Cell Tropism Predicts Long-term Nucleotide Substitution Rates of Mammalian RNA Viruses
The high rates of RNA virus evolution are generally attributed to replication with error-prone RNA-dependent RNA polymerases. However, these long-term nucleotide substitution rates span three orders of magnitude and do not correlate well with mutation rates or selection pressures. This substitution rate variation may be explained by differences in virus ecology or intrinsic genomic properties. We generated nucleotide substitution rate estimates for mammalian RNA viruses and compiled comparable published rates, yielding a dataset of 118 substitution rates of structural genes from 51 different species, as well as 40 rates of non-structural genes from 28 species. Through ANCOVA analyses, we evaluated the relationships between these rates and four ecological factors: target cell, transmission route, host range, infection duration; and three genomic properties: genome length, genome sense, genome segmentation. Of these seven factors, we found target cells to be the only significant predictors of viral substitution rates, with tropisms for epithelial cells or neurons (P<0.0001) as the most significant predictors. Further, one-tailed t-tests showed that viruses primarily infecting epithelial cells evolve significantly faster than neurotropic viruses (P<0.0001 and P<0.001 for the structural genes and non-structural genes, respectively). These results provide strong evidence that the fastest evolving mammalian RNA viruses infect cells with the highest turnover rates: the highly proliferative epithelial cells. Estimated viral generation times suggest that epithelial-infecting viruses replicate more quickly than viruses with different cell tropisms. Our results indicate that cell tropism is a key factor in viral evolvability.
Vyšlo v časopise:
Cell Tropism Predicts Long-term Nucleotide Substitution Rates of Mammalian RNA Viruses. PLoS Pathog 10(1): e32767. doi:10.1371/journal.ppat.1003838
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003838
Souhrn
The high rates of RNA virus evolution are generally attributed to replication with error-prone RNA-dependent RNA polymerases. However, these long-term nucleotide substitution rates span three orders of magnitude and do not correlate well with mutation rates or selection pressures. This substitution rate variation may be explained by differences in virus ecology or intrinsic genomic properties. We generated nucleotide substitution rate estimates for mammalian RNA viruses and compiled comparable published rates, yielding a dataset of 118 substitution rates of structural genes from 51 different species, as well as 40 rates of non-structural genes from 28 species. Through ANCOVA analyses, we evaluated the relationships between these rates and four ecological factors: target cell, transmission route, host range, infection duration; and three genomic properties: genome length, genome sense, genome segmentation. Of these seven factors, we found target cells to be the only significant predictors of viral substitution rates, with tropisms for epithelial cells or neurons (P<0.0001) as the most significant predictors. Further, one-tailed t-tests showed that viruses primarily infecting epithelial cells evolve significantly faster than neurotropic viruses (P<0.0001 and P<0.001 for the structural genes and non-structural genes, respectively). These results provide strong evidence that the fastest evolving mammalian RNA viruses infect cells with the highest turnover rates: the highly proliferative epithelial cells. Estimated viral generation times suggest that epithelial-infecting viruses replicate more quickly than viruses with different cell tropisms. Our results indicate that cell tropism is a key factor in viral evolvability.
Zdroje
1. Holmes EC (2009) The evolution and emergence of RNA viruses. Oxford: Oxford University Press. 254 p.
2. Peters CJ (2007) Emerging viral diseases. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al.., editors. Fields Virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins. pp. 605–625.
3. World Health Organization (2012) Vaccine-preventable diseases. Available: http://www.who.int/immunization_monitoring/diseases/en/. Accessed 20 September 2012.
4. RheingansRD, AntilL, DreibelbisR, PodewilsLJ, BreseeJS, et al. (2009) Economic costs of rotavirus gastroenteritis and cost-effectiveness of vaccination in developing countries. J Infect Dis 200 Suppl 1: S16–27.
5. HanadaK, SuzukiY, GojoboriT (2004) A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Bio Evol 21: 1074–1080.
6. PerelsonAS (2002) Modelling viral and immune system dynamics. Nat Rev Immunol 2: 28–36.
7. GerrishPJ, Garcia-LermaJG (2003) Mutation rate and the efficacy of antimicrobial drug treatment. Lancet Infect Dis 3: 28–32.
8. DomingoE, MartinV, PeralesC, Grande-PerezA, Garcia-ArriazaJ, et al. (2006) Viruses as quasispecies: Biological implications. Curr Top Microbiol Immunol 299: 51–82.
