2 Department of Oral Pathology, Faculty of Odontology, The Sahlgrenska Academy at Göteborg University, Box 450, SE 405 30 Göteborg, Sweden; 3 Department of Clinical Chemistry and Transfusion Medicine, The Sahlgrenska Academy at Göteborg University, SE 413 45 Göteborg, Sweden; and 4 Department of Endodontics and Oral Diagnostics, Faculty of Odontology, The Sahlgrenska Academy at Göteborg University, Box 450, SE 405 30 Göteborg, Sweden
Received on October 30, 2003; revised on February 19, 2004; accepted on March 4, 2004
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Abstract |
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Key words: adhesion / bacterial overlay / chromatogram binding assay / glycolipid / Porphyromonas gingivalis
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Introduction |
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It has been shown that a number of bacteria can bind to glycoconjugates on the cell surfaces (Kelm and Schauer, 1997; Mouricout, 1997
), for example, Streptococcus suis (Haataja et al., 1994
), Escherichia coli (Yang et al., 1994
), and Helicobacter pylori (Borén et al., 1993
). Which receptor(s) the adhesin of P. gingivalis exploit in the adhesion to epithelial cells has not been shown. Theories and studies based on various proteins and glycosylated proteins have been published, but none have yet been able to characterize the structure of the bacterial binding epitope. In vitro studies with glycoprotein from oral epithelium suggest the use of glycoconjugates as bacterial receptors (Agnani et al., 2003
). Adhesion to glycoproteins can occur either to the protein or the carbohydrate part of the molecule. A recently published study showed that the addition of soluble saccharides to the bacterial solution can abolish the binding of P. gingivalis to oral epithelial cells (Agnani et al., 2003
). This fact suggests that the carbohydrate moiety is somehow involved in the adhesion process. Previous studies have also shown that P. gingivalis can hydrolyze proteins and thereby expose previously hidden epitopes (i.e., cryptitopes) (Kontani et al., 1997
). This procedure might be adopted by the bacterium when adhering to carbohydrate epitopes on glycolipids.
Glycoproteins exist in different forms in the membranes of eukaryotic cells. A characteristic feature of glycoproteins is the dominating protein moiety of the molecule, compared to proteoglycans, which consist of a dominating carbohydrate part. Carbohydrates existing on glycoproteins can often also be found on glycolipids on the cell surface. The carbohydrate epitopes on glycolipids and glycoproteins are in many cases identical, but the core chains do vary (Oriol, 1995). When compared to glycoproteins, the core chains on glycolipids are generally shorter and less branched. They are also quite distinct from the core sequences of glycoproteins. The expression of carbohydrate chains can also vary between different animal species (Bäcker et al., 1997
; Björk et al., 1987
; Smith et al., 1975
; Umesaki et al., 1989
), between different organs (Bäcker et al., 1999
; Ulfvin et al., 1989), and also between different cells (Strokan et al., 1998a).
Based on these facts, the aim of the present study was to investigate whether the periodontal pathogen P. gingivalis can use glycolipids as receptors by screening a large array of glycolipid structures with a chromatogram binding assay.
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Results |
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Binding was also obtained to gangliotriaosylceramide and gangliotetraosylceramide, the pure reference glycolipid fractions used for studying binding analogy with other bacteria (Figure 7).
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Discussion |
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The fact that bacteria use short carbohydrate sequences as receptors is well known (Karlsson, 1995) and has been studied at different locations, such as in the human intestine (Borén et al., 1993
; Holgersson et al., 1991a
) and oral cavity (Strömberg and Borén, 1992
). The blood group of the individual (e.g., ABO and Lewis blood group systems) is of importance. In fact, in some cases the blood group has been shown to be a crucial factor for the bacterial capacity to adhere to the specific tissue. This is exemplified by the bacterium H. pylori, which binds to stomach mucosa in individuals expressing the Leb structure (a five-sugar-long carbohydrate) in the tissue (Borén et al., 1993
). Both neutral (nonacid) and acid carbohydrate chains are known to act as bacterial receptors (Ångström et al., 1998
; Borén et al., 1993
; Holgersson et al., 1991a
; Karlsson, 1995
; Miller-Podraza et al., 1996
; Teneberg et al., 2002
, 2004
). It is not known whether the binding of P. gingivalis to carbohydrates is dependent on the type of blood group or not.
