Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding

Journal of Virology

Volumn 82, Issue 21, 2008, Pages 10756-10767

  Shirato, Haruko ^c   Ogawa, Satoko ^c   Ito, Hiromi ^a   Sato, Takashi ^a   Kameyama, Akihiko ^a   Narimatsu, Hisashi ^a   Xiaofan, Zheng ^b   Miyamura, Tatsuo ^c   Wakita, Takaji ^c   Ishii, Koji ^c   Takeda, Naokazu ^c  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b BLOOD CENTER OF ZHEJIANG PROVINCE   (China)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD GROUP A ANTIGEN; BLOOD GROUP ABH ANTIGEN; BLOOD GROUP B ANTIGEN; PENTASACCHARIDE; BLOOD GROUP ANTIGEN; OLIGOSACCHARIDE; VIROSOME; VIRUS RECEPTOR;

ADULT; ARTICLE; BLOOD GROUP LEWIS SYSTEM; CARBOHYDRATE ANALYSIS; FEMALE; GENOTYPE; HUMAN; MALE; NONHUMAN; NORMAL HUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; VIRUS ATTACHMENT; VIRUS LIKE AGENT; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING; SURFACE PLASMON RESONANCE; SYNTHESIS;

NOROVIRUS; NORWALK VIRUS;

ADULT; BLOOD GROUP ANTIGENS; CARBOHYDRATE SEQUENCE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NORWALK VIRUS; OLIGOSACCHARIDES; PROTEIN BINDING; RECEPTORS, VIRUS; SURFACE PLASMON RESONANCE; VIROSOMES; VIRUS ATTACHMENT;

EID: 55249114207     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00802-08     Document Type: Article

References (48)