9. LauringAS, AndinoR (2010) Quasispecies Theory and the Behavior of RNA Viruses. Plos Pathog 6(7): e1001005.
10. MoyaA, HolmesEC, Gonzalez-CandelasF (2004) The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol 2: 279–288.
11. VignuzziM, StoneJK, ArnoldJJ, CameronCE, AndinoR (2006) Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439: 344–348.
12. PybusOG, RambautA (2009) Evolutionary analysis of the dynamics of viral infectious disease. Nat Rev Genet 10: 540–550.
13. DuffyS, ShackeltonLA, HolmesEC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9: 267–276.
14. SanjuánR, NebotMR, ChiricoN, ManskyLM, BelshawR (2010) Viral mutation rates. J Virol 84: 9733–9748.
15. SanjuánR (2012) From molecular genetics to phylodynamics: evolutionary relevance of mutation rates across viruses. Plos Pathog 8: e1002685.
16. ChareER, HolmesEC (2004) Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol 85: 3149–3157.
17. JenkinsGM, RambautA, PybusOG, HolmesEC (2002) Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54: 156–165.
18. EigenM (1993) The origin of genetic information: viruses as models. Gene 135: 37–47.
19. BradwellK, CombeM, Domingo-CalapP, SanjuánR (2013) Correlation between mutation rate and genome size in riboviruses: mutation rate of bacteriophage qβ. Genetics 195: 243–251.
20. DrummondAJ, RambautA (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
21. HolmesEC (2009) The evolutionary genetics of emerging viruses. Annu Rev Ecol Evol Syst 40: 353–372.
22. HughesGJ, OrciariLA, RupprechtCE (2005) Evolutionary timescale of rabies virus adaptation to North American bats inferred from the substitution rate of the nucleoprotein gene. J Gen Virol 86: 1467–1474.
23. de la TorreJC, GiachettiC, SemlerBL, HollandJJ (1992) High frequency of single-base transitions and extreme frequency of precise multiple-base reversion mutations in poliovirus. Proc Natl Acad Sci U S A 89: 2531–2535.
24. de la TorreJC, WimmerE, HollandJJ (1990) Very high frequency of reversion to guanidine resistance in clonal pools of guanidine-dependent type 1 poliovirus. J Virol 64: 664–671.
25. CuevasJM, Gonzalez-CandelasF, MoyaA, SanjuánR (2009) Effect of ribavirin on the mutation rate and spectrum of hepatitis C virus in vivo. J Virol 83: 5760–5764.
26. NobusawaE, SatoK (2006) Comparison of the mutation rates of human influenza A and B viruses. J Virol 80: 3675–3678.
27. ParvinJD, MosconaA, PanWT, LeiderJM, PaleseP (1986) Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1. J Virol 59: 377–383.
28. StechJ, XiongX, ScholtissekC, WebsterRG (1999) Independence of evolutionary and mutational rates after transmission of avian influenza viruses to swine. J Virol 73: 1878–1884.
29. SedivyJM, CaponeJP, RajBhandaryUL, SharpPA (1987) An inducible mammalian amber suppressor: propagation of a poliovirus mutant. Cell 50: 379–389.
30. ZhangX, RennickLJ, DuprexWP, RimaBK (2013) Determination of spontaneous mutation frequencies in measles virus under nonselective conditions. J Virol 87: 2686–2692.
31. SchragSJ, RotaPA, BelliniWJ (1999) Spontaneous mutation rate of measles virus: direct estimation based on mutations conferring monoclonal antibody resistance. J Virol 73: 51–54.
32. SuarezP, ValcarcelJ, OrtinJ (1992) Heterogeneity of the mutation rates of influenza A viruses: isolation of mutator mutants. J Virol 66: 2491–2494.
33. QianXM, ShenQ, GoderieSK, HeWL, CapelaA, et al. (2000) Timing of CNS cell generation: A programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28: 69–80.
34. van der FlierLG, CleversH (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241–260.
35. SavageVM, AllenAP, BrownJH, GilloolyJF, HermanAB, et al. (2007) Scaling of number, size, and metabolic rate of cells with body size in mammals. Proc Natl Acad Sci U S A 104: 4718–4723.
