Hepatitis A virus adaptation to cellular shutoff is driven by dynamic adjustments of codon usage and results in the selection of populations with altered capsids

Journal of Virology

Volumn 88, Issue 9, 2014, Pages 5029-5041

  Isabel Costafreda, M ^a   Pérez Rodriguez, Francisco J ^a   D'Andrea, Lucía ^a   Guix, Susana ^a   Ribes, Enric ^a   Bosch, Albert ^a   Pintó, Rosa M ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AMINO ACID COMPOSITION; ANTIGENICITY; ARTICLE; CODON; CONTROLLED STUDY; HEPATITIS A VIRUS; HIGH TEMPERATURE; INTERNAL RIBOSOME ENTRY SITE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; POPULATION DYNAMICS; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS REPLICATION;

ADAPTATION, BIOLOGICAL; CAPSID PROTEINS; CODON; DNA MUTATIONAL ANALYSIS; HEPATITIS A VIRUS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84897526875     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00087-14     Document Type: Article

References (73)

1. Gingold H, Pilpel Y. 2011. Determinants of translation efficiency and accuracy. Mol. Syst. Biol. 7:481. http://dx.doi.org/10.1038/msb.2011.14.
2. Kramer G, Boehringer D, Ban N, Bukau B. 2009. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16:589-597. http://dx.doi.org/10.1038/nsmb.1614.
3. Komar AA. 2009. A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 34:16-24. http://dx.doi.org/10.1016/j.tibs.2008.10.002.
4. Plant EP, Nguyen P, Russ JR, Pittman YR, Nguyen T, Quesinberry JT, Kinzy TG, Dinman JD. 2007. Differentiating between near-and noncognate codons in Saccharomyces cerevisiae. PLoS One 2:e517. http://dx.doi.org/10.1371/journal.pone.0000517.
5. Kramer EB, Farabaugh PJ. 2007. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13:87-96. http://dx.doi.org/10.1261/rna.294907.
6. Zhou T, Weems M, Wilke CO. 2009. Translationally optimal codons associate with structurally sensitive sites in proteins. Mol. Biol. Evol. 26: 1571-1580. http://dx.doi.org/10.1093/molbev/msp070.
7. Zhang G, Ignatova Z. 2009. Generic algorithm to predict the speed of translational elongation: implications for protein biogenesis. PLoS One 4:e5036. http://dx.doi.org/10.1371/journal.pone.0005036.
8. Widmann M, Clairo M, Dippon J, Pleiss J. 2008. Analysis of the distribution of functionally relevant rare codons. BMC Genomics 9:207. http://dx.doi.org/10.1186/1471-2164-9-207.
9. Cooper GM, Brown CD. 2008. Qualifying the relationship between sequence conservation and molecular function. Genome Res. 18:201-205. http://dx.doi.org/10.1101/gr.7205808.
10. Zhang G, Ignatova Z. 2011. Folding at the birth of the nascent chain: coordinating translation with co-translational folding. Curr. Opin. Struct. Biol. 21:25-31. http://dx.doi.org/10.1016/j.sbi.2010.10.008.
11. 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.
12. Kimchi-Sarfaty C, Oh JM, Kim IW, Sauna ZE, Calcagno AM, Ambudkar SV, Gottesman MM. 2007. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315:525-528. http://dx.doi.org/10.1126/science.1135308.
13. Ali IK, McKendrick L, Morley SJ, Jackson RJ. 2001. Activity of the hepatitis A virus IRES requires association between the cap-binding translation initiation factor (eIF4E) and eIF4G. J. Virol. 75:7854-7863. http://dx.doi.org/10.1128/JVI.75.17.7854-7863.2001.
14. Whetter LE, Day SP, Elroystein O, Brown EA, Lemon SM. 1994. Low efficiency of the 5, nontranslated region of hepatitis A virus RNA in directing cap-independent translation in permissive monkey kidney cells. J. Virol. 68:5253-5263.
15. Sanchez G, Bosch A, Pintó RM. 2003. Genome variability and capsid structural constraints of hepatitis A virus. J. Virol. 77:452-459. http://dx.doi.org/10.1128/JVI.77.1.452-459.2003.
16. Pintó RM, Aragones L, Costafreda MI, Ribes E, Bosch A. 2007. Codon usage and replicative strategies of hepatitis A virus. Virus Res. 127:158-163. http://dx.doi.org/10.1016/j.virusres.2007.04.010.
