Glycosylation changes in the globular head of H3N2 influenza hemagglutinin modulate receptor binding without affecting virus virulence

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Alymova, Irina V ^a   York, Ian A ^a   Air, Gillian M ^b   Cipollo, John F ^c   Gulati, Shelly ^b   Baranovich, Tatiana ^d   Kumar, Amrita ^a,e   Zeng, Hui ^a   Gansebom, Shane ^a   McCullers, Jonathan A ^d,f  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e BATTELLE MEMORIAL INSTITUTE   (United States)

^f UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ, HUMAN INFLUENZA A VIRUS; INFLUENZA VIRUS HEMAGGLUTININ;

A-549 CELL LINE; ANIMAL; CHLOROCEBUS AETHIOPS; DOG; GENETICS; GLYCOSYLATION; HUMAN; INFLUENZA A VIRUS (H3N2); MDCK CELL LINE; METABOLISM; PATHOGENICITY; VERO CELL LINE; VIRUS ATTACHMENT;

A549 CELLS; ANIMALS; CERCOPITHECUS AETHIOPS; DOGS; GLYCOSYLATION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; MADIN DARBY CANINE KIDNEY CELLS; VERO CELLS; VIRUS ATTACHMENT;

EID: 84994013705     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep36216     Document Type: Article

References (50)

