Skip to main content
SpringerLink
Log in

Multiple amino acid substitutions involved in the adaptation of avian-origin influenza A (H10N7) virus in mice

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

To identify substitutions that are possibly associated with the adaptation of avian-origin H10N7 virus to mammals, adaptation of the H10N7 virus in mouse lung was carried out by serial lung-to-lung passage. Genomic analysis of the mouse-adapted virus revealed amino acid changes in the PB2 (E627K), PA (T97I), and HA (G409E) proteins, and this virus was more virulent in mice than the wild-type virus. Our results suggest that these substitutions are involved in the enhancement of the replication efficiency of avian-origin H10N7 virus, resulting in severe disease in mice. Continued poultry surveillance of these substitutions in H10N7 viruses is required.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  1. Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Chan KH, Tsoi HW, Teng JL, Song W, Wang P, Lau SY, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY (2013) Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381:1916–1925

    Article  CAS  PubMed  Google Scholar 

  2. Wei SH, Yang JR, Wu HS, Chang MC, Lin JS, Lin CY, Liu YL, Lo YC, Yang CH, Chuang JH, Lin MC, Chung WC, Liao CH, Lee MS, Huang WT, Chen PJ, Liu MT, Chang FY (2013) Human infection with avian influenza A H6N1 virus: an epidemiological analysis. Lancet Respir Med 1:771–778

    Article  PubMed  Google Scholar 

  3. To KK, Tsang AK, Chan JF, Cheng VC, Chen H, Yuen KY (2014) Emergence in China of human disease due to avian influenza A(H10N8)–cause for concern? J Infect 68:205–215

    Article  PubMed  Google Scholar 

  4. Ma C, Lam TT, Chai Y, Wang J, Fan X, Hong W, Zhang Y, Li L, Liu Y, Smith DK, Webby RJ, Peiris JS, Zhu H, Guan Y (2015) Emergence and evolution of H10 subtype influenza viruses in poultry in China. J Virol 89:3534–3541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Serena Beato M, Terregino C, Cattoli G, Capua I (2006) Isolation and characterization of an H10N7 avian influenza virus from poultry carcasses smuggled from China into Italy. Avian Pathol 35:400–403

    Article  PubMed  Google Scholar 

  6. Su C, Chen S, Liu X, Xu J, Huang K, Liu K, Huang J, Peng D, Liu X (2013) Genome sequence of a novel H10N9 avian influenza virus isolated from chickens in a live poultry market in Eastern China. Genome Announc 1(4). doi:10.1128/genomeA.00386-13

  7. Zohari S, Neimanis A, Harkonen T, Moraeus C, Valarcher JF (2014) Avian influenza A (H10N7) virus involvement in mass mortality of harbour seals (Phoca vitulina) in Sweden, March through October 2014. Euro Surveill 19

  8. Zohari S, Metreveli G, Kiss I, Belak S, Berg M (2010) Full genome comparison and characterization of avian H10 viruses with different pathogenicity in Mink (Mustela vison) reveals genetic and functional differences in the non-structural gene. Virol J 7:145

    Article  PubMed  PubMed Central  Google Scholar 

  9. Arzey GG, Kirkland PD, Arzey KE, Frost M, Maywood P, Conaty S, Hurt AC, Deng YM, Iannello P, Barr I, Dwyer DE, Ratnamohan M, McPhie K, Selleck P (2012) Influenza virus A (H10N7) in chickens and poultry abattoir workers, Australia. Emerg Infect Dis 18:814–816

    Article  PubMed  PubMed Central  Google Scholar 

  10. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, Fan G, Yang F, Li X, Zhou J, Zou S, Yang L, Chen T, Dong L, Bo H, Zhao X, Zhang Y, Lan Y, Bai T, Dong J, Li Q, Wang S, Li H, Gong T, Shi Y, Ni X, Li J, Fan J, Wu J, Zhou X, Hu M, Wan J, Yang W, Li D, Wu G, Feng Z, Gao GF, Wang Y, Jin Q, Liu M, Shu Y (2014) Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383:714–721

    Article  PubMed  Google Scholar 

  11. Montomoli E, Maria TC (2014) Is influenza A/H10N8 a potential candidate for the next pandemic? Pathog Glob Health 108:213

    Article  PubMed  PubMed Central  Google Scholar 

  12. Yao Y, Wang H, Chen Q, Zhang H, Zhang T, Chen J, Xu B, Sun B, Chen Z (2013) Characterization of low-pathogenic H6N6 avian influenza viruses in central China. Arch Virol 158:367–377

