Evolution of the neuraminidase gene of seasonal influenza A and B viruses in Thailand between 2010 and 2015

PLoS One. 2017 Apr 14;12(4):e0175655. doi: 10.1371/journal.pone.0175655. eCollection 2017.

Abstract

The neuraminidase inhibitors (NAIs) oseltamivir and zanamivir are commonly used for the treatment and control of influenza A and B virus infection. However, the emergence of new influenza virus strains with reduced susceptibility to NAIs may appear with the use of these antivirals or even naturally. We therefore screened the neuraminidase (NA) sequences of seasonal influenza virus A(H1N1), A(H1N1)pdm09, A(H3N2), and influenza B virus strains identified in Thailand for the presence of substitutions previously reported to reduce susceptibility to NAIs. We initially examined oseltamivir resistance (characterized by the H275Y mutation in the NA gene) in 485 A(H1N1)pdm09 strains circulating in Thailand and found that 0.82% (4/485) had this substitution. To further evaluate the evolution of the NA gene, we also randomly selected 98 A(H1N1)pdm09, 158 A(H3N2), and 69 influenza B virus strains for NA gene amplification and sequencing, which revealed various amino acid mutations in the active site of the NA protein previously shown to be associated with reduced susceptibility to NAIs. Phylogenetic analysis of the influenza virus strains from this study and elsewhere around the world, together with the estimations of nucleotide substitution rates and selection pressure, and the predictions of B-cell epitopes and N-linked glycosylation sites all provided evidence for the ongoing evolution of NA. The overall rates of NA evolution for influenza A viruses were higher than for influenza B virus at the nucleotide level, although influenza B virus possessed more genealogical diversity than that of influenza A viruses. The continual surveillance of the antigenic changes associated with the NA protein will not only contribute to the influenza virus database but may also provide a better understanding of selection pressure exerted by antiviral use.

MeSH terms

  • Drug Resistance, Viral / genetics
  • Epitopes, B-Lymphocyte / immunology
  • Evolution, Molecular*
  • Genotype
  • Glycosylation
  • Humans
  • Influenza A Virus, H1N1 Subtype / drug effects
  • Influenza A Virus, H1N1 Subtype / enzymology*
  • Influenza A Virus, H1N1 Subtype / genetics
  • Influenza A Virus, H3N2 Subtype / drug effects
  • Influenza A Virus, H3N2 Subtype / enzymology*
  • Influenza A Virus, H3N2 Subtype / genetics
  • Influenza B virus / drug effects
  • Influenza B virus / enzymology*
  • Influenza B virus / genetics
  • Influenza, Human / drug therapy
  • Influenza, Human / epidemiology
  • Influenza, Human / virology*
  • Neuraminidase / classification
  • Neuraminidase / genetics*
  • Neuraminidase / metabolism
  • Oseltamivir / pharmacology
  • Oseltamivir / therapeutic use
  • Phylogeny
  • RNA, Viral / genetics
  • RNA, Viral / metabolism
  • Seasons
  • Thailand / epidemiology

Substances

  • Epitopes, B-Lymphocyte
  • RNA, Viral
  • Oseltamivir
  • Neuraminidase

Grants and funding

This work was supported by the following funding sources: The Research Chair Grant from the National Science and Technology Development Agency (P-15-50004), The National Research University Project, Office of Higher Education Commission (NRU59-002-HR), Chulalongkorn University Centenary Academic Development Project (CU56-HR01), Ratchadaphiseksomphot Endowment Fund of Chulalongkorn University (RES560530093), The Outstanding Professor of Thailand Research Fund (DPG5480002), and The Center of Excellence in Clinical Virology of Chulalongkorn University (GCE 58-014-30-004). NT received the Overseas Research Experience Scholarship for Graduate Students of Chulalongkorn University. The specific roles of these authors are articulated in the ‘author contributions’ section. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.