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 Research

Volumn 42, Issue 7, 2014, Pages 4527-4545

  Atkinson, Nicky J ^a   Witteveldt, Jeroen ^a   Evans, David J ^b   Simmonds, Peter ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; ADENOSINE DEAMINASE RNA SPECIFIC PROTEIN; DINUCLEOTIDE; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; ROSCOVITINE; UNCLASSIFIED DRUG; UPA DINUCLEOTIDE;

ADAPTIVE IMMUNITY; ARTICLE; CODON; CPG ISLAND; DNA BASE COMPOSITION; GENE CONSTRUCT; GENE FREQUENCY; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; NUCLEOTIDE SEQUENCE; PATTERN RECOGNITION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPLICON; REPORTER GENE; RNA ANALYSIS; RNA STRUCTURE; RNA VIRUS; SIGNAL TRANSDUCTION; VIRION; VIRUS ATTENUATION; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS REPLICATION;

BASE COMPOSITION; CELL LINE; DINUCLEOSIDE PHOSPHATES; ENTEROVIRUS B, HUMAN; GC RICH SEQUENCE; MUTATION; RNA, VIRAL; VIRUS REPLICATION;

EID: 84898943386     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku075     Document Type: Article

References (57)

1. Belsham, G.J. and Sonenberg, N. (1996) RNA-protein interactions in regulation of picornavirus RNA translation. Microbiol. Rev., 60, 499-511. (Pubitemid 26303476)
2. Goodfellow, I., Chaudhry, Y., Richardson, A., Meredith, J., Almond, J.W., Barclay, W. and Evans, D.J. (2000) Identification of a cis-acting replication element within the poliovirus coding region. J. Virol., 74, 4590-4600. (Pubitemid 30237884)
3. Tuplin, A., Wood, J., Evans, D.J., Patel, A.H. and Simmonds, P. (2002) Thermodynamic and phylogenetic prediction of RNA secondary structures in the coding region of hepatitis C virus. RNA, 8, 824-841. (Pubitemid 34620458)
4. Simmonds, P., Kakasiliotis, I., Chaudhry, Y., Evans, D.J. and Goodfellow, I.G. (2008) Bioinformatic and functional analysis of RNA secondary structure elements among different genera of human and animal caliciviruses. Nucleic Acids Res., 36, 2530-2546. (Pubitemid 351659569)
5. Belshaw, R., Pybus, O.G. and Rambaut, A. (2007) The evolution of genome compression and genomic novelty in RNA viruses. Genome Res., 17, 1496-1504. (Pubitemid 47529434)
6. Chen, W., Calvo, P.A., Malide, D., Gibbs, J., Schubert, U., Bacik, I., Basta, S., O'Neill, R., Schickli, J., Palese, P. et al. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med., 7, 1306-1312. (Pubitemid 34007934)
7. D'Andrea, L., Pinto, R.M., Bosch, A., Musto, H. and Cristina, J. (2011) A detailed comparative analysis on the overall codon usage patterns in hepatitis A virus. Virus Res., 157, 19-24.
8. Wright, F. (1990) The 'effective number of codons' used in a gene. Gene, 87, 23-29. (Pubitemid 20139850)
9. Puigbo, P., Bravo, I.G. and Garcia-Vallve, S. (2008) CAIcal: a combined set of tools to assess codon usage adaptation. Biol. Direct., 3, 38.
10. Simmonds, P., Xia, W., Baillie, J.K. and McKinnon, K. (2013) Modelling mutational and selection pressures on dinucleotides in eukaryotic phyla-selection against CpG and UpA in cytoplasmically expressed RNA and in RNA viruses. BMC Genomics, 14, 610.
11. Rima, B.K. and McFerran, N.V. (1997) Dinucleotide and stop codon frequencies in single-stranded RNA viruses. J. Gen. Virol., 78, 2859-2870. (Pubitemid 27480826)
12. Karlin, S., Doerfler, W. and Cardon, L.R. (1994) Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses? J. Virol., 68, 2889-2897. (Pubitemid 24129736)
13. Duret, L. and Galtier, N. (2000) The covariation between TpA deficiency, CpG deficiency, and G+C content of human isochores is due to a mathematical artifact. Mol. Biol. Evol., 17, 1620-1625.
14. Lobo, F.P., Mota, B.E., Pena, S.D., Azevedo, V., Macedo, A.M., Tauch, A., Machado, C.R. and Franco, G.R. (2009) Virus-host coevolution: common patterns of nucleotide motif usage in Flaviviridae and their hosts. PLoS One, 4, e6282.
15. Greenbaum, B.D., Rabadan, R. and Levine, A.J. (2009) Patterns of oligonucleotide sequences in viral and host cell RNA identify mediators of the host innate immune system. PLoS One, 4, e5969.
