Sialic acid profiles in the respiratory tracts of selected species of raptors: evidence for potential binding sites for human and avian influenza A viruses
Chun-Hua Han A C , Jian Lin A C , Xiuqing Wang B , Jing-Wen Han A , Hui-Juan Duan A , Jie Pan A and Yue-Huan Liu A D
+ Author Affiliations
- Author Affiliations
A Institute of Animal and Husbandry Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China.
B Department of Biology and Microbiology, South Dakota State University, Brookings, SD, USA.
C Chun-Hua Han and Jian Lin contributed equally to this work.
D Corresponding author. Email: liuyuehuan@sina.com
Wildlife Research 38(8) 647-652 https://doi.org/10.1071/WR11003
Submitted: 5 January 2011 Accepted: 16 August 2011 Published: 23 November 2011
Abstract
Context: The ability of influenza A viruses to recognise and bind to cell surface receptors such as sialic acid linked to galactose by an α2,3 linkage (SAα2,3-gal) and sialic acid linked to galactose by an α2,6 linkage (SAα2,6-gal) is a major determinant of influenza A virus infection. Although the epidemiological surveys of influenza A virus infection in raptors suggest that some raptor species are susceptible to influenza A viruses under natural conditions, the sialic acid profiles in the respiratory and intestinal tracts of raptors are unknown.
Aims: To examine the sialic acid receptor profiles in the respiratory tracts of the selected raptor species and assess the potential susceptibility of raptors to avian and human influenza viruses and the role of raptors in the epidemiology and evolution of influenza A viruses.
Methods: The lectin immunohistochemistry staining method was used to examine the sialic acid profiles in the respiratory tracts of eight different species of raptors.
Key results: A strong staining with Maackia amurensis agglutinin (MAA), specific for sialic acid linked to galactose by an α2,3 linkage (SAα2,3-gal), was observed in the epithelial cells of the respiratory tract of Accipiter nisus and Falco tinnunculus. However, a positive staining for both MAA and Sambucus nigra agglutinin (SNA), specific for sialic acid linked to galactose by an α2,6 linkage (SAα2,6-gal), was detected in the epithelial cells of the upper respiratory tract of Accipiter gularis, Buteo buteo, Otus sunia, Bubo bubo and Asio otus, and in the epithelial cells of the alveoli of Buteo buteo, Falco peregrinus, Otus sunia and Bubo bubo.
Conclusions: Both avian and human influenza A virus receptors are expressed in six species of raptors examined. There are some variations in the type and distribution of sialic acid receptor expression among different raptor species. No correlation between phylogeny of birds and their sialic acid receptor distributions was observed.
Implications: Since SAα2,3-gal and SAα2,6-gal are often considered as the primary receptors for avian influenza A viruses and human influenza A viruses, respectively, our data suggest that raptors could be a potential host for avian and human influenza A viruses.
Additional keywords: influenza A virus, MAA, raptor, SNA, SAα2,3-Gal, SAα2,6-Gal.
References
Alexander, D. J. (2007). Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002–2006. Avian Diseases 51, 161–166.| Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002–2006.Crossref | GoogleScholarGoogle Scholar |
Aly, M. M., Arafa, A., Kilany, W. H., Sleim, A. A., and Hassan, M. K. (2010). Isolation of a low pathogenic avian influenza virus (H7N7) from a black kite (Milvus migrans) in Egypt in 2005. Avian Diseases 54, 457–460.
| Isolation of a low pathogenic avian influenza virus (H7N7) from a black kite (Milvus migrans) in Egypt in 2005.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czpsF2kuw%3D%3D&md5=aad357e1f3d5c4aef05b552726b6affbCAS |
Brown, I. H., Harris, P. A., McCauley, J. W., and Alexander, D. J. (1998). Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. The Journal of General Virology 79, 2947–2955.
| 1:CAS:528:DyaK1cXotVaqtLk%3D&md5=1a1c7da0586c952319434265be5b04cfCAS |
Cameron, K. R., Gregory, V., Banks, J., Brown, I. H., Alexander, D. J., Hay, A. J., and Lin, Y. P. (2000). H9N2 subtype influenza A viruses in poultry in Pakistan are closely related to the H9N2 viruses responsible for human infection in Hong Kong. Virology 278, 36–41.
