Skip to main content
Top
Published in: Virology Journal 1/2010

Open Access 01-12-2010 | Research

Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys

Authors: Smitha PS Pillai, Chang W Lee

Published in: Virology Journal | Issue 1/2010

Login to get access

Abstract

We undertook one of the most detailed studies on the distribution of α2,3 sialic acid (SA)-galactose (gal) (avian type) and α2,6SA-gal (human type) receptors on different tissues of chickens, ducks and turkeys of varying age groups. On the tracheal epithelium, all 3 bird species expressed strong positive staining (80-90%) for α2,3SA-gal receptors in the 3 different age groups. In addition, a lesser amount of α2,6SA-gal receptors (30-90%) were observed with slight differences in distribution with age and species. The epithelium of the small and large intestine of turkeys and ducks showed negligible staining for α2,6SA-gal receptors whereas the large intestine consistently showed 40-70% positive staining for α2,3SA-gal receptors. In contrast, a greater amount of staining for α2,3SA-gal (50-80%) and α2,6SA-gal (20-50%) receptors were observed along the epithelium of small and large intestine of chickens. Kidney and esophagus sections from the 3 bird species also expressed both avian and human type receptors. In other tissues examined, brain, breast muscles, bursa, spleen, cecal tonsils and oviduct, human type receptors were absent. Though different viral and receptor components may play roles in successful viral replication and transmission, understanding the receptor types and distribution in different tissues of domestic birds might be good initial tool to understand host factors that promote successful influenza viral infection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Alexander DJ: A review of avian influenza in different bird species. Vet Microbiol 2000, 74: 3-13. 10.1016/S0378-1135(00)00160-7PubMedCrossRef Alexander DJ: A review of avian influenza in different bird species. Vet Microbiol 2000, 74: 3-13. 10.1016/S0378-1135(00)00160-7PubMedCrossRef
3.
go back to reference Hinshaw VS, Webster RG, Turner B: Water-borne transmission of influenza A viruses? Intervirology 1979, 11: 66-68. 10.1159/000149014PubMedCrossRef Hinshaw VS, Webster RG, Turner B: Water-borne transmission of influenza A viruses? Intervirology 1979, 11: 66-68. 10.1159/000149014PubMedCrossRef
4.
go back to reference Gambarian AS, Iamnikova SS, L'Vov D K, Robertson JS, Webster RG, Matrosovich MN: [Differences in receptor specificity between the influenza A viruses isolated from the duck, chicken, and human]. Mol Biol (Mosk) 2002, 36: 542-549. Gambarian AS, Iamnikova SS, L'Vov D K, Robertson JS, Webster RG, Matrosovich MN: [Differences in receptor specificity between the influenza A viruses isolated from the duck, chicken, and human]. Mol Biol (Mosk) 2002, 36: 542-549.
5.
go back to reference Gambaryan A, Webster R, Matrosovich M: Differences between influenza virus receptors on target cells of duck and chicken. Arch Virol 2002, 147: 1197-1208. 10.1007/s00705-002-0796-4PubMedCrossRef Gambaryan A, Webster R, Matrosovich M: Differences between influenza virus receptors on target cells of duck and chicken. Arch Virol 2002, 147: 1197-1208. 10.1007/s00705-002-0796-4PubMedCrossRef
6.
go back to reference Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 1998, 72: 7367-7373.PubMedPubMedCentral Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 1998, 72: 7367-7373.PubMedPubMedCentral
7.
go back to reference Liu M, Guan Y, Peiris M, He S, Webby RJ, Perez D, Webster RG: The quest of influenza A viruses for new hosts. Avian Dis 2003, 47: 849-856. 10.1637/0005-2086-47.s3.849PubMedCrossRef Liu M, Guan Y, Peiris M, He S, Webby RJ, Perez D, Webster RG: The quest of influenza A viruses for new hosts. Avian Dis 2003, 47: 849-856. 10.1637/0005-2086-47.s3.849PubMedCrossRef
8.
go back to reference Wan H, Perez DR: Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 2006, 346: 278-286. 10.1016/j.virol.2005.10.035PubMedCrossRef Wan H, Perez DR: Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 2006, 346: 278-286. 10.1016/j.virol.2005.10.035PubMedCrossRef
9.
