2Laboratoire de Mycologie Fondamentale et Appliquée, INSERM EPI 9915, Université de Lille II, Faculté de Médecine H. Warembourg, Pôle Recherche, Place Verdun, 59037 Lille Cedex, France, 3Laboratoire de Chimie Biologique, CNRS UMR 8576, Université des Sciences et Technologies de Lille, 59655 Villeneuve dAscq Cedex, France, 4Zentrum für Hygiene und Humangenetik, Göttingen University, 37075 Göttingen, Germany, 5Eurogentec Bel S.A, Parc industriel des Hauts Sarts, B-4040 Herstal, Belgium, and 6INSERM U524, Cité hospitalière, Place de Verdun, 59045 Lille Cedex, France.
Received on February 16, 2001; accepted on March 27, 2001.
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Abstract |
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Key words: peptides/ß-1,2-oligomannosides/epitopes/mimotope
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Introduction |
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In humans (Jouault et al., 1997) and animals (Cassone et al., 1995
; Han and Cutler, 1995
), ß-1,2-oligomannosides elicit antibodies with specificity different from anti-
-linked mannose antibodies (Faille et al., 1992
; Jacquinot et al., 1998
; Trinel et al., 1992
). They interact with the macrophage membrane (Fradin et al., 1996
; Li and Cutler, 1991
, 1993) via a receptor (Fradin et al., 2000
) different from that recognized by
-linked mannose (Stahl and Ezekowitz, 1998
). C. albicans components presenting ß-1,2-oligomannoside epitopes display several biological properties related to yeast pathogenicity (Vecchiarelli et al., 1991
; Bromuro et al., 1994
; Jouault et al., 1994
, 1995, 2000; Pitzurra et al., 1996
; Masuoka and Hazen, 1999
). These observations have prompted attempts to generate anti-ß-1,2-oligomannoside antibodies. Protective antibodies have been obtained using C. albicans mannan extractprotein conjugates or liposome-encapsulated mannoproteins (Han et al., 1998
, 1999). Recently, an alternative approach based on panning of a phage library expressing random peptides with anti-ß-1,2-oligomannosides monoclonal antibody (mAb) has been applied to isolate peptides able to mimic ß-1,2-linked mannosides (Glee et al., 1999
). However, the selected phage-expressing peptides bound to immunoglobulin M (IgM) antibodies in general and the phage-displayed and synthetic peptides inhibited the binding of IgM antibodies to antigens independently of their specificities. Here, we used a different anti-ß-1,2-oligomannoside mAb to isolate phage expressing peptides able to inhibit binding of the mAb to live yeast cell PPM. Phage peptides were recognized by the specific mAb but did not bind to an antiC. albicans
-1,2-oligomannoside mAb. A peptide deduced from the most representative sequence was synthesized after DNA sequencing of the phage inserts. This peptide was recognized specifically by anti-ß-1,2-oligomannoside mAbs. It inhibited binding of anti-ß-1,2-oligomannoside mAb both to live yeast cells and to PPM. In mice, keyhole limpet hemocyanin (KLH)peptide elicited an antibody response to yeast PPM which was inhibited by ß-1,2-mannotetraose.
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Results |
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Specificity of phages isolated by biopanning with DJ2.8
After amplification to 6 x 1010 pfu per ml, the peptide-phages isolated with DJ2.8 were dotted and their recognition by different mAbs determined. The phages were strongly recognized by the anti-ß-1,2-oligomannoside mAb DJ2.8 (112 ± 5 arbitrary units [AU]); low reactivity (15 ± 9 AU) was also observed with another anti-ß-1,2-oligomannoside mAb 5B2; no signal (3 ± 2 AU) was detected with the anti--linked mannoside mAb CA1.
The ability of the selected peptide-phages to inhibit binding of the different mAbs to yeast cells was investigated. First, the reactivity of the mAbs against whole yeast cells in the presence or absence of peptide-phages was determined in an immunofluorescence assay. Compared with the intensity of fluorescence obtained with DJ2.8 in the absence of peptide-phage (Figure 1A), a dramatic decrease in intensity was observed after addition of peptide-phage to the mAb before incubation with yeast cells (Figure 1B). This was dependent on the amount of peptide-phage incubated with the mAb (data not shown), with a maximal effect obtained with a 1:80 dilution of phage suspension (1530 x 106 virions). In contrast to DJ2.8 (Figure 2A), reactivity of anti--linked mannoside mAb CA1 against the yeast cells was not altered by the phages (Figure 2B). With the anti-ß-linked mannoside mAb 5B2, fluorescence decreased slightly when the highest dose of phages was used (Figure 2C).
