Lack of transmission of a human influenza virus with avian receptor specificity between ferrets is not due to decreased virus shedding but rather a lower infectivity in vivo

Journal of General Virology

Volumn 92, Issue 8, 2011, Pages 1822-1831

  Roberts, Kim L ^a   Shelton, Holly ^a   Scull, Margaret ^b,c   Pickles, Raymond ^b   Barclay, Wendy S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; SIALIC ACID; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DISEASE TRANSMISSION; EX VIVO STUDY; FEMALE; FERRET; FOWL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VIRUS A H3N2; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RECEPTOR BINDING; TURBINATE; UPPER RESPIRATORY TRACT; VIRUS ATTACHMENT; VIRUS INFECTIVITY; VIRUS SHEDDING; VIRUS TRANSMISSION; WILD TYPE;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; PROTEIN BINDING; RECEPTORS, VIRUS; RESPIRATORY SYSTEM; SPECIES SPECIFICITY; TURBINATES; VIRUS REPLICATION; VIRUS SHEDDING;

ANIMALIA; AVES; AVIAN INFLUENZA VIRUS; HUMAN INFLUENZA VIRUS; INFLUENZA A VIRUS; MAMMALIA; MUSTELA; ORTHOMYXOVIRIDAE;

EID: 79960364334     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.031203-0     Document Type: Article

References (41)

