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J. Biol. Chem., Vol. 283, Issue 18, 12654-12664, May 2, 2008

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Molecular and Antigenic Characterization of a Streptococcus oralis Coaggregation Receptor Polysaccharide by Carbohydrate Engineering in Streptococcus gordonii^*

Yasuo Yoshida, Jinghua Yang, Paule-Esther Peaker^¶, Hirohisa Kato, C. Allen Bush^¶, and John O. Cisar¹

From the Oral Infection and Immunity Branch, NIDCR, National Institutes of Health, Bethesda, Maryland 20892, the Department of Dental Pharmacology, Iwate Medical University School of Dentistry, Morioka 020-8505, Japan, and the ^¶Department of Chemistry and Biochemistry, University of Maryland Baltimore County, Baltimore, Maryland 21250

The coaggregation receptor polysaccharides (RPS) of Streptococcus oralis and related species are recognized by lectin-like adhesins on other members of the oral biofilm community and by RPS-specific antibodies. The former interactions involve β-GalNAc or β-Gal containing host-like motifs in the oligosaccharide repeating units of these polysaccharides, whereas the latter involves features of these molecules that are immunogenic. In the present investigation, the molecular and corresponding structural basis for the serotype specificity of S. oralis ATCC 10557 RPS was determined by engineering the production of this polysaccharide in transformable Streptococcus gordonii 38. This involved the systematic replacement of genes in the rps cluster of strain 38 with different but related genes from S. oralis 10557 and structural characterization of the resulting polysaccharides. The results identify four unique genes in the rps cluster of strain 10557. These include wefI for an -Gal transferase, wefJ for a GalNAc-1-phosphotransferase that has a unique acceptor specificity, wefK for an acetyl transferase that acts at two positions in the hexasaccharide repeating unit, and a novel wzy associated with the β1-3 linkage between these units. The serotype specificity of engineered polysaccharides correlated with the wefI-dependent presence of -Gal in these molecules rather than with partial O-acetylation or with the linkage between repeating units. The findings illustrate a direct approach for defining the molecular basis of polysaccharide structure and antigenicity.

Received for publication, February 21, 2008

^* This work was supported in part by the Intramural Research Program of the NIDCR, National Institutes of Health, by Grant 96 from the Keiryokai Research Foundation, by Grants-in-Aid for Promoting Technological Seeds and a High-Tech Research Project (2005-2009) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to Y. Y.), and by Grant 02-12702 from the National Science Foundation (to C. A. B.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental data and supplemental Figs. S1-S9.

¹ To whom correspondence should be addressed: Bldg. 30, Rm. 3A-301, 30 Convent Dr., NIDCR, National Institutes of Health, Bethesda, MD 20892-4352. Fax: 301-402-1064; E-mail: john.cisar{at}nih.gov.

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