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Salivary Receptors for the Proline-rich Protein-binding and Lectin-like Adhesins of Oral Actinomyces and Streptococci
S. Ruhl1,
A.L. Sandberg2 and
J.O. Cisar*
Oral Infection and Immunity Branch, National Institute of Dental and Craniofacial Research, Building 30, Room 532, National Institutes of Health, Bethesda, MD 20892;
Correspondence: * corresponding author, john.cisar{at}nih.gov
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ABSTRACT
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Colonization of the tooth surface by actinomyces and viridans group streptococci involves the attachment of these bacteria to adsorbed salivary components of the acquired enamel pellicle. The hypothesis that this attachment depends on specific adhesins has now been assessed from the binding of bacteria with well-defined adhesive properties to blots of SDS-PAGE-separated parotid and submandibular-sublingual (SM-SL) saliva. Streptococcus sanguis and type 2 fimbriated Actinomyces naeslundii, which bound terminal sialic acid and Galβ1-3GalNAc, respectively, recognized only a few SM-SL salivary components, primarily MG2. In contrast, type 1 fimbriated A. naeslundii and S. gordonii, which bound purified proline-rich proteins (PRPs), recognized several other components from both SM-SL and parotid saliva. Significantly, bacteria that lacked PRP-binding and the lectin-like activities detected by binding to MG2 failed to bind any immobilized salivary component. These findings suggest the involvement of specific adhesins in bacterial recognition of many adsorbed salivary proteins and glycoproteins.
Key Words: Actinomyces naeslundii • adhesins • salivary receptors • Streptococcus gordonii • Streptococcus sanguis
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INTRODUCTION
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A limited number of different bacteria, primarily viridans group streptococci and Actinomyces naeslundii, initiate colonization of the tooth surface (Nyvad and Kilian, 1987). These organisms attach to salivary components of the acquired enamel pellicle and, through growth and interactions between species, form a relatively simple biofilm community (Palmer et al., 2003). Members of this community can activate host cells (Sandberg et al., 1988), and the biofilm itself provides a habitat for other species that are associated with the initiation and progression of dental caries and periodontal disease (Gibbons, 1989). Consequently, bacterial recognition of salivary receptors on the tooth surface represents an important early step in the pathogenesis of oral disease.
Studies of the adhesion of viridans group streptococci to saliva-treated hydroxyapatite (SHA) provided early evidence for bacterial recognition of sialic-acid-containing salivary receptors. Thus, the adhesion of certain streptococcal strains to SHA was abolished following treatment of this substrate with sialidase (Gibbons et al., 1985), an enzyme that removes  2-3-linked sialic acid from salivary components such as the low-molecular-weight mucin, MG2 (Murray et al., 1982). The sialic-acid-binding adhesin of Streptococcus gordonii DL1 has recently been identified as a large serine-rich repeat protein, designated Hsa (Takahashi et al., 2002a). Moreover, surface proteins that are antigenically related to Hsa occur on other viridans-group streptococci that bind sialic-acid-containing receptors, including S. sanguis 10556 (Takahashi et al., 1997). Other lectin-like adhesins that bind terminal Galβ1-3GalNAc of asialo O-linked glycoconjugates, including MG2 (Prakobphol et al., 1999) and the heavy chain of IgA1 (Ruhl et al., 1996), are associated with A. naeslundii type 2 fimbriae. In addition, A. naeslundii type 1 fimbriae (Gibbons et al., 1988; Clark et al., 1989) and comparable adhesins of oral streptococci (Hsu et al., 1994) bind peptide motifs of proline-rich proteins (PRPs) (Gibbons et al., 1991; Li et al., 1999), thereby contributing to the attachment of these bacteria to SHA.
