Institute of Medical Biochemistry, Göteborg University, PO Box 440, SE 405 30 Göteborg, Sweden
Received on June 24, 2003; revised on October 17, 2003; accepted on November 11, 2003
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Abstract |
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Key words: binding epitope / derivatization / Helicobacter pylori / sialic acid
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Introduction |
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Helicobacter pylori inflammation in the human stomach is associated with massive phagocyte infiltration of the infected areas (Hatz et al., 1992; Warren and Marshall, 1983
), and it is possible that the bacterium uses the inflammatory products for nutrition (Blaser, 1992
). In line with this are findings that H. pylori actively recruits neutrophils by synthesizing a neutrophil-activating protein, Hp-NAP (Evans et al., 1995
), considered a major virulent factor of the bacterium (Satin et al., 2000
) and shown to bind sialylated sequences (Teneberg et al., 1997
). Because sialylated oligosaccharides inhibit H. pyloriinduced activation of human neutrophils (Teneberg et al., 2000
), Neu5Ac may be an important factor mediating interaction between H. pylori and inflammatory cells. Also of interest are results indicating that sialic acid contributes to H. pylori resistance to phagocytosis (Chmiela et al., 1994
)
The sialic acid content in normal human gastric mucosa, the main target tissue for H. pylori, is very low (Filipe, 1979; Madrid et al., 1990
) and the bacterial binding to gastric cells may be through nonsialylated receptors, like Le b antigenic structures (Borén et al., 1993
), sulfatide (Kamisago et al., 1996
; Osawa et al., 2001
), or lactotetraose (Teneberg et al., 2002
). However, sialylated structures may be of importance in inflamed human mucosa, where it was shown that the level of sialylation rose with grade of inflammation (Mahdavi et al., 2002
). Sialyllactose has been reported to inhibit binding of H. pylori to cultured gastrointestinal epithelial cells (Simon et al., 1997
) and chronic atrophic gastritis in mice has been shown to be associated with increased synthesis of Neu5Ac
3Gal structures (Syder et al., 1999
). In addition, inhibition of the sialic acidspecific adhesion of H. pylori to human gastric mucus by some unidentified components of cranberry juice has been reported (Burger et al., 2000
).
In the present article we investigate structural requirements for sialic acidrelated binding specificities of H. pylori using a panel of different natural gangliosides, neogangliosides, and chemically modified gangliosides.
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Results |
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To minimize energy-costly solvent exposure of the additional hydrophobic tail of the octadecylamide derivative, it is likely that the octadecyl and ceramide tails would have to orient themselves in a coparallel fashion relative to each other when adhering to the polyisobutyl-methacrylate-treated TLC plate. By systematic variation of the glycosidic dihedral angles representing local energy minima of the NeuA5c3Gal (Siebert et al., 1992
) and Glcß1Cer (Nyholm and Pascher, 1993
) linkages while keeping other glycosidic linkages of S-3PG locked, it is found that with the sialic acid residue in the anticlinal conformation (
/
-155°/25°) three different Glcß1Cer conformations give rise to a more or less co-parallel arrangement of the hydrophobic tails. The most favorable one in this respect corresponds to the same conformation seen in the crystal structure of cerebroside (Galß1Cer) having dihedral angles of
/
/
50°/175°/-65° (Pascher and Sundell, 1977
) yielding maximal exposure of the binding epitope as shown in Figure 10. Repeating the same procedure with the sialic acid in the synclinal conformation (
/
-75°/10°) does not yield any configuration compatible with a co-parallel arrangement.
