This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Helander, A.
Right arrow Articles by Neutra, M. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Helander, A.
Right arrow Articles by Neutra, M. R.

 Previous Article  |  Next Article 

Journal of Virology, July 2003, p. 7964-7977, Vol. 77, No. 14
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.14.7964-7977.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

The Viral {sigma}1 Protein and Glycoconjugates Containing {alpha}2-3-Linked Sialic Acid Are Involved in Type 1 Reovirus Adherence to M Cell Apical Surfaces{dagger}

Anna Helander,1 Katherine J. Silvey,1 Nicholas J. Mantis,1 Amy B. Hutchings,1 Kartik Chandran,2 William T. Lucas,2 Max L. Nibert,2 and Marian R. Neutra1*

GI Cell Biology Laboratory, Children's Hospital and Department of Pediatrics,1 Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 021152

Received 6 January 2003/ Accepted 30 April 2003

Type 1 reoviruses invade the intestinal mucosa of mice by adhering selectively to M cells in the follicle-associated epithelium and then exploiting M cell transport activity. The purpose of this study was to identify the apical cell membrane component and viral protein that mediate the M cell adherence of these viruses. Virions and infectious subviral particles of reovirus type 1 Lang (T1L) adhered to rabbit M cells in Peyer's patch mucosal explants and to tissue sections in an overlay assay. Viral adherence was abolished by pretreatment of sections with periodate and in the presence of excess sialic acid or lectins MAL-I and MAL-II (which recognize complex oligosaccharides containing sialic acid linked {alpha}2-3 to galactose). The binding of T1L particles to polarized human intestinal (Caco-2BBe) cell monolayers was correlated with the presence of MAL-I and MAL-II binding sites, blocked by excess MAL-I and -II, and abolished by neuraminidase treatment. Other type 1 reovirus isolates exhibited MAL-II-sensitive binding to rabbit M cells and polarized Caco-2BBe cells, but type 2 or type 3 isolates including type 3 Dearing (T3D) did not. In assays using T1L-T3D reassortants and recoated viral cores containing T1L, T3D, or no {sigma}1 protein, MAL-II-sensitive binding to rabbit M cells and polarized Caco-2BBe cells was consistently associated with the T1L {sigma}1. MAL-II-recognized oligosaccharide epitopes are not restricted to M cells in vivo, but MAL-II immobilized on virus-sized microparticles bound only to the follicle-associated epithelium and M cells. The results suggest that selective binding of type 1 reoviruses to M cells in vivo involves interaction of the type 1 {sigma}1 protein with glycoconjugates containing {alpha}2-3-linked sialic acid that are accessible to viral particles only on M cell apical surfaces.

* Corresponding author. Mailing address: GI Cell Biology Lab, Enders 1220, Children's Hospital, 300 Longwood Ave., Boston, MA 02115. Phone: (617) 355-6229. Fax: (617) 264-2876. E-mail: marian.neutra{at}tch.harvard.edu.

{dagger} This study is dedicated to the memory of our friend, colleague, and mentor Bernard N. Fields.

Journal of Virology, July 2003, p. 7964-7977, Vol. 77, No. 14
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.14.7964-7977.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Taube, S., Perry, J. W., Yetming, K., Patel, S. P., Auble, H., Shu, L., Nawar, H. F., Lee, C. H., Connell, T. D., Shayman, J. A., Wobus, C. E. (2009). Ganglioside-Linked Terminal Sialic Acid Moieties on Murine Macrophages Function as Attachment Receptors for Murine Noroviruses. J. Virol. 83: 4092-4101 [Abstract] [Full Text]  
  • Nochi, T., Yuki, Y., Matsumura, A., Mejima, M., Terahara, K., Kim, D.-Y., Fukuyama, S., Iwatsuki-Horimoto, K., Kawaoka, Y., Kohda, T., Kozaki, S., Igarashi, O., Kiyono, H. (2007). A novel M cell specific carbohydrate-targeted mucosal vaccine effectively induces antigen-specific immune responses. JEM 204: 2789-2796 [Abstract] [Full Text]  
  • Petris, C. K., Golomb, M., Phillips, T. E. (2007). Bacterial Transcytosis across Conjunctival M Cells. IOVS 48: 2172-2177 [Abstract] [Full Text]  
  • Stuart, A. D., Brown, T. D. K. (2007). {alpha}2,6-Linked sialic acid acts as a receptor for Feline calicivirus. J. Gen. Virol. 88: 177-186 [Abstract] [Full Text]  
  • Liu, H., Meagher, C. K., Moore, C. P., Phillips, T. E. (2005). M Cells in the Follicle-Associated Epithelium of the Rabbit Conjunctiva Preferentially Bind and Translocate Latex Beads. IOVS 46: 4217-4223 [Abstract] [Full Text]  
  • Pal, K., Kaetzel, C. S., Brundage, K., Cunningham, C. A., Cuff, C. F. (2005). Regulation of polymeric immunoglobulin receptor expression by reovirus. J. Gen. Virol. 86: 2347-2357 [Abstract] [Full Text]  
  • Campbell, J. A., Schelling, P., Wetzel, J. D., Johnson, E. M., Forrest, J. C., Wilson, G. A. R., Aurrand-Lions, M., Imhof, B. A., Stehle, T., Dermody, T. S. (2005). Junctional Adhesion Molecule A Serves as a Receptor for Prototype and Field-Isolate Strains of Mammalian Reovirus. J. Virol. 79: 7967-7978 [Abstract] [Full Text]  
  • Nokhbeh, M. R., Hazra, S., Alexander, D. A., Khan, A., McAllister, M., Suuronen, E. J., Griffith, M., Dimock, K. (2005). Enterovirus 70 Binds to Different Glycoconjugates Containing {alpha}2,3-Linked Sialic Acid on Different Cell Lines. J. Virol. 79: 7087-7094 [Abstract] [Full Text]  
  • Helander, A., Miller, C. L., Myers, K. S., Neutra, M. R., Nibert, M. L. (2004). Protective Immunoglobulin A and G Antibodies Bind to Overlapping Intersubunit Epitopes in the Head Domain of Type 1 Reovirus Adhesin {sigma}1. J. Virol. 78: 10695-10705 [Abstract] [Full Text]  
  • Delputte, P. L., Nauwynck, H. J. (2004). Porcine Arterivirus Infection of Alveolar Macrophages Is Mediated by Sialic Acid on the Virus. J. Virol. 78: 8094-8101 [Abstract] [Full Text]  
  • Mercier, G. T., Campbell, J. A., Chappell, J. D., Stehle, T., Dermody, T. S., Barry, M. A. (2004). A chimeric adenovirus vector encoding reovirus attachment protein {sigma}1 targets cells expressing junctional adhesion molecule 1. Proc. Natl. Acad. Sci. USA 101: 6188-6193 [Abstract] [Full Text]  
  • Hutchings, A. B., Helander, A., Silvey, K. J., Chandran, K., Lucas, W. T., Nibert, M. L., Neutra, M. R. (2004). Secretory Immunoglobulin A Antibodies against the {sigma}1 Outer Capsid Protein of Reovirus Type 1 Lang Prevent Infection of Mouse Peyer's Patches. J. Virol. 78: 947-957 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»