While the binding of S. sanguis, S. gordonii, and A. naeslundii to specific salivary components including MG2 and PRP-1 is well-established, the extent to which these bacteria bind other salivary proteins and glycoproteins is unclear. Indeed, certain radiolabeled streptococcal strains recognized several different salivary components on nitrocellulose transfers of SDS-PAGE-separated parotid and submandibular-sublingual (SM-SL) saliva (Murray et al., 1992). In the present study, blots of parotid and SM-SL saliva were probed with strains of actinomyces and streptococci that differ in their attachment to purified MG2 and PRPs (Table), associating the corresponding adhesins with complementary salivary receptors.
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MATERIALS & METHODS
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Saliva
Following a clinical protocol that was reviewed and approved by the NIDCR Institutional Review Board, parotid saliva was collected with Lashley cups (Stone Machine Company, Colton, CA, USA) after stimulation of the dorso-lateral surface of the tongue with a 2% citric acid solution. SM-SL saliva was collected by suction after isolation of the sublingual area with cotton rolls. Samples were collected on ice and stored at –20° C. The results presented were those obtained with saliva from a blood group O adult male. Comparable results (not shown) were obtained with saliva from a second donor. Protein concentrations of saliva samples were determined with use of the bicinchoninic acid (BCA) Protein Assay Reagent (Pierce, Rockford, IL, USA) with bovine serum albumin as the standard. Purified MG1 and MG2 and proline-rich glycoprotein (PRG) were obtained from M.J. Levine (Department of Oral Biology, SUNY, Buffalo, NY) and PRP-1 from D.I. Hay (Forsyth Institute, Boston, MA). Purified salivary -amylase was obtained commercially (Sigma-Aldrich, St. Louis, MO, USA).
SDS-PAGE, Transfer and Detection of Salivary Components
Salivary proteins (0.75 µg per lane) were denatured under reducing conditions, separated by SDS-PAGE with the use of 8–16% gradient gels (Novex, San Diego, CA, USA), and visualized by means of an ammoniacal silver stain kit (Daiichi Silver Stain-II, Integrated Separation Systems, Natick, MA, USA). SDS-PAGE-separated salivary proteins and glycoproteins (20 µg per lane) were also transferred to nitrocellulose and chemically labeled as previously described (Ruhl et al., 1996), by means of a DIG Protein Detection Kit (Boehringer Mannheim, Mannheim, Germany) or a modification of the hydrazide method, performed following selective oxidation of sialic acid or additional sugars in the presence of 1 mM or 10 mM sodium meta-periodate, respectively.
Lectin Blotting and Bacterial Overlay
The lectin and bacterial overlay techniques were performed as previously described (Ruhl et al., 2000) with blots that remained untreated or were treated with 0.1 U/mL sialidase (Clostridium perfringens Type X, Sigma-Aldrich). The biotinylated lectins (EY Laboratories, San Mateo, CA, USA) used as probes were: Limax flavus agglutinin (LFA), peanut agglutinin (PNA), or Lotus tetragonolobus agglutinin (LTA) at 5 µg/mL, or Canavalia ensiformis agglutinin (ConA) at 50 µg/mL.
The bacterial strains used as probes were: Actinomyces naeslundii strains T14V, 5519, 5951, and 147 (Cisar et al., 1988); A. naeslundii strains WVU45 (ATCC 12104) and WVU45M (Cisar et al., 1984); Streptococcus gordonii strains DL1 (Challis), M5, and ATCC10558; S. sanguis ATCC10556 (Hsu et al., 1994); and S. gordonii D102 (Takahashi et al., 1997). All bacteria were grown in a complex medium (Hsu et al., 1994) and labeled with sulfosuccinimidyl 6-(biotinamido) hexanoate (NHS-LC-biotin) (Pierce) as previously described (Ruhl et al., 2000). Blots were incubated overnight at 4°C with biotinylated bacteria to allow binding to occur, washed for removal of unbound bacteria, incubated with avidin-D-alkaline phospatase, washed again, and developed.
The assay for binding of salivary -amylase to bacteria has been described (Kilian and Nyvad, 1990).
