A specific cell surface antigen of Streptococcus gordonii is associated with bacterial hemagglutination and adhesion to alpha2-3-linked sialic acid-containing receptors

Abstract

A Ca 2؉-independent lectin activity for ␣2-3-linked sialic acid-containing receptors is associated with Streptococcus gordonii DL1 (Challis) but not with a spontaneous mutant, strain D102, that specifically lacks hemagglutinating activity. Comparison of crossed-immunoelectrophoresis patterns of parent and mutant sonicated cell extracts identified a unique antigen (Hs antigen) in the parent cell extract that was purified by DEAE Sephacel column chromatography and by a wheat germ agglutinin (WGA) lectin affinity column. The purified antigen formed a single arc in crossed immunoelectrophoresis with anti-DL1 serum and migrated as a diffuse band above the 200-kDa marker in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Immunoelectron microscopy with specific anti-Hs antibody revealed labeling of structures in the fibrillar layer of strain DL1 and no labeling of fibrillar structures on strain D102. Rabbit anti-DL1 serum and anti-Hs Fab inhibited the hemagglutinating activity of strain DL1, and the inhibition was specifically neutralized by purified Hs antigen. Anti-Hs Fab did not inhibit the hemagglutinating activities of several heterologous S. gordonii strains; however, these bacteria were agglutinated by anti-Hs immunoglobulin G and also by WGA. In contrast, two S. gordonii strains that lacked hemagglutinating activity did not react with anti-Hs antibody or with WGA. These findings associate the sialic acid-binding lectin activity of S. gordonii DL1 with a specific fibrillar antigen, which is composed of protein and WGA reactive carbohydrate, and indicate that crossreactive antigens occur on other strains of this species that possess hemagglutinating activity.

Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces

“…Consequently, we have proposed that IgA proteins exhibit protective functions through antibodydependent specific immunity as well as glycan-dependent innate immunity [30]. This concept was confirmed in vitro for other microbial ligand-glycan receptors [1,26,29,[60][61][62][63][64][65][66][67][68][69][70][71][72][73][74][75][76][77][78]. In addition to E. coli, many other bacteria such as Helicobacter pylori, Streptococcus pneumoniae, Clostridium difficile, Shigella flexneri, Pseudomonas aeruginosa and Neisseria gonorrhoeae, and some viruses (Table 1) interact with epithelial receptors via their glycan moiety.…”

“…Bacteria 0165-2478/$ -see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.imlet.2009.03.013 Table 1 Examples of glycans as adhesion sites and receptors for selected bacteria and viruses that colonize, or infect, mucosal surfaces (adapted from [1,26,29,[60][61][62][63][64][65][66][67][68][69][70][71][72][73][74][75][76][77][78]132] endogenous to the intestinal tract, oral cavity, and probably also the respiratory and genital tracts, are coated in vivo with S-IgA [9,13,17,[31][32][33][34][35][36][37][38][39] that limits their epithelial adherence and penetration, thereby confining them to the mucosal surfaces. Numerous models have demonstrated the role of antibodies, especially S-IgA, in protecting the intestinal and other mucosal tracts.…”

“…Structural studies of human polyclonal S-IgA and monoclonal (myeloma) IgA1 and IgA2 proteins reveal considerable heterogeneity with respect to number, sites of attachment, composition, and primary structure of their glycan side-chains [30,[71][72][73][74][75][76][77][87][88][89][90][91][92][93][94]115,[122][123][124][125][126][127], which is likely to be of enormous biological importance. Because different microorganisms interact with epithelial cells through diverse glycan receptors, heterogeneity of IgA-associated glycans affords a variety of structures that can effectively inhibit these interactions.…”

Biological roles of glycans

“…The thick layer of mucin glycans on the surface of epithelial cells lining hollow organs (139,418,(448)(449)(450)(451)(452) also plays a critical role by providing decoy binding sites for pathogens, diverting them from their intended targets on the cells. Of course commensals may take advantage of such mucin binding to remain within their preferred ecological niche (797)(798)(799)(800) and to favor dental biofilm development (801). But on the rare occasions when such bacteria accidentally find their way into the bloodstream, these same commensalism-favoring adhesins become virulence factors, mediating interactions with platelets, which act as carriers of the organisms to eventual infection of damaged heart valves (798,(802)(803)(804)(805)(806)(807).…”

Flagellar glycosylation in Clostridium botulinum

“…More recently, a unique family of high-molecular-mass serine-rich proteins found in staphyococcal and streptococcal species that play a major role in bacterial interactions with host components has been characterized. The Fap1 fimbriae of Streptococcus parasanguis and the Fap1-like protein adhesins GspB of Streptococcus gordonii [19] and SrpA of S. sanguis [20] are all glycosylated in a novel fashion through O-linkage. The glycan moieties of the Fap1 fimbriae were recently shown to play a role in biofilm development [21].…”