1887

Abstract

Each year, influenza viruses cause epidemics by evading pre-existing humoral immunity through mutations in the major glycoproteins: the haemagglutinin (HA) and the neuraminidase (NA). In 2004, the antigenic evolution of HA of human influenza A (H3N2) viruses was mapped (Smith , , 371–376, 2004) from its introduction in humans in 1968 until 2003. The current study focused on the genetic evolution of NA and compared it with HA using the dataset of Smith and colleagues, updated to the epidemic of the 2009/2010 season. Phylogenetic trees and genetic maps were constructed to visualize the genetic evolution of NA and HA. The results revealed multiple reassortment events over the years. Overall rates of evolutionary change were lower for NA than for HA1 at the nucleotide level. Selection pressures were estimated, revealing an abundance of negatively selected sites and sparse positively selected sites. The differences found between the evolution of NA and HA1 warrant further analysis of the evolution of NA at the phenotypic level, as has been done previously for HA.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.043059-0
2012-09-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/9/1996.html?itemId=/content/journal/jgv/10.1099/vir.0.043059-0&mimeType=html&fmt=ahah

References

  1. Air G. M. , Els M. C. , Brown L. E. , Laver W. G. , Webster R. G. . ( 1985; ). Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase. . Virology 145:, 237–248. [CrossRef] [PubMed]
    [Google Scholar]
  2. Barr I. G. , McCauley J. , Cox N. , Daniels R. , Engelhardt O. G. , Fukuda K. , Grohmann G. , Hay A. , Kelso A. . & other authors ( 2010; ). Epidemiological, antigenic and genetic characteristics of seasonal influenza A(H1N1), A(H3N2) and B influenza viruses: basis for the WHO recommendation on the composition of influenza vaccines for use in the 2009–2010 Northern Hemisphere season. . Vaccine 28:, 1156–1167. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bhatt S. , Holmes E. C. , Pybus O. G. . ( 2011; ). The genomic rate of molecular adaptation of the human influenza A virus. . Mol Biol Evol 28:, 2443–2451. [CrossRef] [PubMed]
    [Google Scholar]
  4. Blok J. , Air G. M. . ( 1982; ). Variation in the membrane-insertion and “stalk” sequences in eight subtypes of influenza type A virus neuraminidase. . Biochemistry 21:, 4001–4007. [CrossRef] [PubMed]
    [Google Scholar]
  5. Brett I. C. , Johansson B. E. . ( 2005; ). Immunization against influenza A virus: comparison of conventional inactivated, live-attenuated and recombinant baculovirus produced purified hemagglutinin and neuraminidase vaccines in a murine model system. . Virology 339:, 273–280. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chen R. , Holmes E. C. . ( 2008; ). The evolutionary dynamics of human influenza B virus. . J Mol Evol 66:, 655–663. [CrossRef] [PubMed]
    [Google Scholar]
  7. Colman P. M. , Varghese J. N. , Laver W. G. . ( 1983; ). Structure of the catalytic and antigenic sites in influenza virus neuraminidase. . Nature 303:, 41–44. [CrossRef] [PubMed]
    [Google Scholar]
  8. Colman P. M. , Laver W. G. , Varghese J. N. , Baker A. T. , Tulloch P. A. , Air G. M. , Webster R. G. . ( 1987; ). Three-dimensional structure of a complex of antibody with influenza virus neuraminidase. . Nature 326:, 358–363. [CrossRef] [PubMed]
    [Google Scholar]
  9. Couch R. B. , Kasel J. A. , Gerin J. L. , Schulman J. L. , Kilbourne E. D. . ( 1974; ). Induction of partial immunity to influenza by a neuraminidase-specific vaccine. . J Infect Dis 129:, 411–420. [CrossRef] [PubMed]
    [Google Scholar]
  10. Darriba D. , Taboada G. L. , Doallo R. , Posada D. . ( 2011; ). ProtTest 3: fast selection of best-fit models of protein evolution. . Bioinformatics 27:, 1164–1165. [CrossRef] [PubMed]
    [Google Scholar]
  11. de Jong J. C. , Donker G. A. , Meijer A. , van der Hoek W. , Rimmelzwaan G. F. , Osterhaus A. D. M. E. . ( 2011; ). Het influenzaseizoen 2010/2011 in Nederland: het nieuwe A(H1N1)-virus van 2009 blijft actief. . Ned Tijdschr Med Microbiol 19:, 21–27.
