The P domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors

Journal of Virology

Volumn 79, Issue 22, 2005, Pages 14017-14030

  Tan, Ming ^a   Jiang, Xi ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; BLOOD GROUP ANTIGEN; CAPSID PROTEIN; CYSTEINE; DIMER; DISULFIDE; OLIGOPEPTIDE; RECOMBINANT PROTEIN; VIRUS RECEPTOR; VIRUS VACCINE;

ACUTE GASTROENTERITIS; ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; DIMERIZATION; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; NONHUMAN; NOROVIRUS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN POLYMERIZATION; RECEPTOR AFFINITY; VIRUS CAPSID; VIRUS PARTICLE; VIRUS STRAIN;

ANIMALS; BASE SEQUENCE; BINDING SITES; BLOOD GROUP ANTIGENS; CAPSID PROTEINS; CLONING, MOLECULAR; DNA PRIMERS; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NOROVIRUS; PEPTIDE FRAGMENTS; RECOMBINANT PROTEINS; SPODOPTERA;

ESCHERICHIA COLI; MIRIDAE; NOROVIRUS;

EID: 27644437147     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.22.14017-14030.2005     Document Type: Article

References (36)

1. Barcena, J., N. Verdaguer, R. Roca, M. Morales, I. Angulo, C. Risco, J. L. Carrascosa, J. M. Torres, and J. R. Caston. 2004. The coat protein of rabbit hemorrhagic disease virus contains a molecular switch at the N-terminal region facing the inner surface of the capsid. Virology 322:118-134.
2. Bertolotti-Ciarlet, A., L. J. White, R. Chen, B. V. Prasad, and M. K. Estes. 2002. Structural requirements for the assembly of Norwalk virus-like particles. J. Virol. 76:4044-4055.
3. 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.
4. Chen, R., J. D. Neill, J. S. Noel, A. M. Hutson, R. I. Glass, M. K. Estes, and B. V. V. Prasad. 2004. Inter- and intragenus structural variations in caliciviruses and their functional implications. J. Virol. 78:6469-6479.
5. Chen, X. S., R. L. Garcea, I. Goldberg, G. Casini, and S. C. Harrison. 2000. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell 5:557-567.
6. Cuillel, M., B. Jacrot, and M. Zulauf. 1981. AT=1 capsid formed by protein of brome mosaic virus in the presence of trypsin. Virology 110:63-72.
7. Curnis, F., G. Arrigoni, A. Sacchi, L. Fischetti, W. Arap, R. Pasqualini, and A. Corti. 2002. Differential binding of drugs containing the NGR motif to CD13 isoforms in tumor vessels, epithelia, and myeloid cells. Cancer Res. 62:867-874.
8. Erickson, J. W., A. M. Silva, M. R. Murthy, I. Fita, and M. G. Rossmann. 1985. The structure of a T = 1 icosahedral empty particle from southern bean mosaic virus. Science 229:625-629.
9. Fankhauser, R. L., S. S. Monroe, J. S. Noel, C. D. Humphrey, J. S. Bresee, U. D. Parashar, T. Ando, and R. I. Glass. 2002. Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. J. Infect. Dis. 186:1-7.
10. Glass, R. I., J. Bresee, B. Jiang, J. Gentsch, T. Ando, R. Fankhauser, J. Noel, U. Parashar, B. Rosen, and S. S. Monroe. 2001. Gastroenteritis viruses: an overview. Novartis Found. Symp. 238:5-19.
11. Greenberg, H. B., J. R. Valdesuso, A. R. Kalica, R. G. Wyatt, V. J. McAuliffe, A. Z. Kapikian, and R. M. Chanock. 1981. Proteins of Norwalk virus. J. Virol. 37:994-999.
12. Hardy, M. E., L. J. White, J. M. Ball, and M. K. Estes. 1995. Specific proteolytic cleavage of recombinant Norwalk virus capsid protein. J. Virol. 69:1693-1698.
13. 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.
14. 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.
15. Harrison, S. M. 2001. Principles of virus structure, p. p. 53-86. In D. M. Knipe P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
16. 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 histo-blood group antigens: identification of 4 distinct strain-specific patterns. J. Infect. Dis. 188:19-31.
17. Huang, P. W., T. Farkas, W. M. 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 specificity and classification of two major binding groups among multiple binding patterns. J. Virol. 79:6714-6722.
18. Hutson, A. M., R. L. Atmar, and M. K. Estes. 2004. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 12:279-287.
19. 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.
20. Hutson, A. M., S. Charkravarty, R. L. Atmar, B. V. Prasad, and M. Estes. 2004. Loss of carbohydrate binding with point mutations of Norwalk virus virus-like particles. Second International Calicivirus Conference, Dijon, France, 6-10 November, 2004.
21. Jiang, X., M. Wang, D. Y. Graham, and M. K. Estes. 1992. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 66:6527-6532.
22. Lindesmith, L., C. Moe, J. Lependu, J. A. Frelinger, J. Treanor, and R. S. Baric. 2005. Cellular and humoral immunity following Snow Mountain virus challenge. J. Virol. 79:2900-2909.
23. 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.
24. Lokesh, G. L., T. D. Gowri, P. S. Satheshkumar, M. R. Murthy, and H. S. Savithri. 2002. A molecular switch in the capsid protein controls the particle polymorphism in an icosahedral virus. Virology 292:211-223.
25. Marionneau, S., A. Cailleau-Thomas, J. Rocher, B. Le Moullac-Vaidye, N. Ruvoen, M. Clement, and J. Le Pendu. 2001. ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83:565-573.
26. 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.
27. Pasqualini, R., E. Koivunen, R. Kain, J. Lahdenranta, M. Sakamoto, A. Stryhn, R. A. Ashmun, L. H. Shapiro, W. Arap, and E. Ruoslahti. 2000. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res. 60:722-727.
28. Prasad, B. V., M. E. Hardy, T. Dokland, J. Bella, M. G. Rossmann, and M. K. Estes. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286:287-290.
29. Ravn, V., and E. Dabelsteen. 2000. Tissue distribution of histo-blood group antigens. APMIS 108:1-28.
30. Savithri, H. S., and J. W. Erickson. 1983. The self-assembly of the cowpea strain of Southern bean mosaic virus: formation of T=1 and T=3 nucleoprotein particles. Virology 126:328-335.
31. Tan, M., and X. Jiang. 2005. Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol. 13: 285-293.
32. Tan, M., R. S. Hegde, and X. Jiang. 2004. The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J. Virol. 78:6233-6242.
33. 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.
34. Tan, M., W. Zhong, D. Song, S. Thornton, and X. Jiang. 2004. E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. J. Med. Virol. 74:641-649.
35. White, L. J., J. M. Ball, M. E. Hardy, T. N. Tanaka, N. Kitamoto, and M. K. Estes. 1996. Attachment and entry of recombinant Norwalk virus capsids to cultured human and animal cell lines. J. Virol. 70:6589-6597.
36. White, L. J., M. E. Hardy, and M. K. Estes. 1997. Biochemical characterization of a smaller form of recombinant Norwalk virus capsids assembled in insect cells. J. Virol. 71:8066-8072.