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Discussion |
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As shown in Table I, there is a relatively stronger binding to more complex gangliosides, as compared with S-3PG, which suggests that structural factors connected with core carbohydrate parts enhance affinity of the sialylated epitope. The more effective interaction may also depend on the combined action of different bacterial adhesins recognizing both terminal and internal parts of the extended core chains. Helicobacter pylori is known to display binding specificities associated with both sialylated and neutral saccharide chains (Karlsson, 1998). Recently, Roche et al. (2001)
reported binding of H. pylori to gangliosides with repeated lactosamine units prepared from human gastric carcinoma. It is thus likely that Neu5Ac
3Galß4GlcNAc and its extended and fucosylated counterparts represent functioning epitopes during contact of H. pylori with inflammatory cells that are enriched in these structures.
On the other hand, the simpler 3-sugar-containing ganglioside GM3 was negative in our TLC assays, although Neu5Ac3Galß4Glc (sialyl lactose), both free (Evans et al., 1988
) and coupled to albumin (Simon et al., 1997
), is active as inhibitor of the binding. No binding to GM3 in the present studies might be due to an inaccessible binding epitope at the TLC assay surface. Our experience indicates that use of very short glycolipids on TLC plates may lead to false negative results and that spacers in neoglycolipids may influence the binding. It should also be mentioned that GM3 is not expected as a strong binder because Neu5Ac
3Galß4Glc saccharide is less effective as inhibitor of hemagglutination by H. pylori than Neu5Ac
3Gal-ß4GlcNAcß3Galß4Glc (Johansson and Miller-Podraza, unpublished data).
As mentioned, H. pylori is highly variable regarding binding activities, and it has been shown that the expression of different specificities depends both on bacterial strains and growth conditions. We have previously suggested two sialic aciddependent binding specificities of this bacterium (represented by interactions with S-3PG and PGCs, respectively), based on comparison of bacterial cells grown on agar and in liquid cultures (Miller-Podraza et al., 1997b). We have also noticed that binding to S-3PG by H. pylori is stronger after longer growth times on agar plates. Both S-3PG and PGCs contain Neu5Ac
3Galß4GlcNAc (Karlsson H. et al., 2000
), and the question arises whether different presentations of this structural element may result in formation of two different binding epitopes. To better understand this issue, molecular modeling of S-3PG and its chemical derivatives was employed, the results of which suggest that the sialic acid has to adopt the anticlinal conformation for the binding epitope to be presented correctly. However, molecular dynamics investigations of various hypothetical PGC fragments (Ångström et al., unpublished data) indicate, on the other hand, that the synclinal conformation is preferred. The results further indicated that in the S-3PG case a direct involvement of the glycerol tail at the binding interface is likely, whereas in the PGC case the same group is stabilizing an intramolecular conformation in which two neighboring branches become spatially fixed relative each other.
Another important question is whether the binding to different sialylated glycoconjugates is through one or more bacterial adhesins. To investigate this issue we performed binding experiments using H. pylori knockout strains lacking the sialic acidbinding protein SabA (Mahdavi et al., 2002). We found that genetically modified (SabA) strains lose the ability to bind to both PGCs and S-3PG. This result favors the presence in H. pylori of a single adhesin responsible for interactions with both S-3PG and PGCs. Consequently, the two modes of binding observed in our studies (Miller-Podraza et al., 1997b
) could depend on two different binding sites on the SabA adhesin and/or different densities of SabA on H. pylori cells grown under different conditions. The apparently more rigid presentation of Neu5Ac in branched PGCs, as compared to S-3PG (Ångström, unpublished data) may result in an apparent higher affinity of the epitope requiring lower concentrations of the protein. An answer to this may be given when the binding site of the adhesin has been identified.