    [Google Scholar]
  12. Drummond A. J. , Rambaut A. . ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. . BMC Evol Biol 7:, 214. [CrossRef] [PubMed]
    [Google Scholar]
  13. Drummond A. , Pybus O. G. , Rambaut A. . ( 2003; ). Inference of viral evolutionary rates from molecular sequences. . Adv Parasitol 54:, 331–358. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fiore A. E. , Uyeki T. M. , Broder K. , Finelli L. , Euler G. L. , Singleton J. A. , Iskander J. K. , Wortley P. M. , Shay D. K. . & other authors ( 2010; ). Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. . MMWR Recomm Rep 59: (RR-8), 1–62.[PubMed]
    [Google Scholar]
  15. Fitch W. M. , Bush R. M. , Bender C. A. , Cox N. J. . ( 1997; ). Long term trends in the evolution of H(3) HA1 human influenza type A. . Proc Natl Acad Sci U S A 94:, 7712–7718. [CrossRef] [PubMed]
    [Google Scholar]
  16. Fouchier R. A. , Munster V. , Wallensten A. , Bestebroer T. M. , Herfst S. , Smith D. , Rimmelzwaan G. F. , Olsen B. , Osterhaus A. D. . ( 2005; ). Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. . J Virol 79:, 2814–2822. [CrossRef] [PubMed]
    [Google Scholar]
  17. Goldman N. , Yang Z. . ( 1994; ). A codon-based model of nucleotide substitution for protein-coding DNA sequences. . Mol Biol Evol 11:, 725–736.[PubMed]
    [Google Scholar]
  18. Guindon S. , Gascuel O. . ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52:, 696–704. [CrossRef] [PubMed]
    [Google Scholar]
  19. Gulati U. , Hwang C.-C. , Venkatramani L. , Gulati S. , Stray S. J. , Lee J. T. , Laver W. G. , Bochkarev A. , Zlotnick A. , Air G. M. . ( 2002; ). Antibody epitopes on the neuraminidase of a recent H3N2 influenza virus (A/Memphis/31/98). . J Virol 76:, 12274–12280. [CrossRef] [PubMed]
    [Google Scholar]
  20. Hall T. A. . ( 1999; ). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. . Nucleic Acids Symp Ser 41:, 95–98.
    [Google Scholar]
  21. Hanada K. , Suzuki Y. , Gojobori T. . ( 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 Biol Evol 21:, 1074–1080. [CrossRef] [PubMed]
    [Google Scholar]
  22. Holmes E. C. , Ghedin E. , Miller N. , Taylor J. , Bao Y. , St George K. , Grenfell B. T. , Salzberg S. L. , Fraser C. M. . & other authors ( 2005; ). Whole-genome analysis of human influenza A virus reveals multiple persistent lineages and reassortment among recent H3N2 viruses. . PLoS Biol 3:, e300. [CrossRef] [PubMed]
    [Google Scholar]
  23. Huelsenbeck J. P. , Ronquist F. . ( 2001; ). MRBAYES: Bayesian inference of phylogenetic trees. . Bioinformatics 17:, 754–755. [CrossRef] [PubMed]
    [Google Scholar]
  24. Jenkins G. M. , Rambaut A. , Pybus O. G. , Holmes E. C. . ( 2002; ). Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. . J Mol Evol 54:, 156–165. [CrossRef] [PubMed]
    [Google Scholar]
  25. Johansson B. E. , Grajower B. , Kilbourne E. D. . ( 1993; ). Infection-permissive immunization with influenza virus neuraminidase prevents weight loss in infected mice. . Vaccine 11:, 1037–1039. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kaverin N. V. , Matrosovich M. N. , Gambaryan A. S. , Rudneva I. A. , Shilov A. A. , Varich N. L. , Makarova N. V. , Kropotkina E. A. , Sinitsin B. V. . ( 2000; ). Intergenic HA–NA interactions in influenza A virus: postreassortment substitutions of charged amino acid in the hemagglutinin of different subtypes. . Virus Res 66:, 123–129. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kendal A. P. , Schieble J. , Cooney M. K. , Chin J. , Foy H. M. , Noble G. R. . ( 1978; ). Co-circulation of two influenza A (H3N2) antigenic variants detected by virus surveillance in individual communities. . Am J Epidemiol 108:, 308–311.[PubMed]
