Evolutionary changes in the NA and HA genes of H3N2 influenza virus in the Moscow Region during 2003-2009
- Issue: Vol 56, No 5 (2011)
- Pages: 9-15
- Section: Articles
- Submitted: 09.06.2023
- Published: 15.10.2011
- URL: https://virusjour.crie.ru/jour/article/view/12094
- ID: 12094
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Abstract
During the winter 2009 outbreak in the Moscow Region, H3N2 influenza viruses were isolated from the nasopharyngeal washes of patients via their propagation in the human intestinal (Caco-2) and bronchial (Calu-3) epithelial cell cultures maintaining the proteolytic cleavage of HA0 → HA1+HA2 and multicycle virus replication. Analysis of the nucleotide sequences of virus RNA indicated that the 2009 viruses differed from those isolated in 2003 in 14 and 21 amino acids of the neuraminidase (NA) and hemagglutinin (HA) genes, respectively. The NA gene was 1762 nucleotides long whereas the 2003 isolates had a deletion of 66 nucleotides (22 amino acids) in the stalk region (short-stalk NA genotype) of viruses. The NA gene of the 2009 and 2003 isolates possessed an amino acid profile characterized for oseltamivir- and zanamivir-susceptible viral strains. The HA gene of the 2009 viruses contained an N-glycosylation site at Asn181 (an analog to Asn165 numbering from a signal peptide), which correlated with the long-stalk NA gene. The 2009 viruses had Phe209 in the HA receptor binding center whereas the 2003 isolates possessed Ser209, which correlated with their differences in HA activity. Phylogenetic analysis showed that the NA genes of the 2003 and 2009 Moscow strains were located in the same genetic clade with a single common precursor while their HA genes were diverged in more genetic distance and located in different clades. Viral distribution in the phylogenetic tree indicated that the Moscow strains isolated in 2009 were not direct ancestors of those isolated in 2003; and during the period of 2003 to 2009, H3N2 influenza virus with a short-stalk NA genotype was substituted for a migrant virus possessing a long-stalk NA gene.
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References
- Abed Y., Baz M., Boivin G. A novel neuraminidase deletion mutation conferring resistance to oseltamivir in clinical influenza A/H3N2 virus // J. Infect. Dis. - 2009. - Vol. 199, N 2. - P. 180-183.
- Air G. M., Els M. C., Brown L. E. et al. Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase // Virology. - 1985. - Vol. 145, N 2. - P. 237-248.
- Baigent S. J., McCauley J. W. Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture // Virus Res. - 2001. - Vol. 79. - P. 177-185.
- Blok J., Air G. M. Block deletions in the neuraminidase genes from some influenza A viruses of the N1 subtype // Virology. - 1982. - Vol. 118, N 1. - P. 229-234.
- Claas E. C. J., Osterhaus A. D. M. E., van Beek R. et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus // Lancet. - 1998. - Vol. 351. - P. 472-477.
- Els M. C., Air G. M., Murti K. G. et al. An 18-amino acid deletion in an influenza neuraminidase // Virology. - 1985. - Vol. 142, N 2. - P. 241-247.
- Fiore A. E., Uyeki T. M., Broder K. et al. Centers for Disease Control and Prevention (CDC). Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practice (ACIP) // MMWR Recomm. Rep. - 2010. - Vol. 59, N RR-8. - P. 1-62.
- Gulati S., Smith D. F., Air G. M. Deletion of neuraminidase and resistance to oseltamivir may be a consequence of restricted receptor specificity in recent H3N2 influenza viruses // Virol. J. - 2009. - Vol. 6. - P. 22-37.
- Luo G., Chung J., Palese P. Alterations of the stalk of the influenza virus neuraminidase: deletions and insertions // Virus Res. - 1993. - Vol. 29, N 3. - P. 321-330.
- Matrosovich M., Zhou N., Kawaoka Y., Webster R. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties // J. Virol. - 1999. - Vol. 73, N 2. - P. 1146-1155.
- Medeiros R., Escriou N., Naffakh N. et al. Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes // Virology. - 2001. - Vol. 289, N 1. - P. 74-85.
