Protective immunoglobulin A and G antibodies bind to overlapping intersubunit epitopes in the head domain of type 1 reovirus adhesin σ1

Journal of Virology

Volumn 78, Issue 19, 2004, Pages 10695-10705

  Helander, Anna ^a,b,d   Miller, Cathy L ^b   Myers, Kimberly S ^b,c   Neutra, Marian R ^a,b   Nibert, Max L ^b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; DIMER; EPITOPE; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G ANTIBODY; MONOCLONAL ANTIBODY; MONOMER; NEUTRALIZING ANTIBODY; POLYMER; RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN BINDING; ARTICLE; CELL CULTURE; CONJUGATE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EPITHELIUM CELL; FIBER; HYBRIDOMA; INTESTINE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RABBIT; RETROVIRUS; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS STRAIN;

AMINO ACID SUBSTITUTION; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; CAPSID PROTEINS; EPITOPE MAPPING; EPITOPES; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MODELS, MOLECULAR; MUTATION, MISSENSE; NEUTRALIZATION TESTS; ORTHOREOVIRUS, MAMMALIAN; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; RECEPTORS, VIRUS; REOVIRIDAE INFECTIONS; VIRUS ASSEMBLY;

EID: 4544262242     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.19.10695-10705.2004     Document Type: Article

References (61)

