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Influenza Virus Drug Resistance: A Time-Sampled Population Genetics Perspective


The challenge of distinguishing genetic drift from selection remains a central focus of population genetics. Time-sampled data may provide a powerful tool for distinguishing these processes, and we here propose approximate Bayesian, maximum likelihood, and analytical methods for the inference of demography and selection from time course data. Utilizing these novel statistical and computational tools, we evaluate whole-genome datasets of an influenza A H1N1 strain in the presence and absence of oseltamivir (an inhibitor of neuraminidase) collected at thirteen time points. Results reveal a striking consistency amongst the three estimation procedures developed, showing strongly increased selection pressure in the presence of drug treatment. Importantly, these approaches re-identify the known oseltamivir resistance site, successfully validating the approaches used. Enticingly, a number of previously unknown variants have also been identified as being positively selected. Results are interpreted in the light of Fisher's Geometric Model, allowing for a quantification of the increased distance to optimum exerted by the presence of drug, and theoretical predictions regarding the distribution of beneficial fitness effects of contending mutations are empirically tested. Further, given the fit to expectations of the Geometric Model, results suggest the ability to predict certain aspects of viral evolution in response to changing host environments and novel selective pressures.


Vyšlo v časopise: Influenza Virus Drug Resistance: A Time-Sampled Population Genetics Perspective. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004185
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004185

Souhrn

The challenge of distinguishing genetic drift from selection remains a central focus of population genetics. Time-sampled data may provide a powerful tool for distinguishing these processes, and we here propose approximate Bayesian, maximum likelihood, and analytical methods for the inference of demography and selection from time course data. Utilizing these novel statistical and computational tools, we evaluate whole-genome datasets of an influenza A H1N1 strain in the presence and absence of oseltamivir (an inhibitor of neuraminidase) collected at thirteen time points. Results reveal a striking consistency amongst the three estimation procedures developed, showing strongly increased selection pressure in the presence of drug treatment. Importantly, these approaches re-identify the known oseltamivir resistance site, successfully validating the approaches used. Enticingly, a number of previously unknown variants have also been identified as being positively selected. Results are interpreted in the light of Fisher's Geometric Model, allowing for a quantification of the increased distance to optimum exerted by the presence of drug, and theoretical predictions regarding the distribution of beneficial fitness effects of contending mutations are empirically tested. Further, given the fit to expectations of the Geometric Model, results suggest the ability to predict certain aspects of viral evolution in response to changing host environments and novel selective pressures.


Zdroje

1. ThompsonWW, ShayDK, WeintraubE, BrammerL, CoxN, et al. (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289: 179–186.

2. YuH, CowlingBJ, FengL, LauEH, LiaoQ, et al. (2013) Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet

3. NelsonMI, HolmesEC (2007) The evolution of epidemic influenza. Nature Reviews Genetics 8: 196–205.

4. KuikenT, HolmesEC, McCauleyJ, RimmelzwaanGF, WilliamsCS, et al. (2006) Host species barriers to influenza virus infections. Science 312: 394–397.

5. 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.

6. PaleseP, YoungJF (1982) Variation of influenza A, B, and C viruses. Science 215: 1468–1474.

7. NelsonMI, SimonsenL, ViboudC, MillerMA, TaylorJ, et al. (2006) Stochastic processes are key determinants of short-term evolution in influenza a virus. PLoS Pathog 2: e125.

8. TaubenbergerJK, KashJC (2010) Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7: 440–451.

9. MosconaA (2005) Oseltamivir resistance–disabling our influenza defenses. N Engl J Med 353: 2633–2636.

10. CollinsPJ, HaireLF, LinYP, LiuJ, RussellRJ, et al. (2008) Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453: 1258–1261.

11. IvesJAL, CarrJA, MendelDB, TaiCY, LambkinR, et al. (2002) The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo. Antiviral Res 55: 307–317.

12. GhedinE, HolmesEC, DePasseJV, PinillaLT, FitchA, et al. (2012) Presence of oseltamivir-resistant pandemic A/H1N1 minor variants before drug therapy with subsequent selection and transmission. J Infect Dis 206: 1504–1511.