    [Google Scholar]
  28. Kilbourne E. D. . ( 1976; ). Comparative efficacy of neuraminidase-specific and conventional influenza virus vaccines in induction of antibody to neuraminidase in humans. . J Infect Dis 134:, 384–394. [CrossRef] [PubMed]
    [Google Scholar]
  29. Kilbourne E. D. , Johansson B. E. , Grajower B. . ( 1990; ). Independent and disparate evolution in nature of influenza A virus hemagglutinin and neuraminidase glycoproteins. . Proc Natl Acad Sci U S A 87:, 786–790. [CrossRef] [PubMed]
    [Google Scholar]
  30. Kosakovsky Pond S. L. , Frost S. D. , Muse S. V. . ( 2005; ). HyPhy: hypothesis testing using phylogenies. . Bioinformatics 21:, 676–679. [CrossRef] [PubMed]
    [Google Scholar]
  31. Kosakovsky Pond S. L. , Frost S. D. , Grossman Z. , Gravenor M. B. , Richman D. D. , Brown A. J. . ( 2006; ). Adaptation to different human populations by HIV-1 revealed by codon-based analyses. . PLoS Comput Biol 2:, e62. [CrossRef] [PubMed]
    [Google Scholar]
  32. Kosakovsky Pond S. L. , Poon A. F. , Leigh Brown A. J. , Frost S. D. . ( 2008; ). A maximum likelihood method for detecting directional evolution in protein sequences and its application to influenza A virus. . Mol Biol Evol 25:, 1809–1824. [CrossRef] [PubMed]
    [Google Scholar]
  33. Kosakovsky Pond S. L. , Murrell B. , Fourment M. , Frost S. D. , Delport W. , Scheffler K. . ( 2011; ). A random effects branch-site model for detecting episodic diversifying selection. . Mol Biol Evol 28:, 3033–3043. [CrossRef] [PubMed]
    [Google Scholar]
  34. Laver W. G. , Air G. M. , Webster R. G. , Markoff L. J. . ( 1982; ). Amino acid sequence changes in antigenic variants of type A influenza virus N2 neuraminidase. . Virology 122:, 450–460. [CrossRef] [PubMed]
    [Google Scholar]
  35. Lentz M. R. , Air G. M. , Laver W. G. , Webster R. G. . ( 1984; ). Sequence of the neuraminidase gene of influenza virus A/Tokyo/3/67 and previously uncharacterized monoclonal variants. . Virology 135:, 257–265. [CrossRef] [PubMed]
    [Google Scholar]
  36. Lindstrom S. E. , Cox N. J. , Klimov A. . ( 2004; ). Genetic analysis of human H2N2 and early H3N2 influenza viruses, 1957–1972: evidence for genetic divergence and multiple reassortment events. . Virology 328:, 101–119. [CrossRef] [PubMed]
    [Google Scholar]
  37. Liu C. , Eichelberger M. C. , Compans R. W. , Air G. M. . ( 1995; ). Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. . J Virol 69:, 1099–1106.[PubMed]
    [Google Scholar]
  38. Luther P. , Bergmann K. C. , Oxford J. S. . ( 1984; ). An investigation of antigenic drift of neuraminidases of influenza A (H1N1) viruses. . J Hyg (Lond) 92:, 223–229. [CrossRef] [PubMed]
    [Google Scholar]
  39. Minin V. N. , Bloomquist E. W. , Suchard M. A. . ( 2008; ). Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. . Mol Biol Evol 25:, 1459–1471. [CrossRef] [PubMed]
    [Google Scholar]
  40. Mitnaul L. J. , Matrosovich M. N. , Castrucci M. R. , Tuzikov A. B. , Bovin N. V. , Kobasa D. , Kawaoka Y. . ( 2000; ). Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. . J Virol 74:, 6015–6020. [CrossRef] [PubMed]
    [Google Scholar]
  41. Murphy B. R. , Kasel J. A. , Chanock R. M. . ( 1972; ). Association of serum anti-neuraminidase antibody with resistance to influenza in man. . N Engl J Med 286:, 1329–1332. [CrossRef] [PubMed]
    [Google Scholar]
  42. Nagarajan N. , Kingsford C. . ( 2011; ). GiRaF: robust, computational identification of influenza reassortments via graph mining. . Nucleic Acids Res 39:, e34. [CrossRef] [PubMed]
