Intrasubtype Reassortments Cause Adaptive Amino Acid Replacements in H3N2 Influenza Genes

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Neverov, Alexey D ^a,b   Lezhnina, Ksenia V ^b   Kondrashov, Alexey S ^b,c   Bazykin, Georgii A ^b,d  

^a CENTRAL RESEARCH INSTITUTE OF EPIDEMIOLOGY   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF MICHIGAN   (United States)

^d INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; ARTICLE; GENE CLUSTER; GENE INTERACTION; GENE SEQUENCE; GENETIC REASSORTMENT; HA GENE; INFLUENZA VIRUS A H3N2; M1 GENE; MOLECULAR EVOLUTION; NA GENE; NONHUMAN; NS1 GENE; PB1 GENE; PHYLOGENETIC TREE; PHYLOGENY; POINT MUTATION; SEQUENCE ALIGNMENT; VIRUS GENE;

AMINO ACID SUBSTITUTION; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; PHYLOGENY; POINT MUTATION; VIRAL PROTEINS;

EID: 84896736904     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004037     Document Type: Article

References (77)

1. Kilbourne ED, (2006) Influenza pandemics of the 20th century. Emerging Infect Dis 12: 9-14 doi:10.3201/eid1201.051254.
2. Li C, Hatta M, Watanabe S, Neumann G, Kawaoka Y, (2008) Compatibility among polymerase subunit proteins is a restricting factor in reassortment between equine H7N7 and human H3N2 influenza viruses. J Virol 82: 11880-11888 doi:10.1128/JVI.01445-08.
3. Li C, Hatta M, Nidom CA, Muramoto Y, Watanabe S, et al. (2010) Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. PNAS 107: 4687-4692 doi:10.1073/pnas.0912807107.
4. Suzuki Y, (2010) A phylogenetic approach to detecting reassortments in viruses with segmented genomes. Gene 464: 11-16 doi:10.1016/j.gene.2010.05.002.
5. Nelson MI, Holmes EC, (2007) The evolution of epidemic influenza. Nature Reviews Genetics 8: 196-205 doi:10.1038/nrg2053.
6. Lindstrom SE, Hiromoto Y, Nerome R, Omoe K, Sugita S, et al. (1998) Phylogenetic analysis of the entire genome of influenza A (H3N2) viruses from Japan: evidence for genetic reassortment of the six internal genes. J Virol 72: 8021-8031.
7. Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y, et al. (2005) Whole-genome analysis of human influenza A virus reveals multiple persistent lineages and reassortment among recent H3N2 viruses. PLoS Biol 3: e300 doi:10.1371/journal.pbio.0030300.
8. Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J, et al. (2006) Stochastic processes are key determinants of short-term evolution in influenza a virus. PLoS Pathog 2: e125 doi:10.1371/journal.ppat.0020125.
9. Nelson MI, Viboud C, Simonsen L, Bennett RT, Griesemer SB, et al. (2008) Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog 4: e1000012 doi:10.1371/journal.ppat.1000012.
10. Rabadan R, Levine AJ, Krasnitz M, (2008) Non-random reassortment in human influenza A viruses. Influenza Other Respi Viruses 2: 9-22 doi:10.1111/j.1750-2659.2007.00030.x.
11. De Silva UC, Tanaka H, Nakamura S, Goto N, Yasunaga T, (2012) A comprehensive analysis of reassortment in influenza A virus. Biol Open 1: 385-390 doi:10.1242/bio.2012281.
12. Nagarajan N, Kingsford C, (2011) GiRaF: robust, computational identification of influenza reassortments via graph mining. Nucleic Acids Res 39: e34 doi:10.1093/nar/gkq1232.
13. Yurovsky A, Moret BME, (2011) FluReF, an automated flu virus reassortment finder based on phylogenetic trees. BMC Genomics 12: S3 doi:10.1186/1471-2164-12-S2-S3.
14. Svinti V, Cotton JA, McInerney JO, (2013) New approaches for unravelling reassortment pathways. BMC Evol Biol 13: 1 doi:10.1186/1471-2148-13-1.
15. Lubeck MD, Palese P, Schulman JL, (1979) Nonrandom association of parental genes in influenza A virus recombinants. Virology 95: 269-274.
