IAI FigSearch
Home Help [Feedback] [For Subscribers] [Archive] [Search] [Contents]
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Agnani, G.
Right arrow Articles by Bonnaure-Mallet, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Agnani, G.
Right arrow Articles by Bonnaure-Mallet, M.

 Previous Article  |  Next Article 

Infection and Immunity, February 2003, p. 991-996, Vol. 71, No. 2
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.2.991-996.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Epithelial Cell Surface Sites Involved in the Polyvalent Adherence of Porphyromonas gingivalis: a Convincing Role for Neuraminic Acid and Glucuronic Acid

G. Agnani, S. Tricot-Doleux, S. Houalet, and M. Bonnaure-Mallet*

Equipe de Biologie Buccale, UPRES-EA 1256, 35000 Rennes, France

Received 8 May 2002/ Returned for modification 3 July 2002/ Accepted 7 November 2002


   ABSTRACT
Top
 Abstract
Text
 References
 
We investigated the target structures of the epithelial cells responsible for the attachment of Porphyromonas gingivalis by immunocytofluorimetry, enzyme-linked immunosorbent assay, and confocal microscopy. Integrins (ß1, ß3, and {alpha}V) and E-cadherin played no significant role. Carbohydrates (such as {alpha}-D-methylglucoside, L-fucose, D- and L-mannose, N-acetylglucosamine, and N-acetylgalactosamine) had little inhibitory effect on bacterial binding. Enzymatic treatments of the epithelial membranes and sugar competition studies showed that N-acetylneuraminic acid and glucuronic acid were involved in binding.


   TEXT
Top
 Abstract
 Text
References
 
Porphyromonas gingivalis plays an important role in the initiation and progression of periodontal disease. It produces several adherence factors that contribute to bacterial virulence (15). P. gingivalis or P. gingivalis components have been shown to bind to collagen, fibronectin, laminin, vitronectin, and cytokeratin (13, 18, 25), but the ability of the bacteria to bind to glycoaminoglycans has been poorly studied. It has been reported that glycoaminoglycan-binding proteins may mediate the adherence of bacteria to eukaryotic cells (28), making it possible for the bacteria to initiate an infection. The goal of the study was to investigate the potential receptors in mediating the attachment of whole P. gingivalis to oral epithelial cells.

Bacterial cultures and preparation of bacterial cell surface antigens. P. gingivalis (ATCC 33277) was maintained on blood agar plates and grown in Todd-Hewitt broth supplemented with hemin (10 µg/ml) and vitamin K1 (1 µg/ml) for 18 h to the exponential phase in an anaerobic chamber at 37°C (1). Bacterial concentrations were determined by measuring the absorbance at 660 nm. For some experiments, the bacteria were labeled with 0.04% fluorescein isothiocyanate (FITC) in phosphate-buffered saline (PBS) for 30 min in the dark at room temperature.

Bacterial antigens were prepared by a mechanical attrition procedure by using sterile glass beads (glass bead extracts [GBE]) (4, 20). Antisera against the surface soluble antigens of P. gingivalis were raised by subcutaneous injection of young rabbits (<2 kg) with 2 mg of proteins every 3 weeks for 3 months.

KB cell cultures and cell membrane preparations. KB cells (ATCC CCL-17) were grown to confluency in RPMI 1640 medium (BioWhittaker) supplemented with 10% fetal calf serum, 2 mM L-glutamine, and antibiotics (penicillin [100 IU/ml] and streptomycin [100 µg/ml]).

The membrane extract preparation procedure was performed at 4°C. Briefly, the cells were detached by using 0.02% EDTA, resuspended in 10 mM Tris-HCl (pH 7.6) containing 0.5 mM MgCl2 for 10 min, and then disrupted by using a Dounce homogenizer. NaCl was added to a final concentration of 0.15 M, and the cell suspension was centrifuged at 260 x g for 5 min. A protease inhibitor mixture containing 10 µg of aprotinin/ml, 0.5 µg of leupeptin/ml, 1 mM 4-(2-aminoethyl) benzene sulfonylfluoride (AESF), 1 mM EDTA, and 1.8 mg of iodoacetamide/ml was added to the supernatant. The membrane extracts were pelleted at 150,000 x g for 45 min and solubilized in 50 mM Tris-HCl (pH 7.6) containing 300 mM NaCl, 5 mM MgCl2, and 1% Nonidet P-40. After solubilization, the extracts were centrifuged at 10,000 x g for 15 min, and the supernatant were used as a source of KB cell membrane antigens. This soluble material was used to raise polyclonal antisera against the surface antigens of epithelial cells by subcutaneous injection of young rabbits (<2 kg) with 2 mg of proteins every 3 weeks for 3 months.

