Synonymous Virus Genome Recoding as a Tool to Impact Viral Fitness

Trends in Microbiology

Volumn 24, Issue 2, 2016, Pages 134-147

  Martínez, Miguel Angel ^a   Jordan Paiz, Ana ^a   Franco, Sandra ^a   Nevot, Maria ^a  

^a HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

Author keywords

Attenuation; Genome; Recoding; Synonymous; Synthetic; Virus

Indexed keywords

CHIKUNGUNYA VIRUS; CODING; CODON USAGE; DENGUE VIRUS; DNA SEQUENCE; ENTEROVIRUS B; GENE EXPRESSION REGULATION; GENE MUTATION; GENE STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN RESPIRATORY SYNCYTIAL VIRUS A; INFLUENZA VIRUS; INNATE IMMUNITY; NONHUMAN; PHENOTYPE; POLIOMYELITIS VIRUS; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; PRIORITY JOURNAL; REVIEW; RNA SEQUENCE; RNA VIRUS; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; SYNONYMOUS GENOME RECODING; TICK BORNE ENCEPHALITIS VIRUS; VESICULOVIRUS; VIRUS GENE; VIRUS GENOME; ANIMAL; GENETICS; HUMAN; MUTATION; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY; VIRUS; VIRUS INFECTION;

ANIMALS; GENOME, VIRAL; HUMANS; MUTATION; VIRUS DISEASES; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUSES;

EID: 84959181916     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.11.002     Document Type: Review

References (74)