1. Kawaoka, Y., Krauss, S. & Webster, R. G. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J. Virol. 63, 4603-4608 (1989).
2. Doshi P. Trends in recorded influenza mortality: United States, 1900-2004. Am. J. Public Health 98, 939-945 (2008).
3. Fleming, D. M. & Elliot, A. J. Lessons from 40 years' surveillance of influenza in England and Wales. Epidemiol. Infect. 136, 866-875 (2008).
4. Reichert, T. A. et al. Influenza and the winter increase in mortality in the United States, 1959-1999. Am. J. Epidemiol. 160, 492-502 (2004).
5. Suzuki Y. Positive selection for gains of N-linked glycosylation sites in hemagglutinin during evolution of H3N2 human influenza A virus. Genes Genet. Syst. 86, 287-294 (2011).
6. Wiley, D. C., Wilson, I. A. & Skehel, J. J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289, 373-378 (1981).
7. Ekiert, D. C. et al. Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489, 526-532 (2012).
8. Zhirnov, O. P. 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. 45, 322-333 (2009).
9. Schulze, I. T. Effects of glycosylation on the properties and functions of influenza virus hemagglutinin. J. Infect. Dis. 176, 24-28 (1997).
10. Abe, Y. et al. Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. J. Virol. 78, 9605-9611 (2004).
11. Vigerust, D. J. et al. N-linked glycosylation attenuates H3N2 influenza viruses. J. Virol. 81, 8593-8600 (2007).
12. Hrincius, E. R. et al. Acute lung injury results from innate sensing of viruses by an ER stress pathway. Cell Rep. 11, 1591-1603 (2015).
13. Gulati, S. et al. Human H3N2 influenza viruses isolated from 1968 to 2012 show varying preference for receptor substructures with no apparent consequences for disease or spread. PLOS One 8, e66325 (2013).
14. Yang, H. et al. Structure and receptor binding preferences of recombinant human A(H3N2) virus hemagglutinins. Virology 477, 18-31 (2015).
15. Nobusawa, E., Ishihara, H., Morishita, T., Sato, K. & Nakajima, K. 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 278, 587-596 (2000).
16. Mendeiros, R., Escriou, N., Naffakh, N., Manuguerra, J. C. & van der Werf, S. Hemagglutinin residues of recent human A (H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 289, 74-75 (2001).
17. Thompson, C. I., Barclay, W. S. & Zambon, M. C. Changes in in vitro susceptibility of influenza A H3N2 viruses to a neuraminidase inhibitor during evolution in the human host. J. Antimicrob. Chemother. 53, 759-765 (2004).
18. Lin, Y. P. et al. Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc. Nat. Acad. Sci. 109, 21474-21479 (2012).
19. Oh, D. Y., Barr, I. G., Mosse, J. A. & Laurie, K. L. MDCK-SIAT1 cells show improved isolation rates for recent human influenza viruses compared to conventional MDCK cells. J. Clin. Microbiol. 46, 2189-2194 (2008).
20. Stevens J. et al. Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J. Virol. 84, 8287-8299 (2010).
21. Moshin, M. A., Morris, S. J., Smith, H. & Sweet, C. Correlation between levels of apoptosis, levels of infection and haemagglutinin receptor binding interaction of various subtypes of influenza virus: does the viral neuraminidase have a role in this associations. Virus Res. 85, 123-131 (2002).
22. Owen, R. E. et al. Alterations in receptor binding properties of recent human H3N2 viruses are associated with reduced killer cell lysis of infected cells. J. Virol. 81, 11170-11178 (2007).
23. Ohuchi, M., Ohuchi, R., Feldmann, A. & Klenk, H. D. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J. Virol. 71, 8377-8384 (1997).
24. Kasson, P. M. & Pande, V. S. Structural basis for influence of viral glycans on ligand binding by influenza hemagglutinin. Biophys. J. 95, L48-L50 (2008).
25. Wang, C. C. et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc. Natl. Acad. Sci. USA 106, 18137-18142 (2009).
26. Hartley, C. A., Reading, P. C., Ward, A. C. & Anders, E. M. Changes in the hemagglutinin molecule of influenza type A (H3N2) virus associated with increased virulence in mice. Arch. Virol. 142, 75-88 (1997).
27. Walter, T. et al. Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLOS Path. 9, e1003223 (2013).
28. Ito, T. et al. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 227, 493-499 (1997).
29. Aich, U. et al. Glycomics-based analysis of chicken red blood cells provides insight into the selectivity of the vital agglutination assay. FEBS J. 278, 1699-1712 (2011).
30. Abed, Y. et al. Characterization of 2 influenza A(H3N2) clinical isolates with reduced susceptibility to neuraminidase inhibitors due to mutations in the hemagglutinin gene. J. Infect. Dis. 186, 1074-1080 (2002).
31. Grainger, C. I., Greenwell, L. L., Lockley, D. J., Martin, G. P. & Forbes, B. Culture of Calu-3 cells at the air interface provides a representative model of the airway epithelial barrier. Parm. Res. 23, 1482-1490 (2006).
32. Zeng, H. et al. Highly pathogenic avian influenza H5N1 viruses elicit an attenuated type I interferon response in polarized human bronchial epithelial cells. J. Virol. 81, 12439-12449 (2007).
33. Harcourt, J. L. & Haynes, L. M. Establishing a liquid-covered culture of polarized human epithelial Calu-3 cells to study host cell response to respiratory pathogens in vitro. J. Visual. Exp. 72, 1-7 (2013).
34. Tellier, R. Review of aerosol transmission of influenza A virus. Emerg. Infect. Dis. J. 12, 1657-1662 (2006).
35. Gallagher, P., Henneberry, J., Wilson, I., Sambrook, J. & Gething, M. J. Addition of carbohydrate side chains at novel sites on influenza virus hemagglutinin can modulate the folding, transport, and activity of the molecule. J. Cell Biol. 107, 2059-2073 (1988).
36. An, Y., McCullers, J. A., Alymova, I., Parson, L. M. & Cipollo, J. F. Glycosylation analysis of engineered H3N2 influenza A virus hemagglutinins with sequentially added historically relevant glycosylation sites. J. Proteome Res. 14, 3957-3969 (2015).
37. Nunes-Correia, I. & Ramalho-Santos. Interactions of influenza virus with cultured cells: detailed kinetic modeling of binding and endocytosis. Biochem. 38, 1095-1101 (1999).
38. Stray, S. J., Cummings, R. D. & Air, G. M. Influenza virus infection of desialylated cells. Glycobiology 10, 649-658 (2000).
39. Narasaraju, T. et al. Adaptation of human influenza H3N2 virus in a mouse model: insights onto viral virulence, tissue tropism and host pathogenesis. Microbes Infect. 11, 2-11 (2009).
40. Chu, V. C. & Whittaker, G. R. Influenza virus entry and infection require host cell N-linked glycoprotein. Proc. Natl. Acad. Sci. USA 101, 18153-18158 (2004).
41. Leung, H. S. Y. et al. Entry of influenza A virus with a α 2,6-linked sialic acid binding preference requires host fibronectin. J. Virol. 86, 10704-10713 (2012).
42. Eierhoff, T., Hrincius, E. R., Rescher, U., Ludwig, S. & Ehrhardt, C. The epidermal growth factor receptor (EGFR) promotes uptake of influenza A viruses (IAV) into host cells. PLoS Pathog. 6, e1001099 (2010).
43. Nycholat, C. M. et al. Recognition of sialylated poly-LacNAc on N- and O-linked glycans by human and avian influenza A virus hemagglutinins. Angew Chem. Int. Ed. Engl. 51, 4860-4863 (2012).
44. Pickles, R. J. et al. Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer. J. Virol. 72, 6014-6023 (1998).
45. Smith, D. J. et al. Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371-376 (2004).
46. Koel, B. F. et al. Substitutions near receptor binding site determine major antigenic change during influenza virus evolution. Science 342, 976-979 (2013).
47. Condit, R. C. 2007. In Principles of Virology. V. 1, 25-57 (Lippincott Williams & Wilkins, 2007).
48. Thompson, S. D., Laver, W. G., Murti, K. G. & Portner, A. Isolation of a biologically active soluble form of the hemagglutinin-neuraminidase protein of Sendai virus. J. Virol. 62, 4653-4660 (1988).
49. Reece, P. A. Neuraminidase inhibitor resistance to influenza viruses. J. Med. Virol. 79, 1577-1586 (2007).
50. Heimburg-Molinaro, J. et al. Probing virus-glycan interactions using glycan microarrays. Methods Mol. Biol. 808, 251-267 (2012).