    [Google Scholar]
  43. Palese P. , Compans R. W. . ( 1976; ). Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid (FANA): mechanism of action. . J Gen Virol 33:, 159–163. [CrossRef] [PubMed]
    [Google Scholar]
  44. Palese P. , Tobita K. , Ueda M. , Compans R. W. . ( 1974; ). Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. . Virology 61:, 397–410. [CrossRef] [PubMed]
    [Google Scholar]
  45. Pereira M. S. , Chakraverty P. . ( 1977; ). The laboratory surveillance of influenza epidemics in the United Kingdom 1968–1976. . J Hyg (Lond) 79:, 77–87. [CrossRef] [PubMed]
    [Google Scholar]
  46. Posada D. . ( 2008; ). jModelTest: phylogenetic model averaging. . Mol Biol Evol 25:, 1253–1256. [CrossRef] [PubMed]
    [Google Scholar]
  47. Pybus O. G. , Rambaut A. , Belshaw R. , Freckleton R. P. , Drummond A. J. , Holmes E. C. . ( 2007; ). Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. . Mol Biol Evol 24:, 845–852. [CrossRef] [PubMed]
    [Google Scholar]
  48. Rambaut A. , Pybus O. G. , Nelson M. I. , Viboud C. , Taubenberger J. K. , Holmes E. C. . ( 2008; ). The genomic and epidemiological dynamics of human influenza A virus. . Nature 453:, 615–619. [CrossRef] [PubMed]
    [Google Scholar]
  49. Ronquist F. , Huelsenbeck J. P. . ( 2003; ). MrBayes 3: Bayesian phylogenetic inference under mixed models. . Bioinformatics 19:, 1572–1574. [CrossRef] [PubMed]
    [Google Scholar]
  50. Russell C. A. , Jones T. C. , Barr I. G. , Cox N. J. , Garten R. J. , Gregory V. , Gust I. D. , Hampson A. W. , Hay A. J. . & other authors ( 2008; ). Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. . Vaccine 26: (Suppl. 4), D31–D34. [CrossRef] [PubMed]
    [Google Scholar]
  51. Sandbulte M. R. , Westgeest K. B. , Gao J. , Xu X. , Klimov A. I. , Russell C. A. , Burke D. F. , Smith D. J. , Fouchier R. A. , Eichelberger M. C. . ( 2011; ). Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. . Proc Natl Acad Sci U S A 108:, 20748–20753. [CrossRef] [PubMed]
    [Google Scholar]
  52. Sauter N. K. , Bednarski M. D. , Wurzburg B. A. , Hanson J. E. , Whitesides G. M. , Skehel J. J. , Wiley D. C. . ( 1989; ). Hemagglutinins from two influenza virus variants bind to sialic acid derivatives with millimolar dissociation constants: a 500-MHz proton nuclear magnetic resonance study. . Biochemistry 28:, 8388–8396. [CrossRef] [PubMed]
    [Google Scholar]
  53. Schild G. C. , Henry-Aymard M. , Pereira M. S. , Chakraverty P. , Dowdle W. , Coleman M. , Chang W. K. . ( 1973; ). Antigenic variation in current human type A influenza viruses: antigenic characteristics of the variants and their geographic distribution. . Bull World Health Organ 48:, 269–278.[PubMed]
    [Google Scholar]
  54. Schild G. C. , Oxford J. S. , Dowdle W. R. , Coleman M. , Pereira M. S. , Chakraverty P. . ( 1974; ). Antigenic variation in current influenza A viruses: evidence for a high frequency of antigenic ‘drift’ for the Hong Kong virus. . Bull World Health Organ 51:, 1–11.[PubMed]
    [Google Scholar]
  55. Schild G. C. , Newman R. W. , Webster R. G. , Major D. , Hinshaw V. S. . ( 1980; ). Antigenic analysis of influenza A virus surface antigens: considerations for the nomenclature of influenza virus. . Comp Immunol Microbiol Infect Dis 3:, 5–18. [CrossRef] [PubMed]
    [Google Scholar]
  56. Scholtissek C. , Rohde W. , Von Hoyningen V. , Rott R. . ( 1978; ). On the origin of the human influenza virus subtypes H2N2 and H3N2. . Virology 87:, 13–20. [CrossRef] [PubMed]
    [Google Scholar]
