fu SH, Liu HZ, Zhang HL, Li MH, Gao XY, Wang JL, Sun XH, Lu XJ, Zhai YG, Meng WS, He Y, Wang HQ, Han N, Wei B, Wu YG, Feng Y, Yang DJ, Wang LH, Tang Q, Xia G, Kurane I, Rayner S, Liang GD. 2011. Emergence of genotype I of Japanese encephalitis virus as the dominant genotype in Asia. J. Virol. 85:9847-9853.
12. Deng YQ, Dai JX, Ji GH, Jiang T, Wang HJ, Yang HO, Tan WL, Liu R, Yu M, Ge BX, Zhu QY, Qin ED, Guo YJ, Qin CF. 2011. A broadly flavivirus cross-neutralizing monoclonal antibody that recognizes a novel epitope within the fusion loop of E protein. PLoS One 6:e16059. doi:10 .1371/journal.pone.0016059.
13. Ye Q, Li XF, Zhao H, Li SH, Deng YQ, Cao RY, Song KY, Wang HJ, Hua RH, Yu YX, Zhou X, Qin ED, Qin CF. 2012. A single nucleotide mutation in NS2A of Japanese encephalitis-live vaccine virus (SA14-14-2) ablates NS1' formation and contributes to attenuation. J. Gen. Virol. 93: 1959-1964.
14. Kang X, Li Y, Fan L, Lin F, Wei J, Zhu X, Hu Y, Li J, Chang G, Zhu Q, Liu H, Yang Y. 2012. Development of an ELISA-array for simultaneous detection of five encephalitis viruses. Virol. J. 9:56. doi:10.1186/1743 -422X-9-56.
15. Jiang T, Zhao H, Li XF, Deng YQ, Liu J, Xu LJ, Han JF, Cao RY, Qin ED, Qin CF. 2011. CpG oligodeoxynucleotides protect against the 2009 H1N1 pandemic influenza virus infection in a murine model. Antiviral Res. 89:124 -126.
16. Yu Y. 2010. Phenotypic and genotypic characteristics of Japanese encephalitis attenuated live vaccine virus SA14-14-2 and their stabilities. Vaccine 28:3635-3641.
17. Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, Burkard TR, Burckstummer T, Stefanovic A, Krieger S, Bennett KL, Rulicke T, Weber F, Colinge J, Muller M, Superti-Furga G. 2011. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat. Immunol. 12:624-630.
18. Alcaraz-Estrada SL, Manzano MI, Del Angel RM, Levis R, Padmanabhan R. 2010. Construction of a dengue virus type 4 reporter replicon and analysis of temperature-sensitive mutations in non-structural proteins 3 and 5. J. Gen. Virol. 91:2713-2718.
19. Bhattacharya D, Hoover S, Falk SP, Weisblum B, Vestling M, Striker R. 2008. Phosphorylation of yellow fever virus NS5 alters methyltransferase activity. Virology 380:276 -284.
20. Li J, Wang JT, Whelan SP. 2006. A unique strategy for mRNA cap methylation used by vesicular stomatitis virus. Proc. Natl. Acad. Sci. U. S. A. 103:8493- 8498.
21. Fensterl V, Sen GC. 2011. The ISG56/IFIT1 gene family. J. Interferon Cytokine Res. 31:71-78.
22. Fensterl V, Wetzel JL, Ramachandran S, Ogino T, Stohlman SA, Bergmann CC, Diamond MS, Virgin HW, Sen GC. 2012. Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog. 8:e1002712. doi:10.1371/journal.ppat.1002712.
23. Yang Z, Liang H, Zhou Q, Li Y, Chen H, Ye W, Chen D, Fleming J, Shu H, Liu Y. 2012. Crystal structure of ISG54 reveals a novel RNA binding structure and potential functional mechanisms. Cell Res. 22:1328 -1338.
24. Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324 -330.
25. Liang JJ, Liao CL, Liao JT, Lee YL, Lin YL. 2009. A Japanese encephalitis virus vaccine candidate strain is attenuated by decreasing its interferon antagonistic ability. Vaccine 27:2746 -2754.
26. Pu SY, Wu RH, Yang CC, Jao TM, Tsai MH, Wang JC, Lin HM, Chao YS, Yueh A. 2011. Successful propagation of flavivirus infectious cDNAs by a novel method to reduce the cryptic bacterial promoter activity of virus genomes. J. Virol. 85:2927-2941.
27. Yun SI, Kim SY, Rice CM, Lee YM. 2003. Development and application of a reverse genetics system for Japanese encephalitis virus. J. Virol. 77: 6450-6465.
28. Dean CH, Alarcon JB, Waterston AM, Draper K, Early R, Guirakhoo F, Monath TP, Mikszta JA. 2005. Cutaneous delivery of a live, attenuated chimeric flavivirus vaccine against Japanese encephalitis (ChimeriVax)- JE) in non-human primates. Hum. Vaccin. 1:106 -111.
29. Halstead SB, Thomas SJ. 2011. New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev. Vaccines 10:355- 364.
30. Van Gessel Y, Klade CS, Putnak R, Formica A, Krasaesub S, Spruth M, Cena B, Tungtaeng A, Gettayacamin M, Dewasthaly S. 2011. Correlation of protection against Japanese encephalitis virus and JE vaccine (IXIARO) induced neutralizing antibody titers. Vaccine 29:5925-5931.
31. Arroyo J, Guirakhoo F, Fenner S, Zhang ZX, Monath TP, Chambers TJ. 2001. Molecular basis for attenuation of neurovirulence of a yellow fever virus/Japanese encephalitis virus chimera vaccine (ChimeriVax-JE). J. Virol. 75:934 -942.
32. Lee E, Hall RA, Lobigs M. 2004. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J. Virol. 78:8271- 8280.
33. Monath TP, Arroyo J, Levenbook I, Zhang ZX, Catalan J, Draper K, Guirakhoo F. 2002. Single mutation in the flavivirus envelope protein hinge region increases neurovirulence for mice and monkeys but decreases viscerotropism for monkeys: relevance to development and safety testing of live, attenuated vaccines. J. Virol. 76:1932-1943.
34. Zhao Z, Date T, Li Y, Kato T, Miyamoto M, Yasui K, Wakita T. 2005. Characterization of the E-138 (Glu/Lys) mutation in Japanese encephalitis virus by using a stable, full-length, infectious cDNA clone. J. Gen. Virol. 86:2209 -2220.