Helicobacter pylori is a gastric pathogen that causes ulceration and confers a greater risk of stomach cancer. Current treatment is based on the use of antibiotics and this is connected to the development of resistant bacterial strains (Adamsson et al., 2000; Kate and Anathakrishnan, 2001
). Thus new ways of therapeutical strategies are needed, and carbohydrates and their chemical analogs are relevant candidates for antiadhesion therapy. As discussed in the Introduction, various sialylated structures have been reported to inhibit H. pylori binding to gastric cells and artificial surfaces (Burger et al., 2000
; Simon et al., 1997
; Wang et al., 2001
), supporting the relevance of such an approach. An important experiment using rhesus monkeys showed that oral administration of sialyllactose (Neu5Ac
-3Galß4Glc) can eradicate H. pylori or decrease bacterial colonization in animal stomachs (Mysore et al., 1999
). The epitope dissection of this work was limited to two groups of Neu5Ac, the glycerol tail and the carboxyl group. The third functional group of interest is N-acetamido group, which also is essential for binding as will be discussed separately (Johansson and Miller-Podraza, unpublished data).
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Materials and methods |
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Source of oligosaccharides
Neu5Ac3Galß4GlcNAcß3Galß4Glc was prepared in our laboratory from S-3PG (human erythrocytes) using ceramide glycanase (from leech, Boehringer Mannheim GmBH, Germany) digestion (Ito and Yamagata, 1989
) and phase partition in chloroform/methanol/water, 2:1:0.6. The pentasaccharide was recovered from the upper phase. Neu5Ac
3Galß3GlcNAcß3Galß4Glc, Neu5Ac
6Galß-4GlcNAcß3Galß4Glc and Galß3(Neu5Ac
6)GlcNAcß3-Galß4Glc were purchased from IsoSep (Tullinge, Sweden).
Other reagents
4-HDA, methylamine, ethylamine, propylamine, butylamine, and benzylamine were from Aldrich Chemical (Milwaukee, WI). Glycolic acid, ethanolamine, and octadecylamine were purchased from Sigma-Aldrich (Germany). Sephadex LH 20 was from Pharmacia (Uppsala, Sweden) and ethylene glycol from Fluka (Sweden).
Chemical modifications of the sialic acid glycerol tail
Mild periodate oxidation (Veh et al., 1977) followed by reduction (R-CHOH-CHOH-CH2OH
R-CHOH-CH2OH/R-CH2OH): The material (0.51 µmol) was incubated in 500 µl 0.05 mM acetate buffer, pH 5.5, containing 12 mM NaIO4, for 40 min on ice. The reaction was terminated with an excess of ethylene glycol. The sample was then concentrated by freeze-drying (about fivefold) and reduced with an excess of NaBH4 at room temperature overnight. Finally the sample was dialyzed against distilled water for 2 days and freeze-dried.
Mild periodate oxidation of S-3PG followed by coupling with methylamine or ethanolamine (R-CHOH-CHOH-CH2OHR-CH2-NH-CH3 or R-CH2-NH-CH2CH2-OH). After oxidation of S-3PG with mild periodate (see previous methods) and addition of ethylene glycol, the material was dialyzed for 2 days against distilled water and freeze-dried. The oxidized S-3PG was coupled with methylamine or ethanolamine under the following conditions: the glycolipid (0.5 mg) was dissolved in 200 µL methanol/chloroform 3:1 and mixed with 50 µL amine, 200 µL NaBH3CN in methanol (62 mg/mL) and 200 µL glycolic acid in water (136 mg/mL). In the case of methylamine, 50 µL tetrahydrofuran was added to improve solubility. The sample was incubated at 30°C for 4 h and evaporated under nitrogen. The residue was suspended in chloroform/methanol/water, 60:30:4.5 and desalted using Sephadex LH-20 column packed in methanol. After application of the sample (about 0.6 mL per 0.5 x 15 cm column), the column was eluted with methanol, and the glycolipid was recovered by collecting sugar-positive fractions (monitored by TLC and anisaldehyde). For final purification of molecular species (see formulas), the material was separated by preparative TLC using chloroform/methanol/water, 60:35:8, as developing system. The main band (detected with anisaldehyde after cutting off a strip from the plate) was scraped out and extracted with the same solvent.