| H9N2 subtype influenza A viruses in poultry in Pakistan are closely related to the H9N2 viruses responsible for human infection in Hong Kong.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFGgurk%3D&md5=59c421965845826528efae31eda6849aCAS |
Castrucci, M. R., Donatelli, I., Sidoli, L., Barigazzi, G., Kawaoka, Y., and Webster, R. G. (1993). Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology 193, 503–506.
| Genetic reassortment between avian and human influenza A viruses in Italian pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1Knsro%3D&md5=f63a766c9e6995fdf4e10623a70cd6ffCAS |
Connor, R. J., Kawaoka, Y., Webster, R. G., and Paulson, J. C. (1994). Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205, 17–23.
| Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFKktbk%3D&md5=ab3b3029b3148636547b84560b03e5daCAS |
Ellström, P., Jourdain, E., Gunnarsson, O., Waldenstrom, J., and Olsen, B. (2009). The “human influenza receptor” Neu5Ac alpha2,6Gal is expressed among different taxa of wild birds. Archives of Virology 154, 1533–1537.
| The “human influenza receptor” Neu5Ac alpha2,6Gal is expressed among different taxa of wild birds.Crossref | GoogleScholarGoogle Scholar |
Fouchier, R. A., Schneeberger, P. M., Rozendaal, F. W., Broekman, J. M., Kemink, S. A., Munster, V., Kuiken, T., Rimmelzwaan, G. F., Schutten, M., Van Doornum, G. J., Koch, G., Bosman, A., Koopmans, M., and Osterhaus, A. D. (2004). Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proceedings of the National Academy of Sciences of the United States of America 101, 1356–1361.
| Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtlWjtbk%3D&md5=f5c549243355def00f825d1b45b08e78CAS |
Gambaryan, A., Webster, R., and Matrosovich, M. (2002). Differences between influenza virus receptors on target cells of duck and chicken. Archives of Virology 147, 1197–1208.
| Differences between influenza virus receptors on target cells of duck and chicken.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsV2mtbo%3D&md5=053d9034412b456521f619d09ea6a0aeCAS |
Gambotto, A., Barratt-Boyes, S. M., de Jong, M. D., Neumann, G., and Kawaoka, Y. (2008). Human infection with highly pathogenic H5N1 influenza virus. Lancet 371, 1464–1475.
| Human infection with highly pathogenic H5N1 influenza virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsFCisL0%3D&md5=b4aa64e25fbcfbb8c1df05b8f82b2e04CAS |
Goyal, S. M., Jindal, N., Chander, Y., Ramakrishnan, M. A., Redig, P. T., and Sreevatsan, S. (2010). Isolation of mixed subtypes of influenza A virus from a bald eagle (Haliaeetus leucocephalus). Virology Journal 7, 174.
| Isolation of mixed subtypes of influenza A virus from a bald eagle (Haliaeetus leucocephalus).Crossref | GoogleScholarGoogle Scholar |
Guo, Y. (2002). Influenza activity in China: 1998–1999. Vaccine 20, S28–S35.
| Influenza activity in China: 1998–1999.Crossref | GoogleScholarGoogle Scholar |
Hall, J. S., Ip, H. S., Franson, J. C., Meteyer, C., Nashold, S., TeSlaa, J. L., French, J., Redig, P., and Brand, C. (2009). Experimental infection of a North American raptor, American Kestrel (Falco sparverius), with highly pathogenic avian influenza virus (H5N1). PLoS ONE 4, e7555.