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RESULTS
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Detection of Salivary Proteins and Glycoproteins
Chemical labeling revealed a wide range of transferred proteins and glycoproteins from samples of parotid and SM-SL saliva (Fig. 1A ). Purified MG1, MG2, PRG, and salivary -amylase were also readily detected but not PRP-1, which is non-glycosylated and has a relatively low content of free amino groups (Oppenheim et al., 1971). The distribution of salivary glycoproteins was further established by lectin blotting with probes for 2-3-linked sialic acid (LFA), terminal Galβ1-3GalNAc (PNA), L-fucose (LTA), and mannose in N-linked oligosaccharides (ConA) (Fig. 1B).
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Figure 1. Detection of salivary proteins and glycoproteins following separation of parotid (P) and SM-SL (S) saliva by SDS-PAGE. (A) Gels were silver-stained or transferred to nitrocellulose prior to the labeling of amino and sulfhydryl groups. Glycosylated proteins were labeled and detected on blots following oxidation of sialic acids with 1 mM sodium periodate or total carbohydrate with 10 mM sodium periodate (IO4–). (B) Individual blots were overlaid with biotinylated lectins, and bound lectin was detected with avidin-D alkaline phosphatase. The lectin probes used were LFA for terminal sialic acid, PNA for terminal Galβ1-3GalNAc, LTA for L-fucose, and ConA for glucose and mannose. Blots remained untreated (UT) or were sialidase-treated (SIAL) prior to incubation with lectins. The locations of purified MG1, MG2, PRG, -amylase (AMY), and PRP-1 are indicated.
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Fimbriae-specific Recognition of Salivary Proteins and Glycoproteins by A. naeslundii
The expected binding of A. naeslundii wild-type and fimbriae-deficient mutant strains to PRP and Gal/GalNAc-containing receptors (Table) was evident from the adhesion of biotinylated bacteria to different purified salivary components spotted on nitrocellulose (Fig. 2A). In these experiments, type 1 fimbriae-mediated adhesion was noted to as little as 1 ng immobilized PRP-1 or PRG, whereas type 2 fimbriae-mediated adhesion required a minimum of 100 ng MG2 or asialo-MG2 (results not shown). These interactions were abolished in the presence of EGTA, indicating the Ca++ dependency of type 1 and type 2 fimbriae-mediated binding.
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Figure 2. Adhesion of biotinylated A. naeslundii parent and fimbriae-deficient mutant strains to: (A) nitrocellulose membranes spotted with 10 ng purified PRP-1 or PRG and 1 µg MG2 or asialo-MG2; or (B) blots of parotid (P) and SM-SL (S) secretions separated by SDS-PAGE. The presence or absence of type 1 and type 2 fimbriae on each strain is indicated in parentheses. Adherent bacteria were detected with avidin-D alkaline phosphatase. Adhesion assays were also performed in the presence of 2 mM EGTA where indicated. Blots remained untreated (UT) or were sialidase-treated (SIAL) prior to the addition of bacteria.
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Wild-type A. naeslundii T14V bound many parotid and SM-SL salivary components transferred to nitrocellulose, almost all of which were recognized by strain 5519, which possesses only type 1 fimbriae (Fig. 2B ). In contrast, strains 5951 and WVU45, which possess only type 2 fimbriae, recognized MG2 and a component that migrated above the 50-kDa marker, in the region of the O-glycosylated IgA1 heavy chain (Ruhl et al., 1996). Significantly, strains 147 and WVU45M, which lack fimbriae, failed to bind any transferred salivary component.