17. Aragonès L, Guix S, Ribes E, Bosch A, Pintó RM. 2010. Fine-tuning translation kinetics selection as the driving force of codon usage bias in the hepatitis A virus capsid. PLoS Pathog. 6:e1000797. http://dx.doi.org/10.1371/journal.ppat.1000797.
18. Geller R, Vignuzzi M, Andino R, Frydman J. 2007. Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance. Genes Dev. 21:195-205. http://dx.doi.org/10.1101/gad.1505307.
19. Geller R, Taguwa S, Frydman J. 2012. Broad action of Hsp90 as a host chaperone required for viral replication. Biochim. Biophys. Acta 1823: 698-706. http://dx.doi.org/10.1016/j.bbamcr.2011.11.007.
20. Reich E, Franklin RM, Shatkin AJ, Tatumel. 1962. Action of actinomycin Don animal cells and viruses. Proc. Natl. Acad. Sci. U. S. A. 48:1238-1245. http://dx.doi.org/10.1073/pnas.48.7.1238.
21. Costafreda MI, Bosch A, Pintó RM. 2006. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Appl. Environ. Microbiol. 72:3846-3855. http://dx.doi.org/10.1128/AEM.02660-05.
22. Costafreda MI, Ribes E, Franch A, Bosch A, Pintó RM. 2012. A single mutation in the glycophorin A binding site of hepatitis A virus enhances virus clearance from the blood and results in a lower fitness variant. J. Virol. 86:7887-7895. http://dx.doi.org/10.1128/JVI.00707-12.
23. Pintó RM, Costafreda MI, Bosch A. 2009. Risk assessment in shellfishborne outbreaks of hepatitis A. Appl. Environ. Microbiol. 75:7350-7355. http://dx.doi.org/10.1128/AEM.01177-09.
24. Cromeans T, Sobsey MD, Fields HA. 1987. Development of a plaque assay for a cytopathic, rapidly replicating isolate of hepatitis A virus. J. Med. Virol. 22:45-56. http://dx.doi.org/10.1002/jmv.1890220107.
25. Bishop NE, Hugo DL, Borovec SV, Anderson DA. 1994. Rapid and efficient purification of hepatitis-A virus from cell-culture. J. Virol. Methods 47:203-216. http://dx.doi.org/10.1016/0166-0934(94)90078-7.
26. Ping LH, Lemon SM. 1992. Antigenic structure of human hepatitis A virus defined by analysis of escape mutants selected against murine monoclonal antibodies. J. Virol. 66:2208-2216.
27. Sanchez G, Aragonès L, Costafreda MI, Ribes E, Bosch A, Pintó RM. 2004. Capsid region involved in hepatitis a virus binding to glycophorin A of the erythrocyte membrane. J. Virol. 78:9807-9813. http://dx.doi.org/10.1128/JVI.78.18.9807-9813.2004.
28. Stapleton JT, Raina V, Winokur PL, Walters K, Klinzman D, Rosen E, McLinden JH. 1993. Antigenic and immunogenic properties of recombinant hepatitis A virus 14S and 70S subviral particles. J. Virol. 67:1080-1085.
29. Bosch A, Gonzalez-Dankaart JF, Haro I, Gajardo R, Perez JA, Pintó RM. 1998. A new continuous epitope of hepatitis A virus. J. Med. Virol. 54:95-102. http://dx.doi.org/10.1002/(SICI)1096-9071(199802)54:2<95 ::AID-JMV5>3.0.CO;2-J.
30. Lemon SM, Murphy PC, Shields PA, Ping LH, Feinstone SM, Cromeans T, Jansen RW. 1991. Antigenic and genetic variation in cytopathic hepatitis A virus variants arising during persistent infection: evidence for genetic recombination. J. Virol. 65:2056-2065.
31. Pintó RM, Guix S, Gonzalez-Dankaart JF, Caballero S, Sanchez G, Guo KJ, Ribes E, Bosch A. 2002. Hepatitis A virus polyprotein processing by Escherichia coli proteases. J. Gen. Virol. 83:359-368.
32. Crowther D, Melnick JL. 1961. The incorporation of neutral red and acridine orange into developing poliovirus particles making them photosensitive. Virology 14:11-21. http://dx.doi.org/10.1016/0042-6822(61) 90127-1.
33. dos Reis M, Savva R, Wernisch L. 2004. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 32:5036-5044. http://dx.doi.org/10.1093/nar/gkh834.
34. Sanchez G, Bosch A, Gomez-Mariano G, Domingo E, Pintó RM. 2003. Evidence for quasispecies distributions in the human hepatitis A virus genome. Virology 315:34-42. http://dx.doi.org/10.1016/S0042-6822(03) 00483-5.