13. GubarevaLV, KaiserL, MatrosovichMN, Soo-HooY, HaydenFG (2001) Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J Infect Dis 183: 523–531.

14. MosconaA (2009) Global transmission of oseltamivir-resistant influenza. N Engl J Med 360: 953–956.

15. BloomJD, GongLI, BaltimoreD (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272–1275.

16. BouvierNM, RahmatS, PicaN (2012) Enhanced mammalian transmissibility of seasonal influenza A/H1N1 viruses encoding an oseltamivir-resistant neuraminidase. J Virol 86: 7268–7279.

17. GintingTE, ShinyaK, KyanY, MakinoA, MatsumotoN, et al. (2012) Amino acid changes in hemagglutinin contribute to the replication of oseltamivir-resistant H1N1 influenza viruses. J Virol 86: 121–127.

18. WrightS (1931) Evolution in Mendelian Populations. Genetics 16: 97–159.

19. KimuraM, OhtaT (1969) The Average Number of Generations until Fixation of a Mutant Gene in a Finite Population. Genetics 61: 763–771.

20. CrisciJL, PohY-P, BeanA, SimkinA, JensenJD (2012) Recent progress in polymorphism-based population genetic inference. J Hered 103: 287–296.

21. NeiM (1973) Analysis of Gene Diversity in Subdivided Populations. Proc Natl Acad Sci U S A 70: 3321–3323.

22. KrimbasCB, TsakasS (1971) The Genetics of Dacus oleae. V. Changes of Esterase Polymorphism in a Natural Population Following Insecticide Control-Selection or Drift? Evolution 25: 454–460.

23. PamiloP, Varvio-AhoSL (1980) On the estimation of population size from allele frequency changes. Genetics 95: 1055–1057.

24. NeiM, TajimaF (1981) Genetic drift and estimation of effective population size. Genetics 98: 625–640.

25. WaplesRS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121: 379–391.

26. WilliamsonEG, SlatkinM (1999) Using maximum likelihood to estimate population size from temporal changes in allele frequencies. Genetics 152: 755–761.

27. BerthierP, BeaumontMA, CornuetJ-M, LuikartG (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics 160: 741–751.

28. AndersonEC, WilliamsonEG, ThompsonEA (2000) Monte Carlo evaluation of the likelihood for Ne from temporally spaced samples. Genetics 156: 2109–2118.

29. AndersonEC (2005) An Efficient Monte Carlo Method for Estimating Ne From Temporally Spaced Samples Using a Coalescent-Based Likelihood. Genetics 170: 955–967.

30. JordePE, RymanN (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177: 927–935.

31. BollbackJP, YorkTL, NielsenR (2008) Estimation of 2Nes from temporal allele frequency data. Genetics 179: 497–502.

32. MalaspinasA-S, MalaspinasO, EvansSN, SlatkinM (2012) Estimating allele age and selection coefficient from time-serial data. Genetics 192: 599–607.

33. MathiesonI, McVeanG (2013) Estimating selection coefficients in spatially structured populations from time series data of allele frequencies. Genetics 193: 973–984.

34. Durrett R (2008) Probability models for DNA sequence evolution. New York: Springer.

35. GoldringerI, BataillonT (2004) On the distribution of temporal variations in allele frequency: consequences for the estimation of effective population size and the detection of loci undergoing selection. Genetics 168: 563–568.

36. SunnåkerM, WodakS, BusettoAG, NumminenE, CoranderJ, et al. (2013) Approximate Bayesian Computation. PLoS Comput Biol 9: e1002803.

37. GrasslyNC, HarveyPH, HolmesEC (1999) Population dynamics of HIV-1 inferred from gene sequences. Genetics 151: 427–438.

38. de SilvaE, FergusonNM, FraserC (2012) Inferring pandemic growth rates from sequence data. J R Soc Interface 9: 1797–1808.

39. RenzetteN, GibsonL, BhattacharjeeB, FisherD, SchleissMR, et al. (2013) Rapid Intrahost Evolution of Human Cytomegalovirus Is Shaped by Demography and Positive Selection. PLoS Genet 9: e1003735.

