Recoding of the vesicular stomatitis virus L gene by computer-aided design provides a live, attenuated vaccine candidate

mBio

Volumn 6, Issue 2, 2015, Pages

  Wang, Bingyin ^a   Yang, Chen ^a   Tekes, Gergely ^d   Mueller, Steffen ^a,c   Paul, Aniko ^a   Whelan, Sean P J ^b   Wimmer, Eckard ^a,c  

^a STONY BROOK UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Codagenix Inc ^*  (United States)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CODON; CODON PAIR BIAS; COMPUTER AIDED DESIGN; CONTROLLED STUDY; GENE SEQUENCE; GENETIC CODE; IMMUNOGENICITY; L GENE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VESICULAR STOMATITIS; VESICULOVIRUS; VIRUS ATTENUATION; VIRUS GENE; VIRUS RECOMBINANT; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; BAGG ALBINO MOUSE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PROTEIN ENGINEERING; SILENT MUTATION; VIRULENCE;

MUS; ORTHOMYXOVIRIDAE; POLIOVIRUS; RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

L PROTEIN, VESICULAR STOMATITIS VIRUS; LIVE VACCINE; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN; VIRUS VACCINE;

ANIMALS; COMPUTER-AIDED DESIGN; MALE; MICE, INBRED BALB C; PROTEIN ENGINEERING; RNA REPLICASE; SILENT MUTATION; VACCINES, ATTENUATED; VESICULOVIRUS; VIRAL PROTEINS; VIRAL VACCINES; VIRULENCE;

EID: 84928779454     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00237-15     Document Type: Article

References (43)