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Peptide FHENWPS is recognized specifically by anti-ß-1,2-linked mannoside mAbs and inhibits mAb binding to yeast PPM
As the most representative peptide sequence corresponded to that of group 3, the corresponding FHENWPS peptide was synthesized. Recognition of this peptide by DJ2.8 in a dot-blot experiment (Figure 4A) was dose-dependent and reached a maximum with 100 µg peptide. In an enzyme-linked immunosorbent assay (ELISA) (Figure 4B), the FHENWPS peptide was recognized specifically by the two anti-ß-1,2-linked mannoside mAbs DJ2.8 and 5B2 in a dose-dependent manner. In contrast, the anti--linked mannoside mAb CA1 did not react with this peptide.
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Discussion |
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Because the sequence FHENWPS was present in over 60% of the phages isolated with DJ2.8, this peptide was synthesized and its antigenic activity determined. Peptide FHENWPS was recognized specifically by anti-ß-1,2-oligomannoside mAbs. Compared with phages expressing this peptide sequence however, synthesized peptide inhibited recognition of yeast cells by DJ2.8 to a lesser extent. This difference has been noted elsewhere for other peptides that mimic peptidic epitopes (Chirinos-Rojas et al., 1999). One possible explanation for this is that the peptide sequence was present at the phage surface as a part of the minor coat protein. The three-dimensional structure of the short peptide may be stabilized when inserted in the phage protein. The soluble peptide inhibited recognition of C. albicans PPM by the mAb, showing that, although possibly incompletely folded, the peptide structure was sufficiently similar to that of the epitope recognized by the anti-ß-1,2-oligomannoside mAbs. The fact that soluble peptide was not recognized by the mAb specific to
-linked mannosides suggests that the peptide mimicked ß-1,2-linked mannosides.
Although mAbs DJ2.8 and 5B2 both recognized ß-1,2-oligomannosides (Trinel et al., 1992) and FHENWPS peptide in an ELISA, phages selected after biopanning with DJ2.8 only inhibited recognition of C. albicans yeast cells by DJ2.8. A major difference between the two mAbs is that 5B2 recognizes both antigen factors 6 and 5, whereas DJ2.8 is specific to ß-1,2-oligomannoside homopolymers present in antigen factor 5. Studies have shown that the smallest epitope recognized by 5B2 consisted of ß-1,2-linked mannobiose (Sendid et al., unpublished data) present in both antigen factors 5 (Shibata et al., 1992
) and 6 (Kobayashi et al., 1992
). In contrast, DJ2.8 recognized epitopes presenting at least four ß-1,2-linked mannoses, a sequence found only in antigen factor 5 (Shibata et al., 1992
). It therefore appears that although the two anti-ß-1,2-oligomannoside mAbs recognized the peptide by ELISA, only one of the two antigenic interactions involving structures presenting ß-1,2-oligomannosides in live yeasts was altered by the peptide. This suggests that the relative accessibility of the two antigenic factors or the relative affinity of the mAbs for the peptide may be different in the two immunoassays and/or emphasizes the importance of the molecular environment for antibody recognition.
Injection of the FHENWPS peptide into mice induced a high antibody response, which was directed against the cell wall surface of live yeast cells. In ELISA, anti-FHENWPS antibodies recognized PPM by specific binding to ß-1,2 mannotetraose. These results demonstrate that immunization with the peptide lead to the generation of antiC. albicans antibodies that recognized ß-1,2-linked mannosides present in cell wall PPM.
These results demonstrate that peptides may mimic epitopes corresponding to small oligomannosides. To date, most data have been obtained with libraries presenting DNA inserts corresponding to peptides with 1012 amino acids. Although the peptides expressed by our phage library were short (seven amino acids), isolation of a highly specific peptide with antigenic and immunogenic properties was nevertheless possible. Spatial arrangements presented by the mimotope should correspond to the spatial structure presented by ß-1,2 mannotetraose. Computer modeling has indicated that ß-1,2-linked mannosides appear as a tight helix with one face formed predominantly by hydrogens (Bohne et al., 1998). Although mAb recognition involved a conformational epitope mimicked by the peptide, our results show that interaction between the peptide and the mAb was based on very specific recognition. This confirms previous results showing that, in the same way as recognition of peptides by antibodies, recognition of sugar sequences is highly specific and depends on the spatial structure presented by the sugars (Faille et al., 1992
; Han et al., 1997
; Jacquinot et al., 1998
). Such mimicry may lead to binding and stimulatory activity of the mimotope toward macrophages that is identical to that of oligomannosides (Jouault et al., 1995
, 2000). This would imply recognition of the mimotope by identical membrane receptors (Fradin et al., 2000
). Studies to determine whether mimotope peptides have agonistic or antagonistic activity toward macrophage stimulation are under way.