Modifications of the carboxyl group (Lanne et al., 1995)
S-3PG (0.55 mg) was first converted to the methylester (R-COOHR-COOCH3) by incubation with methyl iodide (100 µL) in dimethylsulfoxide (0.5 mL) for 1 h at room temperature. The product was purified using Sephadex LH-20, as already described. To prepare the alcohol derivative (R-COOCH3
R-CH2OH) of S-3PG, the methylester (0.5 mg) was dissolved in 0.5 mL methanol, followed by addition of 5 mg NaBH4. After 1 h at room temperature, the reduced S-3PG was desalted using Sephadex LH-20 (see previous methods). For synthesis of the amide and the methyl-, ethyl-, propyl-, benzyl-, and stearylamide of S-3PG, the methyl ester (0.5 mg in 0.5 mL methanol) was mixed with 0.2 mL 30% NH3 in water, 0.5 mL 40% methylamine in water, 1 mL 70% ethylamine in water, 100 µL propylamine, 100 µL benzylamine, or 200 µL stearylamine in tetrahydrofuran (saturated solution), respectively. After incubation overnight at room temperature, the products were evaporated under nitrogen. Benzyl and stearyl amides were further purified by extraction with hexane/acetone 1:1. The samples were washed with excess of the solvent mixture and centrifuged, and the supernatants were discarded.
PGC derivatives were prepared in the same way with the following exceptions. First, the reduced PGC preparation was separated on a DEAE-Sephadex column and only the neutral fraction was further investigated. Second, the oxidation/reduction procedure was performed twice.
Coupling of HDA to free saccharides
The synthesis was performed as described, with some modifications (Evangelista et al., 1996). Saccharide (0.5 mg) was dissolved in 100 µL methanol and mixed with 100 µL NaBH3CN in methanol (62 mg/mL), 100 µL HDA in tetrahydrofuran (40 mg/mL), and 100 µL of 1.8 M glycolic acid in water (136 mg/mL). Additional 100200 µL tetrahydrofuran was added to improve solubility of the precipitating hexadecylaniline. The sample was incubated at 30°C overnight and the product purified by Sephadex LH 20 chromatography (see previous method description). The yield of this reaction was more than 90%.
Synthesis of branched lipid parts
To obtain neoglycolipids with branched lipid parts, the HDA-derivatized saccharides were further modified by N-acylation (Magnusson et al., 1994; Read et al., 1977
). P-nitrophenylpalmitate (500 µL in dry dimethysulfoxide, saturated solution) was added to 200300 µg of the dried HDA-saccharide. Four drops of triethylamine were added to the sample, which was incubated in nitrogen atmosphere at 37°C for 3 days. Glycolipids were purified using Sephadex LH-20 column chromatography (see described methods) and preparative TLC. The yield was 1020%.
Preparation of lactones
S-3PG was transformed into its lactone form as described elsewhere (Laferriere and Roy, 1994). S-3PG (1 mg) was dissolved in concentrated acetic acid, and the reaction was allowed to proceed at room temperature for 2 days. The acetic acid was then evaporated and the remaining material dissolved in chloroform/methanol/water, 60:35:8 (0.5 mL). The yield of the reaction was controlled by TLC on aluminum-backed high-performance TLC plates coated with 0.1 mm silica gel 60 (Merck, Darmstadt, Germany) and was
50%.
