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The variable codons of H3 influenza A virus haemagglutinin genes

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Summary.

We have analyzed several sets of well-studied haemagglutinin (HA) gene sequences of H3 subtype influenza A viruses to identify codons that are unusually variable, using a simple pairwise sliding window method, DnDscanning. For two of the sets there were results of detailed phylogenetic modeling studies of selection already published. A third set had been the subject of an antigen mapping study, the results of which provide a completely independent benchmark of selected changes in H3 HA genes. Our analyses show that the codons with greatest DnDscan scores (i.e. the most variable) were mostly those reported in the published studies as being positively selected; indeed the DnDscan results matched the antigenic mapping results more closely than did those of the phylogenetic modeling methods. These results suggest that codons under selection can be found even when, as with some sets of virus sequences, a phylogeny is uncertain or cannot be obtained because, for example, the sequences are recombinants, or when selection is not necessarily linked with phylogeny, as in host-switching events. The program DnDscan is available at http://biojanus.anu.edu.au.

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References

  • RM Bush WM Fitch CA Bender NJ Cox (1999) ArticleTitlePositive selection on the H3 hemagglutinin gene of human influenza virus A Mol Biol Evol 16 1457–1465 Occurrence Handle10555276 Occurrence Handle1:CAS:528:DyaK1MXntlGqu7c%3D

    PubMed  CAS  Google Scholar 

  • L Chen A Perlina CJ Lee (2004) ArticleTitlePositive selection detection in 40,000 human immunodeficiency virus (HIV) type 1 sequences automatically identifies drug resistance and positive fitness mutations in HIV protease and reverse transcriptase J Virol 78 3722–3732 Occurrence Handle15016892 Occurrence Handle10.1128/JVI.78.7.3722-3732.2004 Occurrence Handle1:CAS:528:DC%2BD2cXis1Klu7w%3D

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. John Murray, London, 1st edn. (van Wyhe, J. The writings of Charles Darwin on the web. http://pages.britishlibrary.net/charles.darwin2/texts.html)

  • MT Dixon DM Hillis (1993) ArticleTitleRibosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis Mol Biol Evol 10 256–267 Occurrence Handle8450759 Occurrence Handle1:CAS:528:DyaK3sXps1Cmsg%3D%3D

    PubMed  CAS  Google Scholar 

  • JC Fay GJ Wyckoff CI Wu (2002) ArticleTitleTesting the neutral theory of molecular evolution with genomic data from Drosophila Nature 415 1024–1026 Occurrence Handle11875569 Occurrence Handle10.1038/4151024a Occurrence Handle1:CAS:528:DC%2BD38XhvVWjsLc%3D

    Article  PubMed  CAS  Google Scholar 

  • WM Fitch RM Bush CA Bender NJ Cox (1997) ArticleTitleLong term trends in the evolution of H(3) HA1 human influenza type A Proc Natl Acad Sci USA 94 7712–7718 Occurrence Handle9223253 Occurrence Handle10.1073/pnas.94.15.7712 Occurrence Handle1:CAS:528:DyaK2sXksl2nsL0%3D

    Article  PubMed  CAS  Google Scholar 

  • T Gojobori EN Moriyama M Kimura (1990) ArticleTitleMolecular clock of viral evolution, and the neutral theory Proc Natl Acad Sci USA 87 10015–10018 Occurrence Handle2263602 Occurrence Handle10.1073/pnas.87.24.10015 Occurrence Handle1:CAS:528:DyaK3MXls1GjtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • B Golding J Felsenstein (1990) ArticleTitleA maximum likelihood approach to the detection of selection from a phylogeny J Mol Evol 31 511–523 Occurrence Handle2176699 Occurrence Handle10.1007/BF02102078 Occurrence Handle1:STN:280:By6C3c7it1I%3D

    Article  PubMed  CAS  Google Scholar 

  • AJ Hay V Gregory AR Douglas YP Lin (2001) ArticleTitleThe evolution of human influenza viruses Phil Trans Roy Soc Lond B 356 1851–1870 Occurrence Handle10.1098/rstb.2001.0999

    Article  Google Scholar 

  • RE Hill ND Hastie (1987) ArticleTitleAccelerated evolution in the reactive centre regions of serine protease inhibitors Nature 326 96–99 Occurrence Handle3493437 Occurrence Handle10.1038/326096a0 Occurrence Handle1:CAS:528:DyaL2sXktVWktb8%3D

    Article  PubMed  CAS  Google Scholar 

  • IL Hofacker PF Stadler RR Stocsits (2004) ArticleTitleConserved RNA secondary structures in viral genomes: a survey Bioinformatics 20 1495–1499 Occurrence Handle15231541 Occurrence Handle10.1093/bioinformatics/bth108 Occurrence Handle1:CAS:528:DC%2BD2cXltlOqt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • E Hoffmann AS Lipatov RJ Webby EA Govorkova RG Webster (2005) ArticleTitleRole of specific hemagglutinin amino acids in the immunogenicity and protection of H5N1 influenza virus vaccines Proc Natl Acad Sci USA 102 12915–12920 Occurrence Handle16118277 Occurrence Handle10.1073/pnas.0506416102 Occurrence Handle1:CAS:528:DC%2BD2MXhtVWktb%2FI