36. ShorterRG, TitusJL, DivertieMB (1964) Cell Turnover in the Respiratory Tract. Dis Chest 46: 138–142.
37. StreickerDG, LemeyP, Velasco-VillaA, RupprechtCE (2012) Rates of viral evolution are linked to host geography in bat rabies. Plos Pathog 8: e1002720.
38. Maljkovic BerryI, RibeiroR, KothariM, AthreyaG, DanielsM, et al. (2007) Unequal evolutionary rates in the human immunodeficiency virus type 1 (HIV-1) pandemic: the evolutionary rate of HIV-1 slows down when the epidemic rate increases. J Virol 81: 10625–10635.
39. Virgin S (2007) Pathogenesis of viral infection. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al.., editors. Fields Virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins. pp. 327–388.
40. Lemon SM, Walker C, Alter M, Yi M (2007) Hepatitis C virus. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al.., editors. Fields Virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins. pp. 1253–1304.
41. WoelkCH, HolmesEC (2002) Reduced positive selection in vector-borne RNA viruses. Mol Bio Evol 19: 2333–2336.
42. CoffeyLL, VasilakisN, BraultAC, PowersAM, TripetF, et al. (2008) Arbovirus evolution in vivo is constrained by host alternation. Proc Natl Acad Sci U S A 105: 6970–6975.
43. WeaverSC, BraultAC, KangW, HollandJJ (1999) Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73: 4316–4326.
44. HicksAL, DuffyS (2011) Genus-specific substitution rate variability among picornaviruses. J Virol 85: 7942–7947.
45. HoSYW, LanfearR, BromhamL, PhillipsMJ, SoubrierJ, et al. (2011) Time dependent rates of molecular evolution. Mol Ecol 20: 3087–3101.
46. PybusOG, RambautA, BelshawR, FreckletonRP, DrummondAJ, et al. (2007) Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol Bio Evol 24: 845–852.
47. WertheimJO, Kosakovsky PondSL (2011) Purifying selection can obscure the ancient age of viral lineages. Mol Bio Evol 28: 3355–3365.
48. GreeneIP, WangE, DeardorffER, MilleronR, DomingoE, et al. (2005) Effect of alternating passage on adaptation of sindbis virus to vertebrate and invertebrate cells. J Virol 79: 14253–14260.
49. HolmesEC (2003) Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J Virol 77: 11296–11298.
50. FredericoLA, KunkelTA, ShawBR (1990) A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 29: 2532–2537.
51. HoltzCM, ManskyLM (2013) Variation of HIV-1 mutation spectra among cell types. J Virol 87: 5296–5299.
52. SalemiM, LewisM, EganJF, HallWW, DesmyterJ, et al. (1999) Different population dynamics of human T cell lymphotropic virus type II in intravenous drug users compared with endemically infected tribes. Proc Natl Acad Sci U S A 96: 13253–13258.
53. VandammeAM, BertazzoniU, SalemiM (2000) Evolutionary strategies of human T-cell lymphotropic virus type II. Gene 261: 171–180.
54. MiddelboeM (2000) Bacterial Growth Rate and Marine Virus-Host Dynamics. Microb Ecol 40: 114–124.
55. RabinovitchA, FishovI, HadasH, EinavM, ZaritskyA (2002) Bacteriophage T4 development in Escherichia coli is growth rate dependent. J Theor Biol 216: 1–4.
56. ScholleF, LiK, BodolaF, IkedaM, LuxonBA, et al. (2004) Virus-host cell interactions during hepatitis C virus RNA replication: impact of polyprotein expression on the cellular transcriptome and cell cycle association with viral RNA synthesis. J Virol 78: 1513–1524.
57. FeuerR, WhittonJL (2008) Preferential coxsackievirus replication in proliferating/activated cells: implications for virus tropism, persistence, and pathogenesis. Curr Top Microbiol Immunol 323: 149–173.
58. HondaM, KanekoS, MatsushitaE, KobayashiK, AbellGA, et al. (2000) Cell cycle regulation of hepatitis C virus internal ribosomal entry site-directed translation. Gastroenterology 118: 152–162.
59. NelsonHB, TangH (2006) Effect of cell growth on hepatitis C virus (HCV) replication and a mechanism of cell confluence-based inhibition of HCV RNA and protein expression. J Virol 80: 1181–1190.
60. KusovYY, GosertR, Gauss-MullerV (2005) Replication and in vivo repair of the hepatitis A virus genome lacking the poly(A) tail. J Gen Virol 86: 1363–1368.