Specific Recognition of Salivary Receptors by S. sanguis and S. gordonii
The PRP- and sialic-acid-binding activities of 4 S. gordonii or S. sanguis strains (Table) were closely correlated with adhesion to different populations of parotid and SM-SL salivary components. S. gordonii DL1, which bound to purified PRPs and MG2 but not asialo-MG2 on dot blots (Fig. 3A), recognized many transferred parotid and SM-SL salivary components (Fig. 3B). Attachment to certain SM-SL components was abolished by pre-incubation of an identical blot with sialidase. These sialidase-sensitive receptors were not recognized on untreated blots by mutant strain D102 or heterologous strain M5, which lack sialic-acid-binding adhesins (Table, Fig. 3A). However, strains D102 and M5 did bind to purified PRPs (Fig. 3A) and recognized the same population of parotid salivary components as strain DL1 (Fig. 3B). These interactions were greatly reduced in the presence of EGTA, suggesting a requirement for Ca++. S. sanguis 10556, which recognized the sialic acid termini of MG2 but not purified PRPs (Fig. 3A), failed to bind any parotid salivary component (Fig. 3B) but bound MG2 in SM-SL saliva. S. gordonii 10558, which lacks PRP- and sialic-acid-binding activities (Fig. 3A), failed to bind any transferred parotid or SM-SL salivary component (Fig. 3B).
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Figure 3. Adhesion of biotinylated S. gordonii DL1, homologous mutant strain D102, S. gordonii M5, S. sanguis 10556, or S. gordonii 10558 to: (A) nitrocellulose membranes spotted with 10 ng purified PRP-1 or PRG and 1 µg MG2 or asialo-MG2; or (B) blots of parotid (P) and SM-SL (S) secretions separated by SDS-PAGE. Adherent bacteria were detected with avidin-D alkaline phosphatase. Adhesion assays were also performed in the presence of 2 mM EGTA where indicated. Blots remained untreated (UT) or were sialidase-treated (SIAL) prior to the addition of bacteria.
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Strains of S. gordonii did not attach to salivary -amylase on blots of parotid or SM-SL saliva, nor did they bind purified salivary -amylase following SDS-PAGE and transfer to nitrocellulose. These bacteria also failed to interact with native -amylase spotted directly on nitrocellulose. However, binding of the native soluble enzyme to S. gordonii DL1, M5, and 10558, but not S. sanguis 10556, was readily demonstrated (data not shown).
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DISCUSSION
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The present results of bacteria overlay experiments suggest that specific adhesins on representative A. naeslundii, S. gordonii, and S. sanguis strains recognize distinct populations of salivary receptors. Thus, bacterial strains that bound the sialo- or asialo-termini of MG2, but not purified PRPs (i.e., A. naeslundii strains 5951 and WVU45 and S. sanguis 10556), recognized only a few SM-SL but no parotid salivary components, while strains that bound purified PRPs but not MG2 (i.e., A. naeslundii 5519 and S. gordonii strains D102 and M5) recognized many additional components from both SM-SL and parotid saliva. Moreover, strains that bound purified MG2 and PRPs (i.e., S. gordonii DL1 and A. naeslundii T14V) recognized all of the above-mentioned SM-SL and parotid salivary receptors, while others that lacked these specific activities (A. naeslundii strains 147 and WVU45M and S. gordonii 10558) failed to bind any immobilized salivary component. Thus, all interactions observed could be attributed to the known adhesive properties of these bacteria.
The involvement of PRP-binding adhesins in bacterial colonization of the tooth surface is consistent with the established presence of PRPs in the acquired pellicle (Lendenmann et al., 2000). In contrast, MG2, the most prominent salivary receptor for the lectin-like adhesins examined, has not been identified as a constituent of salivary pellicles formed either in vitro or in vivo (Lendenmann et al., 2000). Thus, other O-glycosylated salivary components may function as receptors for the sialidase-sensitive interaction of S. sanguis 10556 with SHA (Hsu et al., 1994). Similarly, A. naeslundii type 2 fimbriae-mediated recognition of adsorbed MG2 or other glycoproteins plays little role in adhesion of this species to SHA, which depends primarily on type 1 fimbriae-mediated binding of adsorbed PRPs (Cisar et al., 1988). However, the Gal/GalNAc-binding type 2 fimbriae of A. naeslundii as well as the GalNAc-binding adhesins present on each S. gordonii and S. sanguis strain included in the present investigation (Table) do interact with specific receptor polysaccharides present on other streptococci, such as strains of S. oralis (Cisar et al., 1997), favoring a primary role for these carbohydrate-binding adhesins in biofilm development (Palmer et al., 2003).