1. Amerongen, H. M., G. A. R. Wilson, B. N. Fields, and M. R. Neutra. 1994. Proteolytic processing of reovirus is required for adherence to intestinal M cells. J. Virol. 68:8428-8432.
2. Attoui, H., P. Biagini, J. Stirling, P. P. Mertens, J. F. Cantaloube, A. Meyer, P. de Micco, and X. de Lamballerie. 2001. Sequence characterization of Ndelle virus genome segments 1, 5, 7, 8, and 10: evidence for reassignment to the genus Orthoreovirus, family Reoviridae. Biochem. Biophys. Res. Commun. 287:583-588.
3. Barton, E. S., J. L. Connolly, J. C. Forrest, J. D. Chappell, and T. S. Dermody. 2000. Utilization of sialic acid as a coreceptor enhances reovirus attachment by multi-step adhesion-strengthening. J. Biol. Chem. 276:2200-2211.
4. Barton, E. S., J. C. Forrest, J. L. Connolly, J. D. Chappell, Y. Liu, F. J. Schnell, A. Nusrat, C. A. Parkos, and T. S. Dermody. 2001. Junction adhesion molecule is a receptor for reovirus. Cell 104:441-451.
5. Bassel-Duby, R., A. Jayasuriya, D. Chatterjee, N. Sonenberg, J. V. Maizel, Jr., and B. N. Fields. 1985. Sequence of reovirus haemagglutinin predicts a coiled-coil structure. Nature 315:421-423.
6. Bassel-Duby, R., D. R. Spriggs, K. L. Tyler, and B. N. Fields. 1986. Identification of attenuating mutations on the reovirus type 3 S1 double-stranded RNA segment with a rapid sequencing technique. J. Virol. 60:64-67.
7. Bizebard, T., C. Barbey-Martin, D. Fleury, B. Gigant, B. Barrere, J. J. Skehel, and M. Knossow. 2001. Structural studies on viral escape from antibody neutralization. Curr. Top. Microbiol. Immunol. 260:55-64.
8. Burstin, S. J., D. R. Spriggs, and B. N. Fields. 1982. Evidence for functional domains on the reovirus type 3 hemagglutinin. Virology 117:146-155.
9. Chandran, K., X. Zhang, N. O. Olson, S. B. Walker, J. D. Chappell, T. S. Dermody, T. S. Baker, and M. L. Nibert. 2001. Complete in vitro assembly of the reovirus outer capsid produces highly infectious particles suitable for genetic studies of the receptor-binding protein. J. Virol. 75:5335-5342.
10. Chappell, J. D., E. S. Barton, T. H. Smith, G. S. Baer, D. T. Duong, M. L. Nibert, and T. S. Dermody. 1998. Cleavage susceptibility of reovirus attachment protein σ1 during proteolytic disassembly of virions is determined by a sequence polymorphism in the σ1 neck. J. Virol. 72:8205-8213.
11. Chappell, J. D., J. L. Duong, B. W. Wright, and T. S. Dermody. 2000. Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J. Virol. 74:8472-8479.
12. Chappell, J. D., V. L. Gunn, J. D. Wetzel, G. S. Baer, and T. S. Dermody. 1997. Mutations in type 3 reovirus that determine binding to sialic acid are contained in the fibrous tail domain of viral attachment protein σ1. J. Virol. 71:1834-1841.
13. Chappell, J. D., A. E. Porta, T. S. Dermody, and T. Stehle. 2002. Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J. 21:1-11.
14. Davis, A. C., K. H. Roux, and M. J. Shulman. 1988. On the structure of polymeric IgM. Eur. J. Immunol. 18:1001-1008.
15. Dermody, T. S., M. L. Nibert, R. Bassel-Duby, and B. N. Fields. 1990. A σ1 region important for hemagglutination by serotype 3 reovirus strains. J. Virol. 64:5173-5176.
16. Dryden, K. A., G. Wang, M. Yeager, M. L. Nibert, K. M. Coombs, D. B. Furlong, B. N. Fields, and T. S. Baker. 1993. Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J. Cell Biol. 122:1023-1041.
17. Duncan, R., D. Home, L. W. Cashdollar, W. K. Joklik, and P. W. K. Lee. 1990. Identification of conserved domains in the cell attachment proteins of the three serotypes of reovirus. Virology 174:399-409.
18. Fraser, R. D., D. B. Furlong, B. L. Trus, M. L. Nibert, B. N. Fields, and A. C. Steven. 1990. Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. J. Virol. 64:2990-3000.
19. Furlong, D. B., M. L. Nibert, and B. N. Fields. 1988. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 62:246-256.
20. Goral, M. I., M. Mochow Grundy, and T. S. Dermody. 1996. Sequence diversity within the reovirus S3 gene: reoviruses evolve independently of host species, geographic locale, and date of isolation. Virology 216:265-271.