35. Bosch A, Mueller S, Pintó RM. 2010. Codon biases and viral fitness, p 271-283. In Ehrenfeld E, Domingo E, Roos R (ed), The picornaviruses. ASM Press, Washington, DC.
36. Perales C, Martin V, Ruiz-Jarabo CM, Domingo E. 2005. Monitoring sequence space as a test for the target of selection in viruses. J. Mol. Biol. 345:451-459. http://dx.doi.org/10.1016/j.jmb.2004.10.066.
37. Grantham R, Gautier C, Gouy M. 1980. Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res. 8:1893-1912. http://dx.doi.org/10.1093/nar/8.9.1893.
38. Grantham R, Gautier C, Gouy M, Mercier R, Pave A. 1980. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 8:r49-r62.
39. Ma MR, Ha XQ, Ling H, Wang ML, Zhang FX, Zhang SD, Li G, Yan W. 2011. The characteristics of the synonymous codon usage in hepatitis B virus and the effects of host on the virus in codon usage pattern. Virol. J. 8:544. http://dx.doi.org/10.1186/1743-422X-8-544.
40. Jenkins GM, Pagel M, Gould EA, de A Zanotto PM, Holmes EC. 2001. Evolution of base composition and codon usage bias in the genus Flavivirus. J. Mol. Evol. 52:383-390. http://dx.doi.org/10.1007/s002390010168.
41. Jenkins GM, Holmes EC. 2003. The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Res. 92:1-7. http://dx.doi.org/10.1016/S0168-1702(02)00309-X.
42. Hu JS, Wang QQ, Zhang J, Chen HT, Xu ZW, Zhu L, Ding YZ, Ma LN, Xu K, Gu YX, Liu YS. 2011. The characteristic of codon usage pattern and its evolution of hepatitis C virus. Infect. Genet. Evol. 11:2098-2102. http://dx.doi.org/10.1016/j.meegid.2011.08.025.
43. Zhao KN, Chen J. 2011. Codon usage roles in human papillomavirus. Rev. Med. Virol. 21:397-411. http://dx.doi.org/10.1002/rmv.707.
44. Zhi N, Wan Z, Liu X, Wong S, Kim DJ, Young NS, Kajigaya S. 2010. Codon optimization of human parvovirus B19 capsid genes greatly increases their expression in nonpermissive cells. J. Virol. 84:13059-13062. http://dx.doi.org/10.1128/JVI.00912-10.
45. Karlin S, Blaisdell BE, Schachtel GA. 1990. Contrasts in codon usage of latent versus productive genes of Epstein-Barr virus: data and hypotheses. J. Virol. 64:4264-4273.
46. Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I. 1999. Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J. Virol. 73:4972-4982.
47. Cladel NM, Budgeon LR, Hu J, Balogh KK, Christensen ND. 2013. Synonymous codon changes in the oncogenes of the cottontail rabbit papillomavirus lead to increased oncogenicity and immunogenicity of the virus. Virology 438:70-83. http://dx.doi.org/10.1016/j.virol.2013.01.005.
48. Sugiyama T, Gursel M, Takeshita F, Coban C, Conover J, Kaisho T, Akira S, Klinman DM, Ishii KJ. 2005. CpG RNA: identification of novel single-strandedRNAthat stimulates human CD14+CD11c+monocytes. J. Immunol. 174:2273-2279.
49. Takeshita F, Gursel I, Ishii KJ, Suzuki K, Gursel M, Klinman DM. 2004. Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin. Immunol. 16:17-22. http://dx.doi.org/10.1016/j.smim.2003.10.009.
50. Hershberg R, Petrov DA. 2008. Selection on codon bias. Annu. Rev. Genet. 42:287-299. http://dx.doi.org/10.1146/annurev.genet.42.110807.091442.
51. D' Andrea L, Pintó RM, Bosch A, Musto H, Cristina J. 2011. A detailed comparative analysis on the overall codon usage patterns in hepatitis A virus. Virus Res. 157:19-24. http://dx.doi.org/10.1016/j.virusres.2011.01.012.
52. Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. 2008. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathog. 4:e1000079. http://dx.doi.org/10.1371/journal.ppat.1000079.
53. Pintó RM, D'Andrea L, Perez-Rodriguez FJ, Costafreda MI, Ribes E, Guix S, Bosch A. 2012. Hepatitis A virus evolution and the potential emergence of new variants escaping the presently available vaccines. Future Microbiol. 7:331-346. http://dx.doi.org/10.2217/fmb.12.5.