1. Belser, J. A., Blixt, O., Chen, L.-M., Pappas, C., Maines, T. R., Van Hoeven, N., Donis, R., Busch, J., McBride, R. & other authors (2008). Contemporary North American influenza H7 viruses possess human receptor specificity: implications for virus transmissibility. Proc Natl Acad Sci U S A 105, 7558-7563.
2. Bouvier, N. M., Lowen, A. C. & Palese, P. (2008). Oseltamivirresistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J Virol 82, 10052-10058.
3. Connor, R. J., Kawaoka, Y., Webster, R. G. & Paulson, J. C. (1994). Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205, 17-23.
4. Couceiro, J. N. S. S., Paulson, J. C. & Baum, L. G. (1993). Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 29, 155-165.
5. de Jong, M. D., Simmons, C. P., Thanh, T. T., Hien, V. M., Smith, G. J., Chau, T. N., Hoang, D. M., Chau, N. V., Khanh, T. H. & other authors (2006). Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12, 1203-1207.
6. Duan, S., Boltz, D. A., Seiler, P., Li, J., Bragstad, K., Nielsen, L. P., Webby, R. J., Webster, R. G. & Govorkova, E. A. (2010). Oseltamivirresistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. PLoS Pathog 6, e1001022.
7. Elleman, C. J. & Barclay, W. S. (2004). The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321, 144-153.
8. Ha, Y., Stevens, D. J., Skehel, J. J. & Wiley, D. C. (2003). X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus. Virology 309, 209-218.
9. Kesimer, M., Scull, M., Brighton, B., DeMaria, G., Burns, K., O'Neal, W., Pickles, R. J. & Sheehan, J. K. (2009). Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J 23, 1858-1868.
10. Kirkeby, S., Martel, C. J. & Aasted, B. (2009). Infection with human H1N1 influenza virus affects the expression of sialic acids of metaplastic mucous cells in the ferret airways. Virus Res 144, 225-232.
11. Lai, S. K., Wang, Y.-Y., Wirtz, D. & Hanes, J. (2009). Micro- and macrorheology of mucus. Adv Drug Deliv Rev 61, 86-100.
12. Leigh, M. W., Connor, R. J., Kelm, S., Baum, L. G. & Paulson, J. C. (1995). Receptor specificity of influenza virus influences severity of illness in ferrets. Vaccine 13, 1468-1473.
13. Maines, T. R., Chen, L.-M., Matsuoka, Y., Chen, H., Rowe, T., Ortin, J., Falcón, A., Nguyen, T. H., Mai, Q. & other authors (2006). Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103, 12121-12126.
14. Matrosovich, M. & Klenk, H.-D. (2003). Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor binding. Rev Med Virol 13, 85-97.
15. Matrosovich, M. N., Gambaryan, A. S., Teneberg, S., Piskarev, V. E., Yamnikova, S. S., Lvov, D. K., Robertson, J. S. & Karlsson, K.-A. (1997). Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233, 224-234.
16. Matrosovich, M., Tuzikov, A., Bovin, N., Gambaryan, A., Klimov, A., Castrucci, M. R., Donatelli, I. & Kawaoka, Y. (2000). Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74, 8502-8512.
17. Matrosovich, M. N., Matrosovich, T. Y., Gray, T., Roberts, N. A. & Klenk, H.-D. (2004). Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A 101, 4620-4624.
18. Matrosovich, M., Matrosovich, T., Uhlendorff, J., Garten, W. & Klenk, H.-D. (2007). Avian-virus-like receptor specificity of the hemagglutinin impedes influenza virus replication in cultures of human airway epithelium. Virology 361, 384-390.
19. Matsuoka, Y., Lamirande, E. W. & Subbarao, K. (2009). The ferret model for influenza. Curr Protoc Microbiol 13, 15G.2.1-15G.2.29.
20. Mubareka, S., Lowen, A. C., Steel, J., Coates, A. L., García-Sastre, A. & Palese, P. (2009). Transmission of influenza virus via aerosols and fomites in the guinea pig model. J Infect Dis 199, 858-865.
21. Naeve, C. W., Hinshaw, V. S. & Webster, R. G. (1984). Mutations in the hemagglutinin receptor-binding site can change the biological properties of an influenza virus. J Virol 51, 567-569.
22. Neumann, G., Watanabe, T., Ito, H., Watanabe, S., Goto, H., Gao, P., Hughes, M., Perez, D. R., Donis, R. & other authors (1999). Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96, 9345-9350.
23. Pappas, C., Viswanathan, K., Chandrasekaran, A., Raman, R., Katz, J. M., Sasisekharan, R. & Tumpey, T. M. (2010). Receptor specificity and transmission of H2N2 subtype viruses isolated from the pandemic of 1957. PLoS ONE 5, e11158.
24. Scull, M. A., Gillim-Ross, L., Santos, C., Roberts, K. L., Bordonali, E., Subbarao, K., Barclay, W. S. & Pickles, R. J. (2009). Avian influenza virus glycoproteins restrict virus replication and spread through human airway epithelium at temperatures of the proximal airways. PLoS Pathog 5, e1000424.
25. Shelton, H., Ayora-Talavera, G., Ren, J., Loureiro, S., Pickles, R. J., Barclay, W. S. & Jones, I. M. (2011). Receptor binding profiles of avian influenza virus hemagglutinin subtypes on human cells as a predictor of pandemic potential. J Virol 85, 1875-1880.
26. Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N. & Kawaoka, Y. (2006). Avian flu: influenza virus receptors in the human airway. Nature 440, 435-436.
27. Song, H., Wan, H., Araya, Y. & Perez, D. R. (2009). Partial direct contact transmission in ferrets of a mallard H7N3 influenza virus with typical avian-like receptor specificity. Virol J 6, 126.
28. Sorrell, E. M., Wan, H., Araya, Y., Song, H. & Perez, D. R. (2009). Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci U S A 106, 7565-7570.
29. Steel, J., Lowen, A. C., Mubareka, S. & Palese, P. (2009). Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5, e1000252.
30. Steel, J., Staeheli, P., Mubareka, S., García-Sastre, A., Palese, P. & Lowen, A. C. (2010). Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J Virol 84, 21-26.
31. Taubenberger, J. K. & Morens, D. M. (2010). Influenza: the once and future pandemic. Public Health Rep 125 (Suppl. 3), 16-26.
32. Tellier, R. (2009). Aerosol transmission of influenza A virus: a review of new studies. J R Soc Interface 6 (Suppl. 6), S783-S790.
33. Thomas, Y., Vogel, G., Wunderli, W., Suter, P., Witschi, M., Koch, D., Tapparel, C. & Kaiser, L. (2008). Survival of influenza virus on banknotes. Appl Environ Microbiol 74, 3002-3007.
34. Thompson, C. I., Barclay, W. S., Zambon, M. C. & Pickles, R. J. (2006). Infection of human airway epithelium by human and avian strains of influenza A virus. J Virol 80, 8060-8068.
35. Tumpey, T. M., Maines, T. R., Van Hoeven, N., Glaser, L., Solórzano, A., Pappas, C., Cox, N. J., Swayne, D. E., Palese, P. & other authors (2007). A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315, 655-659.
36. Van Hoeven, N., Pappas, C., Belser, J. A., Maines, T. R., Zeng, H., García-Sastre, A., Sasisekharan, R., Katz, J. M. & Tumpey, T. M. (2009). Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc Natl Acad Sci U S A 106, 3366-3371.
37. van Riel, D., Munster, V. J., de Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D. & Kuiken, T. (2006). H5N1 virus attachment to lower respiratory tract. Science 312, 399.
38. van Riel, D., Munster, V. J., de Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D. & Kuiken, T. (2007). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171, 1215-1223.
39. Wan, H., Sorrell, E. M., Song, H., Hossain, M. J., Ramirez-Nieto, G., Monne, I., Stevens, J., Cattoli, G., Capua, I. & other authors (2008). Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS ONE 3, e2923.
40. Xu, Q., Wang, W., Cheng, X., Zengel, J. & Jin, H. (2010). Influenza H1N1 A/Solomon Island/3/06 virus receptor binding specificity correlates with virus pathogenicity, antigenicity, and immunogenicity in ferrets. J Virol 84, 4936-4945.
41. Yen, H.-L., Lipatov, A. S., Ilyushina, N. A., Govorkova, E. A., Franks, J., Yilmaz, N., Douglas, A., Hay, A., Krauss, S. & other authors (2007). Inefficient transmission of H5N1 influenza viruses in a ferret contact model. J Virol 81, 6890-6898.