Infection of host cells with the influenza virus is mediated by specific interactions between the viral haemagglutinin (HA) and cell oligosaccharides containing sialic acid (SA) residues. Avian and human influenza viruses bind to alpha-2, 3 and alpha-2, 6 sialic acid-linked receptors, respectively. To date, there have been no detailed tissue distribution data on alpha-2, 3 and alpha-2, 6 sialic acid-linked receptors in the domestic cat, a relatively new mammalian host for influenza virus infections. In this study, the tissue distribution of human and avian type sialic acid influenza receptors was determined in various organs (respiratory tract, gastrointestinal tract, brain, cerebellum, spleen, kidney, heart and pancreas) of domestic cat by binding with the lectins Maackia amurensis agglutinin II (MAA II) and Sambucus nigra agglutinin (SNA), respectively. The results revealed that both alpha-2, 3 and alpha-2, 6 sialic acid-linked receptors were extensively detected in the trachea, bronchus, lung, kidney, spleen, pancreas and gastrointestinal tract. Endothelial cells of gastrointestinal tract organs were negative for alpha-2, 3 sialic acid-linked receptors in cats. The presence of alpha-2, 3 and alpha-2, 6 sialic acid-linked receptors in the major organs examined in the present study suggests that each major organ may be affected by influenza virus infection. Because of receptor distribution in the gastrointestinal tract, the experimental infection of cats with human influenza virus may be relatively easy while their infection with avian influenza virus may be difficult. These data can explain the involvement of multiple organs in influenza virus infection and should help investigators interpret the results obtained when cats are infected with influenza virus and estimate the risk of infection between cats and humans.
Cardona, C. J., Xing, Z., Sandrock, C. E. and Davis, C. E. (2009): Avian influenza in birds and mammals. Comp. Immunol. Microbiol. Infect. Dis. 32, 255–273.
Davis C. E. , 'Avian influenza in birds and mammals ' (2009 ) 32 Comp. Immunol. Microbiol. Infect. Dis. : 255 -273.
Ge, S. and Wang, Z. (2011): An overview of influenza A virus receptors. Crit. Rev. Microbiol. 37, 157–165.
Wang Z. , 'An overview of influenza A virus receptors ' (2011 ) 37 Crit. Rev. Microbiol. : 157 -165.
Harder, T. C. and Vahlenkamp, T. W. (2010): Influenza virus infections in dogs and cats. Vet. Immunol. Immunopathol. 134, 54–60.
Vahlenkamp T. W. , 'Influenza virus infections in dogs and cats ' (2010 ) 134 Vet. Immunol. Immunopathol. : 54 -60.
Ibricevic, A., Pekosz, A., Walter, M. J., Newby, C., Battaile, J. T., Brown, E. G., Holtzman, M. J. and Brody, S. L. (2006): Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J. Virol. 80, 7469–7480.
Brody S. L. , 'Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells ' (2006 ) 80 J. Virol. : 7469 -7480.
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. J. Virol. 72, 7367–7373.
Kawaoka Y. , 'Molecular basis for the generation in pigs of influenza A viruses with pandemic potential ' (1998 ) 72 J. Virol. : 7367 -7373.
Kishimoto, C., Hiraoka, Y., Takada, H., Kurokawa, M. and Ochiai, H. (2005): Effects of immunoglobulin on murine myocarditis caused by influenza A virus: experimental study. J. Cardiol. 45, 247–255.
Ochiai H. , 'Effects of immunoglobulin on murine myocarditis caused by influenza A virus: experimental study ' (2005 ) 45 J. Cardiol. : 247 -255.
Kuiken, T., Rimmelzwaan, G., van Riel, D., van Amerongen, G., Baars, M., Fouchier, R. and Osterhaus, A. (2004): Avian H5N1 influenza in cats. Science 306, 241.
Osterhaus A. , 'Avian H5N1 influenza in cats ' (2004 ) 306 Science : 241 -.