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Materials and methods |
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C. albicans
C. albicans VW32 (serotype A) was used throughout this study. Yeasts were grown on Sabourauds dextrose agar for 24 h at 28°C, washed twice with phosphate buffer (10 mM PO4, pH 7.4; phosphate buffered saline [PBS]), resuspended at the appropriate concentration, and seeded onto slides for microscopic observation. PPM and ß-1,2 mannotetraose were obtained from C. albicans cell walls as described previously (Kocourek and Ballou, 1969).
Peptide library and biopanning with anti-ß-1,2-oligomannoside mAb
The Ph.D.-7 Phage display library kit (Biolabs, Beverly, MA) was based on a combined library of random peptide 7-mers fused to the minor coat protein pIII of the filamentous coliphage M13. The heptapeptides were expressed directly at the N-terminus of pIII. The library consisted of 2 x 109 different available sequences.
Biopanning was performed according to the manufacturers instructions. Briefly, 100 µg DJ2.8 in 750 µl 0.1 M NaHCO3 (pH 8.6) was coated onto 3-cm2 individual sterile polystyrene petri dishes for 20 h at 4°C with gentle agitation. The dishes were saturated for 1 h at 20°C with the same buffer supplemented with 5 mg/ml bovine serum albumin (BSA) and washed with Tris buffer (Tris 50 mM, HCl pH 7.5, NaCl 150 mM) containing 0.1% (v/v) Tween-20. For the first round of biopanning, mAb-coated dishes were incubated with 10 µl of phage suspension (1011 virions in 1 ml of Tris bufferTween) for 1 h at 20°C with gentle agitation. Supernatants were discarded and dishes were washed 10 times with 1 ml Tris bufferTween. Bound virions were washed off with 1 ml of 200 mM glycineHCl (pH 2.2) containing 1.5 mg/ml BSA at 20°C for 10 min, and neutralized with 150 µl of 1 M TrisHCl (pH 9.1). Eluted phages were amplified and titrated. For the two subsequent rounds, an identical method was used except that the washing buffer contained a higher concentration of Tween-20 (0.5% v/v) to eliminate phages bound to the mAb with low avidity. After each round, the eluted phages were amplified and titrated using Escherichia coli ER2537.
Amplifications were carried out by infection of 20 ml of bacterial suspension in Luria-Bertani (LB) medium with eluted phages for 4.5 h at 37°C. Cultures were centrifuged twice at 10,000 r.p.m. for 10 min at 4°C. The supernatants were then precipitated at 4°C for 20 h with a 1:6 (v/v) dilution of PEG (20% [w/v] polyethylene glycol-8000, 2.5 M NaCl). The phages were pelleted by centrifugation at 10,000 r.p.m. for 15 min at 4°C, and dissolved in 1 ml Tris buffer. After centrifugation at 10,000 r.p.m. for 5 min at 4°C, the clarified supernatants were precipitated at 4°C for 1 h, centrifuged at 10,000 r.p.m. for 5 min, and the pellets resuspended in 200 µl Tris buffer.
Ten microliters of 10-fold serial dilutions of the biopanning eluate or the purified amplified phage supernatant in LB medium were added to 200 µl of a midlog phase culture of ER2537. After 5 min incubation, infected cultures were transferred to LB agar plates and incubated at 37°C for 20 h. The phage concentration in each eluate was determined by counting the phage-infected colonies.
Determination of phage recognition by the mAb
After three rounds of biopanning, 10 µl of the eluate was dotted onto a nitrocellulose membrane. The membrane was blocked with PBS containing 5% BSA at 20°C for 1 h and incubated at 4°C for 20 h with a 1:100 dilution of anti-ß-1,2-oligomannoside or anti--oligomannoside mAbs in PBSBSA. After extensive washing in PBS, the membrane was incubated at 20°C for 2 h with the corresponding HRP-labeled goat anti-Ig. The membrane was then washed, treated for chemiluminescence detection (SuperSignal; Pierce, Rockford, IL) and exposed to X-ray film for 2 min. Third-round eluates were titrated, and several phage-infected colonies were stabbed with a pipette tip and transferred to a culture tube for amplification and purification of the corresponding phages. Ten microliters of the different purified phage suspensions were dotted onto nitrocellulose membranes. After blocking with PBSBSA, membranes were incubated at 4°C for 20 h with a 1:100 dilution of DJ2.8 in PBSBSA. The membranes were washed with PBS, incubated at 20°C for 2 h with the corresponding HRP-labeled goat anti-mouse IgM, and revealed as described.