1. Plotkin J.B., Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat. Rev. Genet. 2011, 12:32-42.
2. Hunt R.C., et al. Exposing synonymous mutations. Trends Genet. 2014, 30:308-321.
3. Grantham R., et al. Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res. 1980, 8:1893-1912.
4. Quax T.E., et al. Codon bias as a means to fine-tune gene expression. Mol. Cell 2015, 59:149-161.
5. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 1985, 2:13-34.
6. Warnecke T., et al. Why there is more to protein evolution than protein function: splicing, nucleosomes and dual-coding sequence. Biochem. Soc. Trans. 2009, 37:756-761.
7. Lin M.F., et al. Locating protein-coding sequences under selection for additional, overlapping functions in 29 mammalian genomes. Genome Res. 2011, 21:1916-1928.
8. Birnbaum R.Y., et al. Coding exons function as tissue-specific enhancers of nearby genes. Genome Res. 2012, 22:1059-1068.
9. Shabalina S.A., et al. A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res. 2006, 34:2428-2437.
10. Kudla G., et al. Coding-sequence determinants of gene expression in Escherichia coli. Science 2009, 324:255-258.
11. Presnyak V., et al. Codon optimality is a major determinant of mRNA stability. Cell 2015, 160:1111-1124.
12. Brest P., et al. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat. Genet. 2011, 43:242-245.
13. Pechmann S., Frydman J. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat. Struct. Mol. Biol. 2013, 20:237-243.
14. Stergachis A.B., et al. Exonic transcription factor binding directs codon choice and affects protein evolution. Science 2013, 342:1367-1372.
15. Weatheritt R.J., Babu M.M. Evolution. The hidden codes that shape protein evolution. Science 2013, 342:1325-1326.
16. Carr P.A., Church G.M. Genome engineering. Nat. Biotechnol. 2009, 27:1151-1162.
17. Kosuri S., Church G.M. Large-scale de novo DNA synthesis: technologies and applications. Nat. Methods 2014, 11:499-507.
18. Cello J., et al. Chemical synthesis of poliovirus cDNA: generation of infectious virus in the absence of natural template. Science 2002, 297:1016-1018.
19. Wimmer E., et al. Synthetic viruses: a new opportunity to understand and prevent viral disease. Nat. Biotechnol. 2009, 27:1163-1172.
20. Burns C.C., et al. Modulation of poliovirus replicative fitness in HeLa cells by deoptimization of synonymous codon usage in the capsid region. J. Virol. 2006, 80:3259-3272.
21. Mueller S., et al. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J. Virol. 2006, 80:9687-9696.
22. Aragones L., et al. Fine-tuning translation kinetics selection as the driving force of codon usage bias in the hepatitis A virus capsid. PLoS Pathog. 2010, 6:e1000797.
23. Meng J., et al. Refining the balance of attenuation and immunogenicity of respiratory syncytial virus by targeted codon deoptimization of virulence genes. MBio 2014, 5:e01704-e01714.
24. Nougairede A., et al. Random codon re-encoding induces stable reduction of replicative fitness of Chikungunya virus in primate and mosquito cells. PLoS Pathog. 2013, 9:e1003172.
25. de Fabritus L., et al. Attenuation of tick-borne encephalitis virus using large-scale random codon re-encoding. PLoS Pathog. 2015, 11:e1004738.
26. Coleman J.R., et al. Virus attenuation by genome-scale changes in codon pair bias. Science 2008, 320:1784-1787.
27. Mueller S., et al. Live attenuated influenza virus vaccines by computer-aided rational design. Nat. Biotechnol. 2010, 28:723-726.
28. Martrus G., et al. Changes in codon-pair bias of human immunodeficiency virus type 1 have profound effects on virus replication in cell culture. Retrovirology 2013, 10:78.
29. Yang C., et al. 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. 2013, 110:9481-9486.
30. Le Nouen C., et al. Attenuation of human respiratory syncytial virus by genome-scale codon-pair deoptimization. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:13169-13174.
31. Ni Y.Y., et al. Computer-aided codon-pairs deoptimization of the major envelope GP5 gene attenuates porcine reproductive and respiratory syndrome virus. Virology 2014, 450-451:132-139.
32. Wang B., et al. Recoding of the vesicular stomatitis virus L gene by computer-aided design provides a live, attenuated vaccine candidate. MBio 2015, 6:e00237-e315.
33. Shen S.H., et al. Large-scale recoding of an arbovirus genome to rebalance its insect versus mammalian preference. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:4749-4754.
34. Burns C.C., et al. Genetic inactivation of poliovirus infectivity by increasing the frequencies of CpG and UpA dinucleotides within and across synonymous capsid region codons. J. Virol. 2009, 83:9957-9969.
35. Atkinson N.J., et al. 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. 2014, 42:4527-4545.
36. Tulloch F., et al. RNA virus attenuation by codon pair deoptimisation is an artefact of increases in CpG/UpA dinucleotide frequencies. Elife 2014, 3:e04531.
37. Chen S.L., et al. Codon usage between genomes is constrained by genome-wide mutational processes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:3480-3485.