  57. Schulman J. L. , Kilbourne E. D. . ( 1969; ). Independent variation in nature of hemagglutinin and neuraminidase antigens of influenza virus: distinctiveness of hemagglutinin antigen of Hong Kong-68 virus. . Proc Natl Acad Sci U S A 63:, 326–333. [CrossRef] [PubMed]
    [Google Scholar]
  58. Schulman J. L. , Khakpour M. , Kilbourne E. D. . ( 1968; ). Protective effects of specific immunity to viral neuraminidase on influenza virus infection of mice. . J Virol 2:, 778–786.[PubMed]
    [Google Scholar]
  59. Shapiro B. , Rambaut A. , Drummond A. J. . ( 2006; ). Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. . Mol Biol Evol 23:, 7–9. [CrossRef] [PubMed]
    [Google Scholar]
  60. Smith D. J. , Lapedes A. S. , de Jong J. C. , Bestebroer T. M. , Rimmelzwaan G. F. , Osterhaus A. D. , Fouchier R. A. . ( 2004; ). Mapping the antigenic and genetic evolution of influenza virus. . Science 305:, 371–376. [CrossRef] [PubMed]
    [Google Scholar]
  61. Smith G. J. , Vijaykrishna D. , Bahl J. , Lycett S. J. , Worobey M. , Pybus O. G. , Ma S. K. , Cheung C. L. , Raghwani J. . & other authors ( 2009; ). Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. . Nature 459:, 1122–1125. [CrossRef] [PubMed]
    [Google Scholar]
  62. Stöhr K. . ( 2002; ). Influenza – WHO cares. . Lancet Infect Dis 2:, 517. [CrossRef] [PubMed]
    [Google Scholar]
  63. Swofford D. L. . ( 2003; ). paup*: Phylogenetic analysis using parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates.
  64. Taubenberger J. K. , Morens D. M. . ( 2006; ). 1918 Influenza: the mother of all pandemics. . Emerg Infect Dis 12:, 15–22.[PubMed] [CrossRef]
    [Google Scholar]
  65. Tong S. , Li Y. , Rivailler P. , Conrardy C. , Castillo D. A. , Chen L. M. , Recuenco S. , Ellison J. A. , Davis C. T. . & other authors ( 2012; ). A distinct lineage of influenza A virus from bats. . Proc Natl Acad Sci U S A 109:, 4269–4274.[PubMed] [CrossRef]
    [Google Scholar]
  66. Varghese J. N. , McKimm-Breschkin J. L. , Caldwell J. B. , Kortt A. A. , Colman P. M. . ( 1992; ). The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor. . Proteins 14:, 327–332. [CrossRef] [PubMed]
    [Google Scholar]
  67. Wagner R. , Matrosovich M. , Klenk H. D. . ( 2002; ). Functional balance between haemagglutinin and neuraminidase in influenza virus infections. . Rev Med Virol 12:, 159–166. [CrossRef] [PubMed]
    [Google Scholar]
  68. Webster R. G. , Bean W. J. , Gorman O. T. , Chambers T. M. , Kawaoka Y. . ( 1992; ). Evolution and ecology of influenza A viruses. . Microbiol Rev 56:, 152–179.[PubMed]
    [Google Scholar]
  69. WHO . ( 2003; ). Fact sheet Number 211. Influenza http://www.who.int/mediacentre/factsheets/fs211.
  70. Wiley D. C. , Wilson I. A. , Skehel J. J. . ( 1981; ). Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. . Nature 289:, 373–378. [CrossRef] [PubMed]
    [Google Scholar]
  71. Wilson I. A. , Cox N. J. . ( 1990; ). Structural basis of immune recognition of influenza virus hemagglutinin. . Annu Rev Immunol 8:, 737–771. [CrossRef] [PubMed]
    [Google Scholar]
  72. Xu X. , Cox N. J. , Bender C. A. , Regnery H. L. , Shaw M. W. . ( 1996; ). Genetic variation in neuraminidase genes of influenza A (H3N2) viruses. . Virology 224:, 175–183. [CrossRef] [PubMed]
    [Google Scholar]
  73. Yang Z. . ( 2007; ). paml4: phylogenetic analysis by maximum likelihood. . Mol Biol Evol 24:, 1586–1591. [CrossRef] [PubMed]
    [Google Scholar]
  74. Zwickl D. J. . ( 2007; ). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, The University of Texas at Austin, TX, USA.
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.043059-0
Loading
/content/journal/jgv/10.1099/vir.0.043059-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error