1. White JM, Schornberg K. 2012. A new player in the puzzle of filovirus entry. Nat Rev Microbiol 10:317-322. http://dx.doi.org/10.1038/nrmicro2764.
2. Eaton BT, Broder CC, Middleton D, Wang L. 2006. Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 4:23-35. http://dx.doi.org/10.1038/nrmicro1323.
3. Collins PL, Melero J. 2011. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res 162: 80-99. http://dx.doi.org/10.1016/j.virusres.2011.09.020.
4. Lichty BD, Power AT, Stojdl DF, Bell J. 2004. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 10:210-216. http://dx.doi.org/10.1016/j.molmed.2004.03.003.
5. Quiroz E, Moreno N, Peralta PH, Tesh R. 1988. A human case of encephalitis associated with vesicular stomatitis virus (Indiana serotype) infection. Am J Trop Med Hyg 39:312-314.
6. Brown F, Bishop DH, Crick J, Francki RI, Holland JJ, Hull R, Johnson K, Martelli G, Murphy FA, Obijeski JF, Peters D, Pringle CR, Reichmann ME, Schneider LG, Shope RE, Simpson DI, Summers DF, Wagner R. 1979. Rhabdoviridae. Report of the Rhabdovirus Study Group, International Committee on Taxonomy of Viruses. Intervirology 12:1-7. http://dx.doi.org/10.1159/000149062.
7. Das K, Aramini JM, Ma LC, Krug RM, Arnold E. 2010. Structures of influenza A proteins and insights into antiviral drug targets. Nat Struct Mol Biol 17:530-538. http://dx.doi.org/10.1038/nsmb.1779.
8. Sleat DE, Banerjee A. 1993. Transcriptional activity and mutational analysis of recombinant vesicular stomatitis virus RNA polymerase. J Virol 67:1334-1339.
9. Li J, Fontaine-Rodriguez EC, Whelan S. 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. http://dx.doi.org/10.1128/JVI.79.21.13373-13384.2005.
10. Li J, Rahmeh A, Morelli M, Whelan S. 2008. A conserved motif in regionVof the large polymerase proteins of nonsegmented negative-sense RNA viruses that is essential for mRNA capping. J Virol 82:775-784. http://dx.doi.org/10.1128/JVI.02107-07.
11. Rahmeh AA, Li J, Kranzusch PJ, Whelan S. 2009. Ribose 2=-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. http://dx.doi.org/10.1128/JVI.01426-09.
12. Poch O, Blumberg BM, Bougueleret L, Tordo N. 1990. Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol 71:1153-1162. http://dx.doi.org/10.1099/0022-1317-71-5-1153.
13. Johnson JE, Nasar F, Coleman JW, Price RE, Javadian A, Draper K, Lee M, Reilly PA, Clarke DK, Hendry RM, Udem S. 2007. Neurovirulence properties of recombinant vesicular stomatitis virus vectors in nonhuman primates. Virology 360:36-49. http://dx.doi.org/10.1016/j.virol.2006.10.026.
14. Hou YJ, Banerjee R, Thomas B, Nathan C, García-Sastre A, Ding A, Uccellini M. 2013. SARM is required for neuronal injury and cytokine production in response to central nervous system viral infection. J Immunol 191:875-883. http://dx.doi.org/10.4049/jimmunol.1300374.
15. Gutman GA, Hatfield G. 1989. Nonrandom utilization of codon pairs in Escherichia coli. Proc Natl Acad Sci U S A 86:3699-3703. http://dx.doi.org/10.1073/pnas.86.10.3699.
16. Hatfield GW, Gutman G. 1993. Codon pair utilization bias in bacteria, yeast and mammals, p 164-171. In Hatfield D, Lee BJ, Pirtle RM (ed), Transfer RNA in protein synthesis. CRC Press, Boca Raton, F.
17. Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S. 2008. Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784-1787. http://dx.doi.org/10.1126/science.1155761.
18. Mueller S, Coleman JR, Papamichail D, Ward CB, Nimnual A, Futcher B, Skiena S, Wimmer E. 2010. Live attenuated influenza virus vaccines by computer-aided rational design. Nat Biotechnol 28:723-726. http://dx.doi.org/10.1038/nbt.1636.
19. Yang C, Skiena S, Futcher B, Mueller S, Wimmer E. 2013. Deliberate reduction of hemagglutinin and neuraminidase expression of influenza virus leads to an ultraprotective live vaccine in mice. Proc Natl Acad Sci U S A 110:9481-9486. http://dx.doi.org/10.1073/pnas.1307473110.
20. Le Nouën C, Brock LG, Luongo C, McCarty T, Yang L, Mehedi M, Wimmer E, Mueller S, Collins PL, Buchholz UJ, DiNapoli J. 2014. Attenuation of human respiratory syncytial virus by genome-scale codonpair deoptimization. Proc Natl Acad Sci U S A 111:13169-13174. http://dx.doi.org/10.1073/pnas.1411290111.
21. Mueller S, Coleman JR, Wimmer E. 2009. Putting synthesis into biology: a viral view of genetic engineering through de novo gene and genome synthesis. Chem Biol 16:337-347. http://dx.doi.org/10.1016/j.chembiol.2009.03.002.
22. Combe M, Sanjuán R. 2014. Variation in RNA virus mutation rates across host cells. PLopS Pathog 10:e1003855. http://dx.doi.org/10.1371/journal.ppat.1003855.
