Abstract
The surface of microorganisms is covered with polysaccharide structures which are in immediate contact with receptor structures on host’s cells and antibodies. The interaction between microorganisms and their host is dependent on surface glycosylation and in this study we have tested the interaction of plant lectins with different microorganisms. Enzyme-linked lectin sorbent assay - ELLSA was used to test the binding of recombinant Musa acuminata lectin - BL to 27 selected microorganisms and 7 other lectins were used for comparison: Soy bean agglutinin - SBA, Lens culinaris lectin - LCA, Wheat germ agglutinin - WGA, RCA120 - Ricinus communis agglutinin, Con A - from Canavalia ensiformis, Sambucus nigra agglutinin - SNA I and Maackia amurensis agglutinin - MAA. The goal was to define the microorganisms’ surface glycosylation by means of interaction with the selected plant lectins and to make a comparison with BL. Among the tested lectins most selective binding was observed for RCA120 which preferentially bound Lactobacillus casei DG. Recombinant banana lectin showed specific binding to all of the tested fungal species. The binding of BL to Candida albicans was further tested with fluorescence microscopy and flow cytometry and it was concluded that this lectin can differentiate ß-glucan rich surfaces. The binding of BL to S. boulardii could be inhibited with ß-glucan from yeast with IC50 1.81 μg mL−1 and to P. roqueforti with 1.10 μg mL−1. This unique specificity of BL could be exploited for screening purposes and potentially for the detection of ß-glucan in solutions.
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References
Weintraub, A.: Immunology of bacterial polysaccharide antigens. Carbohydr. Res. (2003). https://doi.org/10.1016/j.carres.2003.07.008
Hirabayashi, J.: Concept, strategy and realization of lectin-based glycan profiling. J. Biochem. (2008). https://doi.org/10.1093/jb/mvn043
Kuno, A., Uchiyama, N., Koseki-Kuno, S., Ebe, Y., Takashima, S., Yamada, M., Hirabayashi, J.: Evanescent-field fluorescence-assisted lectin microarray: a new strategy for glycan profiling. Nat. Methods. (2005). https://doi.org/10.1038/nmeth803
Campanero-Rhodes, M.A., Llobetc, E., Bengoechea, J.A., Solís, D.: Bacteria microarrays as sensitive tool for exploring pathogen surface epitopes and recognition by host receptors. RSC Adv. (2015). https://doi.org/10.1039/C4RA14570D
Gao, J., Liu, D., Wang, Z.: Screening lectin-binding specificity of bacterium by lectin microarray with gold nanoparticle probes. Anal. Chem. (2010). https://doi.org/10.1021/ac1022309
Hirabayashi, J., Yamada, M., Kuno, A., Tateno, H.: Lectin microarrays: concept, principle and applications. Chem. Soc. Rev. (2013). https://doi.org/10.1039/c3cs35419a
Koshte, V.L., van Dijk, W., van der Stelt, M.E., Aalberse, R.C.: Isolation and characterisation of BanLec-I, a mannoside-binding lectin from Musa paradisiac (banana). Biochem. J. (1990). https://doi.org/10.1042/bj2720721
Gavrovic-Jankulovic, M., Poulsen, K., Brckalo, T., Bobic, S., Lindner, B., Petersen, A.: A novel recombinantly produced banana lectin isoform is a valuable tool for glycoproteomics and a potent modulator of the proliferation response in CD3+, CD4+, and CD8+ populations of human. PBMCs. Int. J. Biochem. Cell Biol. (2008). https://doi.org/10.1016/j.biocel.2007.10.033
Mo, H., Winter, H.C., Van Damme, E.J., Peumans, W.J., Misaki, A., Goldstein, I.J.: Carbohydrate binding properties of banana (Musa acuminata) lectin I. Novel recognition of internal alpha1,3-linked glucosyl residues. Eur. J. Biochem. (2001). https://doi.org/10.1046/j.1432-1327.2001.02148.x
Peumans, W.J., Zhang, W., Barre, A., Houles-Astoul, C., Balint-Kurti, P.J., Rovira, P., Rouge, P., May, G.D., Van Leuven, F., Truffa-Bachi, P., Van Damme, E.J.M.: Fruit-specific lectins from banana and plantain. Planta. (2000). https://doi.org/10.1007/s004250000307