ELISA test. Some experiments were performed to determine the optimal conditions for bacterial binding to the KB cell membrane extracts. Cell membrane extracts in 50 mM Na2CO3-NaHCO3 buffer (pH 9.6) were incubated in 96-well microtiter plates (0.5 µg/100 µl/well) overnight at 4°C. The wells were washed three times with PBS containing 0.1% bovine serum albumin (BSA) and 0.05% Tween 20 (PBT). After a saturation step with PBS-3% BSA (200 µl/well), GBE suspensions (100 µl in PBS-0.1% BSA) ranging in concentration from 0.156 to 20 µg/ml were added to the wells, and the plates were incubated for 1 h at room temperature. The wells were then rinsed three times with PBT, and anti-P. gingivalis antiserum (100 µl; 1:1,000 dilution in PBT) was allowed to bind to the plates for 1 h at room temperature. After a washing step with PBT, the plates were incubated for 1 h at room temperature with horseradish peroxidase-conjugated goat anti-rabbit immunoglobulin G (100 µl, 1:1,000 dilution in PBT) and then rinsed again. The substrate solution containing 0.4 mg o-phenyldiamine (Dako)/ml in 0.05 M phosphate-citrate buffer (pH 5.0)-0.012% H2O2 was added, and the A492 values were determined after the reaction had been quenched with 3 N HCl. Duplicate assays were performed for each GBE concentration. When the mean A492 values were plotted against the bacterial membrane concentrations, the linear slopes of the exponential curves fell between 0.625 and 10 µg/ml for GBE. The amounts of KB surface antigens attached to the plates were assayed by enzyme-linked immunosorbent assay (ELISA). This assay differed from the one described above by the omission of GBE and by the use of the rabbit anti-epithelial cell membrane antisera (1:1,000 dilution in PBT) instead of anti-P. gingivalis antibodies. There were no significant differences in levels of detectable KB cells antigens with or without enzyme pretreatment.

Effects of heparinase, chondroitinase, neuraminidase, and trypsin on GBE binding to KB membrane extracts. Heparinase type III (from Flavobacterium heparinum), chondroitinase type ABC (from Proteus vulgaris), trypsin type I (from bovine pancreas), and neuraminidase type V (from Clostridium perfringens) were purchased from Sigma.

KB membrane extracts (20 µg/250 µl) were treated for 1 h at 37°C with heparinase III (2.5 to 10 U/ml) in PBS, chondroitinase ABC (2.5 to 10 U/ml) in PBS, trypsin (5 to 120 µg/ml) in PBS, or neuraminidase (2.5 to 10 U/ml) in 50 mM acetate sodium (pH 5.5) containing 5 mM CaCl2 and 0.1% BSA. ELISA buffer (3.75 ml) was then added to the reaction mixtures in order to assess the GBE-binding capacity of the treated cell membrane extracts.

Treatments with heparinase III (2.5 to 10 U/ml) or chondroitinase ABC (2.5 to 10 U/ml) had no negative effect on bacterial binding to the KB cell membrane antigens (Fig. 1). In fact, the heparinase treatment (10 U/ml) caused a significant 32% increase in GBE binding (P < 0.001), which may be due to conformational changes to epithelial antigens that unmask the receptor sites commonly referred to as cryptitopes. Treatment with 10 U of neuraminidase/ml (Fig. 1) or with 30 µg of (~300 U/ml) trypsin/ml (data not shown) caused a 80% decrease in the GBE-KB cell membrane interaction (P < 0.001) compared to the results obtained in the absence of enzyme treatment. These results indicate that the GBE can bind to KB cell membrane antigens through close interactions between proteins and sugars.



View larger version (13K):
[in this window]
[in a new window]
  		FIG. 1. Effect of various enzymes on GBE binding to KB membrane extracts. The KB membrane extracts were pretreated for 1 h at 37°C with heparinase III (x), chondroitinase ABC ({triangleup}), neuraminidase ({blacksquare}), and then allowed to bind to the wells of 96-well microtiter plates (0.5 µg/well). The plates were incubated for 1 h at room temperature and binding was assessed by ELISA as described above. The results are expressed as the means of duplicate tests with three GBE concentrations (1.25, 2.5, and 5 µg/ml).

