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J. Biol. Chem., Vol. 278, Issue 22, 20140-20153, May 30, 2003

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Secretory IgA N- and O-Glycans Provide a Link between the Innate and Adaptive Immune Systems^*

Louise Royle , Anja Roos , David J. Harvey , Mark R. Wormald , Daniëlle Van Gijlswijk-Janssen , El-Rashdy M. Redwan ¶, Ian A. Wilson ¶, Mohamed R. Daha , Raymond A. Dwek  and Pauline M. Rudd  ||

From the Glycobiology Institute, Department of Biochemistry, Oxford University, Oxford OX1 3QU, United Kingdom, the Department of Nephrology, Leiden University Medical Center, Leiden, The Netherlands, and the ^¶Department of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037

Secretory IgA (SIgA) is a multi-polypeptide complex consisting of a secretory component (SC) covalently attached to dimeric IgA containing one joining (J) chain. We present the analysis of both the N- and O-glycans on the individual peptides from this complex. Based on these data, we have constructed a molecular model of SIgA1 with all its glycans, in which the Fab arms form a T shape and the SC is wrapped around the heavy chains. The O-glycan regions on the heavy (H) chains and the SC N-glycans have adhesin-binding glycan epitopes including galactose-linked 1-4 and 1-3 to GlcNAc, fucose-linked 1-3 and 1-4 to GlcNAc and 1-2 to galactose, and 2-3 and 2-6-linked sialic acids. These glycan epitopes provide SIgA with further bacteria-binding sites in addition to the four Fab-binding sites, thus enabling SIgA to participate in both innate and adaptive immunity. We also show that the N-glycans on the H chains of both SIgA1 and SIgA2 present terminal GlcNAc and mannose residues that are normally masked by SC, but that can be unmasked and recognized by mannose-binding lectin, by disrupting the SC-H chain noncovalent interactions.

Received for publication, February 10, 2003

^* This work was supported by grants from the Biotechnology and Biological Sciences Research Council, the Higher Education Funding Council for England, and Dutch Kidney Foundation Grant PC95. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed. Tel.: 44-1865-275340; Fax: 44-1865-275216; E-mail: pauline.rudd{at}bioch.ox.ac.uk.

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