1. Atmar, R. L., and M. K. Estes. 2001. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 14:15-37.
2. Bjork, S., M. E. Breimer, G. C. Hansson, K. A. Karlsson, and H. Leffler. 1987. Structures of blood group glycosphingolipids of human small intestine. A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J. Biol. Chem. 262:6758-6765.
3. Cao, S., Z. Lou, M. Tan, Y. Chen, Y. Liu, Z. Zhang, X. C. Zhang, X. Jiang, X. Li, and Z. Rao. 2007. Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 81:5949-5957.
4. Chakravarty, S., A. M. Hutson, M. K. Estes, and B. V. Prasad. 2005. Evolutionary trace residues in noroviruses: importance in receptor binding, antigenicity, virion assembly, and strain diversity. J. Virol. 79:554-568.
5. Cheetham, S., M. Souza, R. McGregor, T. Meulia, Q. Wang, and L. J. Saif. 2007. Binding patterns of human norovirus-like particles to buccal and intestinal tissues of gnotobiotic pigs in relation to A/H histo-blood group antigen expression. J. Virol. 81:3535-3544.
6. Connor, R. J., Y. Kawaoka, R. G. Webster, and J. C. Paulson. 1994. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205:17-23.
7. Dabelsteen, E., P. Vedtofte, S. I. Hakomori, and W. W. Young. 1982. Carbohydrate chains specific for blood group antigens in differentiation of human oral epithelium. J. Investig. Dermatol. 79:3-7.
8. Estes, M. K., J. M. Ball, S. E. Crawford, C. O'Neal, A. A. Opekun, D. Y. Graham, and M. E. Conner. 1997. Virus-like particle vaccines for mucosal immunization. Adv. Exp. Med. Biol. 412:387-395.
9. Grubb, R. 1948. Correlation between Lewis blood group and secretor character in man. Nature 162:933.
10. Hakomori, S. 1981. Blood group ABH and Ii antigens of human erythrocytes: chemistry, polymorphism, and their developmental change. Semin. Hematol. 18:39-62.
11. Hansman, G. S., K. Natori, H. Shirato-Horikoshi, S. Ogawa, T. Oka, K. Katayama, T. Tanaka, T. Miyoshi, K. Sakae, S. Kobayashi, M. Shinohara, K. Uchida, N. Sakurai, K. Shinozaki, M. Okada, Y. Seto, K. Kamata, N. Nagata, K. Tanaka, T. Miyamura, and N. Takeda. 2006. Genetic and antigenic diversity among noroviruses. J. Gen. Virol. 87:909-919.
12. Harrington, P. R., L. Lindesmith, B. Yount, C. L. Moe, and R. S. Baric. 2002. Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J. Virol. 76:12335-12343.
13. Harrington, P. R., J. Vinje, C. L. Moe, and R. S. Baric. 2004. Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. J. Virol. 78:3035-3045.
14. Huang, P., T. Farkas, S. Marionneau, W. Zhong, N. Ruvoen-Clouet, A. L. Morrow, M. Altaye, L. K. Pickering, D. S. Newburg, J. LePendu, and X. Jiang. 2003. Noroviruses bind to human ABO, Lewis, and secretor histoblood group antigens: identification of 4 distinct strain-specific patterns. J. Infect. Dis. 188:19-31.
15. Huang, P., T. Farkas, W. Zhong, M. Tan, S. Thornton, A. L. Morrow, and X. Jiang. 2005. Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J. Virol. 79:6714-6722.
16. Hutson, A. M., R. L. Atmar, D. Y. Graham, and M. K. Estes. 2002. Norwalk virus infection and disease is associated with ABO histo-blood group type. J. Infect. Dis. 185:1335-1337.
17. Hutson, A. M., R. L. Atmar, D. M. Marcus, and M. K. Estes. 2003. Norwalk virus-like particle hemagglutination by binding to H histo-blood group antigens. J. Virol. 77:405-415.
18. Isshiki, S., A. Togayachi, T. Kudo, S. Nishihara, M. Watanabe, T. Kubota, M. Kitajima, N. Shiraishi, K. Sasaki, T. Andoh, and H. Narimatsu. 1999. Cloning, expression, and characterization of a novel UDP-galactose:beta-N- acetylglucosamine beta1,3-galactosyltransferase (beta3Gal-T5) responsible for synthesis of type 1 chain in colorectal and pancreatic epithelia and tumor cells derived therefrom. J. Biol. Chem. 274:12499-12507.
19. Ito, H., A. Kameyama, T. Sato, M. Sukegawa, H. K. Ishida, and H. Narimatsu. 2007. Strategy for the fine characterization of glycosyltransferase specificity using isotopomer assembly. Nat. Methods 4:577-582.
20. Kageyama, T., M. Shinohara, K. Uchida, S. Fukushi, F. B. Hoshino, S. Kojima, R. Takai, T. Oka, N. Takeda, and K. Katayama. 2004. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan. J. Clin. Microbiol. 42:2988-2995.
21. Kamata, K., K. Shinozaki, M. Okada, Y. Seto, S. Kobayashi, K. Sakae, M. Oseto, K. Natori, H. Shirato-Horikoshi, K. Katayama, T. Tanaka, N. Takeda, and K. Taniguchi. 2005. Expression and antigenicity of virus-like particles of norovirus and their application for detection of noroviruses in stool samples. J. Med. Virol. 76:129-136.
22. Kaneko, M., S. Nishihara, N. Shinya, T. Kudo, H. Iwasaki, T. Seno, Y. Okubo, and H. Narimatsu. 1997. Wide variety of point mutations in the H gene of Bombay and para-Bombay individuals that inactivate H enzyme. Blood 90:839-849.
23. Kapikian, A. Z. 1996. Overview of viral gastroenteritis. Arch. Virol. Suppl. 12:7-19.
24. Kitamoto, N., T. Tanaka, K. Natori, N. Takeda, S. Nakata, X. Jiang, and M. K. Estes. 2002. Cross-reactivity among several recombinant calicivirus virus-like particles (VLPs) with monoclonal antibodies obtained from mice immunized orally with one type of VLP. J. Clin. Microbiol. 40:2459-2465.