go back to reference Pillai SP, Pantin-Jackwood M, Jadhao SJ, Suarez DL, Wang L, Yassine HM, Saif YM, Lee CW: Pathobiology of triple reassortant H3N2 influenza viruses in breeder turkeys and its potential implication for vaccine studies in turkeys. Vaccine 2009, 27: 819-824. 10.1016/j.vaccine.2008.11.076PubMedCrossRef Pillai SP, Pantin-Jackwood M, Jadhao SJ, Suarez DL, Wang L, Yassine HM, Saif YM, Lee CW: Pathobiology of triple reassortant H3N2 influenza viruses in breeder turkeys and its potential implication for vaccine studies in turkeys. Vaccine 2009, 27: 819-824. 10.1016/j.vaccine.2008.11.076PubMedCrossRef
10.
go back to reference Matrosovich M, Zhou N, Kawaoka Y, Webster R: The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 1999, 73: 1146-1155.PubMedPubMedCentral Matrosovich M, Zhou N, Kawaoka Y, Webster R: The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 1999, 73: 1146-1155.PubMedPubMedCentral
11.
go back to reference Klenk E, Faillard H, Lempfrid H: [Enzymatic effect of the influenza virus.]. Hoppe Seylers Z Physiol Chem 1955, 301: 235-246.PubMedCrossRef Klenk E, Faillard H, Lempfrid H: [Enzymatic effect of the influenza virus.]. Hoppe Seylers Z Physiol Chem 1955, 301: 235-246.PubMedCrossRef
12.
go back to reference Carroll SM, Higa HH, Paulson JC: Different cell-surface receptor determinants of antigenically similar influenza virus hemagglutinins. J Biol Chem 1981, 256: 8357-8363.PubMed Carroll SM, Higa HH, Paulson JC: Different cell-surface receptor determinants of antigenically similar influenza virus hemagglutinins. J Biol Chem 1981, 256: 8357-8363.PubMed
13.
go back to reference Rogers GN, Paulson JC: Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127: 361-373. 10.1016/0042-6822(83)90150-2PubMedCrossRef Rogers GN, Paulson JC: Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127: 361-373. 10.1016/0042-6822(83)90150-2PubMedCrossRef
14.
go back to reference Gambaryan AS, Tuzikov AB, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Bovin NV, Matrosovich MN: Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6'-sialyl(N-acetyllactosamine). Virology 1997, 232: 345-350. 10.1006/viro.1997.8572PubMedCrossRef Gambaryan AS, Tuzikov AB, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Bovin NV, Matrosovich MN: Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6'-sialyl(N-acetyllactosamine). Virology 1997, 232: 345-350. 10.1006/viro.1997.8572PubMedCrossRef
15.
go back to reference Brown JD, Stallknecht DE, Beck JR, Suarez DL, Swayne DE: Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg Infect Dis 2006, 12: 1663-1670.PubMedPubMedCentralCrossRef Brown JD, Stallknecht DE, Beck JR, Suarez DL, Swayne DE: Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg Infect Dis 2006, 12: 1663-1670.PubMedPubMedCentralCrossRef
16.
go back to reference Alexander DJ, Allan WH, Parsons DG, Parsons G: The pathogenicity of four avian influenza viruses for fowls, turkeys and ducks. Res Vet Sci 1978, 24: 242-247.PubMed Alexander DJ, Allan WH, Parsons DG, Parsons G: The pathogenicity of four avian influenza viruses for fowls, turkeys and ducks. Res Vet Sci 1978, 24: 242-247.PubMed
17.
go back to reference Alexander DJ, Lister SA, Johnson MJ, Randall CJ, Thomas PJ: An outbreak of highly pathogenic avian influenza in turkeys in Great Britain in 1991. Vet Rec 1993, 132: 535-536. 10.1136/vr.132.21.535PubMedCrossRef Alexander DJ, Lister SA, Johnson MJ, Randall CJ, Thomas PJ: An outbreak of highly pathogenic avian influenza in turkeys in Great Britain in 1991. Vet Rec 1993, 132: 535-536. 10.1136/vr.132.21.535PubMedCrossRef
18.
go back to reference Kida H, Yanagawa R, Matsuoka Y: Duck influenza lacking evidence of disease signs and immune response. Infect Immun 1980, 30: 547-553.PubMedPubMedCentral Kida H, Yanagawa R, Matsuoka Y: Duck influenza lacking evidence of disease signs and immune response. Infect Immun 1980, 30: 547-553.PubMedPubMedCentral
19.
go back to reference Tumpey TM, Suarez DL, Perkins LE, Senne DA, Lee JG, Lee YJ, Mo IP, Sung HW, Swayne DE: Characterization of a highly pathogenic H5N1 avian influenza A virus isolated from duck meat. J Virol 2002, 76: 6344-6355. 10.1128/JVI.76.12.6344-6355.2002PubMedPubMedCentralCrossRef Tumpey TM, Suarez DL, Perkins LE, Senne DA, Lee JG, Lee YJ, Mo IP, Sung HW, Swayne DE: Characterization of a highly pathogenic H5N1 avian influenza A virus isolated from duck meat. J Virol 2002, 76: 6344-6355. 10.1128/JVI.76.12.6344-6355.2002PubMedPubMedCentralCrossRef