 
Role of epithelial glycoprotein adhesins in the P. gingivalis-KB cell interaction. Many studies have demonstrated the involvement of eukaryotic cell adherence molecules (CAM) in bacterial binding. Isberg et al. (9) have shown that Yersinia species have a high binding affinity for ß1 integrin receptors on the epithelial cell surface, whereas Mengaud et al. (16) have shown that the binding of Listeria monocytogenes to E-cadherin epithelial cell receptors results in phagocytosis of the bacteria. ß3 integrin receptors are also involved in microbial binding (3, 27). More specifically, Nagakawa et al. (17) have found that anti-{alpha}5 ß1 integrin antibodies inhibited the adhesion of fimbriae conjugated to microspheres to epithelial cells.

The role of cadherins and the ß1, ß3, and {alpha}V integrins in epithelial cell recognition of P. gingivalis antigenic structures was assessed by flow cytofluorimetry (FACScan; Becton Dickinson). Suspended KB cells (2 x 105) were fixed in 1 ml of 1% paraformaldehyde then blocked for 1 h in PBS-1% BSA. After centrifugation (260 x g for 5 min), they were incubated with 5 µg of anti-pan cadherin (Sigma) or of anti-ß1, -ß3, or -{alpha}V integrin polyclonal antibodies (Chemicon)/ml in PBS-0.1% BSA for 45 min at 4°C. The cells were then rinsed three times with PBS and incubated in PBS-0.1% BSA containing either FITC-conjugated anti-rabbit antibody (diluted 1:20; positive control) for 45 min at 4°C or FITC-labeled bacteria for 30 min at room temperature. The bacteria were used at an infection multiplicity of 100 (i.e., 100 bacteria per epithelial cell). Bacterial adherence to epithelial cells was optimum at this bacterium/epithelial cell ratio (8). Positive controls for inhibition of P. gingivalis binding to KB cells were carried out by pretreatment of the KB cells or the bacteria with the respective immune sera diluted 1:5. The inhibition of fluorescence intensity was of 33 and 35%, respectively (Fig. 2). Negative controls were carried out with nonimmune serum. No change in the intensity of the fluorescence of the KB cells was observed compared to the negative controls, indicating that none of the anti-CAM antibodies had an inhibitory effect on the adherence of P. gingivalis to the KB cells. Cadherins and the ß1, ß3 and {alpha}V integrins thus do not play an important role in mediating P. gingivalis binding to epithelial cells. However, due to the complexity of the receptor-ligand interactions involved in the adherence of P. gingivalis to KB epithelial cells, a direct role for integrin or cadherin in bacterial internalization cannot be ruled out. For instance, it is well known that integrin ligand uptake is regulated from inside the cell (12, 14, 23). Recent works underlined the importance of ß1 integrin on epithelial cell invasion by P. gingivalis (30). Since we used cell membranes as well as whole cells fixed with paraformaldehyde, only the binding phenomenon was studied here.



View larger version (28K):
[in this window]
[in a new window]
  		FIG. 2. Flow cytometry histograms showing inhibition of adherence of P. gingivalis to KB cells. FITC-labeled P. gingivalis (100 bacteria per cell) were allowed to bind to suspended KB cells (2 x 105). (A) The eukaryotic cells were preincubated for 45 min at 4°C with anti-keratinocyte immunserum (red line) or nonimmune serum (blue line) at 1:5 dilution. (B) The FITC-labeled P. gingivalis were preincubated for 1 h at room temperature with anti-P. gingivalis antiserum (red line) or nonimmune serum (blue line) at 1:5 dilution. In both figures, cell autofluorescence is visualized in green.

 
Identification of KB membrane sugars involved in the GBE-KB cell interaction. Sugars (N-acetylglucosamine, N-acetylgalactosamine, L-mannose, D-mannose, L-fucose, and {alpha}-D-methylglucoside) were purchased from Sigma. Inhibition assays of the GBE-KB cell interaction were performed with GBE (1.25, 2.5, and 5 µg/ml in PBS-0.1% BSA) preincubated for 1 h at room temperature with sugars at various concentrations (from 0 to 200 mM).