Goldstein, I.J., Winter, H.C., Mo, H., Misaki, A., Van Damme, E.J., Peumans, W.J.: Carbohydrate binding properties of banana (Musa acuminata) lectin II. Binding of laminaribiose oligosaccharides and beta-glucans containing beta1,6-glucosyl end groups. Eur. J. Biochem. (2001). https://doi.org/10.1046/j.1432-1327.2001.02149.x
Winter, H.C., Oscarson, S., Slattegard, R., Tian, M., Goldstein, I.J.: Banana lectin is unique in its recognition of the reducing unit of 3-O-β-glucosyl/mannosyl disaccharides: a calorimetric study. Glycobiology. (2005). https://doi.org/10.1093/glycob/cwi074
Meagher, J.L., Winter, H.C., Ezell, P., Goldstein, I.J., Stuckey, J.A.: Crystal structure of banana lectin reveals a novel second sugar binding site. Glycobiology. (2005). https://doi.org/10.1093/glycob/cwi088
Singh, D.D., Saikrishnan, K., Kumar, P., Surolia, A., Sekar, K., Vijayan, M.: Unusual sugar specificity of banana lectin from Musa paradisiaca and its probable evolutionary origin. Crystallographic and modeling studies. Glycobiology. (2005). https://doi.org/10.1093/glycob/cwi087
Minić, R., Papić, Z., Đorđević, B., Michaličkova, D., Mathiesen, G., Živković, I., Pantic, V., Dimitrijevic, L.: Profiling of microorganism binding serum antibody specificities in professional athletes. PLoS One. (2018). https://doi.org/10.1371/journal.pone.0203665
LeVine, D., Kaplan, M.J., Greenaway, P.J.: The purification and characterization of wheat-germ agglutinin. Biochem. J. (1972). https://doi.org/10.1042/bj1290847
Young, N.M., Leon, M.A., Takahashi, T., Howard, I.K., Sage, H.J.: Studies on a phytohemagglutinin from the lentil. 3. Reaction of Lens culinaris hemagglutinin with polysaccharides, glycoproteins, and lymphocytes. J Biol Chem. 246(6), 1596–1601 (1971) Mar 25) http://www.jbc.org/content/246/6/1596
Rao, V.S., Lam, K., Qasba, P.K.: Three dimensional structure of the soybean agglutinin gal/GalNAc complexes by homology modeling. J. Biomol. Struct. Dyn. (1998). https://doi.org/10.1080/07391102.1998.10508207
Olsnes, S., Saltvedt, E., Pihl, A.: Isolation and comparison of galactose-binding lectins from Abrusprecatorius and Ricinuscommunis. J. Biol. Chem. Feb10. 249(3), 803–810 (1974)
Knibbs, R.N., Goldstein, I.J., Ratcliffe, R.M., Shibuya, N.: Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J. Biol. Chem. 266(1), 83–88 (1991) Jan 5)
Shibuya, N., Goldstein, I.J., Broekaert, W.F., Nsimba-Lubaki, M. Peeters, B., Peumans, W.J.: The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2–6)Gal/GalNAc sequence. J. Biol. Chem. (1987) Feb5; 262(4):1596–1601
Becker, J.W., Reeke Jr., G.N., Wang, J.L., Cunningham, B.A., Edelman, G.M.: The covalent and three-dimensional structure of concanavalin A. III. Structure of the monomer and its interactions with metals and saccharides. J. Biol. Chem. 250(4), 1513–1524 (1975) Feb 25)
Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the Folin phenol reagent. J. Biol. Chem.193, 265–275 (1951) May 28)
Chiani, P., Bromuro, C., Cassone, A., Torosantucci, A.: Anti-beta-glucan antibodies in healthy human subjects. Vaccine. (2009). https://doi.org/10.1016/j.vaccine.2008.11.030
Brown, G.D., Gordon, S.: Immune recognition of fungal beta-glucans. Cell Microbiol. (2005). https://doi.org/10.1111/j.1462-5822.2005.00505
de Groot, P.W., Kraneveld, E.A., Yin, Q.Y., Dekker, H.L., Gross, U., Crielaard, W., de Koster, C.G., Bader, O., Klis, F.M., Weig, M.: The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot. Cell. (2008). https://doi.org/10.1128/EC.00284-08
Gow, N.A., Hube, B.: Importance of the Candida albicans cell wall during commensalism and infection. Curr. Opin.Microbiol. (2012). https://doi.org/10.1016/j.mib.2012.04.005