Leschnik, M., Weikel, J., Mostl, K., Revilla-Fernandez, S., Wodak, E., Bago, Z., Vanek, E., Benetka, V., Hess, M. and Thalhammer, J. G. (2007): Subclinical infection with avian influenza A (H5N1) virus in cats. Emerg. Infect. Dis. 13, 243–247.
Thalhammer J. G. , 'Subclinical infection with avian influenza A (H5N1) virus in cats ' (2007 ) 13 Emerg. Infect. Dis. : 243 -247.
Liu, J., Xiao, H., Lei, F., Zhu, Q., Qin, K., Zhang, X. W., Zhang, X. L., Zhao, D., Wang, G., Feng, Y., Ma, J., Liu, W., Wang, J. and Gao, G. F. (2005): Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309, 1206.
Gao G. F. , 'Highly pathogenic H5N1 influenza virus infection in migratory birds ' (2005 ) 309 Science : 1206 -.
Lohr, C. V., DeBess, E. E., Baker, R. J., Hiett, S. L., Hoffman, K. A., Murdoch, V. J., Fischer, K. A., Mulrooney, D. M., Selman, R. L. and Hammill-Black, W. M. (2010): Pathology and viral antigen distribution of lethal pneumonia in domestic cats due to pandemic (H1N1) 2009 influenza A virus. Vet. Pathol. 47, 378–386.
Hammill-Black W. M. , 'Pathology and viral antigen distribution of lethal pneumonia in domestic cats due to pandemic (H1N1) 2009 influenza A virus ' (2010 ) 47 Vet. Pathol. : 378 -386.
Maines, T. R., Lu, X. H., Erb, S. M., Edwards, L., Guarner, J., Greer, P. W., Nguyen, D. C., Szretter, K. J., Chen, L. M., Thawatsupha, P., Chittaganpitch, M., Waicharoen, S., Nguyen, D. T., Nguyen, T., Nguyen, H. H., Kim, J. H., Hoang, L. T., Kang, C., Phuong, L. S., Lim, W., Zaki, S., Donis, R. O., Cox, N. J., Katz, J. M. and Tumpey, T. M. (2005): Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J. Virol. 79, 11788–11800.
Tumpey T. M. , 'Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals ' (2005 ) 79 J. Virol. : 11788 -11800.
Matrosovich, M. N., Gambaryan, A. S., Teneberg, S., Piskarev, V. E., Yamnikova, S. S., Lvov, D. K., Robertson, J. S. and 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.
Karlsson K. A. , '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 ' (1997 ) 233 Virology : 224 -234.
Nelli, R. K., Kuchipudi, S. V., White, G. A., Perez, B. B., Dunham, S. P. and Chang, K. C. (2010): Comparative distribution of human and avian type sialic acid influenza receptors in the pig. BMC Vet. Res. 6, 4.
Chang K. C. , 'Comparative distribution of human and avian type sialic acid influenza receptors in the pig ' (2010 ) 6 BMC Vet. Res. : 4 -.
Neumann, G., Noda, T. and Kawaoka, Y. (2009): Emergence and pandemic potential of swineorigin H1N1 influenza virus. Nature 459, 931–939.
Kawaoka Y. , 'Emergence and pandemic potential of swineorigin H1N1 influenza virus ' (2009 ) 459 Nature : 931 -939.
Ning, Z. Y., Luo, M. Y., Qi, W. B., Yu, B., Jiao, P. R. and Liao, M. (2009): Detection of expression of influenza virus receptors in tissues of BALB/c mice by histochemistry. Vet. Res. Commun. 33, 895–903.
Liao M. , 'Detection of expression of influenza virus receptors in tissues of BALB/c mice by histochemistry ' (2009 ) 33 Vet. Res. Commun. : 895 -903.
Rimmelzwaan, G. F., van Riel, D., Baars, M., Bestebroer, T. M., van Amerongen, G., Fouchier, R. A., Osterhaus, A. D. and Kuiken, T. (2006): Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am. J. Pathol. 168, 176–183.
