Abstract
The current circulating influenza B viruses can be divided into two major phylogenetic lineages: the Victoria and Yamagata lineages. We conducted a survey of influenza B viruses in Hubei and Zhejiang provinces during 2009–2010. Out of 341 throat swabs, 18 influenza B viruses were isolated. Five isolates were selected for genetic and phylogenetic analysis. The molecular analyses revealed that all the isolates had similar antigenic characteristics to B/Brisbane/60/2008. However, in the three viruses isolated from Zhejiang, a single asparagine to aspartic acid substitution in position 197 was observed, thereby eliminating the glycosylation at that site and possibly causing an antigenic change. None of the viruses had amino acid mutations at positions 116, 149, 152, 198, 222, 250, 291, and 402 of the neuraminidase (NA) gene, predicting that the viruses would still be sensitive to NA inhibitors. Phylogenetic analyses revealed that all five isolates were closely related to B/Brisbane/60/2008—the 2010 vaccine strain—and contained Victoria-like hemagglutinin and Yamagata-like NA genes, suggesting that reassortment may had occurred. In addition, similar phylogenetic patterns among the acidic polymerase, nucleoprotein and matrix protein genes, as well as between the basic polymerase 1 and basic polymerase 2 genes, were observed, suggesting possible functional interactions among these proteins. All the results highlighted the importance of molecular monitoring of influenza B viruses for reassortment and antigenic drift.
Similar content being viewed by others
References
D. Jackson, R.A. Elderfield, W.S. Barclay, Molecular studies of influenza B virus in the reverse genetics era. J. Gen. Virol. 92, 1–17 (2011)
D. Bonn, Wild birds, poultry, and avian influenza. Lancet Infect. Dis. 6, 262 (2006)
H. Chen, G.J. Smith, S.Y. Zhang, K. Qin, J. Wang, K.S. Li, R.G. Webster, J.S. Peiris, Y. Guan, Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436, 191–192 (2005)
P. Davies, R.D. Barry, Nucleic acid of influenza virus. Nature 211, 384–387 (1966)
A.D. Osterhaus, G.F. Rimmelzwaan, B.E. Martina, T.M. Bestebroer, R.A. Fouchier, Influenza B virus in Seals. Science 288, 1051–1053 (2000)
S.E. Lindstrom, Y. Hiromoto, H. Nishimura, T. Saito, R. Nerome, K. Nerome, Comparative analysis of evolutionary mechanisms of the hemagglutinin and three internal protein genes of influenza B virus: multiple cocirculating lineages and frequent reassortment of the NP, M and NS genes. J. Virol. 73, 4413–4426 (1999)
R. Nerome, Y. Hiromoto, S. Sugita, N. Tanabe, M. Ishida, M. Matsumoto, S.E. Lindstrom, T. Takahashi, K. Nerome, Evolutionary characteristics of influenza B virus since its first isolation in 1940: dynamic circulation of deletion and insertion mechanism. Arch. Virol. 143, 1569–1583 (1998)
P.A. Rota, T.R. Wallis, M.W. Harmon, J.S. Rota, A.P. Kendal, K. Nerome, Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 175, 59–68 (1990)
M.W. Shaw, X. Xu, Y. Li, S. Normand, R.T. Ueki, G.Y. Kunimoto, H. Hall, A. Klimov, N.J. Cox, K. Subbarao, Reappearance and global spread of variants of influenza B/Victoria/2/87 lineage viruses in the 2000–2001 and 2001–2002 seasons. Virology 303, 1–8 (2002)
J.A. McCullers, T. Saito, A.R. Iverson, Multiple genotypes of influenza B virus circulated between 1979 and 2003. J. Virol. 78, 2817–12828 (2004)
S.R. Shih, G.W. Chen, C.C. Yang, W.Z. Yang, D.P. Liu, J.H. Lin, S.C. Chiu, H.Y. Chen, K.C. Tsao, C.G. Huang, Y.L. Huang, C.K. Mok, C.J. Chen, T.Y. Lin, J.R. Wang, C.L. Kao, K.H. Lin, L.K. Chen, H.L. Eng, Y.C. Liu, P.Y. Chen, J.S. Lin, J.H. Wang, C.W. Lin, Y.J. Chan, J.J. Lu, C.A. Hsiung, P.J. Chen, I.J. Su, Laboratory-based surveillance and molecular epidemiology of influenza virus in Taiwan. J. Clin. Microbiol. 43, 1651–1661 (2005)
F.C. Motta, M.M. Siqueira, A.K. Lugon, S.M. Straliotto, S.B. Fernandes, M.M. Krawczuk, The reappearance of Victoria lineage influenza B virus in Brazil, antigenic and molecular analysis. J. Clin. Virol. 36, 208–214 (2006)
World Health Organization, Recommended composition of influenza virus vaccines for use in the 2003 influenza season. Wkly. Epidemiol. Rec. 77, 341–348 (2002)
J.M. Chen, Y.J. Guo, J.F. Guo, J. Dong, Characterization of HA1 gene of influenza B virus circulated in 1990 through 2000 in China. Zhonghua Shi Yan he Lin Chuang Bing Du Xue Za Zhi 16, 278–280 (2002)
C.L. Wu, X.W. Chen, X. Wang, X. Lv, F. Yang, S.S. Fang, P.F. Wu, Phylogenetic evolution and molecular variation of influenza B viruses in Shenzhen, 2009. Dis. Surveill. 26, 442–445 (2011)