    Article  PubMed  CAS  Google Scholar 

  • JP Huelsenbeck KA Dyer (2004) ArticleTitleBayesian Estimation of Positively Selected Sites J Mol Evol 58 661–672 Occurrence Handle15461423 Occurrence Handle10.1007/s00239-004-2588-9 Occurrence Handle1:CAS:528:DC%2BD2cXkvVOiu7k%3D

    Article  PubMed  CAS  Google Scholar 

  • AL Hughes M Nei (1988) ArticleTitlePattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection Nature 335 167–170 Occurrence Handle3412472 Occurrence Handle10.1038/335167a0 Occurrence Handle1:CAS:528:DyaL1cXlvVCktrY%3D

    Article  PubMed  CAS  Google Scholar 

  • MD Inkster VS Hinshaw IT Schulze (1993) ArticleTitleThe hemagglutinins of duck and human H1 influenza viruses differ in sequence conservation and in glycosylation J Virol 67 7436–7443 Occurrence Handle8230464 Occurrence Handle1:CAS:528:DyaK2cXhtVWgt7o%3D

    PubMed  CAS  Google Scholar 

  • F Jeanmougin JD Thompson M Gouy DG Higgins TJ Gibson (1998) ArticleTitleMultiple sequence alignment with Clustal X Trends Biochem Sci 23 403–405 Occurrence Handle9810230 Occurrence Handle10.1016/S0968-0004(98)01285-7 Occurrence Handle1:CAS:528:DyaK1cXntlansLg%3D

    Article  PubMed  CAS  Google Scholar 

  • M Kimura (1983) The Neutral Theory of Molecular Evolution Cambridge University Press New York

    Google Scholar 

  • M Knossow M Gaudier A Douglas B Barrere T Bizebard C Barbey B Gigant J Skehel (2002) ArticleTitleMechanism of neutralization of influenza virus infectivity by antibodies Virology 302 294–298 Occurrence Handle12441073 Occurrence Handle10.1006/viro.2002.1625 Occurrence Handle1:CAS:528:DC%2BD38XosFWns7c%3D

    Article  PubMed  CAS  Google Scholar 

  • SL Kosakovsky Pond SDW Frost (2005) ArticleTitleNot so different after all: a comparison of methods for detecting amino acid sites under selection Mol Biol Evol 22 1208–1222 Occurrence Handle15703242 Occurrence Handle10.1093/molbev/msi105

    Article  PubMed  Google Scholar 

  • WH Li CI Wu CC Luo (1985) ArticleTitleA new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes Mol Evol Biol 2 150–174

    Google Scholar 

  • WH Li (1993) ArticleTitleUnbiased estimates of the rates of synonymous and non-synonymous substitution J Mol Evol 36 96–99 Occurrence Handle8433381 Occurrence Handle10.1007/BF02407308 Occurrence Handle1:CAS:528:DyaK3sXnsVCmsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S-M Luoh MW Mcgregor VS Hinshaw (1992) ArticleTitleHemagglutinin mutations related to antigenic variation in H1 swine infuenza viruses J Virol 66 1066–1073 Occurrence Handle1731091 Occurrence Handle1:CAS:528:DyaK3sXltFKh

    PubMed  CAS  Google Scholar 

  • Luscombe N, Qian J, Zhang Z, Johnson T, Gerstein M (2002) The dominance of the population by a selected few: power-law behaviour applies to a wide variety of genomic properties. Genome Biol 3(8)

  • M Matrosovich A Tuzikov N Bovin A Gambaryan A Klimov MR Castrucci I Donatelli Y Kawaoka (2000) ArticleTitleEarly alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals J Virol 74 8502–8512 Occurrence Handle10954551 Occurrence Handle10.1128/JVI.74.18.8502-8512.2000 Occurrence Handle1:CAS:528:DC%2BD3cXmsVantrw%3D

    Article  PubMed  CAS  Google Scholar 

  • W Messier CB Stewart (1997) ArticleTitleEpisodic adaptive evolution of primate lysozymes Nature 385 151–154 Occurrence Handle8990116 Occurrence Handle10.1038/385151a0 Occurrence Handle1:CAS:528:DyaK2sXks1Sjug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • M Nei (1987) Molecular Evolutionary Genetics Columbia University Press New York

    Google Scholar 

  • T Ohta (1992) ArticleTitleThe nearly neutral theory of molecular evolution Ann Rev Ecol Syst 23 263–286 Occurrence Handle10.1146/annurev.es.23.110192.001403

    Article  Google Scholar 

  • T Ohta (1996) ArticleTitleThe current significance and standing of neutral and nearly neutral theories Bioessays 18 673–677 Occurrence Handle8779656 Occurrence Handle10.1002/bies.950180811 Occurrence Handle1:CAS:528:DyaK28XlslyntLg%3D