20.
go back to reference Kuchipudi SV, Nelli R, White GA, Bain M, Changand KC, Dunham S: Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. J Mol Genet Med 2009, 3: 143-151.PubMedPubMedCentralCrossRef Kuchipudi SV, Nelli R, White GA, Bain M, Changand KC, Dunham S: Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. J Mol Genet Med 2009, 3: 143-151.PubMedPubMedCentralCrossRef
21.
go back to reference Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992, 56: 152-179.PubMedPubMedCentral Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992, 56: 152-179.PubMedPubMedCentral
22.
go back to reference Alexander DJ, Parsons G, Manvell RJ: Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. Avian Pathol 1986, 15: 647-662. 10.1080/03079458608436328PubMedCrossRef Alexander DJ, Parsons G, Manvell RJ: Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. Avian Pathol 1986, 15: 647-662. 10.1080/03079458608436328PubMedCrossRef
23.
go back to reference Andral B, Toquin D, Madec F, Aymard M, Gourreau JM, Kaiser C, Fontaine M, Metz MH: Disease in turkeys associated with H1N1 influenza virus following an outbreak of the disease in pigs. Vet Rec 1985, 116: 617-618. 10.1136/vr.116.23.617PubMedCrossRef Andral B, Toquin D, Madec F, Aymard M, Gourreau JM, Kaiser C, Fontaine M, Metz MH: Disease in turkeys associated with H1N1 influenza virus following an outbreak of the disease in pigs. Vet Rec 1985, 116: 617-618. 10.1136/vr.116.23.617PubMedCrossRef
24.
go back to reference Ladman BS, Rosenberger SC, Rosenberger JK, Pope CR, Gelb J Jr: Virulence of low pathogenicity H7N2 avian influenza viruses from the Delmarva peninsula for broiler and leghorn chickens and turkeys. Avian Dis 2008, 52: 623-631. 10.1637/8282-031208-Reg.1PubMedCrossRef Ladman BS, Rosenberger SC, Rosenberger JK, Pope CR, Gelb J Jr: Virulence of low pathogenicity H7N2 avian influenza viruses from the Delmarva peninsula for broiler and leghorn chickens and turkeys. Avian Dis 2008, 52: 623-631. 10.1637/8282-031208-Reg.1PubMedCrossRef
25.
go back to reference Swayne DE, Slemons RD: Using mean infectious dose of high- and low-pathogenicity avian influenza viruses originating from wild duck and poultry as one measure of infectivity and adaptation to poultry. Avian Dis 2008, 52: 455-460. 10.1637/8229-012508-Reg.1PubMedCrossRef Swayne DE, Slemons RD: Using mean infectious dose of high- and low-pathogenicity avian influenza viruses originating from wild duck and poultry as one measure of infectivity and adaptation to poultry. Avian Dis 2008, 52: 455-460. 10.1637/8229-012508-Reg.1PubMedCrossRef
26.
go back to reference Choi YK, Seo SH, Kim JA, Webby RJ, Webster RG: Avian influenza viruses in Korean live poultry markets and their pathogenic potential. Virology 2005, 332: 529-537. 10.1016/j.virol.2004.12.002PubMedCrossRef Choi YK, Seo SH, Kim JA, Webby RJ, Webster RG: Avian influenza viruses in Korean live poultry markets and their pathogenic potential. Virology 2005, 332: 529-537. 10.1016/j.virol.2004.12.002PubMedCrossRef
27.
go back to reference Mo IP, Brugh M, Fletcher OJ, Rowland GN, Swayne DE: Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity. Avian Dis 1997, 41: 125-136. 10.2307/1592452PubMedCrossRef Mo IP, Brugh M, Fletcher OJ, Rowland GN, Swayne DE: Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity. Avian Dis 1997, 41: 125-136. 10.2307/1592452PubMedCrossRef
28.
go back to reference Barkhordari A, Stoddart RW, McClure SF, McClure J: Lectin histochemistry of normal human lung. J Mol Histol 2004, 35: 147-156. 10.1023/B:HIJO.0000023384.02037.bbPubMedCrossRef Barkhordari A, Stoddart RW, McClure SF, McClure J: Lectin histochemistry of normal human lung. J Mol Histol 2004, 35: 147-156. 10.1023/B:HIJO.0000023384.02037.bbPubMedCrossRef
29.
go back to reference Nicholls JM, Chan RW, Russell RJ, Air GM, Peiris JS: Evolving complexities of influenza virus and its receptors. Trends Microbiol 2008, 16: 149-157. 10.1016/j.tim.2008.01.008PubMedCrossRef Nicholls JM, Chan RW, Russell RJ, Air GM, Peiris JS: Evolving complexities of influenza virus and its receptors. Trends Microbiol 2008, 16: 149-157. 10.1016/j.tim.2008.01.008PubMedCrossRef