L.R. Zhang, Y.X. Lin, H.X. Li, Q.D. Wei, Phylogenetic analysis of HA1 gene of Victoria-like strain of influenza B viruses isolated in Zhuhai in 2008. Huanan Yu Fang Yi Xue 36, 33–35 (2010)
L. Zhou, X. Lv, X.W. Chen, S.S. Fang, Phylogenetic analysis of HA1 gene of Victoria-like strain of influenza B viruses isolated in Shenzhen in 2006–2007. Zhongguo Wei Sheng Jian Yan Za Zhi 18, 847–849 (2008)
S. Zou, A practical approach to genetic screening for influenza virus variants. J. Clin. Microbiol. 35, 2623–2627 (1997)
A.S. Agrawal, M. Sarkar, S. Chakrabarti, K. Rajendran, H. Kaur, A.C. Mishra, M.K. Chatterjee, T.N. Naik, M.S. Chadha, M. Chawla-Sarkar, Comparative evaluation of real-time PCR and conventional RT-PCR during a 2 year surveillance for influenza and respiratory syncytial virus among children with acute respiratory infections in Kolkata, India, reveals a distinct seasonality of infection. J. Med. Microbiol. 58, 1616–1622 (2009)
P.A. Rota, M.L. Hemphill, T. Whistler, H.L. Regnery, A.P. Kendal, Antigenic and genetic characterization of the haemagglutinins of recent cocirculating strains of influenza B virus. J. Gen. Virol. 73, 2737–2742 (1992)
J.C. Nancy, A.B. Catherine, The molecular epidemiology of influenza viruses. Semin. Virol. 6, 359–370 (1995)
I.G. Barr, N. Komadina, A. Hurt, R. Shaw, C. Durrant, P. Iannello, C. Tomasov, H. Sjogren, A.W. Hampson, Reassortants in recent influenza A and B isolates from South East Asia and Oceania. Virus Res. 98, 35–44 (2003)
X.S. Chi, T.V. Bolar, P. Zhao, R. Rappaport, S.M. Cheng, Cocirculation and evolution of two lineages of influenza B viruses in Europe and Israel in the 2001–2002 season. J. Clin. Microbiol. 41, 5770–5773 (2003)
J.A. McCullers, G.C. Wang, S. He, R.G. Webster, Reassortment and insertion-deletion are strategies for the evolution of influenza B viruses in nature. J. Virol. 73, 7343–7348 (1999)
Y. Hiromoto, T. Saito, S.E. Lindstrom, Y. Li, R. Nerome, S. Sugita, M. Shinjoh, K. Nerome, Phylogenetic analysis of the three polymerase genes (PB1, PB2 and PA) of influenza B virus. J. Gen. Virol. 81, 929–937 (2000)
C. Luo, T. Morishita, K. Satou, Y. Tateno, K. Nakajima, E. Nobusawa, Evolutionary pattern of influenza B viruses based on the HA and NS genes during 1940–1999: origin of the NS genes after 1997. Arch. Virol. 144, 1881–1891 (1999)
P. Davies, R.D. Barry, Nucleic acid of influenza virus. Nature 211, 384–387 (1966)
J. Shen, B.D. Kirk, J. Ma, Q. Wang, Diversifying selective pressure on influenza B virus hemagglutinin. J. Med. Virol. 81, 114–124 (2009)
Q. Wang, F. Cheng, M. Lu, X. Tian, J. Ma, Crystal structure of unliganded influenza B virus hemagglutinin. J. Virol. 82, 3011–3020 (2008)
S. Hatakeyama, N. Sugaya, M. Ito, M. Yamazaki, M. Ichikawa, K. Kimura, M. Kiso, H. Shimizu, C. Kawakami, K. Koike, K. Mitamura, Y. Kawaoka, Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA 297, 1435–1442 (2007)
T. Roy, A.S. Agrawal, A. Mukherjee, A.C. Mishra, M.S. Chadha, H. Kaur, M. Chawla-Sarkar, Surveillance and molecular characterization of human influenza B viruses during 2006–2010 revealed co-circulation of Yamagata-like and Victoria-like strains in eastern India. Infect. Genet. Evol. 11, 1595–1601 (2011)
E.D. Kilbourneil, The influenza viruses and influenza [M] (Academic Press, Orlando, 1975), pp. 449–481
T. Betakova, M.V. Nermut, A.J. Hay, The NB protein is an integral component of the membrane of influenza B virus. J. Gen. Virol. 77, 2689–2694 (1996)
D.L. Brassard, G.P. Leser, R.A. Lamb, Influenza B virus NB glycoprotein is a component of the virion. Virology 220, 350–360 (1996)
N.A. Sunstrom, L.S. Premkumar, A. Premkumar, G. Ewart, G.B. Cox, P.W. Gage, Ion channels formed by NB, an influenza B virus protein. J. Membr. Biol. 150, 127–132 (1996)
D. Jackson, W. Barclay, T. Zurcher, Characterization of recombinant influenza B viruses with key neuraminidase inhibitors resistance mutations. J. Antimicrob. Chemother. 55, 162–169 (2005)
Acknowledgments
This research was supported by the Ministry of Science and Technology of China (2010CB534005), the National Natural Science Foundation of China (30970024, 30900060) and Ninbo2011A610063; The Chinese Academy of Sciences INFO-115-C01-SDB3-01, SDB2-02, SDB4-21.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhu, N., Li, P., Yu, J. et al. Molecular characterization of influenza B viruses isolated in east-central China in 2009–2010. Virus Genes 46, 28–38 (2013). https://doi.org/10.1007/s11262-012-0826-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-012-0826-6