38. Plotkin J.B., et al. Tissue-specific codon usage and the expression of human genes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12588-12591.
39. Tats A., et al. Preferred and avoided codon pairs in three domains of life. BMC Genomics 2008, 9:463.
40. Moura G.R., et al. Species-specific codon context rules unveil non-neutrality effects of synonymous mutations. PLoS ONE 2011, 6:e26817.
41. Vabret N., et al. Large-scale nucleotide optimization of simian immunodeficiency virus reduces its capacity to stimulate type I interferon in vitro. J. Virol. 2014, 88:4161-4172.
42. Sitaraman V., et al. Computationally designed adeno-associated virus (AAV) Rep 78 is efficiently maintained within an adenovirus vector. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14294-14299.
43. Cladel N.M., et al. Synonymous codon changes in the oncogenes of the cottontail rabbit papillomavirus lead to increased oncogenicity and immunogenicity of the virus. Virology 2013, 438:70-83.
44. Mas A., et al. Unfinished stories on viral quasispecies and Darwinian views of evolution. J. Mol. Biol. 2010, 397:865-877.
45. Song Y., et al. Identification of two functionally redundant RNA elements in the coding sequence of poliovirus using computer-generated design. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:14301-14307.
46. Li M., et al. Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature 2012, 491:125-128.
47. Shin Y.C., et al. Importance of codon usage for the temporal regulation of viral gene expression. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:14030-14035.
48. Lauring A.S., et al. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 2012, 12:623-632.
49. Minor P.D. Attenuation and reversion of the Sabin vaccine strains of poliovirus. Dev. Biol. Stand. 1993, 78:17-26.
50. Gutman G.A., Hatfield G.W. Nonrandom utilization of codon pairs in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:3699-3703.
51. Wimmer E., Paul A.V. Synthetic poliovirus and other designer viruses: what have we learned from them?. Annu. Rev. Microbiol. 2011, 65:583-609.
52. Lauring A.S., et al. The role of mutational robustness in RNA virus evolution. Nat. Rev. Microbiol. 2013, 11:327-336.
53. Sitaraman V., et al. Synthetic sequence design for signal location search. Lect. Notes Comput. Sci. 2012, 7262:165-179.
54. Malim M.H., et al. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989, 338:254-257.
55. Kypr J., Mrazek J. Unusual codon usage of HIV. Nature 1987, 327:20.
56. Meintjes P.L., Rodrigo A.G. Evolution of relative synonymous codon usage in Human Immunodeficiency Virus type-1. J. Bioinform. Comput. Biol. 2005, 3:157-168.
57. Sohn W.J., et al. Novel transcriptional regulation of the schlafen-2 gene in macrophages in response to TLR-triggered stimulation. Mol. Immunol. 2007, 44:3273-3282.
58. Coleman J.R., et al. Designed reduction of Streptococcus pneumoniae pathogenicity via synthetic changes in virulence factor codon-pair bias. J. Infect. Dis. 2011, 203:1264-1273.
59. Dimaio D. Is virology dead?. MBio 2014, 5:e01003-e01014.
60. Weber W., Fussenegger M. Emerging biomedical applications of synthetic biology. Nat. Rev. Genet. 2011, 13:21-35.
61. Lienert F., et al. Synthetic biology in mammalian cells: next generation research tools and therapeutics. Nat. Rev. Mol. Cell Biol. 2014, 15:95-107.
62. Stemmer W.P., et al. Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides. Gene 1995, 164:49-53.
63. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.
64. Wright F. The 'effective number of codons' used in a gene. Gene 1990, 87:23-29.
65. Simmonds P. SSE: a nucleotide and amino acid sequence analysis platform. BMC Res. Notes 2012, 5:50.
66. Fan R.L., et al. Generation of live attenuated influenza virus by using codon usage bias. J. Virol. 2015, 89:10762-10773.
67. Chevance F.F., et al. The effects of codon context on in vivo translation speed. PLoS Genet. 2014, 10:e1004392.
68. Futcher B., et al. Reply to Simmonds et al.: Codon pair and dinucleotide bias have not been functionally distinguished. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:E3635-E3636.
69. Simmonds P., et al. Attenuation of dengue (and other RNA viruses) with codon pair recoding can be explained by increased CpG/UpA dinucleotide frequencies. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:E3633-E3634.
70. Rima B.K., McFerran N.V. Dinucleotide and stop codon frequencies in single-stranded RNA viruses. J. Gen. Virol. 1997, 78:2859-2870.
71. van der Kuyl A.C., Berkhout B. The biased nucleotide composition of the HIV genome: a constant factor in a highly variable virus. Retrovirology 2012, 9:92.
72. Kumagai Y., et al. TLR9 as a key receptor for the recognition of DNA. Adv. Drug Deliv. Rev. 2008, 60:795-804.
73. Simmonds P., et al. 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 2013, 14:610.
74. Hodgkinson A., Eyre-Walker A. Variation in the mutation rate across mammalian genomes. Nat. Rev. Genet. 2011, 12:756-766.