Alpha-D-methylglucoside (200 mM) did not affect significantly the binding of GBE to KB cell membrane antigens. At a concentration of 100 mM, other sugars caused no more than an average 26% decrease in GBE binding compared to the basal level. We obtained a binding percentage of 74.0 ± 16.1, 87.5 ± 1.3, and 84.1 ± 5.5 with L-mannose, D-mannose and L-fucose (P < 0.05), respectively, and 81.1 ± 7.0 and 86.7 ± 8.8 with N-acetylglucosamine and N-acetylgalactosamine, respectively (P < 0.001). At a concentration of 200 mM, N-acetylglucosamine and D-mannose slightly decreased GBE binding of 2 to 5% compared to the percentage obtained with 100 mM (P < 0.01). A 31% inhibition of the GBE-epithelial cell membrane antigen interaction was obtained by using 200 mM L-mannose (P < 0.001). The slight inhibitory effect of simple sugars on P. gingivalis binding can be explained by the low affinity of multiple bacterial ligands at individual sites. There may also be more than one P. gingivalis recognition site on the KB cell surface.

A number of bacteria have been shown to interact with mannose-containing domains of phagocytes (2, 11, 21, 26). It has also been reported that type I Escherichia coli fimbriae mediate bacterial binding to mannose residues (5, 22). Several studies have shown that P. gingivalis fimbriae can attach to a wide range of extracellular matrix molecules (18, 24) and cell receptors (10, 19, 25, 29). The competition between sugars (including mannose) and sugar-containing epithelial cell sites for fimbriae would shed some light on the mechanisms involved in host cell-fimbria interactions.

KB cell membrane extracts were also preincubated with concanavalin A, PNA, ECA, SBA, RCA, and UEA lectins (Sigma), which possess the following glycan specificities: {alpha}-Man, {alpha}-Glc; ß-Gal (1->3)GalNAc; ß-Gal(1->4)GlcNAc; GalNAc; ß-Gal; and {alpha}-L-Fuc, respectively. The effect of lectins on GBE binding to KB cell membrane extracts was assessed by adding lectins (6.25 to 200 µg/ml in PBS-0.1% BSA) to the wells after the saturation step. The plates were incubated for 1 h at room temperature and then rinsed three times with PBT before being incubated with GBE suspensions (at 2.5 and 5 µg/ml). None of the lectins interfered with the epithelial cell binding sites (data not shown).

GBE preincubated with different concentrations of N-acetylneuraminate (sodium salt, pH 7) displayed a dose-dependent inhibition of binding to KB membrane extracts (Fig. 3). This result confirmed that sialic residues are involved in the binding process. Interestingly, 200 mM glucuronate (sodium salt, pH 7) also inhibited binding by more than 80% (P < 0.0001) (Fig. 3). Whole-bacteria binding to KB cells was assessed by confocal microscopy by using the protocol of Houalet-Jeanne et al. (7). KB cells were first detached with EDTA 0.02%, resuspended in PBS and then incubated with FITC-labeled P. gingivalis, in the presence or absence of sugars, at an infection multiplicity of 100 for 30 min at room temperature. The addition of 25 mM glucuronate (Fig. 4) or 100 mM neuraminate (data not shown) caused a significant decrease in ATCC 33277 P. gingivalis adherence to KB cells compared to the controls.



View larger version (12K):
[in this window]
[in a new window]
  		FIG. 3. Inhibition of GBE binding to KB membrane extracts by N-acetylneuraminic acid or glucuronic acid (ELISA). GBE were incubated for 1 h at 37°C with N-acetylneuraminic acid ({blacksquare}) or with glucuronic acid ({square}) at the indicated concentrations before being added to wells coated with KB membrane extracts. The results are expressed as the means of duplicate tests with two GBE concentrations (1.25 and 2.5 µg/ml).

 


View larger version (63K):
[in this window]
[in a new window]
  		FIG. 4. Confocal photomicrographs. KB cells were incubated with FITC-labeled P. gingivalis at an infection multiplicity of 100 for 30 min at room temperature, in the presence of 25 mM glucuronate (A) or not (B).

 
Sialic residues and glucuronic acid thus played an important role in P. gingivalis binding to epithelial cells. N-Acetylneuraminic acid and glucuronic acid are both highly polar molecules found in proteoglycans. Neuraminic acid is a structural component of hyaluronan, which has been also shown to mediate Treponema denticola binding to periodontal tissue (6).

The aim of our study was to identify the main eukaryotic structures involved in the P. gingivalis adherence process. We have demonstrated the predominant role played by complex sugars (N-acetylneuraminic acid and glucuronic acid) in bacterial binding to oral epithelial cells. Their involvement in adherence, and thus the subsequent stages of the infectious process, indicates that they may be plausible targets for new anti-infective agents.