40. CrowJF, DennistonC (1988) Inbreeding and Variance Effective Population Numbers. Evolution 42: 482–495.

41. ThangavelRR, ReedA, NorcrossEW, DixonSN, MarquartME, et al. (2011) “Boom” and “Bust” cycles in virus growth suggest multiple selective forces in influenza a evolution. Virol J 8: 180.

42. StraySJ, AirGM (2001) Apoptosis by influenza viruses correlates with efficiency of viral mRNA synthesis. Virus Res 77: 3–17.

43. BeaumontMA, BaldingDJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13: 969–980.

44. BaoY, BolotovP, DernovoyD, KiryutinB, ZaslavskyL, et al. (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82: 596–601.

45. EwensWJ (1967) The probability of survival of a new mutant in a fluctuating environment. Heredity (Edinb) 22: 438–443.

46. HeC-Q, DingN-Z, MouX, XieZ-X, SiH-L, et al. (2012) Identification of three H1N1 influenza virus groups with natural recombinant genes circulating from 1918 to 2009. Virology 427: 60–66.

47. BartonNH (2000) Genetic hitchhiking. Philos Trans R Soc Lond B Biol Sci 355: 1553–1562.

48. StrelkowaN, LässigM (2012) Clonal interference in the evolution of influenza. Genetics 192: 671–682.

49. MillerCR, JoyceP, WichmanHA (2011) Mutational effects and population dynamics during viral adaptation challenge current models. Genetics 187: 185–202.

50. Fisher RA (1930) The Genetical Theory Of Natural Selection. At The Clarendon Press.

51. EfronB (1987) Better Bootstrap Confidence Intervals. Journal of the American Statistical Association 82: 171–185.

52. MartinG, LenormandT (2006) A general multivariate extension of Fisher's geometrical model and the distribution of mutation fitness effects across species. Evolution 60: 893–907.

53. MartinG, LenormandT (2008) The Distribution of Beneficial and Fixed Mutation Fitness Effects Close to an Optimum. Genetics 179: 907–916.

54. BeiselCJ, RokytaDR, WichmanHA, JoyceP (2007) Testing the extreme value domain of attraction for distributions of beneficial fitness effects. Genetics 176: 2441–2449.

55. OrrHA (2006) The distribution of fitness effects among beneficial mutations in Fisher's geometric model of adaptation. J Theor Biol 238: 279–285.

56. KassenR, BataillonT (2006) Distribution of fitness effects among beneficial mutations before selection in experimental populations of bacteria. Nat Genet 38: 484–488.

57. MacLeanRC, BucklingA (2009) The distribution of fitness effects of beneficial mutations in Pseudomonas aeruginosa. PLoS Genet 5: e1000406.

58. RokytaDR, BeiselCJ, JoyceP, FerrisMT, BurchCL, et al. (2008) Beneficial fitness effects are not exponential for two viruses. J Mol Evol 67: 368–376.

59. BataillonT, ZhangT, KassenR (2011) Cost of adaptation and fitness effects of beneficial mutations in Pseudomonas fluorescens. Genetics 189: 939–949.

60. BarrettRDH, MacLeanRC, BellG (2006) Mutations of intermediate effect are responsible for adaptation in evolving Pseudomonas fluorescens populations. Biol Lett 2: 236–238.

61. RozenDE, de VisserJAGM, GerrishPJ (2002) Fitness effects of fixed beneficial mutations in microbial populations. Current Biology 12: 1040–1045.

62. NewtonMA, RafteryAE (1994) Approximate Bayesian Inference with the Weighted Likelihood Bootstrap. Journal of the Royal Statistical Society. Series B (Methodological) 56: 3–48.

63. BankC, HietpasRT, WongA, BolonDNA, JensenJD (2014) A Bayesian MCMC approach to assess the complete distribution of fitness effects of new mutations: uncovering the potential for adaptive walks in challenging environments. Genetics [Epub ahead of print].