16. Downie JC (2004) Reassortment of influenza A virus genes linked to PB1 polymerase gene. In: Kawaoka Y, editor. Options for the Control of Influenza V. Amsterdam: Elsevier Science Bv, Vol. 1263. pp. 714-718.
17. Varich NL, Gitelman AK, Shilov AA, Smirnov YA, Kaverin NV, (2008) Deviation from the random distribution pattern of influenza A virus gene segments in reassortants produced under non-selective conditions. Arch Virol 153: 1149-1154 doi:10.1007/s00705-008-0070-5.
18. Chen L-M, Davis CT, Zhou H, Cox NJ, Donis RO, (2008) Genetic Compatibility and Virulence of Reassortants Derived from Contemporary Avian H5N1 and Human H3N2 Influenza A Viruses. PLoS Pathog 4: e1000072 doi:10.1371/journal.ppat.1000072.
19. Greenbaum BD, Li OTW, Poon LLM, Levine AJ, Rabadan R, (2012) Viral reassortment as an information exchange between viral segments. Proc Natl Acad Sci USA 109: 3341-3346 doi:10.1073/pnas.1113300109.
20. Schrauwen EJA, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM, et al. (2013) Reassortment between Avian H5N1 and Human Influenza Viruses Is Mainly Restricted to the Matrix and Neuraminidase Gene Segments. PLoS ONE 8: e59889 doi:10.1371/journal.pone.0059889.
21. Khiabanian H, Trifonov V, Rabadan R, (2009) Reassortment Patterns in Swine Influenza Viruses. PLoS ONE 4: e7366 doi:10.1371/journal.pone.0007366.
22. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, et al. (2008) The genomic and epidemiological dynamics of human influenza A virus. Nature 453: 615-619 doi:10.1038/nature06945.
23. Rudneva IA, Timofeeva TA, Ilyushina NA, Varich NL, Kochergin-Nikitsky KS, et al. (2008) Post-reassortment amino acid change in the hemagglutinin of a human-avian influenza H5N1 reassortant virus alters its antigenic specificity. Acta Virol 52: 181-184.
24. Vijaykrishna D, Smith GJD, Pybus OG, Zhu H, Bhatt S, et al. (2011) Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473: 519-522 doi:10.1038/nature10004.
25. Golding GB, (1987) The detection of deleterious selection using ancestors inferred from a phylogenetic history. Genetics Research 49: 71-82 doi:10.1017/S0016672300026768.
26. Bush RM, Fitch WM, Bender CA, Cox NJ, (1999) Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol Biol Evol 16: 1457-1465.
27. Rocha EPC, Smith JM, Hurst LD, Holden MTG, Cooper JE, et al. (2006) Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239: 226-235 doi:10.1016/j.jtbi.2005.08.037.
28. Pybus OG, Rambaut A, Belshaw R, Freckleton RP, Drummond AJ, et al. (2007) Phylogenetic Evidence for Deleterious Mutation Load in RNA Viruses and Its Contribution to Viral Evolution. Mol Biol Evol 24: 845-852 doi:10.1093/molbev/msm001.
29. Kryazhimskiy S, Bazykin GA, Dushoff J, (2008) Natural selection for nucleotide usage at synonymous and nonsynonymous sites in influenza A virus genes. J Virol 82: 4938-4945 doi:10.1128/JVI.02415-07.
30. Kryazhimskiy S, Plotkin JB, (2008) The Population Genetics of dN/dS. PLoS Genet 4: e1000304 doi:10.1371/journal.pgen.1000304.
31. Gillespie JH, (1984) Molecular evolution over the mutational landscape. Evolution 38: 1116-1129.
32. Kauffman S, Levin S, (1987) Towards a general theory of adaptive walks on rugged landscapes. Journal of Theoretical Biology 128: 11-45 doi:10.1016/S0022-5193(87)80029-2.
33. Smith DJ, Lapedes AS, Jong JC de, Bestebroer TM, Rimmelzwaan GF, et al. (2004) Mapping the Antigenic and Genetic Evolution of Influenza Virus. Science 305: 371-376 doi:10.1126/science.1097211.
34. Kryazhimskiy S, Dushoff J, Bazykin GA, Plotkin JB, (2011) Prevalence of epistasis in the evolution of influenza A surface proteins. PLoS Genet 7: e1001301 doi:10.1371/journal.pgen.1001301.