Horimoto, T., and Kawaoka, Y. (2005). Influenza: lessons from past pandemics, warnings from current incidents. Nature Reviews Microbiologyl 3, 591–600.
| Influenza: lessons from past pandemics, warnings from current incidents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVGhur4%3D&md5=47d4668df3fb1c0c48aeeed39e7b4258CAS |
Ito, T., Couceiro, J. N., Kelm, S., Baum, L. G., Krauss, S., Castrucci, M. R., Donatelli, I., Kida, H., Paulson, J. C., Webster, R. G., and Kawaoka, Y. (1998). Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. Journal of Virology 72, 7367–7373.
| 1:CAS:528:DyaK1cXlsVSmsrs%3D&md5=bde3eb6cd20df0f75e13ffe00391191aCAS |
Ito, T., Suzuki, Y., Suzuki, T., Takada, A., Horimoto, T., Wells, K., Kida, H., Otsuki, K., Kiso, M., Ishida, H., and Kawaoka, Y. (2000). Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. Journal of Virology 74, 9300–9305.
| Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslymtb8%3D&md5=f1cf999b540122786eb9b7c9198cc4a0CAS |
Kawaoka, Y., Krauss, S., and Webster, R. G. (1989). Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. Journal of Virology 63, 4603–4608.
| 1:CAS:528:DyaK3cXntFWjtQ%3D%3D&md5=41ca6336cf99f72ccd6ec67b0b9926bdCAS |
Khan, O. A., Shuaib, M. A., Rhman, S. S., Ismail, M. M., Hammad, Y. A., Baky, M. H., Fusaro, A., Salviato, A., and Cattoli, G. (2009). Isolation and identification of highly pathogenic avian influenza H5N1 virus from Houbara bustards (Chlamydotis undulata macqueenii) and contact falcons. Avian Pathology 38, 35–39.
| Isolation and identification of highly pathogenic avian influenza H5N1 virus from Houbara bustards (Chlamydotis undulata macqueenii) and contact falcons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1OitLw%3D&md5=6f9e447b6c557b832a2afb884eb41e53CAS |
Kogure, T., Suzuki, T., Takahashi, T., Miyamoto, D., Hidari, K. I., Guo, C. T., Ito, T., Kawaoka, Y., and Suzuki, Y. (2006). Human trachea primary epithelial cells express both sialyl(alpha2–3)Gal receptor for human parainfluenza virus type 1 and avian influenza viruses, and sialyl(alpha2–6)Gal receptor for human influenza viruses. Glycoconjugate Journal 23, 101–106.
| Human trachea primary epithelial cells express both sialyl(alpha2–3)Gal receptor for human parainfluenza virus type 1 and avian influenza viruses, and sialyl(alpha2–6)Gal receptor for human influenza viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVKnsL4%3D&md5=9382a5ee47b26ad38649aec72fbb5f75CAS |
Kuchipudi, S. V., Nelli, R., White, G. A., Bain, M., Chang, K. C., and Dunham, S. (2009). Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. Journal of Molecular Genetic Medicine 3, 143–151.
| 1:CAS:528:DC%2BD1MXhtVWmtL%2FO&md5=3cb19103db238d2e0d6eb0ac1f63c706CAS |
Liu, Y., Zhou, J., Yang, H., Yao, W., Bu, W., Yang, B., Song, W., Meng, Y., Lin, J., Han, C., Zhu, J., Ma, Z., Zhao, J., and Wang, X. (2007). Susceptibility and transmissibility of pigeons to Asian lineage highly pathogenic avian influenza virus subtype H5N1. Avian Pathology 36, 461–465.
| Susceptibility and transmissibility of pigeons to Asian lineage highly pathogenic avian influenza virus subtype H5N1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yntb7K&md5=d76da5be0fa5156690c41a29d858f0beCAS |
Liu, Y., Han, C., Wang, X., Lin, J., Ma, M., Shu, Y., Zhou, J., Yang, H., Liang, Q., Guo, C., Zhu, J., Wei, H., Zhao, J., Ma, Z., and Pan, J. (2009). Influenza A virus receptors in the respiratory and intestinal tracts of pigeons. Avian Pathology 38, 263–266.
| Influenza A virus receptors in the respiratory and intestinal tracts of pigeons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKmsL3M&md5=42ede0d8d6be564f2f6146a263aea32fCAS |
Ma, W., Kahn, R. E., and Richt, J. A. (2008). The pig as a mixing vessel for influenza viruses: Human and veterinary implications. Journal of Molecular Genetic Medicine 3, 158–166.