Inhibitory effect of phages on recognition of C. albicans by DJ2.8
The ability of phages to interfere with recognition of C. albicans yeast cells by DJ2.8 was examined by indirect immunofluorescence. MAbs (1:100 dilution in PBS) were incubated with serial dilutions of eluted phages at 20°C for 30 min. Fifty microliters of each dilution of the mixture were then incubated with C. albicans yeast cells bound to microscope slides. After incubation for 2 h at 20°C, the slides were washed with PBSBSA, incubated with a 1:100 dilution of the corresponding FITC-conjugated goat anti-Ig, washed again, and examined by direct microscopy.
Sequencing of phage DNA insert
DNA sequencing of the purified phages was performed according to manufacturers instructions (Biolabs). Each clone to be sequenced was amplified as described. After extraction, phage DNA was precipitated with ethanol and dissolved in water. The sequencing reactions were performed by the dideoxy chain termination method (AutoRead Sequencing Kit; Amersham-Pharmacia), using the 96gIII primer 5' CCC TCA TAG TTA GCG TAA CG 3' (Biolabs) and analyzed on an ALF ExpressTM DNA automatic sequencer (Amersham-Pharmacia).
Antigen recognition of synthesized phage-peptide
The peptide corresponding to the most representative sequence displayed by the isolated phages was synthesized (Eurogentec, Seraing, Belgium). Recognition of the peptide by mAb DJ2.8 was determined in a dot-blot experiment. Different amounts of peptide (20110 µg in 20 µl water) were dotted onto a nitrocellulose membrane. After blocking with PBS containing 5% BSA at 20°C for 1 h, DJ2.8 diluted 1:100 in PBSBSA was added. Incubation was performed overnight at 20°C, and after extensive washing in PBS the membrane was incubated with a 1:500 dilution of alkaline phosphatase-conjugated goat anti-mouse IgM at 20°C for 2 h. Specificity of antigen recognition was also determined by ELISA. Peptide (3 µg per well in 100 µl of carbonate buffer, pH 9) was coated onto wells. After blocking with PBS containing 5% BSA for 1 h at 20°C, the mAbs diluted 1:4000 in PBSBSA were added. Incubation was performed at 20°C for 2 h and after extensive washing, the reactivity of each mAb was revealed with the corresponding HRP conjugate.
Inhibitory effect of phage-peptide on recognition of C. albicans PPM by DJ2.8
The ability of the peptide to interfere with recognition of C. albicans by DJ2.8 was examined by indirect immunofluorescence using C. albicans yeast cells. MAb (diluted 1:300 in PBS) was incubated with serial dilutions of the peptide (0.33 mg/ml) at 20°C for 60 min. Fifty microliters of each dilution of the mixture were then incubated with C. albicans yeast cells coated on microscope slides. After incubation at 20°C for 90 min, the slides were washed with PBSBSA, incubated with a 1:100 dilution of the corresponding FITC-conjugated goat anti-Ig, washed again, and examined by direct microscopy.
The specificity of the inhibition of DJ2.8 recognition by the peptide was evaluated in an ELISA using C. albicans PPM. Briefly, DJ2.8 was incubated at 20°C for 2 h with different concentrations of peptide (0.11 mg/ml) in PBS supplemented with 0.5% milk and 0.05% Tween-20. The mixture was then added to wells coated with C. albicans PPM and saturated with PBS containing 5% milk. After incubation at 20°C for 2 h, the wells were washed and incubated with a 1:1000 dilution of HRP-conjugated anti-mouse IgM at 20°C for 1 h. The presence of bound mAb to PPM was measured by determining the absorbance at 450 nm.
Peptide immunization and specificity of anti-peptide-DJ polyclonal serum
Mice were immunized by intradermic injections of 200 µg of peptide coupled to 700 µg of KLH with complete (first injection) or incomplete (second injection) Freunds adjuvant. The antibody response of immunized mice was tested after 38 days. The recognition of C. albicans yeast cells by the antibodies was examined in an immunofluorescence assay and by ELISA using C. albicans PPM. The specificity of the polyclonal antibodies for anti-ß-1,2-linked mannosides was verified by inhibition of their reactivity against PPM with soluble ß-1,2-mannotetraose. Briefly, polyclonal antibodies were incubated with different concentrations of ß-1,2-mannotetraose at 20°C for 60 min. The mixtures were added to PPM-coated wells and incubated at 20°C for 90 min. After washing, bound antibodies were revealed with the corresponding HRP conjugate.
Densitometry
Autoradiograms were scanned and densitometry analyses were quantified on a Macintosh computer using the public domain NIH Image program (developed at the U.S. National Institute of Health and available on the Internet at http://rsb.info.nih.gov/nih-image/). Results were expressed as the mean ± SD of signal density in AUs.
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Acknowledgments |
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Abbreviations |
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Footnotes |
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References |
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