The denaturing effects of SDS-PAGE on the binding activities of certain salivary components may well limit the interactions detected by the bacteria overlay technique. For example, while the binding of native salivary agglutinin to S. gordonii M5 is well-established (Demuth et al., 1990), this strain did not interact with any transferred salivary component that migrated between MG1 and MG2 (Fig. 1A) in the region expected for gp-340 (Prakobphol et al., 2000), the major constituent of salivary agglutinin (Fig. 3B). The binding of salivary -amylase to S. gordonii is another interaction that was not detected by the bacteria overlay technique. Thus, strains of S. gordonii bound soluble -amylase as expected (Scannapieco et al., 1989; Kilian and Nyvad, 1990), but failed to bind this protein on blots of parotid or SM-SL saliva. These bacteria also failed to bind the native protein spotted on nitrocellulose, a finding that is consistent with the previously reported failure of S. gordonii HG 222 to bind -amylase-coated microtiter wells (Ligtenberg et al., 1992). Bacterial adhesion to -amylase-coated hydroxyapatite has been observed, however (Scannapieco et al., 1995), and appears to be mediated by a specific -amylase-binding protein on S. gordonii (Rogers et al., 2001). In addition, this protein mediates the binding of soluble -amylase to S. gordonii, an interaction that promotes the utilization of starch by this species (Rogers et al., 2001). Thus, the primary ecological role of the -amylase-binding protein may involve binding of the soluble salivary component.
A significant property of oral microbial adhesins is their ability to recognize surface-associated receptors in the presence of soluble receptor molecules that could act competitively to inhibit adhesion. Interestingly, strains of S. gordonii and A. naeslundii that recognized many immobilized parotid and SM-SL salivary components in the present study (Figs. 2, 3) failed to bind the corresponding radiolabeled soluble components in a previous study (Scannapieco et al., 1989). The latter results are consistent with our own unpublished observations. Adhesion of bacteria to adsorbed salivary components and their failure to bind the same molecules in solution can be explained in either of two ways, one based on the specificity and the other on the avidity of bacterial adhesin binding. The specificity of A. naeslundii and S. gordonii for surface-associated PRP-1 may depend on recognition of hidden structural features, referred to as "cryptitopes", which become exposed by a conformational change associated with adsorption of the protein to a surface (Gibbons, 1989). Alternatively, selective recognition of surface-associated over soluble glycoconjugate receptors has been explained by the increased avidity associated with multivalent binding, which magnifies the strength of many low-affinity interactions between adhesin binding sites on the bacterial surface and complementary receptors displayed on an opposing surface (Cisar, 1986). Further studies are needed for clearer definition of the specificities, affinities, and the distribution of different adhesins on bacteria that initiate colonization of the tooth surface. The insights gained may have broad application in the development of new approaches to prevent and control diseases associated with microbial colonization of host mucosal surfaces, both within and outside of the oral environment.
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ACKNOWLEDGMENTS
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We thank Philip C. Fox for his help in collecting ductal saliva, Michael J. Levine and Donald I. Hay for providing purified salivary components, and Jacob Donkersloot, Jamie Foster, and Paul Kolenbrander for their helpful reviews of the manuscript.
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FOOTNOTES
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1 present address, Department of Operative Dentistry and Periodontology, Dental School, University of Regensburg, 93042 Regensburg, Germany; 
2 present address, Building 45, Room 4AN-12B, NIH, Bethesda, MD 20892;
Received for publication May 13, 2003.
Revision received April 7, 2004.
Accepted for publication April 19, 2004.
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Journal of Dental Research, Vol. 83, No. 6,
505-510 (2004)
DOI: 10.1177/154405910408300614
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Journal of Dental Research,
January 1, 2005;
84(1):
29 - 34.
[Abstract]
[Full Text]
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ABSTRACT
INTRODUCTION