16. Greenbaum, B.D., Levine, A.J., Bhanot, G. and Rabadan, R. (2008) Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS. Pathog., 4, e1000079.
17. Burns, C.C., Campagnoli, R., Shaw, J., Vincent, A., Jorba, J. and 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.
18. Buchan, J.R., Aucott, L.S. and Stansfield, I. (2006) tRNA properties help shape codon pair preferences in open reading frames. Nucleic Acids Res., 34, 1015-1027. (Pubitemid 43380684)
19. Coleman, J.R., Papamichail, D., Skiena, S., Futcher, B., Wimmer, E. and Mueller, S. (2008) Virus attenuation by genome-scale changes in codon pair bias. Science, 320, 1784-1787. (Pubitemid 351931294)
20. Simmonds, P. (2012) SSE: a nucleotide and amino acid sequence analysis platform. BMC. Res. Notes, 5, 50.
21. Simmonds, P., Tuplin, A. and Evans, D.J. (2004) Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: Implications for virus evolution and host persistence. RNA, 10, 1337-1351. (Pubitemid 39122104)
22. Burge, C., Campbell, A.M. and Karlin, S. (1992) Over-and under-representation of short oligonucleotides in DNA sequences. Proc. Natl Acad. Sci. USA, 89, 1358-1362.
23. Simmen, M.W. (2008) Genome-scale relationships between cytosine methylation and dinucleotide abundances in animals. Genomics, 92, 33-40.
24. Samuel, C.E. (2011) Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology, 411, 180-193.
25. Hilton, L., Moganeradj, K., Zhang, G., Chen, Y.H., Randall, R.E., McCauley, J.W. and Goodbourn, S. (2006) The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J Virol., 80, 11723-11732. (Pubitemid 44788885)
26. Jammi, N.V., Whitby, L.R. and Beal, P.A. (2003) Small molecule inhibitors of the RNA-dependent protein kinase. Biochem. Biophys. Res. Commun., 308, 50-57. (Pubitemid 36904120)
27. Chen, H.M., Wang, L. and D'Mello, S.R. (2008) A chemical compound commonly used to inhibit PKR, {8-(imidazol-4-ylmethylene)-6H-azolidino[5, 4-g] benzothiazol-7-one}, protects neurons by inhibiting cyclin-dependent kinase. Eur. J. Neurosci., 28, 2003-2016.
28. Burns, C.C., Shaw, J., Campagnoli, R., Jorba, J., Vincent, A., Quay, J. and Kew, O. (2006) Modulation of poliovirus replicative fitness in HeLa cells by deoptimization of synonymous codon usage in the capsid region. J. Virol., 80, 3259-3272.
29. Mueller, S., Papamichail, D., Coleman, J.R., Skiena, S. and Wimmer, E. (2006) Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J. Virol., 80, 9687-9696. (Pubitemid 44435643)
30. Haller, A.A., Stewart, S.R. and Semler, B.L. (1996) Attenuation stem-loop lesions in the 5' noncoding region of poliovirus RNA: neuronal cell-specific translation defects. J. Virol., 70, 1467-1474.
31. Lauring, A.S., Frydman, J. and Andino, R. (2013) The role of mutational robustness in RNA virus evolution. Nat. Rev. Microbiol., 11, 327-336.
32. Sanjuan, R., Moya, A. and Elena, S.F. (2004) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc. Natl Acad. Sci. USA, 101, 8396-8401. (Pubitemid 38736586)
33. Cuevas, J.M., Domingo-Calap, P. and Sanjuan, R. (2012) The fitness effects of synonymous mutations in DNA and RNA viruses. Mol. Biol. Evol., 29, 17-20.
34. Lauring, A.S., Acevedo, A., Cooper, S.B. and Andino, R. (2012) Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host. Microbe., 12, 623-632.
35. Abdulhaqq, S.A. and Weiner, D.B. (2008) DNA vaccines: developing new strategies to enhance immune responses. Immunol. Res., 42, 219-232.
36. Wang, B., Xi, X., Lei, X., Zhang, X., Cui, S., Wang, J., Jin, Q. and Zhao, Z. (2013) Enterovirus 71 protease 2A(pro) targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog., 9, e1003231.
37. Lu, J., Yi, L., Zhao, J., Yu, J., Chen, Y., Lin, M.C., Kung, H.F. and He, M.L. (2012) Enterovirus 71 disrupts interferon signaling by reducing the level of interferon receptor 1. J. Virol., 86, 3767-3776.
38. Oshiumi, H., Okamoto, M., Fujii, K., Kawanishi, T., Matsumoto, M., Koike, S. and Seya, T. (2011) The TLR3/TICAM-1 pathway is mandatory for innate immune responses to poliovirus infection. J. Immunol., 187, 5320-5327.