21. Haneberg, B., D. Kendall, H. M. Amerongen, F. M. Apter, J. P. Kraehenbuhl, and M. R. Neutra. 1994. Induction of secretory immune responses in small intestine, colon-rectum, and vagina measured with a new method for collection of specific IgA from local mucosal surfaces. Infect. Immun. 62:15-23.
22. Helander, A., K. J. Silvey, N. J. Mantis, A. B. Hutchings, K. Chandran, W. T. Lucas, M. L. Nibert, and M. R. Neutra. 2003. The viral σ1 protein and glycoconjugates containing α2,3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. J. Virol. 77:7964-7977.
23. Hrdy, D. B., L. Rosen, and B. N. Fields. 1979. Polymorphism of the migration of double-stranded RNA genome segments of reovirus isolates from humans, cattle, and mice. J. Virol. 31:104-111.
24. Hutchings, A. B., A. Helander, K. J. Silvey, W. T. Lucas, and M. R. Neutra. 2003. Secretory IgA antibodies against the σ1 outer capsid protein of reovirus type 1 Lang prevent infection of mouse Peyer's patches. J. Virol. 77:947-957.
25. Jané-Valbuena, J., M. L. Nibert, S. M. Spencer, S. B. Walker, T. S. Baker, Y. Chen, V. E. Centonze, and L. A. Schiff. 1999. Reovirus virion-like particles obtained by recoating infectious subvirion particles with baculovirus-expressed σ3 protein: an approach for analyzing σ3 functions during virus entry. J. Virol. 73:2963-2973.
26. Johansson, L., P. Johansson, and H. Miller-Podraza. 1999. Detection by the lectins from Maackia amurensis and Sambucus nigra of 3- and 6-linked sialic acid in gangliosides with neolacto chains separated on thin-layer chromatograms and blotted to PVDF membranes. Anal. Biochem. 267:239-241.
27. Kato, H., R. Kato, K. Fujihashi, and J. R. McGhee. 2001. Role of mucosal antibodies in viral infections. Curr. Top. Microbiol. Immunol. 260:201-228.
28. Klasse, P. J., and Q. J. Sattentau. 2002. Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J. Gen. Virol. 83:2091-2108.
29. Knibbs, R. N., I. J. Goldstein, R. M. Ratcliffe, and N. Shibuya. 1991. Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J. Biol. Chem. 266:83-88.
30. Konami, Y., K. Yamamoto, T. Osawa, and T. Irimura. 1994. Strong affinity of Maackia amurensis hemagglutinin (MAH) for sialic acid-containing Ser/Thr-linked carbohydrate chains of N-terminal octapeptides from human glycophorin A. FEBS Lett. 342:334-338.
31. Lee, P. W. K., and R. Gilmore. 1998. Reovirus cell attachment protein σ1: structure-function relationships and biogenesis. Curr. Top. Microbiol. Immunol. 233/I:137-154.
32. Liu, Y., A. Nusrat, F. J. Schnell, T. A. Reaves, S. Welsh, M. Pochet, and C. A. Parkos. 2000. Human junction adhesion molecule regulates tight junction resealing in epithelia. J. Cell Sci. 113:2363-2374.
33. Mantis, N. J., A. Frey, and M. R. Neutra. 2000. Accessibility of glycolipid and oligosaccharide epitopes on rabbit villus and follicle-associated epithelium. Am. J. Physiol. 278:G915-G923.
34. Neutra, M. R., N. J. Mantis, A. Frey, and P. J. Giannasca. 1999. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Semin. Immunol. 11:171-181.
35. Nibert, M. L., J. D. Chappell, and T. S. Dermody. 1995. Infectious subvirion particles of reovirus type 3 Dearing exhibit a loss in infectivity and contain a cleaved σ1 protein. J. Virol. 69:5057-5067.
36. Nibert, M. L., T. S. Dermody, and B. N. Fields. 1990. Structure of the reovirus cell-attachment protein: a model for the domain organization of σ1. J. Virol. 64:2976-2989.
37. Organ, E. L., and D. H. Rubin. 1998. Pathogenesis of reovirus gastrointestinal and hepatobiliary disease. Curr. Top. Microbiol. Immunol. 233/II:67-83.
38. Phalipon, A., A. Cardona, J. P. Kraehenbuhl, L. Edelman, P. J. Sansonetti, and B. Corthesy. 2002. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity 17:107-115.
39. Paul, R. W., A. H. C. Choi, and P. W. K. Lee. 1989. The α-anomeric form of sialic acid is the minimal receptor determinant recognized by reovirus. Virology 172:382-385.
40. Porta, C., G. Wang, H. Cheng, Z. Chen, T. S. Baker, and J. E. Johnson. 1994. Direct imaging of interactions between an icosahedral virus and conjugate F(ab) fragments by cryoelectron microscopy and X-ray crystallography. Virology 204:777-788.
