Glycobiology Advance Access originally published online on March 27, 2007
Glycobiology 2007 17(7):713-724; doi:10.1093/glycob/cwm038
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The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors
2 Department of Biomedical Sciences, College of Life and Health Sciences, Chubu University, 11200 Matsumoto-cho, Kasugai-shi, Aichi 487-8501, Japan
3 Institute of Bioengineering, Zhejiang Academy of Medical Sciences, 182 Tianmushan Road, Hangzhou 310016, China
4 CREST, Japan Science and Technology Agency, 4-1-8 Honcho, Kawaguchi, Japan
5 Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences, Suruga-ku, Shizuoka 422-8526, Japan
6 Graduate School of Pharmaceutical Sciences, Nagoya City University, 3-1 Tanabe-dori, Mizuho-ku, Nagoya 467-8603, Japan
7 GLYENCE Co., Ltd, 2-22-8 Chikusa, Chikusa-ku, Nagoya 464-0858, Japan
8 Department of Anatomy, Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku-ku, Tokyo 160-8402, Japan
9 Departments of Veterinary Public Health and
10 Veterinary Microbiology, Faculty of Agriculture, Tottori University, Tottori-shi, Tottori 680-8553, Japan
11 Laboratory of Microbiology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan
12 Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan
13 Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706
1 To whom correspondence should be addressed; Tel/Fax: +81 568 51 6391; e-mail: suzukiy{at}isc.chubu.ac.jp
Received on October 12, 2006; revised on March 13, 2007; accepted on March 22, 2007
The receptor specificity of influenza viruses is one factor that allows avian influenza viruses to cross the species barrier. The recent transmissions of avian H5N1 and H9N2 influenza viruses from chickens and/or quails to humans indicate that avian influenza viruses can directly infect humans without an intermediate host, such as pigs. In this study, we used two strains of influenza A virus (A/PR/8/34, which preferentially binds to an avian-type receptor, and A/Memphis/1/71, which preferentially binds to a human-type receptor) to probe the receptor specificities in host cells. Epithelial cells of both quail and chicken intestines (colons) could bind both avian- and human-type viruses. Infected cultured quail colon cells expressed viral protein and allowed replication of the virus strain A/PR/8/34 or A/Memphis/1/71. To understand the molecular basis of these phenomena, we further investigated the abundance of sialic acid (Sia) linked to galactose (Gal) by the 
2-3 linkage (Sia2-3Gal) and Sia2-6Gal in host cells. In glycoprotein and glycolipid fractions from quail and chicken colon epithelial cells, there were some bound components of Sia–Gal linkage-specific lectins, Maackia amurensis agglutinin (specific for Sia2-3 Gal) and Sambucus nigra agglutinin (specific for Sia2-6Gal), indicating that both Sia2–3Gal and Sia2-6Gal exist in quail and chicken colon cells. Furthermore, we demonstrated by fluorescence high-performance liquid chromatography (HPLC) analysis that 5-N-acetylneuraminic acid was the main molecular species of Sia, and we demonstrated by multi-dimensional HPLC mapping and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry analysis that bi-antennary complex-type glycans 2-6 sialylated at the terminal Gal residue(s) are major (more than 79%) sialyl N-glycans expressed by intestinal epithelial tissues in both the chicken and quail. Taken together, these results indicate that quails and chickens have molecular characterization as potential intermediate hosts for avian influenza virus transmission to humans and could generate new influenza viruses with pandemic potential.
Key words: influenza virus / receptor / sialic acid / chicken / quail
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