61. FeuerR, MenaI, PagariganR, SlifkaMK, WhittonJL (2002) Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 76: 4430–4440.
62. KaminskiA, HuntSL, PattonJG, JacksonRJ (1995) Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA 1: 924–938.
63. MarshmanE, BoothC, PottenCS (2002) The intestinal epithelial stem cell. Bioessays 24: 91–98.
64. BhardwajRD, CurtisMA, SpaldingKL, BuchholzBA, FinkD, et al. (2006) Neocortical neurogenesis in humans is restricted to development. Pro Natl Acad Sci USA 103: 12564–12568.
65. CiarletM, SchodelF (2009) Development of a rotavirus vaccine: clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine, RotaTeq. Vaccine 27 Suppl 6: G72–81.
66. ZhangD, LuJ (2010) Enterovirus 71 vaccine: close but still far. Int J Infect Dis 14: e739–743.
67. HayAJ, GregoryV, DouglasAR, LinYP (2001) The evolution of human influenza viruses. Phil Trans R Soc B 356: 1861–1870.
68. BullRA, EdenJS, RawlinsonWD, WhitePA (2010) Rapid evolution of pandemic noroviruses of the GII.4 lineage. Plos Pathog 6: e1000831.
69. NgKK, ArnoldJJ, CameronCE (2008) Structure-function relationships among RNA-dependent RNA polymerases. Curr Top Microbiol Immunol 320: 137–156.
70. ChongYL, PadhiA, HudsonPJ, PossM (2010) The effect of vaccination on the evolution and population dynamics of avian paramyxovirus-1. Plos Pathog 6: e1000872.
71. FirthC, TokarzR, SimithDB, NunesMR, BhatM, et al. (2012) Diversity and distribution of hantaviruses in South America. J Virol 86: 13756–13766.
72. SwitzerWM, SalemiM, ShanmugamV, GaoF, CongME, et al. (2005) Ancient co-speciation of simian foamy viruses and primates. Nature 434: 376–380.
73. RobinsonM, GouyM, GautierC, MouchiroudD (1998) Sensitivity of the relative655 rate test to taxonomic sampling. Mol Bio Evol 15: 1091–1098.
74. HeathTA, HedtkeSM, HillisDM (2008) Taxon sampling and the accuracy of phylogenetic analyses. J Syst Evol 46: 239–257.
75. DuffyS, HolmesEC (2009) Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. J Gen Virol 90: 1539–1547.
76. FirthC, KitchenA, ShapiroB, SuchardMA, HolmesEC, et al. (2010) Using time-structured data to estimate evolutionary rates of double-stranded DNA viruses. Mol Bio Evol 27: 2038–2051.
77. HicksAL, DuffyS (2012) One misdated sequence of rabbit hemorrhagic disease virus prevents accurate estimation of its nucleotide substitution rate. BMC Evol Biol 12: 74.
78. ChenRB, HolmesEC (2006) Avian influenza virus exhibits rapid evolutionary dynamics. Mol Bio Evol 23: 2336–2341.
79. AraujoJMG, NogueiraRMR, SchatzmayrHG, ZanottoPMD, BelloG (2009) Phylogeography and evolutionary history of dengue virus type 3. Infection Genetics and Evolution 9: 716–725.
80. PadhiA, VergheseB (2008) Positive natural selection in the evolution of human metapneumovirus attachment glycoprotein. Virus Res 131: 121–131.
81. TullyDC, FaresMA (2008) The tale of a modern animal plague: Tracing the evolutionary history and determining the time-scale for foot and mouth disease virus. Virology 382: 250–256.
82. Rambaut A (2002) Se-Al: sequence alignment editor, version 2.0a11. Available: http://tree.bio.ed.ac.uk/software/seal/. Accessed 12 September 2009.
83. MartinDP, LemeyP, LottM, MoultonV, PosadaD, et al. (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26: 2462–2463.
84. PosadaD, CrandallKA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817–818.
85. Rambaut A, Drummond AJ (2009) Tracer, version 1.5: MCMC trace analyses tool. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 1 December 2009.
86. PondSL, FrostSD (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531–2533.
87. R Development Core Team (2011) R: A language and environment for statistical computing, version 2.14.1. Vienna, AT: R Foundation for Statistical Computing.
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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