    Article  PubMed  CAS  Google Scholar 

  • F Perler A Efstratiadis P Lomedico W Gilbert R Kolodner J Dodgson (1980) ArticleTitleThe evolution of genes: the chicken preproinsulin gene Cell 20 555–566 Occurrence Handle7388949 Occurrence Handle10.1016/0092-8674(80)90641-8 Occurrence Handle1:CAS:528:DyaL3cXlsVCrur0%3D

    Article  PubMed  CAS  Google Scholar 

  • N Saitou M Nei (1986) ArticleTitlePolymorphism and evolution of influenza A virus genes Mol Biol Evol 3 57–74 Occurrence Handle3444396 Occurrence Handle1:CAS:528:DyaL28XosFagsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • PM Sharp (1997) ArticleTitleIn search of molecular darwinism Nature 385 111–112 Occurrence Handle8990106 Occurrence Handle10.1038/385111a0

    Article  PubMed  Google Scholar 

  • DJ Smith AS Lapedes JC de Jong TM Bestebroer GF Rimmelzwaan AD Osterhaus RA Fouchier (2004) ArticleTitleMapping the antigenic and genetic evolution of influenza virus Science 305 371–376 Occurrence Handle15218094 Occurrence Handle10.1126/science.1097211 Occurrence Handle1:CAS:528:DC%2BD2cXls1egtr4%3D

    Article  PubMed  CAS  Google Scholar 

  • S Sugita Y Yoshioka S Itamura Y Kanegae K Oguchi T Gojobori K Nerome A Oya (1991) ArticleTitleMolecular evolution of hemagglutinin genes of H1N1 swine and human influenza A viruses J Mol Evol 32 16–23 Occurrence Handle1901364 Occurrence Handle10.1007/BF02099924 Occurrence Handle1:CAS:528:DyaK3MXhsF2hu7w%3D

    Article  PubMed  CAS  Google Scholar 

  • Y Suzuki T Gojobori (1999) ArticleTitleA method for detecting positive selection at single amino acid sites Mol Biol Evol 16 1315–1328 Occurrence Handle10563013 Occurrence Handle1:CAS:528:DyaK1MXms1Ojt70%3D

    PubMed  CAS  Google Scholar 

  • Y Suzuki (2004) ArticleTitleNew methods for detecting positive selection at single amino acid sites J Mol Evol 59 11–19 Occurrence Handle15383903 Occurrence Handle1:CAS:528:DC%2BD2cXlsleisLc%3D

    PubMed  CAS  Google Scholar 

  • DC Wiley IA Wilson JJ Skehel (1981) ArticleTitleStructural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation Nature 289 373–378 Occurrence Handle6162101 Occurrence Handle10.1038/289373a0 Occurrence Handle1:CAS:528:DyaL3MXhvFSjtbw%3D

    Article  PubMed  CAS  Google Scholar 

  • IA Wilson JJ Skehel DC Wiley (1981) ArticleTitleStructure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution Nature 289 366–373 Occurrence Handle7464906 Occurrence Handle10.1038/289366a0 Occurrence Handle1:CAS:528:DyaL3MXhvFSjtb8%3D

    Article  PubMed  CAS  Google Scholar 

  • WS Wong Z Yang N Goldman R Nielsen (2004) ArticleTitleAccuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites Genetics 168 1041–1051 Occurrence Handle15514074 Occurrence Handle10.1534/genetics.104.031153 Occurrence Handle1:CAS:528:DC%2BD2cXhtVKms7jN

    Article  PubMed  CAS  Google Scholar 

  • Z Yang (2000) ArticleTitleMaximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A J Mol Evol 51 423–432 Occurrence Handle11080365 Occurrence Handle1:CAS:528:DC%2BD3MXptFGk

    PubMed  CAS  Google Scholar 

  • Z Yang R Nielsen (2002) ArticleTitleCodon-substitution models for detecting molecular adaptation at individual sites along specific lineages Mol Biol Evol 19 908–917 Occurrence Handle12032247 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojtbk%3D

    PubMed  CAS  Google Scholar 

  • PM Zanotto EG Kallas RF de Souza EC Holmes (1999) ArticleTitleGenealogical evidence for positive selection in the nef gene of HIV-1 Genetics 153 1077–1089 Occurrence Handle10545443 Occurrence Handle1:CAS:528:DyaK1MXnslSjs7s%3D

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Botany and Zoology, Faculty of Science, Australian National University, Canberra, Australia

    M. J. Gibbs, P. Wayper, M. L. A. Fourment & J. S. Armstrong

  2. Statistical Consulting Unit, Graduate Research School, Australian National University, Canberra, Australia

    J. T. Wood

  3. Laboratory of Plant Virology, Faculty of Agriculture, Saga University, Japan

    K. Ohshima

  4. Yarralumla, Australia

    A. J. Gibbs

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  1. M. J. Gibbs
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Gibbs, M., Wayper, P., Fourment, M. et al. The variable codons of H3 influenza A virus haemagglutinin genes. Arch Virol 152, 11–24 (2007). https://doi.org/10.1007/s00705-006-0834-8

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