- Memoli M. J., Hrabal R. J., Hassantoufighi A. et al. Rapid selection of a transmissible multidrug-resistant influenza A/H3N2 virus in an immunocompromised host // J. Infect. Dis. - 2010. - Vol. 201, N 9. - P. 1397-1403.
- Moules V., Ferraris O., Terrier O. et al. In vitro characterization of naturally occurring influenza H3NA-viruses lacking the NA gene segment: toward a new mechanism of viral resistance? // Virology. - 2010. - Vol. 404, N 2. - P. 215-224.
- Nelson M. I., Simonsen L., Viboud C. et al. Stochastic processes are key determinants of short-term evolution in influenza A virus // PLoS Pathog. - 2006. - Vol. 2, N 12. - P. e125.
- Nelson M. I., Simonsen L., Viboud C. et al. Phylogenetic analysis reveals the global migration of seasonal influenza A viruses // PLoS Pathog. - 2007. - Vol. 3, N 9. - P. 1220-1228.
- Nobusawa E., Ishihara H., Morishita T. et al. Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides // Virology. - 2000. - Vol. 278. - P. 587-596.
- Okada J., Ohshima N., Kubota-Koketsu R. et al. Localization of epitopes recognized by monoclonal antibodies that neutralized the H3N2 influenza viruses in man // J. Gen. Virol. - 2011. - Vol. 92, N 1. - P. 230-241.
- Okomo-Adhiambo M., Nguyen H. T., Sleeman K. et al. Host cell selection of influenza neuraminidase variants: implications for drug resistance monitoring in A(H1N1) viruses // Antiviral Res. - 2010. - Vol. 85, N 2. - P. 381-388.
- Ruiz-Carrascoso G., Casas I., Pozo F. et al. Prolonged shedding of amantadine- and oseltamivir-resistant influenza A(H3N2) virus with dual mutations in an immunocompromised infant // Antiviral Ther. - 2010. - Vol. 15, N 7. - P. 1059-1063.
- Russell C. A., Jones T. C., Barr I. G. et al. The global circulation of seasonal influenza A(H3N2) viruses // Science. - 2008. - Vol. 320, N 5874. - P. 340-346.
- Sheu T. G., Deyde V. M., Okomo-Adhiambo M. et al. Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008 // Antimicrob. Agents Chemother. - 2008. - Vol. 52, N 9. - P. 3284-3292.
- Skehel J. J., Wiley D. C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin // Annu. Rev. Biochem. - 2000. - Vol. 69. - P. 531-569.
- Sorrell E. M., Song H., Pena L., Perez D. R. A 27-amino-acid deletion in the neuraminidase stalk supports replication of an avian H2N2 influenza A virus in the respiratory tract of chickens // J. Virol. - 2010. - Vol. 84, N 22. - P. 11831-11840.
- Taubenberger J. K., Kash J. C. Influenza virus evolution, host adaptation, and pandemic formation // Cell Host Microbe. - 2010. - Vol. 7, N 6. - P. 440-451.
- Wagner R., Matrosovich M., Klenk H. D. Functional balance between haemagglutinin and neuraminidase in influenza virus infections // Rev. Med. Virol. - 2002. - Vol. 12. - P. 159-166.
- Wright P. F., Neumann G., Kawaoka Y. // Fields virology / Eds D. M. Knipe et al. - Philadelphia, 2007. - P. 1691-1740.
- Zhirnov O. P., Klenk H. D. Human influenza viruses are proteolytically activated and do not induce apoptosis in CACO-2 cells // Virology. - 2003. - Vol. 313. - P. 198-200.
- Zhirnov O. P., Vorobjeva I. V., Saphonova O. A. et al. Biochemical properties of clinical influenza viruses propagated in human intestinal cell line // Biochemistry. - 2007. - Vol. 72, N 4. - P. 493-505.
- Zhirnov O. P., Vorobjeva I. V., Saphonova O. A. et al. Structural and evolutionary characteristics of HA, NA, NS, and M genes of clinical influenza A/H3N2 viruses passaged in human and canine cells // J. Clin. Virol. - 2009. - Vol. 45. - P. 332-343.