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Functions of Cell Surface-Anchored Antigen I/II Family and Hsa Polypeptides in Interactions of Streptococcus gordonii with Host Receptors

Nicholas S. Jakubovics,^1, Steven W. Kerrigan,² Angela H. Nobbs,^1, Nicklas Strömberg,³ Craig J. van Dolleweerd,^4, Dermot M. Cox,² Charles G. Kelly,⁴ and Howard F. Jenkinson^1*

Department of Oral and Dental Science, University of Bristol, Bristol BS1 2LY, United Kingdom,¹ Royal College of Surgeons in Ireland, Dublin 2, Ireland,² Department of Cariology, Umeå University, Umeå, Sweden,³ Department of Oral Medicine and Immunology, GKT Dental Institute, London SE1 9RT, United Kingdom⁴

Received 4 March 2005/ Returned for modification 10 May 2005/ Accepted 13 June 2005

Streptococcus gordonii colonizes multiple sites within the human oral cavity. This colonization depends upon the initial interactions of streptococcal adhesins with host receptors. The adhesins that bind salivary agglutinin glycoprotein (gp340) and human cell surface receptors include the antigen I/II (AgI/II) family polypeptides SspA and SspB and a sialic acid-binding surface protein designated Hsa or GspB. In this study we determined the relative functions of the AgI/II polypeptides and Hsa in interactions of S. gordonii DL1 (Challis) with host receptors. For an isogenic mutant with the sspA and sspB genes deleted the levels of adhesion to surface-immobilized gp340 were reduced 40%, while deletion of the hsa gene alone resulted in >80% inhibition of bacterial cell adhesion to gp340. Adhesion of S. gordonii DL1 cells to gp340 was sialidase sensitive, verifying that Hsa has a major role in mediating sialic acid-specific adhesion to gp340. Conversely, aggregation of S. gordonii cells by fluid-phase gp340 was not affected by deletion of hsa but was eliminated by deletion of the sspA and sspB genes. Deletion of the AgI/II polypeptide genes had no measurable effect on hsa mRNA levels or Hsa surface protein expression, and deletion of hsa did not affect AgI/II polypeptide expression. Further analysis of mutant phenotypes showed that the Hsa and AgI/II proteins mediated adhesion of S. gordonii DL1 to human HEp-2 epithelial cells. Hsa was also a principal streptococcal cell surface component promoting adhesion of human platelets to immobilized streptococci, but Hsa and AgI/II polypeptides acted in concert in mediating streptococcal cell-platelet aggregation. The results suggest that Hsa directs primary adhesion events for S. gordonii DL1 (Challis) with immobilized gp340, epithelial cells, and platelets. AgI/II polypeptides direct gp340-mediated aggregation, facilitate multimodal interactions necessary for platelet aggregation, and modulate S. gordonii-host engagements into biologically productive phenomena.

Editor: J. N. Weiser

Present address: National Institutes of Health/NIDCR, Bldg. 30 Room 310, 30 Convent Drive MSC 4350, Bethesda, MD 20892-4350.

Present address: Department of Oral Sciences, University Of Minnesota, 17-164 Moos Tower, 515 Delaware St. SE, Minneapolis, MN 55455.

Present address: Department of Cellular and Molecular Medicine, St. George's Hospital Medical School, Cranmer Terrace, Tooting, London SW17 0RE, United Kingdom.

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