   ACKNOWLEDGMENTS
 
We thank Roselyne Primault for technical assistance and Gene Bourgeau and Céline Allaire for editorial assistance.

This study was supported in part by the Institut Francais de Recherche en Odontologie.


   FOOTNOTES
 
* Corresponding author. Mailing address: Université de Rennes I, 2 Place Pasteur, 35000 Rennes, France. Phone: 33-2-23-23-43-58. Fax: 33-2-23-23-43-04. E-mail: martine.bonnaure{at}univ-rennes1.fr. Back

Editor: V. J. DiRita


   REFERENCES
Top
 Abstract
 Text
 References
 
1. Agnani, G., S. Tricot-Doleux, L. Du, and M. Bonnaure-Mallet. 2000. Adherence of Porphyromonas gingivalis to gingival epithelial cells: modulation of bacterial protein expression. Oral Microbiol. Immunol. 15:48-52.[CrossRef][Medline]
2. Brunetti, C. R., R. L. Burke, S. Kornfeld, W. Gregory, F. R. Masiarz, K. S. Dingwell, and D. C. Johnson. 1994. Herpes simplex virus glycoprotein D acquires mannose 6-phosphate residues and binds to mannose 6-phosphate receptors. J. Biol. Chem. 269:17067-17074.[Abstract/Free Full Text]
3. Coburn, J., L. Magoun, S. C. Bodary, and J. M. Leong. 1998. Integrins {alpha}vß3 and {alpha}5ß1 mediate attachment of lyme disease spirochetes to human cells. Infect. Immun. 66:1946-1952.[Abstract/Free Full Text]
4. Du, L., P. Pellen-Mussi, F. Chandad, C. Mouton, and M. Bonnaure-Mallet. 1997. Fimbriae and the hemagglutinating adhesin HA-Ag2 mediate adhesion of Porphyromonas gingivalis to epithelial cells. Infect. Immun. 65:3875-3881.[Abstract]
5. Firon, N., I. Ofek, and N. Sharon. 1982. Interaction of mannose-containing oligosaccharides with the fimbrial lectin of Escherichia coli. Biochem. Biophys. Res. Commun. 105:1426-1432.[CrossRef][Medline]
6. Haapasalo, M., P. Hannam, B. C. mc Bride, and V. J. Uitto. 1996. Hyaluronan, a possible ligand mediating Treponema denticola binding to periodontal tissue. Oral Microbiol. Immunol. 11:156-160.[Medline]
7. Houalet-Jeanne, S., P. Pellen-Mussi, S. Tricot-Doleux, J. Apiou, and M. Bonnaure-Mallet. 2001. Assessment of internalization and viability of Porphyromonas gingivalis in KB epithelial cells by confocal microscopy. Infect. Immun. 69:7146-7151.[Abstract/Free Full Text]
8. Huard-Delcourt, A., L. Du, P. Pellen-Mussi, S. Tricot-Doleux, and M. Bonnaure-Mallet. 1998. Adherence of Porphyromonas gingivalis to epithelial cells: analysis by flow cytometry. Eur. J. Oral. Sci. 106:938-944.[CrossRef][Medline]
9. Isberg, R. R., and J. M. Leong. 1990. Multiple ß1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861-871.[CrossRef][Medline]
10. Isogai, H., E. Isogai, F. Yoshimura, T. Suzuki, W. Kagota, and K. Takano. 1988. Specific inhibition of adherence of an oral strain of Bacteroides gingivalis 381 to epithelial cells by monoclonal antibodies against the bacterial fimbriae. Arch. Oral Biol. 33:479-485.[CrossRef][Medline]
11. Kitz, D. J., P. D. Stahl, and J. R. Little. 1992. The effect of a mannose binding protein on macrophage interactions with Candida albicans. Cell. Mol. Biol. 38:407-412.[Medline]
12. Kolanus, W., and B. Seed. 1997. Integrins and inside-out signal transduction: converging signals from PKC and PIP3. Curr. Opin. Cell Biol. 9:725-731.[CrossRef][Medline]
13. Kontani, M., H. Ono, H. Shibata, Y. Okamura, T. Tanaka, T. Fujiwara, S. Kimura, and S. Hamada. 1996. Cysteine protease of Porphyromonas gingivalis 381 enhances binding of fimbriae to cultured human fibroblasts and matrix proteins. Infect. Immun. 64:756-762.[Abstract]
14. Kumar, C. C. 1998. Signaling by integrin receptors. Oncogene 17:1365-1373.[CrossRef][Medline]
15. Lamont, R. J., and H. F. Jenkinson. 2000. Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol. Immunol. 15:341-349.[CrossRef][Medline]