39. Barral, P.M., Sarkar, D., Fisher, P.B. and Racaniello, V.R. (2009) RIG-I is cleaved during picornavirus infection. Virology, 391, 171-176.
40. Etchison, D., Milburn, S.C., Edery, I., Sonenberg, N. and Hershey, J.W. (1982) Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220, 000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J. Biol. Chem., 257, 14806-14810. (Pubitemid 13159573)
41. Qu, L., Feng, Z., Yamane, D., Liang, Y., Lanford, R.E., Li, K. and Lemon, S.M. (2011) Disruption of TLR3 signaling due to cleavage of TRIF by the hepatitis A virus protease-polymerase processing intermediate, 3CD. PLoS Pathog., 7, e1002169.
42. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S., Jung, A., Kawai, T., Ishii, K.J. et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature, 441, 101-105.
43. Pichlmair, A., Schulz, O., Tan, C.P., Rehwinkel, J., Kato, H., Takeuchi, O., Akira, S., Way, M., Schiavo, G. and Reis e Sousa, C. (2009) Activation of MDA5 requires higher-order RNA structures generated during virus infection. J. Virol., 83, 10761-10769.
44. Hornung, V., Ellegast, J., Kim, S., Brzozka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K.K., Schlee, M. et al. (2006) 5'-Triphosphate RNA is the ligand for RIG-I. Science, 314, 994-997.
45. Feng, Q., Hato, S.V., Langereis, M.A., Zoll, J., Virgen-Slane, R., Peisley, A., Hur, S., Semler, B.L., van Rij, R.P. and van Kuppeveld, F.J. (2012) MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep., 2, 1187-1196.
46. Meijer, L., Borgne, A., Mulner, O., Chong, J.P., Blow, J.J., Inagaki, N., Inagaki, M., Delcros, J.G. and Moulinoux, J.P. (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem., 243, 527-536. (Pubitemid 27060443)
47. Bach, S., Knockaert, M., Reinhardt, J., Lozach, O., Schmitt, S., Baratte, B., Koken, M., Coburn, S.P., Tang, L., Jiang, T. et al. (2005) Roscovitine targets, protein kinases and pyridoxal kinase. J. Biol. Chem., 280, 31208-31219. (Pubitemid 41291858)
48. Feuer, R., Mena, I., Pagarigan, R., Slifka, M.K. and Whitton, J.L. (2002) Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J. Virol., 76, 4430-4440. (Pubitemid 34309580)
49. Feuer, R. and Whitton, J.L. (2008) Preferential coxsackievirus replication in proliferating/activated cells: implications for virus tropism, persistence, and pathogenesis. Curr. Top. Microbiol. Immunol., 323, 149-173.
50. Wang, T., Yu, B., Lin, L., Zhai, X., Han, Y., Qin, Y., Guo, Z., Wu, S., Zhong, X., Wang, Y. et al. (2012) A functional nuclear localization sequence in the VP1 capsid protein of coxsackievirus B3. Virology, 433, 513-521.
51. Dalton, L.E., Healey, E., Irving, J. and Marciniak, S.J. (2012) Phosphoproteins in stress-induced disease. Prog. Mol. Biol. Transl. Sci., 106, 189-221.
52. Joshi, M., Kulkarni, A. and Pal, J.K. (2013) Small molecule modulators of eukaryotic initiation factor 2alpha kinases, the key regulators of protein synthesis. Biochimie, 95, 1980-1990.
53. Vabret, N., Bailly-Bechet, M., Najburg, V., Muller-Trutwin, M., Verrier, B. and Tangy, F. (2012) The biased nucleotide composition of HIV-1 triggers type I interferon response and correlates with subtype D increased pathogenicity. PLoS One, 7, e33502.
54. van der Kuyl, A.C. and Berkhout, B. (2012) The biased nucleotide composition of the HIV genome: a constant factor in a highly variable virus. Retrovirology, 9, 92.
55. Floyd-Smith, C., Slattery, E. and Lengyel, P. (1991) Interferon action: RNA cleavage pattern of a (29-59)oligoadenylate-dependent endonuclease. Science, 212, 1030-1032.
56. Han, J.Q. and Barton, D.J. (2002) Activation and evasion of the antiviral 2'-5' oligoadenylate synthetase/ribonuclease L pathway by hepatitis C virus mRNA. RNA, 8, 512-525. (Pubitemid 34437720)
57. Duan, J. and Antezana, M.A. (2003) Mammalian mutation pressure, synonymous codon choice, and mRNA degradation. J. Mol. Evol., 57, 694-701. (Pubitemid 37543983)