30.
go back to reference Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y: Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 2000, 74: 8502-8512. 10.1128/JVI.74.18.8502-8512.2000PubMedPubMedCentralCrossRef Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y: Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 2000, 74: 8502-8512. 10.1128/JVI.74.18.8502-8512.2000PubMedPubMedCentralCrossRef
31.
go back to reference Guo CT, Takahashi N, Yagi H, Kato K, Takahashi T, Yi SQ, Chen Y, Ito T, Otsuki K, Kida H, et al.: The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 2007, 17: 713-724. 10.1093/glycob/cwm038PubMedCrossRef Guo CT, Takahashi N, Yagi H, Kato K, Takahashi T, Yi SQ, Chen Y, Ito T, Otsuki K, Kida H, et al.: The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 2007, 17: 713-724. 10.1093/glycob/cwm038PubMedCrossRef
32.
go back to reference Slemons RD, Condobery PK, Swayne DE: Assessing pathogenicity potential of waterfowl-origin type A influenza viruses in chickens. Avian Dis 1991, 35: 210-215. 10.2307/1591316PubMedCrossRef Slemons RD, Condobery PK, Swayne DE: Assessing pathogenicity potential of waterfowl-origin type A influenza viruses in chickens. Avian Dis 1991, 35: 210-215. 10.2307/1591316PubMedCrossRef
33.
go back to reference Slemons RD, Swayne DE: Tissue tropism and replicative properties of waterfowl-origin influenza viruses in chickens. Avian Dis 1995, 39: 521-527. 10.2307/1591804PubMedCrossRef Slemons RD, Swayne DE: Tissue tropism and replicative properties of waterfowl-origin influenza viruses in chickens. Avian Dis 1995, 39: 521-527. 10.2307/1591804PubMedCrossRef
34.
go back to reference Lee CW, Jung K, Jadhao SJ, Suarez DL: Evaluation of chicken-origin (DF-1) and quail-origin (QT-6) fibroblast cell lines for replication of avian influenza viruses. J Virol Methods 2008, 153: 22-28. 10.1016/j.jviromet.2008.06.019PubMedCrossRef Lee CW, Jung K, Jadhao SJ, Suarez DL: Evaluation of chicken-origin (DF-1) and quail-origin (QT-6) fibroblast cell lines for replication of avian influenza viruses. J Virol Methods 2008, 153: 22-28. 10.1016/j.jviromet.2008.06.019PubMedCrossRef
35.
go back to reference Perkins LE, Swayne DE: Susceptibility of laughing gulls (Larus atricilla) to H5N1 and H5N3 highly pathogenic avian influenza viruses. Avian Dis 2002, 46: 877-885. 10.1637/0005-2086(2002)046[0877:SOLGLA]2.0.CO;2PubMedCrossRef Perkins LE, Swayne DE: Susceptibility of laughing gulls (Larus atricilla) to H5N1 and H5N3 highly pathogenic avian influenza viruses. Avian Dis 2002, 46: 877-885. 10.1637/0005-2086(2002)046[0877:SOLGLA]2.0.CO;2PubMedCrossRef
36.
go back to reference Perkins LE, Swayne DE: Varied pathogenicity of a Hong Kong-origin H5N1 avian influenza virus in four passerine species and budgerigars. Vet Pathol 2003, 40: 14-24. 10.1354/vp.40-1-14PubMedCrossRef Perkins LE, Swayne DE: Varied pathogenicity of a Hong Kong-origin H5N1 avian influenza virus in four passerine species and budgerigars. Vet Pathol 2003, 40: 14-24. 10.1354/vp.40-1-14PubMedCrossRef
37.
go back to reference Vascellari M, Granato A, Trevisan L, Basilicata L, Toffan A, Milani A, Mutinelli F: Pathologic findings of highly pathogenic avian influenza virus A/Duck/Vietnam/12/05 (H5N1) in experimentally infected pekin ducks, based on immunohistochemistry and in situ hybridization. Vet Pathol 2007, 44: 635-642. 10.1354/vp.44-5-635PubMedCrossRef Vascellari M, Granato A, Trevisan L, Basilicata L, Toffan A, Milani A, Mutinelli F: Pathologic findings of highly pathogenic avian influenza virus A/Duck/Vietnam/12/05 (H5N1) in experimentally infected pekin ducks, based on immunohistochemistry and in situ hybridization. Vet Pathol 2007, 44: 635-642. 10.1354/vp.44-5-635PubMedCrossRef
Metadata
Title
Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys
Authors
Smitha PS Pillai
Chang W Lee
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2010
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-7-5

Other articles of this Issue 1/2010

Virology Journal 1/2010 Go to the issue