We found that it was adequate to cultivate the bacteria for 3 days prior to the bacterial overlay assays. At this point P. gingivalis seems to express properties necessary for adhesion to glycolipid structures. The bacteria in the study were cultured on agar plates. Other glycolipid binding bacteria, like H. pylori, show the same binding pattern when cultured on agar as in broth (Teneberg et al., 2002). It is also known that the use of different coating solutions in the chromatogram binding assay can affect the reproducibility of binding (Teneberg et al., 2002
). The use of 2% bovine serum albumin (w/v) in phosphate buffered saline (PBS) with 0.1% Tween 20 (v/v) and 0.01% sodium azid (w/v) was found to be useful in our bacterial overlays.
The bacterial overlay assay showed binding of P. gingivalis to human nonacid and acid fractions and to pig nonacid fractions. Acid fractions of pig origin tested negative despite the close similarity of glycolipid expression in human and pig organs. Binding was found in the four-sugar region but not to longer sugar chains in the glycolipid fractions. The bacterial binding sites are presumably not located on the terminal sugars of the glycolipid carbohydrate chain but on the core chain. This is an important observation because previous studies have shown that P. gingivalis has the ability to enzymatically cleave proteins (Kontani et al., 1997) and thereby reveal cryptitopes of protein origin. Enzymatic cleavage might also be used by the bacterium on structures of carbohydrate origin, thus enabling adhesion of the bacterium to cell surfaces. If we expose P. gingivalis solely to carbohydrate epitopes that normally are expressed only in oral mucosa, there would in fact be a reduced chance of finding the actual binding epitopes used by the bacterium in vivo. The glycolipid expression in oral epithelium varies between different individuals because of, among other things, genetic conditions such as the type of blood group (Ravn and Dabelsteen, 2000
). Therefore, it is of great importance to use a variety of species (in this case human, pig, and sheep) to find structures of carbohydrate origin that are normally not exposed in human tissue. These structures can be exposed as cryptitopes, for example, as previously mentioned. Consideration must also be taken of the fact that it is difficult to purify glycolipids from human pocket epithelium because it is very hard to gain access to the large amount of tissue necessary for glycolipid purification. Studies on glycolipid expression in gingival tissue only consists of assays with monoclonal antibodies on surfaces of gingival epithelial cells (Mackenzie et al., 1989
). The glycolipids constitute only a small part of the total weight of the tissue which results in approximately only 20 mg total glycolipid fraction from 200 g tissue. Another important reason for using glycolipids from different species and different organs is that information can be determined about the possible influence and/or involvement on the binding of the bacterium to the ceramide part of the glycolipid chain. Studies with H. pylori have shown that the ceramide part is involved in the binding of this bacterium to glycolipids (Ångström et al., 1998
).
The blood group type of the organ that the glycolipid fraction originated from did not seem to be significant. The blood group epitopes are in most cases terminally expressed on precursor chains with four to five sugar residues. One can speculate whether the presence of a blood group epitope might inhibit bacterial binding to the carbohydrate. Instead, binding might occur to the core chain or the intermediate part of the carbohydrate chain depending on the 3D structure of the carbohydrate chain. A core chain similarity is indicated in the bacterial binding region in the non-acid glycolipid fractions from pig. In this region of the TLC plate the globo chain and its precursors are often found (Bäcker et al., 1998).