35. Wolf YI, Viboud C, Holmes EC, Koonin EV, Lipman DJ, (2006) Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biology Direct 1: 34 doi:10.1186/1745-6150-1-34.
36. Shih AC-C, Hsiao T-C, Ho M-S, Li W-H, (2007) Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc Natl Acad Sci USA 104: 6283-6288 doi:10.1073/pnas.0701396104.
37. Gillespie JH (1991) The Causes of Molecular Evolution. Oxford University Press. 354 p.
38. Strelkowa N, Lässig M, (2012) Clonal interference in the evolution of influenza. Genetics 192: 671-682 doi:10.1534/genetics.112.143396.
39. Illingworth CJR, Mustonen V, (2012) Components of Selection in the Evolution of the Influenza Virus: Linkage Effects Beat Inherent Selection. PLoS Pathog 8: e1003091 doi:10.1371/journal.ppat.1003091.
40. Fourment M, Wood JT, Gibbs AJ, Gibbs MJ, (2010) Evolutionary dynamics of the N1 neuraminidases of the main lineages of influenza A viruses. Mol Phylogenet Evol 56: 526-535 doi:10.1016/j.ympev.2010.04.039.
41. Furuse Y, Suzuki A, Oshitani H, (2010) Reassortment between swine influenza A viruses increased their adaptation to humans in pandemic H1N1/09. Infect Genet Evol 10: 569-574 doi:10.1016/j.meegid.2010.01.010.
42. Rabadan R, Levine AJ, Robins H, (2006) Comparison of Avian and Human Influenza A Viruses Reveals a Mutational Bias on the Viral Genomes. J Virol 80: 11887-11891 doi:10.1128/JVI.01414-06.
43. Dos Reis M, Hay AJ, Goldstein RA, (2009) Using non-homogeneous models of nucleotide substitution to identify host shift events: application to the origin of the 1918 "Spanish" influenza pandemic virus. J Mol Evol 69: 333-345 doi:10.1007/s00239-009-9282-x.
44. Wong EH, Smith DK, Rabadan R, Peiris M, Poon LL, (2010) Codon usage bias and the evolution of influenza A viruses. Codon Usage Biases of Influenza Virus. BMC Evolutionary Biology 10: 253 doi:10.1186/1471-2148-10-253.
45. Sandbulte MR, Westgeest KB, Gao J, Xu X, Klimov AI, et al. (2011) Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. Proc Natl Acad Sci USA 108: 20748-20753 doi:10.1073/pnas.1113801108.
46. Hensley SE, Das SR, Gibbs JS, Bailey AL, Schmidt LM, et al. (2011) Influenza A virus hemagglutinin antibody escape promotes neuraminidase antigenic variation and drug resistance. PLoS ONE 6: e15190 doi:10.1371/journal.pone.0015190.
47. Myers JL, Wetzel KS, Linderman SL, Li Y, Sullivan CB, et al. (2013) Compensatory hemagglutinin mutations alter antigenic properties of influenza viruses. J Virol 87: 11168-11172 doi:10.1128/JVI.01414-13.
48. Yurovsky A, Moret BME, (2011) FluReF, an automated flu virus reassortment finder based on phylogenetic trees. BMC Genomics 12: S3 doi:10.1186/1471-2164-12-S2-S3.
49. Wolf YI, Viboud C, Holmes EC, Koonin EV, Lipman DJ, (2006) Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biol Direct 1: 34 doi:10.1186/1745-6150-1-34.
50. Kryazhimskiy S, Bazykin GA, Plotkin J, Dushoff J, (2008) Directionality in the evolution of influenza A haemagglutinin. Proc R Soc B-Biol Sci 275: 2455-2464 doi:10.1098/rspb.2008.0521.
51. Rimmelzwaan GF, Berkhoff EGM, Nieuwkoop NJ, Fouchier RAM, Osterhaus ADME, (2004) Functional compensation of a detrimental amino acid substitution in a cytotoxic-T-lymphocyte epitope of influenza a viruses by comutations. J Virol 78: 8946-8949 doi:10.1128/JVI.78.16.8946-8949.2004.
52. Rimmelzwaan GF, Berkhoff EGM, Nieuwkoop NJ, Smith DJ, Fouchier RAM, et al. (2005) Full restoration of viral fitness by multiple compensatory co-mutations in the nucleoprotein of influenza A virus cytotoxic T-lymphocyte escape mutants. J Gen Virol 86: 1801-1805 doi:10.1099/vir.0.80867-0.
53. Koelle K, Cobey S, Grenfell B, Pascual M, (2006) Epochal Evolution Shapes the Phylodynamics of Interpandemic Influenza A (H3N2) in Humans. Science 314: 1898-1903 doi:10.1126/science.1132745.