64. HietpasRT, BankC, JensenJD, BolonDNA (2013) Shifting fitness landscapes in response to altered environments. Evolution 67: 3512–3522.

65. ShaB, LuoM (1997) Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat Struct Biol 4: 239–244.

66. ArztS, BaudinF, BargeA, TimminsP, BurmeisterWP, et al. (2001) Combined results from solution studies on intact influenza virus M1 protein and from a new crystal form of its N-terminal domain show that M1 is an elongated monomer. Virology 279: 439–446.

67. KoernerI, MatrosovichMN, HallerO, StaeheliP, KochsG (2012) Altered receptor specificity and fusion activity of the haemagglutinin contribute to high virulence of a mouse-adapted influenza A virus. Journal of General Virology 93: 970–979.

68. DanielsRS, DownieJC, HayAJ, KnossowM, SkehelJJ, et al. (1985) Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40: 431–439.

69. SteinhauerDA, MartínJ, LinYP, WhartonSA, OldstoneMB, et al. (1996) Studies using double mutants of the conformational transitions in influenza hemagglutinin required for its membrane fusion activity. Proceedings of the National Academy of Sciences of the United States of America 93: 12873–12878.

70. EnamiM, EnamiK (1996) Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. J Virol 70: 6653–6657.

71. JinH, LeserGP, ZhangJ, LambRA (1997) Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J 16: 1236–1247.

72. RossmanJS, LambRA (2011) Influenza virus assembly and budding. Virology 411: 229–236.

73. NotonSL, MedcalfE, FisherD, MullinAE, EltonD, et al. (2007) Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol 88: 2280–2290.

74. ReedML, YenH-L, DuBoisRM, BridgesOA, SalomonR, et al. (2009) Amino acid residues in the fusion peptide pocket regulate the pH of activation of the H5N1 influenza virus hemagglutinin protein. J Virol 83: 3568–3580.

75. ThoennesS, LiZ-N, LeeB-J, LangleyWA, SkehelJJ, et al. (2008) Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology 370: 403–414.

76. SriwilaijaroenN, SuzukiY (2012) Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad Ser B Phys Biol Sci 88: 226–249.

77. LinYP, WhartonSA, MartínJ, SkehelJJ, WileyDC, et al. (1997) Adaptation of egg-grown and transfectant influenza viruses for growth in mammalian cells: selection of hemagglutinin mutants with elevated pH of membrane fusion. Virology 233: 402–410.

78. IlyushinaNA, GovorkovaEA, RussellCJ, HoffmannE, WebsterRG (2007) Contribution of H7 haemagglutinin to amantadine resistance and infectivity of influenza virus. J Gen Virol 88: 1266–1274.

79. RenzetteN, CaffreyDR, ZeldovichKB, LiuP, GallagherGR, et al. (2014) Evolution of the influenza A virus genome during development of oseltamivir resistance in vitro. J Virol 88: 272–81.

80. BazinE, DawsonKJ, BeaumontMA (2010) Likelihood-free inference of population structure and local adaptation in a Bayesian hierarchical model. Genetics 185: 587–602.

81. RubinDB (1981) The Bayesian Bootstrap. The Annals of Statistics 9: 130–134.

82. HallP (1985) Resampling a coverage pattern. Stochastic Processes and their Applications 20: 231–246.

83. Ewens WJ (2004) Mathematical population genetics : theoretical introduction. New York: Springer.

84. NelderJA, MeadR (1965) A Simplex Method for Function Minimization. The Computer Journal 7: 308–313.

85. EwingG, HermissonJ (2010) MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics 26: 2064–2065.

86. RodrigoAG, ShpaerEG, DelwartEL, IversenAK, GalloMV, et al. (1999) Coalescent estimates of HIV-1 generation time in vivo. Proceedings of the National Academy of Sciences of the United States of America 96: 2187–2191.

87. IgarashiM, ItoK, YoshidaR, TomabechiD, KidaH, et al. (2010) Predicting the antigenic structure of the pandemic (H1N1) 2009 influenza virus hemagglutinin. PLoS One 5: e8553.

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