Binding of P. gingivalis to acid glycolipid fractions from organs of human origin was noticed in the upper part of the chromatogram. In this region of the TLC plates sulfatide fractions are usually found, which indicates that this may be a tentative structure for adhesion of this specific bacterium. Sulfatide fractions have also been included in our screening of glycolipid structures and positive binding was obtained (Figure 2, lane 5, 6 and 11; and Figure 3, lane 5), a result that supports our hypothesis. This has recently also been indicated in the case of glycoprotein binding of P. gingivalis (Agnani et al., 2003). In sulfatide glycolipid fractions the sugar chain shows a one- or two-sugar residue length with terminal sulfate group (SO3). The core structure tentatively consists of a galactose connected to glucose before connecting to the polar ceramide chain.
Sugar chains consisting of one-, two-, three-, and four-sugar residues are used by P. gingivalis as receptor structures in nonacid fractions from pig organs. A comparison of the binding areas in this study, with earlier published structural characterization studies of the pig organs (Bäcker et al., 1998), indicated that the bacterial glycolipid receptor structure might be a so-called type 4 chain, that is, the globo chain and its core structures (Holgersson et al., 1992
). Considering the binding in the two-sugar region, it is not possible to distinguish between binding to lactosylceramide and/or to galabiosylceramide, because these glycolipids do not separate on the TLC plates due to similar polarities.
Our results also showed that P. gingivalis has the ability to adhere to gangliotriaosylceramide (GgO3) and gangliotetraosylceramide (GgO4). These purified reference glycolipid fractions were used to study analogy of binding patterns to other bacteria. Previous studies has shown that, among others, Actinobacillus pleuropneumoniae (Abul-Milh et al., 1999) and E. coli (Teneberg et al., 2004
) can bind to GgO3 and GgO4. The fact that P. gingivalis also can use these glycolipids as receptor structures shows that this bacterium has a similar binding pattern. What type of other pure glycolipid structures P. gingivalis recognizes will be fully described in our following study.
Our screening of a large library of glycolipid carbohydrate chains with TLC and bacterial overlay assay showed that P. gingivalis can bind to sugar residues on glycolipids. A screening of more than 120 different fractions by TLC where each fraction was tested at least three times is very time-consuming. Therefore, this screening will be followed in a forthcoming study by further purification of the glycolipid fractions with positive binding of the bacterium.
In this screening study we show for the first time that the periodontal pathogen P. gingivalis strain FDC381 can use glycolipid sugar chains as bacterial receptors. Both nonacid and acid glycolipids can be used by the bacterium and shorter carbohydrate chains are mainly preferred. We have also found that sulfated glycolipids probably are favored by the bacterium in acid glycolipid fractions. Glycolipids based on the globo chain with a core chain of lactosylceramide bound to the ceramide part, seem to be preferred in the nonacid glycolipid fractions.
The carbohydrate binding of the bacterium might act as a first step in the bacterial invasion process of the pocket epithelium, subsequently leading to periodontal damage in the tissue. A mapping of the receptor structures that P. gingivalis uses for adhesion and invasion of eukaryotic cells would increase the knowledge of the origin of periodontitis. This knowledge might in turn be used in new treatment strategies, for example receptor analogs, to inhibit bacterial binding and the production of vaccines and other antimicrobial therapies specifically directed against P. gingivalis. The future goal is to reduce the incidence, onset, and spread of periodontal disease.
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Materials and methods |
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Sample criteria
The aim of the experiments was to perform a screening of a wide range of glycolipid structures with TLC and bacterial overlay assay. In this way P. gingivalis is exposed to a large number of different carbohydrate structures, which enables detection of receptor structures that are used by the bacterium. Different types of organs with different blood groups were analyzed and compared for differences in binding patterns and/or to study special bacterial preferences for any particular blood group epitope. Several fractions from the same kind of organ, but from different organ donors, were used in the experiments as well as organs with different blood group subgroups. Glycolipid fractions of both acid and nonacid origin were used to see if, for example, sialic acid is necessary for adhesion. In the majority of the screening experiments, total glycolipid fractions were used.
Fractions used in TLC and bacterial overlay
The following section is a listing of all fractions that were used in the TLC and bacterial overlay assays. Any subgrouping, such as serological typing (e.g., A2), blood group Lewis (Le(ab)), and Secretor (Se) status, is shown in parentheses. Fractions named transplantation indicate organs that originate from a human transplantation donor.