    Article  CAS  PubMed  Google Scholar 

  13. Chen Q, Yu Z, Sun W, Li X, Chai H, Gao X, Guo J, Zhang K, Feng N, Zheng X, Wang H, Zhao Y, Qin C, Huang G, Yang S, Qian J, Gao Y, Xia X, Wang T, Hua Y (2015) Adaptive amino acid substitutions enhance the virulence of an H7N7 avian influenza virus isolated from wild waterfowl in mice. Vet Microbiol 177:18–24

    Article  CAS  PubMed  Google Scholar 

  14. Wu H, Lu R, Wu X, Peng X, Xu L, Cheng L, Lu X, Jin C, Xie T, Yao H, Wu N (2015) Novel reassortant H10N7 avian influenza viruses isolated from chickens in Eastern China. J Clin Virol 65:58–61

    Article  CAS  PubMed  Google Scholar 

  15. Reed L, Muench H (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27:493–497

    Google Scholar 

  16. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275–2289

    Article  CAS  PubMed  Google Scholar 

  17. Shinya K, Hamm S, Hatta M, Ito H, Ito T, Kawaoka Y (2004) PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320:258–266

    Article  CAS  PubMed  Google Scholar 

  18. Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, Tyler S, Brown EG (2010) PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol 84:10606–10618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tan L, Su S, Smith DK, He S, Zheng Y, Shao Z, Ma J, Zhu H, Zhang G (2014) A combination of HA and PA mutations enhances virulence in a mouse-adapted H6N6 influenza A virus. J Virol 88:14116–14125

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, Brown EG, Liu J (2012) Mouse-adapted H9N2 influenza A virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One 7:e40752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Song MS, Pascua PN, Lee JH, Baek YH, Lee OJ, Kim CJ, Kim H, Webby RJ, Webster RG, Choi YK (2009) The polymerase acidic protein gene of influenza a virus contributes to pathogenicity in a mouse model. J Virol 83:12325–12335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Belser JA, Gustin KM, Pearce MB, Maines TR, Zeng H, Pappas C, Sun X, Carney PJ, Villanueva JM, Stevens J, Katz JM, Tumpey TM (2013) Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 501:556–559

    Article  CAS  PubMed  Google Scholar 

  23. Brown EG (1990) Increased virulence of a mouse-adapted variant of influenza A/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol 64:4523–4533

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Yu Z, Sun W, Li X, Chen Q, Chai H, Gao X, Guo J, Zhang K, Wang T, Feng N, Zheng X, Wang H, Zhao Y, Qin C, Huang G, Yang S, Hua Y, Zhang X, Gao Y, Xia X (2015) Adaptive amino acid substitutions enhance the virulence of a reassortant H7N1 avian influenza virus isolated from wild waterfowl in mice. Virology 476:233–239

    Article  CAS  PubMed  Google Scholar 

  25. Yu Z, Cheng K, Xin Y, Sun W, Li X, Huang J, Zhang K, Yang S, Wang T, Zheng X, Wang H, Hua Y, Chai H, Qin C, Qian J, Gao Y, Xia X (2014) Multiple amino acid substitutions involved in the adaptation of H6N1 avian influenza virus in mice. Vet Microbiol 174:316–321

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by Grants from the National Science Foundation of the People’s Republic of China (81502852), Zhejiang Provincial Natural Science Foundation of China (Y15H190006), and the Independent Task of State Key Laboratory for Diagnosis and Treatment of Infectious Diseases (Nos. 2014ZZ12 and 2015ZZ05).

Author information

Authors and Affiliations

  1. State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, 79 Qingchun Road, Hangzhou, 310003, Zhejiang, China

    Haibo Wu, Xiuming Peng, Xiaorong Peng, Linfang Cheng, Changzhong Jin, Xiangyun Lu, Tiansheng Xie, Hangping Yao & Nanping Wu

Authors
  1. Haibo Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiuming Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaorong Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Linfang Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Changzhong Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiangyun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tiansheng Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hangping Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nanping Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nanping Wu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 77 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, H., Peng, X., Peng, X. et al. Multiple amino acid substitutions involved in the adaptation of avian-origin influenza A (H10N7) virus in mice. Arch Virol 161, 977–980 (2016). https://doi.org/10.1007/s00705-015-2722-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-015-2722-6

Keywords

Search

Navigation