Kuiken T. , 'Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts ' (2006 ) 168 Am. J. Pathol. : 176 -183.
Shinya, K. and Kawaoka, Y. (2006): Influenza virus receptors in the human airway. Uirusu 56, 85–89.
Kawaoka Y. , 'Influenza virus receptors in the human airway ' (2006 ) 56 Uirusu : 85 -89.
Song, D., Kang, B., Lee, C., Jung, K., Ha, G., Kang, D., Park, S., Park, B. and Oh, J. (2008): Transmission of avian influenza virus (H3N2) to dogs. Emerg. Infect. Dis. 14, 741–746.
Oh J. , 'Transmission of avian influenza virus (H3N2) to dogs ' (2008 ) 14 Emerg. Infect. Dis. : 741 -746.
Songserm, T., Amonsin, A., Jam-on, R., Sae-Heng, N., Meemak, N., Pariyothorn, N., Payungporn, S., Theamboonlers, A. and Poovorawan, Y. (2006): Avian influenza H5N1 in naturally infected domestic cat. Emerg. Infect. Dis. 12, 681–683.
Poovorawan Y. , 'Avian influenza H5N1 in naturally infected domestic cat ' (2006 ) 12 Emerg. Infect. Dis. : 681 -683.
Sponseller, B. A., Strait, E., Jergens, A., Trujillo, J., Harmon, K., Koster, L., Jenkins-Moore, M., Killian, M., Swenson, S., Bender, H., Waller, K., Miles, K., Pearce, T., Yoon, K. J. and Nara, P. (2010): Influenza A pandemic (H1N1) 2009 virus infection in domestic cat. Emerg. Infect. Dis. 16, 534–537.
Nara P. , 'Influenza A pandemic (H1N1) 2009 virus infection in domestic cat ' (2010 ) 16 Emerg. Infect. Dis. : 534 -537.
Stevens, J., Blixt, O., Tumpey, T. M., Taubenberger, J. K., Paulson, J. C. and Wilson, I. A. (2006): Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312, 404–410.
Wilson I. A. , 'Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus ' (2006 ) 312 Science : 404 -410.
Suzuki, Y. (2005): Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull. 28, 399–408.
Suzuki Y. , 'Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses ' (2005 ) 28 Biol. Pharm. Bull. : 399 -408.
Thompson, C. I., Barclay, W. S., Zambon, M. C. and Pickles, R. J. (2006): Infection of human airway epithelium by human and avian strains of influenza A virus. J. Virol. 80, 8060–8068.
Pickles R. J. , 'Infection of human airway epithelium by human and avian strains of influenza A virus ' (2006 ) 80 J. Virol. : 8060 -8068.
Thongratsakul, S., Suzuki, Y., Hiramatsu, H., Sakpuaram, T., Sirinarumitr, T., Poolkhet, C., Moonjit, P., Yodsheewan, R. and Songserm, T. (2010): Avian and human influenza A virus receptors in trachea and lung of animals. Asian Pac. J. Allergy Immunol. 28, 294–301.
Songserm T. , 'Avian and human influenza A virus receptors in trachea and lung of animals ' (2010 ) 28 Asian Pac. J. Allergy Immunol. : 294 -301.
Vandegrift, K. J., Sokolow, S. H., Daszak, P. and Kilpatrick, A. M. (2010): Ecology of avian influenza viruses in a changing world. Ann. N. Y. Acad. Sci. 1195, 113–128.
Kilpatrick A. M. , 'Ecology of avian influenza viruses in a changing world ' (2010 ) 1195 Ann. N. Y. Acad. Sci. : 113 -128.
Yao, L., Korteweg, C., Hsueh, W. and Gu, J. (2008): Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB J. 22, 733–740.
Gu J. , 'Avian influenza receptor expression in H5N1-infected and noninfected human tissues ' (2008 ) 22 FASEB J. : 733 -740.