Fractions of human origin
Total fractions originating from human organs of blood group A used for screening included acid and nonacid kidney (A2), nonacid transplantation kidney (A1), nonacid transplantation kidney (A1 Le(a+b)), nonacid transplantation kidney (A2 Le(a+b)), nonacid liver (A1B), nonacid liver (A1 Le(ab+)), nonacid liver (A1B Le(ab)), nonacid liver (A1 Le(a+b)), nonacid liver (A2B Le(ab+)), acid transplantation liver (A1), nonacid jejunum, nonacid ileum (A1), nonacid pancreas, acid plasma (A1 Le(ab)Se), acid plasma (A2 Le(ab+)), nonacid thrombocytes (A1), and nonacid thrombocytes (A2).
Total fractions originating from human organs of blood group B type used for screening included acid and nonacid kidney, nonacid transplantation kidney (Le(ab+)), acid intestine, acid and nonacid ureter (Le(ab+)), acid and nonacid artery (Le(ab+)), acid and nonacid vein (Le(ab+)), nonacid liver, nonacid liver (Le(ab+)), acid erythrocytes (Le(ab+)), and acid plasma (A1 Le(ab+)).
Total fractions originating from human organs of blood group AB type used for screening included nonacid liver (A1B) and nonacid transplantation kidney (AB Le(ab+)).
Total fractions originating from human organs of blood group O type used for screening included nonacid kidney, nonacid transplantation kidney (Le(ab+)), nonacid erythrocytes (Le(ab+)), and nonacid plasma (Le(ab+)).
Total fractions originating from human organs with pooled and/or mixed nonspecified blood group included acid kidney, acid and nonacid human liver, acid ureter, acid transplantation kidney, acid and nonacid colon, and acid small intestine.
HPLC-purified human fractions used in the screening included ganglioside fraction from colon, brain ganglioside fraction, pancreas ganglioside fraction, pancreas sulfatide fraction, ureter ganglioside fraction, transplantation kidney ganglioside fraction, sulfolipid fraction from ureter (residual stroma) blood group B, sulfolipid fraction from kidney blood group B, kidney ganglioside fraction, sulfolipid fraction from kidney, and a pure globoside fraction.
Fractions of nonhuman origin
Total fractions originating from pig organs of blood group O used for screening included nonacid small intestine, nonacid kidney, nonacid liver, nonacid spleen, and acid erythrocytes.
Total fractions originating from pig organs of blood group A included nonacid salivary gland and nonacid heart. A total fraction originating from about 80 pig blood group A and O aortas was also used.
HPLC-purified pig organ fractions used included ganglioside, globotriaosylceramide and globotetraosylceramide fractions from heart; sulfolipid fractions from heart, salivary gland, kidney, small intestine, liver, and spleen; and ganglioside fractions from intestine, kidney, salivary gland, heart, and liver. Fractions from small intestine, kidney, liver, salivary gland, spleen, and heart have also been purified and pooled into fractions with nonspecified monosaccharides, disaccharides, trisaccharides, tetrasaccharides, and fractions with tetrasaccharide glycolipids (e.g., four to eight sugars in the sugar chain), respectively.
Total fractions originating from sheep organs of blood group A type included acid pancreas, acid small intestine, acid colon, acid lung, and acid kidney. Purified reference glycolipid fractions included gangliotriaosylceramide from guinea pig erythrocytes and gangliotetraosylceramide from mouse feces.
Thin Layer Chromatography
TLC was performed as previously described (Hansson et al., 1985) on aluminum-backed silica gel 60 high-performance TLC plates (Merck, Darmstadt, Germany and HP-KF, Whatman, Maidstone, U.K.). Glycolipid fractions (210 µg/ lane) were added to the TLC plates and separated in a specific mixture of organic solvents and water. The nonacid components were chromatographed in chloroform/methanol/water, 60:35:8 by volume, and the acid components in chloroform/methanol/water with 0.2% CaCl2, 60:40:9 by volume. On all TLC plates, a reference fraction from human kidney blood group A (an acid glycolipid fraction) that was positive for bacterial binding was added in lane 1.
