The viral σ1 protein and glycoconjugates containing α2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces

Anna Helander, Katherine J. Silvey, Nicholas J. Mantis, Amy B. Hutchings, Kartik Chandran, William T. Lucas, Max L. Nibert, Marian R. Neutra

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Abstract

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 α2-3 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 σ1 protein, MAL-II-sensitive binding to rabbit M cells and polarized Caco-2BBe cells was consistently associated with the T1L σ1. 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 σ1 protein with glycoconjugates containing α2-3-linked sialic acid that are accessible to viral particles only on M cell apical surfaces.

Original languageEnglish (US)
Pages (from-to)7964-7977
Number of pages14
JournalJournal of Virology
Volume77
Issue number14
DOIs
StatePublished - Jul 2003
Externally publishedYes

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Mammalian Orthoreovirus
glycoconjugates
Reoviridae
Glycoconjugates
sialic acids
N-Acetylneuraminic Acid
Viral Proteins
proteins
cells
rabbits
Rabbits
Oligosaccharides
Virion
virion
oligosaccharides
Epithelium
epithelium
Viruses
Peyer's Patches
Caco-2 Cells

ASJC Scopus subject areas

  • Immunology

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The viral σ1 protein and glycoconjugates containing α2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. / Helander, Anna; Silvey, Katherine J.; Mantis, Nicholas J.; Hutchings, Amy B.; Chandran, Kartik; Lucas, William T.; Nibert, Max L.; Neutra, Marian R.

In: Journal of Virology, Vol. 77, No. 14, 07.2003, p. 7964-7977.

Research output: Contribution to journalArticle

Helander, Anna ; Silvey, Katherine J. ; Mantis, Nicholas J. ; Hutchings, Amy B. ; Chandran, Kartik ; Lucas, William T. ; Nibert, Max L. ; Neutra, Marian R. / The viral σ1 protein and glycoconjugates containing α2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. In: Journal of Virology. 2003 ; Vol. 77, No. 14. pp. 7964-7977.
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abstract = "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 α2-3 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 σ1 protein, MAL-II-sensitive binding to rabbit M cells and polarized Caco-2BBe cells was consistently associated with the T1L σ1. 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 σ1 protein with glycoconjugates containing α2-3-linked sialic acid that are accessible to viral particles only on M cell apical surfaces.",
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AU - Lucas, William T.

AU - Nibert, Max L.

AU - Neutra, Marian R.

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