41. Prota, A. E., J. A. Campbell, P. Schelling, J. C. Forrest, M. J. Watson, T. R. Peters, M. Aurrand-Lions, B. A. Imhof, T., S. Dermody, and T. Stehle. 2003. Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc. Natl. Acad. Sci. USA 100:5366-5371.
42. Rubin, D. H., J. D. Wetzel, W. V. Williams, J. A. Cohen, C. Dworkin, and T. S. Dermody. 1992. Binding of type 3 reovirus by a domain of the σ1 protein important for hemagglutination leads to infection of murine erythroleukemia cells. J. Clin. Investig. 90:2536-2542.
43. Sherry, B., A. G. Mosser, R. J. Colonno, and R. R. Rueckert. 1986. Use of monoclonal antibodies to identify four neutralization immunogens on a common cold picornavirus, human rhinovirus 14. J. Virol. 57:246-257.
44. Silvey, K. J., A. B. Hutchings, M. Vajdy, M. M. Petzke, and M. R. Neutra. 2001. Role of immunoglobulin A in protection against reovirus entry into murine Peyer's patches. J. Virol. 75:10870-10879.
45. Smith, T. J. 2001. Antibody interactions with rhinovirus: lessons for mechanisms of neutralization and the role of immunity in viral evolution. Curr. Top. Microbiol. Immunol. 260:1-28.
46. Spriggs, D. R., and B. N. Fields. 1982. Attenuated reovirus type 3 strains generated by selection of haemagglutinin antigenic variants. Nature 297:68-70.
47. Spriggs, D. R., K. Kaye, and B. N. Fields. 1983. Topological analysis of the reovirus type 3 hemagglutinin. Virology 127:220-224.
48. Stehle, T., and T. S. Dermody. 2003. Structural evidence for common functions and ancestry of the reovirus and adenovirus attachment proteins. Rev. Med. Virol. 13:123-132.
49. Strong, J. E., G. Leone, R. Duncan, R. K. Sharma, and P. W. K. Lee. 1991. Biochemical and biophysical characterization of the reovirus cell attachment protein σ1: evidence that it is a homotrimer. Virology 184:23-32.
50. Tyler, K. L. 2001. Mammalian reoviruses, p. 1729-1748. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott/The Williams & Wilkins Co., Philadelphia, Pa.
51. Tyler, K. L., M. A. Mann, B. N. Fields, and H. W. Virgin, IV. 1993. Protective anti-reovirus monoclonal antibodies and their effects on viral pathogenesis. J. Virol. 67:3446-3453.
52. Tyler, K. L., H. W. Virgin IV., R. Bassel-Duby, and B. N. Fields. 1989. Antibody inhibits defined stages in the pathogenesis of reovirus serotype 3 infection of the central nervous system. J. Exp. Med. 170:887-900.
53. Verdin, E. M., G. L. King, and E. Maratos-Flier. 1989. Characterization of a common high-affinity receptor for reovirus serotypes 1 and 3 on endothelial cells. J. Virol. 63:1318-1325.
54. Verdin, E. M., S. P. Lynn, B. N. Fields, and E. Maratos-Flier. 1988. Uptake of reovirus serotype 1 by the lungs from the bloodstream is mediated by the viral hemagglutinin. J. Virol. 62:545-551.
55. Virgin, H. W., IV, M. A. Mann, B. N. Fields, and K. L. Tyler. 1991. Monoclonal antibodies to reovirus reveal structure/function relationships between capsid proteins and genetics of susceptibility to antibody action. J. Virol. 65:6772-6781.
56. Virgin, H. W., IV, R. Bassel-Duby, B. N. Fields, and K. L. Tyler. 1988. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J. Virol. 62:4594-4604.
57. Weiner, H. L., and B. N. Fields. 1977. Neutralization of reovirus: the gene responsible for the neutralization antigen. J. Exp. Med. 146:1305-1310.
58. Weltzin, R., P. Lucia-Jandris, P. Michetti, B. N. Fields, J. P. Kraehenbuhl, and M. R. Neutra. 1989. Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J. Cell Biol. 108:1673-1685.
59. Whitton, J. L., and M. B. A. Oldstone. 2001. The immune response to viruses, p. 285-320. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott/The Williams & Wilkins Co., Philadelphia, Pa.
60. Wolf, J. L., D. H. Rubin, R. Finberg, R. S. Kauffman, A. H. Sharpe, J. S. Trier, and B. N. Fields. 1981. Intestinal M cells: a pathway for entry of reovirus into the host. Science 212:471-472.
61. Wolf, J. L., R. S. Kauffman, R. Finberg, R. Dambrauskas, B. N. Fields, and J. S. Trier. 1983. Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology 85:291-300.