54. Shapiro B, Rambaut A, Pybus OG, Holmes EC, (2006) A phylogenetic method for detecting positive epistasis in gene sequences and its application to RNA virus evolution. Mol Biol Evol 23: 1724-1730 doi:10.1093/molbev/msl037.
55. Mitnaul LJ, Matrosovich MN, Castrucci MR, Tuzikov AB, Bovin NV, et al. (2000) Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J Virol 74: 6015-6020.
56. Ferguson NM, Fraser C, Donnelly CA, Ghani AC, Anderson RM, (2004) Public Health Risk from the Avian H5N1 Influenza Epidemic. Science 304: 968-969 doi:10.1126/science.1096898.
57. Yong E, (2012) Influenza: Five questions on H5N1. Nature 486: 456-458 doi:10.1038/486456a.
58. Butler D, (2012) Death-rate row blurs mutant flu debate. Nature 482: 289 doi:10.1038/482289a.
59. Herfst S, Schrauwen EJA, Linster M, Chutinimitkul S, Wit Ede, et al. (2012) Airborne Transmission of Influenza A/H5N1 Virus Between Ferrets. Science 336: 1534-1541 doi:10.1126/science.1213362.
60. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, et al. (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486: 420-428 doi:10.1038/nature10831.
61. Russell CA, Fonville JM, Brown AEX, Burke DF, Smith DL, et al. (2012) The Potential for Respiratory Droplet-Transmissible A/H5N1 Influenza Virus to Evolve in a Mammalian Host. Science 336: 1541-1547 doi:10.1126/science.1222526.
62. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, et al. (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82: 596-601 doi:10.1128/JVI.02005-07.
63. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797 doi:10.1093/nar/gkh340.
64. Edgar RC, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113 doi:10.1186/1471-2105-5-113.
65. Li W, Godzik A, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659 doi:10.1093/bioinformatics/btl158.
66. Huelsenbeck JP, Ronquist F, (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
67. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
68. Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F, (2004) Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407-415 doi:10.1093/bioinformatics/btg427.
69. Olsen CW, Karasin AI, Carman S, Li Y, Bastien N, et al. (2006) Triple reassortant H3N2 influenza A viruses, Canada, 2005. Emerging Infect Dis 12: 1132-1135 doi:10.3201/eid1207.060268.
70. Pond SLK, Frost SDW, Muse SV, (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679 doi:10.1093/bioinformatics/bti079.
71. Pond SLK, (2004) A Genetic Algorithm Approach to Detecting Lineage-Specific Variation in Selection Pressure. Molecular Biology and Evolution 22: 478-485 doi:10.1093/molbev/msi031.
72. Guindon S, Delsuc F, Dufayard J-F, Gascuel O, (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 537: 113-137 doi:_10.1007/978-1-59745-251-9_6.
73. Grenfell BT, Pybus OG, Gog JR, Wood JLN, Daly JM, et al. (2004) Unifying the Epidemiological and Evolutionary Dynamics of Pathogens. Science 303: 327-332 doi:10.1126/science.1090727.
74. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, et al. (2012) Detecting Individual Sites Subject to Episodic Diversifying Selection. PLoS Genetics 8: e1002764 doi:10.1371/journal.pgen.1002764.
75. Vos RA, Caravas J, Hartmann K, Jensen MA, Miller C, (2011) BIO::Phylo-phyloinformatic analysis using perl. BMC Bioinformatics 12: 63 doi:10.1186/1471-2105-12-63.
76. R Development Core Team (2008) R: a language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing. Available: http://www.r-project.org./. Accessed 29 May 2013.
77. Scornavacca C, Zickmann F, Huson DH, (2011) Tanglegrams for rooted phylogenetic trees and networks. Bioinformatics 27: i248-i256 doi:10.1093/bioinformatics/btr210.