54. Scholz E, Heinricy U, Flehmig B. 1989. Acid stability of hepatitis A virus. J. Gen. Virol. 70:2481-2485. http://dx.doi.org/10.1099/0022-1317-70-9-2481.
55. Siegl G, Weitz M, Kronauer G. 1984. Stability of hepatitis A virus. Intervirology 22:218-226. http://dx.doi.org/10.1159/000149554.
56. Siegl G, Frosner GG, Gauss-Muller V, Tratschin JD, Deinhardt F. 1981. The physicochemical properties of infectious hepatitis A virions. J. Gen. Virol. 57:331-341. http://dx.doi.org/10.1099/0022-1317-57-2-331.
57. Domingo E, Sheldon J, Perales C. 2012. Viral quasispecies evolution. Microbiol. Mol. Biol. Rev. 76:159-216. http://dx.doi.org/10.1128/MMBR.05023-11.
58. Ruiz-Jarabo CM, Arias A, Baranowski E, Escarmis C, Domingo E. 2000. Memory in viral quasispecies. J. Virol. 74:3543-3547. http://dx.doi.org/10.1128/JVI.74.8.3543-3547.2000.
59. Ruiz-Jarabo CM, Arias A, Molina-Paris C, Briones C, Baranowski E, Escarmis C, Domingo E. 2002. Duration and fitness dependence of quasispecies memory. J. Mol. Biol. 315:285-296. http://dx.doi.org/10.1006/jmbi.2001.5232.
60. Burns CC, Shaw J, Campagnoli R, Jorba J, Vincent A, Quay J, 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. http://dx.doi.org/10.1128/JVI.80.7.3259-3272.2006.
61. Mueller S, Papamichail D, Coleman JR, Skiena S, 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. http://dx.doi.org/10.1128/JVI.00738-06.
62. Graci JD, Gnädig NF, Galarraga JE, Castro C, Vignuzzi M, Cameron CE. 2012. Mutational robustness of an RNA virus influences sensitivity to lethal mutagenesis. J. Virol. 86:2869-2873. http://dx.doi.org/10.1128/JVI.05712-11.
63. Konduru K, Kaplan GG. 2010. Determinants in 3Dpol modulate the rate of growth of hepatitis A virus. J. Virol. 84:8342-8347. http://dx.doi.org/10.1128/JVI.01470-09.
64. Bishop NE, Anderson DA. 2000. Uncoating kinetics of hepatitis A virus virions and provirions. J. Virol. 74:3423-3426. http://dx.doi.org/10.1128/JVI.74.7.3423-3426.2000.
65. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, Hogle JM. 2007. Imaging poliovirus entry in live cells. PLoS Biol. 5:e183. http://dx.doi.org/10.1371/journal.pbio.0050183.
66. 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.
67. Aragonès L, Bosch A, Pintó RM. 2008. Hepatitis A virus mutant spectra under the selective pressure of monoclonal antibodies: codon usage constraints limit capsid variability. J. Virol. 82:1688-1700. http://dx.doi.org/10.1128/JVI.01842-07.
68. Jimenez-Baranda S, Greenbaum B, Manches O, Handler J, Rabadan R, Levine A, Bhardwaj N. 2011. Oligonucleotide motifs that disappear during the evolution of influenza virus in humans increase alpha interferon secretion by plasmacytoid dendritic cells. J. Virol. 85:3893-3904. http://dx.doi.org/10.1128/JVI.01908-10.
69. Duan J, Antezana M. 2003. Mammalian mutation pressure, synonymous codon choice, and mRNA degradation. J. Mol. Evol. 57:694-701. http://dx.doi.org/10.1007/s00239-003-2519-1.
70. Lauring AS, Acevedo A, Cooper SB, Andino R. 2012. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12:623-632. http://dx.doi.org/10.1016/j.chom.2012.10.008.
71. Xu Y, Ma P, Shah P, Rokas A, Liu Y, Johnson CH. 2013. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 495:116-120. http://dx.doi.org/10.1038/nature11942.
72. Zhou M, Guo J, Cha J, Chae M, Chen S, Barral JM, Sachs MS, Liu Y. 2013. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 495:111-115. http://dx.doi.org/10.1038/nature11833.
73. Frenkel-Morgenstern M, Danon T, Christian T, Igarashi T, Cohen L, Hou YM, Jensen LJ. 2012. Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. Mol. Syst. Biol. 8:572. http://dx.doi.org/10.1038/msb.2012.3.