Carbohydrates act as receptors for the periodontitis-associated bacterium Porphyromonas gingivalis: a study of bacterial binding to glycolipids

Abstract

In this study we show for the first time the use of carbohydrate chains on glycolipids as receptors for the periodontitis-associated bacterium Porphyromonas gingivalis. Previous studies have shown that this bacterium has the ability to adhere to and invade the epithelial lining of the dental pocket. Which receptor(s) the adhesin of P. gingivalis exploit in the adhesion to epithelial cells has not been shown. Therefore, the binding preferences of this specific bacterium to structures of carbohydrate origin from more than 120 different acid and nonacid glycolipid fractions were studied. The bacteria were labeled externally with (35)S and used in a chromatogram binding assay. To enable detection of carbohydrate receptor structures for P. gingivalis, the bacterium was exposed to a large number of purified total glycolipid fractions from a variety of organs from different species and different histo-blood groups. P. gingivalis showed a preference for fractions of human and pig origin for adhesion. Both nonacid and acid glycolipids were used by the bacterium, and a preference for shorter sugar chains was noticed. Bacterial binding to human acid glycolipid fractions was mainly obtained in the region of the chromatograms where sulfated carbohydrate chains usually are found. However, the binding pattern to nonacid glycolipid fractions suggests a core chain of lactose bound to the ceramide part as a tentative receptor structure. The carbohydrate binding of the bacterium might act as a first step in the bacterial invasion process of the dental pocket epithelium, subsequently leading to damage to periodontal tissue and tooth loss.

Glycolipid binding epitopes involved in adherence of the periodontitis-associated bacterium Porphyromonas gingivalis

“…Both nonacid and acid carbohydrate chains are known to act as bacterial receptors [3,9,21,29,37,55,56]. In our previous study we showed for the first time that also the P. gingivalis strain FDC381 can utilize glycolipid sugar chains as potential bacterial receptors [20].…”

“…In addition, binding to galabiosylceramide (Galα4Galβ1Cer), globotriaosylceramide (Galα4Galβ4Glcβ1Cer) and globotetraosylceramide (GalNAcβ3Galα4Galβ4Glcβ1Cer) are found (not shown) Table 1. Moreover, in our previous study, binding to gangliotriaosylceramide (GalNAcβ4 Galβ4Glcβ1Cer) and gangliotetraosylceramide (Galβ3Gal NAcβ4Galβ4Glcβ1Cer) was obtained [20].…”

“…They mainly consist of total glycolipid fractions, which tested positively for bacterial binding [20] complemented with specific pure reference glycolipid fractions.…”

“…In a previous study, we were able to show that P. gingivalis has the ability to bind to total glycolipid fractions originating from human and porcine organs [20] by screening of a large array of glycolipid structures with the thin-layer chromatogram binding assay. Binding was obtained to both acid and nonacid glycolipids of human origin and to nonacid glycolipids of porcine origin.…”

Transglutaminase 2 is essential for adherence of Porphyromonas gingivalis to host cells

“…The adhesin domains of arg-gingipain A and lys-gingipain were shown to bind to epithelial cells, and the adhesin peptide A44 of the former has a high affinity for host FN (7,13). In addition to integrins and ECM proteins, P. gingivalis interacts with several other receptors (14)(15)(16). In the present study, we provide evidence that cell surface transglutaminase 2 (TG2) plays an essential role in the interaction of P. gingivalis with host cells.…”