Manvell, R. J., McKinney, P., Wernery, U., and Frost, K. (2000). Isolation of a highly pathogenic influenza A virus of subtype H7N3 from a peregrine falcon (Falco peregrinus). Avian Pathology 29, 635–637.
| Isolation of a highly pathogenic influenza A virus of subtype H7N3 from a peregrine falcon (Falco peregrinus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7htFCitw%3D%3D&md5=58c5dc33c1ac689af8a45b64ca26218dCAS |
Marjuki, H., Wernery, U., Yen, H. L., Franks, J., Seiler, P., Walker, D., Krauss, S., and Webster, R. G. (2009). Isolation of highly pathogenic avian influenza H5N1 virus from Saker falcons (Falco cherrug) in the Middle East. Advances in Virology 2009, 1–7.
| Isolation of highly pathogenic avian influenza H5N1 virus from Saker falcons (Falco cherrug) in the Middle East.Crossref | GoogleScholarGoogle Scholar |
Nicholls, J. M., Bourne, A. J., Chen, H., Guan, Y., and Peiris, J. S. (2007). Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respiratory Research 8, 73.
| Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses.Crossref | GoogleScholarGoogle Scholar |
Pillai, S. P., and Lee, C. W. (2010). Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys. Virology Journal 7, 5.
| Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys.Crossref | GoogleScholarGoogle Scholar |
Rogers, G. N., and D’Souza, B. L. (1989). Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173, 317–322.
| Receptor binding properties of human and animal H1 influenza virus isolates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhvFOrsQ%3D%3D&md5=0323ae9787bf4f53adef2598422f0221CAS |
Rogers, G. N., and Paulson, J. C. (1983). Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127, 361–373.
| Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlslersbo%3D&md5=0beca17b0e44bdbc31511fb7b632b662CAS |
Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N., and Kawaoka, Y. (2006). Avian flu: influenza virus receptors in the human airway. Nature 440, 435–436.
| Avian flu: influenza virus receptors in the human airway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Omu7s%3D&md5=1f492355627f7c788cf1f5e4ef14d3caCAS |
Suzuki, Y., Ito, T., Suzuki, T., Holland, R. J., Chambers, T. M., Kiso, M., Ishida, H., and Kawaoka, Y. (2000). Sialic acid species as a determinant of the host range of influenza A viruses. Journal of Virology 74, 11825–11831.
| Sialic acid species as a determinant of the host range of influenza A viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitVGisLs%3D&md5=d746af697422cccd971dc9efcfff1eb3CAS |
Taubenberger, J. K., Reid, A. H., Krafft, A. E., Bijwaard, K. E., and Fanning, T. G. (1997). Initial genetic characterization of the 1918 “Spanish” influenza virus. Science 275, 1793–1796.
| Initial genetic characterization of the 1918 “Spanish” influenza virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitVGrurc%3D&md5=68b5eb721e7021a8ee504fd733b654bdCAS |
Tweed, S. A., Skowronski, D. M., David, S. T., Larder, A., Petric, M., Lees, W., Li, Y., Katz, J., Krajden, M., Tellier, R., Halpert, C., Hirst, M., Astell, C., Lawrence, D., and Mak, A. (2004). Human illness from avian influenza H7N3, British Columbia. Emerging Infectious Diseases 10, 2196–2199.
Van Borm, S., Thomas, I., Hanquet, G., Lambrecht, B., Boschmans, M., Dupont, G., Decaestecker, M., Snacken, R., and van den Berg, T. (2005). Highly pathogenic H5N1 influenza virus in smuggled Thai eagles, Belgium. Emerging Infectious Diseases 11, 702–705.
van Riel, D., Munster, V. J., de Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D., and Kuiken, T. (2007). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. American Journal of Pathology 171, 1215–1223.
| Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Smtr7F&md5=fd1549875523135dacbeb9b780d71b3bCAS |
Wan, H., and Perez, D. R. (2006). Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 346, 278–286.
| Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Cis7g%3D&md5=a478a0420f845b557eb4f75b2c4b2ea7CAS |
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., and Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiological Reviews 56, 152–179.
| 1:STN:280:DyaK383lt1OqtQ%3D%3D&md5=d3825e3f08387f8c87391f519f66293dCAS |