For each chromatogram with bacterial overlay, two sets of identical glycolipid fractions were separated on the same TLC plate. In this manner we received two TLC plates with as identical a separation pattern as possible. The TLC plate was dried at room temperature until the organic solvents had evaporated from the silica gel, and thereafter it was cut in two halves, thus separating the identical TLC sets. The TLC plate that was used in the bacterial overlay experiment was coated in 0.3% (w/v) polyisobutylmethacrylate, P28 (Sigma-Aldrich), in diethyl ether/n-hexane (1:1 by volume), or in 0.5% P28 in diethyl ether/n-hexane (1:4 by volume) and left to polymerize overnight to avoid unspecific binding to nonpolymerized monomers. The identical TLC plate was visualized chemically by anisaldehyde reagent and used for inspection of the separation pattern and for identification of the bacterial binding region in the autoradiogram (Karlsson, 1987). All glycolipid-containing lines were visualized by chemical detection with anisaldehyde reagent. This TLC plate was then compared with the identical plate used in the chromatogram binding assay, where only lines with positive binding can be seen.
Bacterial strains and growth conditions
In this study P. gingivalis FDC381 (collection of Forsyth Dental Center, Boston, MA), a strain isolated from a periodontitis patient, was used. The bacteria were grown on Brucella agar plates (BBL Microbiology Systems, Cockeysville, MD) enriched with 5% defibrinated horse blood, 0.5% hemolyzed blood, and 5 µl/ml menadione in jars with 95% H2 and 5% CO2 at 37°C. A suspension of 5 µl L-[35S]methionine and L-[35S]cysteine in PBS with a concentration of 14.3 mCi/ml and t1/2 of 87.4 days (Redivue ProMix L-[35S] in vitro labeling mix, Amersham Biosciences, Uppsala, Sweden) was added to the agar plates. After 3 days of growth, bacterial cultures were collected and washed three times by centrifugation at approximately 5000 rpm in PBS. A spectrophotometer analysis at 550 nm was performed for evaluation of the bacterial concentration and compared to an absorbance standard curve for P. gingivalis. The bacteria were suspended in PBS with 2% bovine serum albumin (w/v), 0.1% Tween 20 (v/v), and 0.01% sodium azid (w/v) and diluted to a final concentration of 1.53 x 108 bacteria/ml used in the bacterial overlay assays.
Bacterial overlay and detection of bacterial binding
The method used in the bacterial overlay assays is a modified version of the method by Karlsson and Strömberg (1987). The TLC plates were coated with 2% bovine serum albumin (w/v), 0.1% Tween 20 (v/v), and 0.01% sodium azid (w/v) in PBS for 2 h at room temperature to block nonspecific binding sites. Thereafter, the coating solution was carefully removed from the TLC plates. Approximately 5 ml of the bacterial suspension was sprinkled over the TLC plates with a Pasteur pipette and then incubated at room temperature for 9 h or overnight. The TLC plates were gently washed four times with PBS, dried in room temperature for at least 1 h, and autoradiographed for approximately 714 days using a ß-sensitive film (Kodak BioMax MR, Amersham Biosciences). After development of the film (on Agfa Curix HT-530 U equipment), bacterial binding was analyzed by visual inspection. Significant staining/darkening of the film was registered as positive binding and marked with asterisks (one to four, depending on intensity of the binding; one asterisk = weak staining, four asterisks = strong staining). When positive binding was detected in the autoradiogram, the film was placed on top of the identical anisaldehyde-stained TLC plate by means of easily identified landmarks. In this way the specific sugar binding region was identified. A comparison to the TLC plate in the reference article for that specific organ enabled estimation of the glycolipid structure that P. gingivalis can use as a receptor.
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Acknowledgements |
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Footnotes |
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Abbreviations |
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References |
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