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Entry of the bat influenza H17N10 virus into mammalian cells is enabled by the MHC class II HLA-DR receptor

Nature Microbiology volume 4, pages 2035–2038 (2019)Cite this article

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Abstract

Haemagglutinin and neuraminidase surface glycoproteins of the bat influenza H17N10 virus neither bind to nor cleave sialic acid receptors, indicating that this virus employs cell entry mechanisms distinct from those of classical influenza A viruses. We observed that certain human haematopoietic cancer cell lines and canine MDCK II cells are susceptible to H17-pseudotyped viruses. We identified the human HLA-DR receptor as an entry mediator for H17 pseudotypes, suggesting that H17N10 possesses zoonotic potential.

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Fig. 1: The H17N10 cellular receptor(s) is not ubiquitous and is proteinaceous.
Fig. 2: Surface expression of HLA-DR is a key determinant for entry of H17 pseudotypes into mammalian cells.

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Data availability

Microarray data are available at the Gene Expression Omnibus (GEO) repository under the series record number GSE14837. All other data supporting the findings of this study are available from the corresponding author on request.

References

  1. Tong, S. et al. Proc. Natl Acad. Sci. USA 109, 4269–4274 (2012).

    Article  CAS  Google Scholar 

  2. Tong, S. et al. PLoS Pathog. 9, e1003657 (2013).

    Article  Google Scholar 

  3. Ciminski, K. et al. J. Gen. Virol. 98, 2393–2400 (2017).

    Article  CAS  Google Scholar 

  4. Long, J. S., Mistry, B., Haslam, S. M. & Barclay, W. S. Nat. Rev. Microbiol. 17, 67–81 (2019).

    Article  CAS  Google Scholar 

  5. Sun, X. et al. Cell Rep. 3, 769–778 (2013).

    Article  CAS  Google Scholar 

  6. Zhu, X. et al. Proc. Natl Acad. Sci. USA 109, 18903–18908 (2012).

    Article  CAS  Google Scholar 

  7. Juozapaitis, M. et al. Nat. Commun. 5, 4448 (2014).

    Article  CAS  Google Scholar 

  8. Wu, Y. et al. Trends Microbiol. 22, 183–191 (2014).

    Article  CAS  Google Scholar 

  9. Maruyama, J. et al. Virology 488, 43–50 (2016).

    Article  CAS  Google Scholar 

  10. Moreira, E. A. et al. Proc. Natl Acad. Sci. USA 113, 12797–12802 (2016).

    Article  CAS  Google Scholar 

  11. Hoffmann, M. et al. PLoS ONE 11, e0152134 (2016).

    Article  Google Scholar 

  12. Carnell, G. W. et al. Front. Immunol. 6, 161 (2015).

    Article  Google Scholar 

  13. Carnell, G. et al. Preprint at https://www.biorxiv.org/content/10.1101/499947v2 (2018).

  14. Dukes, J. D. et al. BMC Cell Biol. 12, 43 (2011).

    Article  CAS  Google Scholar 

  15. Roche, P. A. et al. Nat. Rev. Immunol. 15, 203–216 (2015).

    Article  CAS  Google Scholar 

  16. Ziegler, A. et al. Immunobiology 171, 77–92 (1986).

    Article  CAS  Google Scholar 

  17. Karakus, U. et al. Nature 567, 109–112 (2019).

    Article  CAS  Google Scholar 

  18. de Vries, E. et al. Proc. Natl Acad. Sci. USA 109, 7457–7462 (2012).

    Article  Google Scholar 

  19. Giotis, E. S. et al. Sci. Rep. 7, 17485 (2017).

    Article  CAS  Google Scholar 

  20. Kall, L. et al. Nucleic Acids Res. 35, W429–W432 (2007).

    Article  Google Scholar 

  21. Krogh, A. et al. J. Mol. Biol. 305, 567–580 (2001).

    Article  CAS  Google Scholar 

  22. Almagro-Armenteros, J. J. et al. Bioinformatics 33, 4049 (2017).

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. Kaufman, Y. Guo, I. Elbusifi, D. Quinn, A. Ho, K. Ciminski and M. Schwemmle for their support. Cells were kindly provided by E. Wright (University of Sussex, Falmer, UK), K. Paschos, R. White, M. Dorner, M. Edwards, P. Farrell and R. Shattock (Imperial College London, London, UK). This research was undertaken with the financial support of the Biotechnology and Biological Sciences Research Council (BBSRC) (http://www.bbsrc.ac.uk) via the Strategic LoLa grant BB/K002465/1 ‘Developing Rapid Responses to Emerging Virus Infections of Poultry (DRREVIP)’ and the Octoberwoman Foundation. L.-F.W. is supported by the Singapore National Research Foundation grants (NRF2012NRF-CRP001-056 and NRF2016NRF-NSFC002-013).

Author information

Author notes

  1. George Carnell

    Present address: Laboratory of Viral Zoonotics, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK

  2. Erik F. Young

    Present address: Bioelectronic Systems Lab, Columbia University, New York, NY, USA

Authors and Affiliations

  1. Section of Virology, Department of Medicine, Imperial College London, London, UK

    Efstathios S. Giotis, Wendy S. Barclay & Michael A. Skinner

  2. Viral Pseudotype Unit, Medway School of Pharmacy, University of Kent and University of Greenwich, Chatham, UK

    George Carnell & Nigel Temperton

  3. Department of Surgery, Hackensack University Medical Center, Hackensack, NJ, USA

    Erik F. Young

  4. The Genomics Center, New Jersey Medical School, Rutgers University, Newark, NJ, USA

    Saleena Ghanny & Patricia Soteropoulos

  5. Programme in Emerging Infectious Disease, Duke-NUS Medical School, Singapore, Singapore

    Lin-Fa Wang

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  1. Efstathios S. Giotis
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Contributions

E.S.G. conceived, designed and performed the experiments, analysed the data and wrote the manuscript. G.C. generated the luciferase reporter plasmids, produced the pseudotype viral stocks and wrote the manuscript. E.F.Y., S.G. and P.S. performed the microarray work. W.S.B., M.A.S. and N.T. designed the experiments and wrote the manuscript. L.-F.W. provided materials and engaged in discussion of the project.

Corresponding author

Correspondence to Efstathios S. Giotis.

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Ethics statement

The buffy coat residues for the isolation of CD19+ primary B cells were purchased from the UK Blood Transfusion Service from anonymous volunteer blood donors. Therefore, no ethical approval is required.

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The authors declare no competing interests.

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Supplementary Information

Supplementary Discussion, Supplementary Tables 1 and 2, Supplementary Figs. 1–7 and Supplementary References.

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Giotis, E.S., Carnell, G., Young, E.F. et al. Entry of the bat influenza H17N10 virus into mammalian cells is enabled by the MHC class II HLA-DR receptor. Nat Microbiol 4, 2035–2038 (2019). https://doi.org/10.1038/s41564-019-0517-3

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