25. Kobayashi, S., K. Sakae, Y. Suzuki, K. Shinozaki, M. Okada, H. Ishiko, K. Kamata, K. Suzuki, K. Natori, T. Miyamura, and N. Takeda. 2000. Molecular cloning, expression, and antigenicity of Seto virus belonging to geno-group I Norwalk-like viruses. J. Clin. Microbiol. 38:3492-3494.
26. Kobayashi, S., K. Sakae, K. Natori, N. Takeda, T. Miyamura, and Y. Suzuki. 2000. Serotype-specific antigen ELISA for detection of Chiba virus in stools. J. Med. Virol. 62:233-238.
27. Kobayashi, S., K. Sakae, Y. Suzuki, H. Ishiko, K. Kamata, K. Suzuki, K. Natori, T. Miyamura, and N. Takeda. 2000. Expression of recombinant capsid proteins of chitta virus, a genogroup II Norwalk virus, and development of an ELISA to detect the viral antigen. Microbiol. Immunol. 44:687-693.
28. Kudo, T., H. Iwasaki, S. Nishihara, N. Shinya, T. Ando, I. Narimatsu, and H. Narimatsu. 1996. Molecular genetic analysis of the human Lewis histo-blood group system. II. Secretor gene inactivation by a novel single missense mutation A385T in Japanese nonsecretor individuals. J. Biol. Chem. 271:9830-9837.
29. Lindesmith, L., C. Moe, S. Marionneau, N. Ruvoen, X. Jiang, L. Lindblad, P. Stewart, J. LePendu, and R. Baric. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9:548-553.
30. Lopman, B., H. Vennema, E. Kohli, P. Pothier, A. Sanchez, A. Negredo, J. Buesa, E. Schreier, M. Reacher, D. Brown, J. Gray, M. Iturriza, C. Gallimore, B. Bottiger, K. O. Hedlund, M. Torven, C. H. von Bonsdorff, L. Maunula, M. Poljsak-Prijatelj, J. Zimsek, G. Reuter, G. Szucs, B. Melegh, L. Svennson, Y. van Duijnhoven, and M. Koopmans. 2004. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363:682-688.
31. Marionneau, S., N. Ruvoen, B. Le Moullac-Vaidye, M. Clement, A. Cailleau-Thomas, G. Ruiz-Palacois, P. Huang, X. Jiang, and J. Le Pendu. 2002. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122:1967-1977.
32. Mollicone, R., J. Bara, J. Le Pendu, and R. Oriol. 1985. Immunohistologic pattern of type 1 (Lea, Leb) and type 2 (X, Y, H) blood group-related antigens in the human pyloric and duodenal mucosae. Lab. Investig. 53:219-227.
33. Narimatsu, H., S. Sinha, K. Brew, H. Okayama, and P. K. Qasba. 1986. Cloning and sequencing of cDNA of bovine N-acetylglucosamine (beta 1-4)galactosyltransferase. Proc. Natl. Acad. Sci. USA 83:4720-4724.
34. Noel, J. S., R. L. Fankhauser, T. Ando, S. S. Monroe, and R. I. Glass. 1999. Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution. J. Infect. Dis. 179:1334-1344.
35. Okada, M., T. Ogawa, I. Kaiho, and K. Shinozaki. 2005. Genetic analysis of noroviruses in Chiba Prefecture, Japan, between 1999 and 2004. J. Clin. Microbiol. 43:4391-4401.
36. Oriol, R. 1990. Genetic control of the fucosylation of ABH precursor chains. Evidence for new epistatic interactions in different cells and tissues. J. Immunogenet. 17:235-245.
37. Oriol, R., J. Le Pendu, and R. Mollicone. 1986. Genetics of ABO, H, Lewis, X and related antigens. Vox Sang. 51:161-171.
38. Orntoft, T. F., E. H. Holmes, P. Johnson, S. Hakomori, and H. Clausen. 1991. Differential tissue expression of the Lewis blood group antigens: enzymatic, immunohistologic, and immunochemical evidence for Lewis a and b antigen expression in Le(a-b-) individuals. Blood 77:1389-1396.
39. Rockx, B. H., H. Vennema, C. J. Hoebe, E. Duizer, and M. P. Koopmans. 2005. Association of histo-blood group antigens and susceptibility to norovirus infections. J. Infect. Dis. 191:749-754.
40. Rogers, G. N., and J. C. Paulson. 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.
41. Rogers, G. N., T. J. Pritchett, J. L. Lane, and J. C. Paulson. 1983. Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology 131:394-408.
42. b, X, and Y blood group antigens in human colonic tumors and normal tissue and in human tumor-derived cell lines. Cancer Res. 46:1553-1561.
43. Shiraishi, N., A. Natsume, A. Togayachi, T. Endo, T. Akashima, Y. Yamada, N. Imai, S. Nakagawa, S. Koizumi, S. Sekine, H. Narimatsu, and K. Sasaki. 2001. Identification and characterization of three novel beta 1,3-N-acetylglucosaminyltransferases structurally related to the beta 1,3-galactosyltransferase family. J. Biol. Chem. 276:3498-3507.
44. Shirato-Horikoshi, H., S. Ogawa, T. Wakita, N. Takeda, and G. S. Hansman. 2007. Binding activity of norovirus and sapovirus to histo-blood group antigens. Arch. Virol. 152:457-461.
45. Sidmann, F. K. (ed.). 1981. Appendix 2: saliva testing for ABH and Lewis, p. 122-123. In Technical Manual of the American Association of Blood Banks, 8th ed. J. B. Lippincott, Philadelphia, PA.
46. Soejima, M., and Y. Koda. 2005. Molecular mechanisms of Lewis antigen expression. Leg. Med. (Tokyo) 7:266-269.
47. Tamura, M., K. Natori, M. Kobayashi, T. Miyamura, and N. Takeda. 2000. Interaction of recombinant Norwalk virus particles with the 105-kilodalton cellular binding protein, a candidate receptor molecule for virus attachment. J. Virol. 74:11589-11597.
48. Tan, M., P. Huang, J. Meller, W. Zhong, T. Farkas, and X. Jiang. 2003. Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. J. Virol. 77:12562-12571.