23. Burns CC, Campagnoli R, Shaw J, Vincent A, Jorba J, Kew O. 2009. Genetic inactivation of poliovirus infectivity by increasing the frequencies of CpG and UpA dinucleotides within and across synonymous capsid region codons. J Virol 83:9957-9969. http://dx.doi.org/10.1128/JVI.00508-09.
24. Al-Saif M, Khabar K. 2012. UU/UA dinucleotide frequency reduction in coding regions results in increased mRNA stability and protein expression. Mol Ther 20:954-959. http://dx.doi.org/10.1038/mt.2012.29.
25. Chen CY, Shyu AB, 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20:465-470.
26. Song Y, Liu Y, Ward CB, Mueller S, Futcher B, Skiena S, Paul AV, Wimmer E. 2012. Identification of two functionally redundant RNA elements in the coding sequence of poliovirus using computer-generated design. Proc Natl Acad Sci U S A 109:14301-14307. http://dx.doi.org/10.1073/pnas.1211484109.
27. Whelan SP, Ball LA, Barr JN, Wertz G. 1995. Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc Natl Acad Sci U S A 92:8388-8392. http://dx.doi.org/10.1073/pnas.92.18.8388.
28. Canter DM, Perrault J. 1996. Stabilization of vesicular stomatitis virus L polymerase protein by P protein binding: a small deletion in the C-terminal domain of L abrogates binding. Virology 219:376-386. http://dx.doi.org/10.1006/viro.1996.0263.
29. Connor JH, McKenzie MO, Parks GD, Lyles D. 2007. Antiviral activity and RNA polymerase degradation following Hsp90 inhibition in a range of negative strand viruses. Virology 362:109-119. http://dx.doi.org/10.1016/j.virol.2006.12.026.
30. Ma Y, Wei Y, Zhang X, Zhang Y, Cai H, Zhu Y, Shilo K, Oglesbee M, Krakowka S, Whelan SP, Li J. 2014. MRNA cap methylation influences pathogenesis of vesicular stomatitis virus in vivo. J Virol 88:2913-2926. http://dx.doi.org/10.1128/JVI.03420-13.
31. Ozduman K, Wollmann G, Piepmeier JM, van den Pol A. 2008. Systemic vesicular stomatitis virus selectively destroys multifocal glioma and metastatic carcinoma in brain. J Neurosci 28:1882-1893. http://dx.doi.org/10.1523/JNEUROSCI.4905-07.2008.
32. Bi Z, Barna M, Komatsu T, Reiss C. 1995. Vesicular stomatitis virus infection of the central nervous system activates both innate and acquired immunity. J Virol 69:6466-6472.
33. Rahmeh AA, Schenk AD, Danek EI, Kranzusch PJ, Liang B, Walz T, Whelan S. 2010. Molecular architecture of the vesicular stomatitis virus RNA polymerase. Proc Natl Acad Sci U S A 107:20075-20080. http://dx.doi.org/10.1073/pnas.1013559107.
34. Alff-Steinberger C. 1987. Codon usage in Homo sapiens: evidence for a coding pattern on the non-coding strand and evolutionary implications of dinucleotide discrimination. J Theor Biol 124:89-95. http://dx.doi.org/10.1016/S0022-5193(87)80254-0.
35. Rima BK, McFerran N. 1997. Dinucleotide and stop codon frequencies in single-stranded RNA viruses. J Gen Virol 78:2859-2870.
36. Rothberg PG, Wimmer E. 1981. Mononucleotide and dinucleotide frequencies, and codon usage in poliovirion RNA. Nucleic Acids Res 9:6221-6229. http://dx.doi.org/10.1093/nar/9.23.6221.
37. Atkinson NJ, Witteveldt J, Evans DJ, Simmonds P. 2014. The influence of CpG and UpA dinucleotide frequencies on RNA virus replication and characterization of the innate cellular pathways underlying virus attenuation and enhanced replication. Nucleic Acids Res 42:4527-4545. http://dx.doi.org/10.1093/nar/gku075.
38. Liu WJ, Wang XJ, Clark DC, Lobigs M, Hall RA, Khromykh A. 2006. A single amino acid substitution in the West Nile virus nonstructural protein NS2A disables its ability to inhibit alpha/beta interferon induction and attenuates virus virulence in mice. J Virol 80:2396-2404. http://dx.doi.org/10.1128/JVI.80.5.2396-2404.2006.
39. Zhang G, Hubalewska M, Ignatova Z. 2009. Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat Struct Mol Biol 16:274-280. http://dx.doi.org/10.1038/nsmb.1554.
40. Pechmann S, Frydman J. 2013. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat Struct Mol Biol 20:237-243. http://dx.doi.org/10.1038/nsmb.2466.
41. Irwin B, Heck JD, Hatfield G. 1995. Codon pair utilization biases influence translational elongation step times. J Biol Chem 270: 22801-22806. http://dx.doi.org/10.1074/jbc.270.39.22801.
42. Jones SM, Feldmann H, Ströher U, Geisbert JB, Fernando L, Grolla A, Klenk HD, Sullivan NJ, Volchkov VE, Fritz EA, Daddario KM, Hensley LE, Jahrling PB, Geisbert T. 2005. Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses. Nat Med 11:786-790. http://dx.doi.org/10.1038/nm1258.
43. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, D.