Shibata, N., Suzuki, A., Kobayashi, H., Okawa, Y.: Chemical structure of the cell-wall mannan of Candida albicans serotype a and its difference in yeast and hyphal forms. Biochem. J. (2007). https://doi.org/10.1042/BJ20070081
Snarr, B.D., Qureshi, S.T., Sheppar, D.C.: Immune recognition of fungal polysaccharides. J. Fungi. (2017). https://doi.org/10.3390/jof3030047
Bain, J.M., Louw, J., Lewis, L.E., Okai, B., Walls, C.A., Ballou, E.R., Walker, L.A., Reid, D., Munro, C.A., Brown, A.J., Brown, G.D., Gow, N.A., Erwig, L.P.: Candida albicans hypha formation and mannan masking of β-glucan inhibit macrophage phagosome maturation. MBio. (2014). https://doi.org/10.1128/mBio.01874-14
Cambi, A., Netea, M.G., Mora-Montes, H.M., Gow, N.A.R., Hato, S.V., Lowman, D.W., Kullberg, B.J., Torensma, R., Williams, D.L., Figdor, C.G.: Dendritic cell interaction with Candida albicans critically depends on N-linked Mannan. J. Biol. Chem. (2008). https://doi.org/10.1074/jbc.M709334200
Netea, M.G., Gow, N.A., Munro, C.A., Bates, S., Collins, C., Ferwerda, G., Hobson, R.P., Bertram, G., Hughes, H.B., Jansen, T., Jacobs, L., Buurman, E.T., Gijzen, K., Williams, D.L., Torensma, R., McKinnon, A., MacCallum, D.M., Odds, F.C., Van der Meer, J.W., Brown, A.J., Kullberg, B.J.: Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and toll-like receptors. J. Clin. Invest. (2006). https://doi.org/10.1172/JCI27114
Vautier, S., MacCallum, D.M., Brown, G.D.: C-type lectin receptors and cytokines in fungal immunity. Cytokine. (2012). https://doi.org/10.1016/j.cyto.2011.08.031
Lillegard, J.B., Sim, R.B., Thorkildson, P., Gates, M.A., Kozel, T.R.: Recognition of Candida albicans by mannan-binding lectin in vitro and in vivo. J. Infect. Dis. (2006). https://doi.org/10.1086/503804
McIntosh, M., Stone, B.A., Stanisich, V.A.: Curdlan and other bacterial (1-->3)-beta-D-glucans. Appl. Microbiol. Biotechnol. (2005). https://doi.org/10.1007/s00253-005-1959-5
Yasuda, E., Tateno, H., Hirabayashi, J., Iino, T.: Sako, T:ectin microarray reveals binding profiles of Lactobacillus casei strains in a comprehensive analysis of bacterial cell wall polysaccharides. Appl. Environ. Microbiol. (2011). https://doi.org/10.1128/AEM.00240-11
Balzaretti, S., Taverniti, V., Guglielmetti, S., Fiore, W., Minuzzo, M., Ngo, H.N., Ngere, J.B., Sadoq, S., Humphreys, P.N., Laws, A.P.: A novel Rhamnose-rich hetero-exopolysaccharide isolated from Lactobacillus paracasei DG activates THP-1 human Monocytic cells. Appl. Environ. Microbiol. (2017). https://doi.org/10.1128/AEM.02702-16
Wu, A.M., Liu, J.H.: Lectins and ELLSA as powerful tools for glycoconjugate recognition analyses. Glycoconj. J. 36, 175–183 (2019). https://doi.org/10.1007/s10719-019-09865-3
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This work is supported by Ministry of Education, Science and Technological Development of the Republic of Serbia (Project No. OI 172049 and III 46009). The authors thank Ivan Minic for graphical assistance.
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Rajna Minic, Vesna Ilic and Marija Gavrovic-Jankulovic made substantial contributions to conception and design of the study. Material preparation and data collection was done by Luka Dragacevic and Danijela Kanazir. Data analysis and interpretation was done by all authors. The first draft of the manuscript was written by Rajna Minic and Luka Dragacevic, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Dragacevic, L., Djordjevic, B., Gavrovic-Jankulovic, M. et al. ELLSA based profiling of surface glycosylation in microorganisms reveals that ß-glucan rich yeasts’ surfaces are selectively recognized with recombinant banana lectin. Glycoconj J 37, 95–105 (2020). https://doi.org/10.1007/s10719-019-09898-8
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DOI: https://doi.org/10.1007/s10719-019-09898-8