Synthesis and preparation of ganglioside GM1b
Gangliotetraosylceramide, prepared by desialylation of the ganglioside GM1, was sialylated at the terminal galactose using an -2,3-(0)-sialyltransferase, EC number 2.4.99.4 (recombinant, rat liver-Spodoptera frugiperda) from Calbiochem (Darmstadt, Germany). The conditions were as described in Lee et al. (1994)
with slight modifications, as follows. Gangliotetraosylceramide (100 µg) was dissolved in 10 µL 500 mM 4-morpholineethanesulfonic acid buffer, pH 6.0, containing Triton CF-54 (2%) and diluted with 74 µL water. Then, 10 µL CMP-NeuAc (15 mM in water) and 6 µL
-2,3-sialyltransferase (338 mU/mL) were added to the reaction mixture, and the sample was left at room temperature overnight. The progress of the reaction was analyzed by TLC using chloroform/methanol/0.25% KClaq (50:40:10) as eluent. The reaction mixture was then evaporated under a stream of nitrogen, dissolved in chloroform/methanol/H2O (60:30:4.5) (2 mL) and applied to a small column (
2.5 x 0.6 cm) packed with Sephadex G-25 (prewashed with 5 mL of the same solvent system). The glycolipid material was eluted with 2.5 mL of the solvent mixture and 2.5 mL chloroform/methanol (2:1, by volume). Finally, the material was evaporated and dissolved in a small volume of chloroform/methanol/H2O (60:30:4.5).
H. pylori strains
Helicobacter pylori strain CCUG 17874 was from Culture Collection (Göteborg University, Sweden) and H. pylori strain 032 was a gift from Prof. T. Wadström (Department of Medical Microbiology, Lund University, Sweden). Helicobacter pylori strains J99 and J99(SabA) were kindly donated by Dr. Thomas Borén from Department of Odontology/Oral Microbiology (Umeå University, Sweden) (Mahdavi et al., 2002).
Overlay of TLC plates with H. pylori
Overlay of gangliosides on silica-gel TLC plates with 35S-labeled H. pylori was performed as described elsewhere (Miller-Podraza et al., 1996).
MS
FAB MS of glycolipids was performed on a JEOL SX-102 mass spectrometer in the negative ion mode. The spectra were produced by Xe atoms using triethanolamine as a matrix. EI MS of permethylated PGCs was performed using the same mass spectrometer. Samples were evaporated in the ion source between 150 and 410°C, and the spectra were recorded at different points of broad peaks in the end of the run. The electron energy was 70 eV and ion current 300 µA.
Molecular modeling
Minimum energy conformations of the glycosphingolipids and chemical derivatives thereof used in this study were calculated within the Quanta2000/CHARMm25 software (Accelrys) on an Indigo2Extreme workstation (Silicon Graphics) using a dielectric constant of = 8. Glycosidic dihedral angles are defined as follows:
= H1-C1-O1-C'X and
= C1-O1-C'X-H'X for 2-, 3-, or 4-linked residues other than NeuAc;
= C1-C2-O2-C'3 and
= C2-O2-C'3-H'3 for
3-linked NeuAc;
= H1-C1-O1-C'1,
= C1-O1-C'1-C'2, and
= O1-C'1-C'2-C'3 for the Glcß1Cer linkage, whereas the orientation of the modified carboxyl moiety is defined as
= O5-C2-C1-O1. The Glcß1Cer glycosidic dihedral angles of S-3PG were varied according to Nyholm and Pascher (1993)
, whereas the angles of the Galß4GlcNAcß3Galß4Glc segment were kept constant at their respective constituent disaccharide global minima (Imberty et al., 1991
; Poppe et al., 1990
). The terminal disaccharides of native S-3PG and its chemical derivatives were subjected to molecular dynamics simulations (1 ns) after initial heating (300 K) and equilibration periods using a 1 fs time step to determine the conformational preferences of the modified sialic acid. All bonds to hydrogens were constrained by the SHAKE algorithm. Frames were written to the trajectories once every ps. Simulations were carried out starting from both the anticlinal and synclinal conformations.
The carbohydrate and glycosphingolipid nomenclature are according to recommendations of the Joint Commission on Biochemical Nomenclature (JCBN). Nomenclature of carbohydrates: Carbohydr. Res. (1997) 297, 1. Nomenclature of glycolipids: Carbohydr. Res. (1998) 312, 167 and Eur. J. Biochem. (1998) 257, 293. All solvent mixtures were prepared volume by volume, unless otherwise stated.
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Acknowledgements |
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Footnotes |
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Abbreviations |
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References |
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