16. Mengaud, J., H. Ohayon, P. Gounon, R. M. Mege, and P. Cossart. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923-932.[CrossRef][Medline]
17. Nakagawa, I., A. Amano, M. Kuboniwa, T. Nakamura, S. Kawabata, and S. Hamada. 2002. Functional differences among FimA variants of Porphyromonas gingivalis and their effects on adhesion to and invasion of human epithelial cells. Infect. Immun. 70:277-285.[Abstract/Free Full Text]
18. Nakamura, T., A. Amano, I. Nakagawa, and S. Hamada. 1999. Specific interactions betwen Porphyromonas gingivalis fimbriae and human extracellular matrix proteins. FEMS Microbiol. Lett. 175:267-272.[CrossRef][Medline]
19. Njoroge, T., R. J. Genco, H. T. Sojar, N. Hamada, and C. A. Genco. 1997. A role for fimbriae in Porphyromonas gingivalis invasion of oral epithelial cells. Infect. Immun. 65:1980-1984.[Abstract]
20. Parent, R., C. Mouton, L. Lamonde, and D. Bouchard. 1986. Human and animal serotypes of Bacteroides gingivalis defined by crossed immunoelectrophoresis. Infect. Immun. 51:909-918.[Abstract/Free Full Text]
21. Reading, P. C., J. L. Miller, and E. M. Anders. 2000. Involvement of the mannose receptor in infection of macrophages by influenza virus. J. Virol. 74:5190-5197.[Abstract/Free Full Text]
22. Schembri, M. A., H. Hasman, and P. Klemm. 2000. Expression and purification of the mannose recognition domain of the FimH adhesin. FEMS Microbiol. Lett. 188:147-151.[CrossRef][Medline]
23. Schwartz, M. A., M. D. Schaller, and M. H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11:549-599.[CrossRef][Medline]
24. Sojar, H. T., J. Y. Lee, and R. J. Genco. 1995. Fibronectin binding domain of P. gingivalis fimbriae. Biochem. Biophys. Res. Commun. 216:785-792.[CrossRef][Medline]
25. Sojar, H. T., A. Sharma, and R. J. Genco. 2002. Porphyromonas gingivalis fimbriae bind to cytokeratin of epithelial cells. Infect. Immun. 70:96-101.[Abstract/Free Full Text]
26. Stehle, S. E., R. A. Rogers, A. G. Harmsen, and R. A. Ezekowitz. 2000. A soluble mannose receptor immunoadhesin enhances phagocytosis of Pneumocystis carinii by human polymorphonuclear leukocytes in vitro. Scand. J. Immunol. 52:131-137.[CrossRef][Medline]
27. Stockbauer, K. E., L. Magoun, M. Liu, E. H. Burns, S. Gubba, S. Renish, X. Pan, S. C. Bodary, E. Baker, J. Coburn, J. M. Leong, and J. M. Musser. 1999. A natural variant of the cysteine protease virulence factor of group A streptococcus with an arginine-glycine-aspartic acid (RGD) motif preferentially binds human integrins {alpha}vß3 and {alpha}IIbß3. Proc. Natl. Acad Sci. USA 96:242-247.[Abstract/Free Full Text]
28. Wadstrom, T., and A. Ljungh. 1999. Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J. Med. Microbiol. 48:223-233.[Abstract]
29. Weinberg, A., C. M. Belton, Y. Park, and R. J. Lamont. 1997. Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 65:313-316.[Abstract]
30. Yilmaz, O., K. Watanabe, and R. J. Lamont. 2002. Involvement of integrins in fimbriae-mediated binding and invasion by Porphyromonas gingivalis. Cell Microbiol. 4:305-314.[CrossRef][Medline]

Infection and Immunity, February 2003, p. 991-996, Vol. 71, No. 2
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.2.991-996.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Agnani, G.
Right arrow Articles by Bonnaure-Mallet, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Agnani, G.
Right arrow Articles by Bonnaure-Mallet, M.

Home Help [Feedback] [For Subscribers] [Archive] [Search] [Contents]
J. Bacteriol. J. Virol. Eukaryot. Cell
Microbiol. Mol. Biol. Rev. Clin. Vaccine Immunol. All ASM Journals