Fimbriae are long, proteinaceous adhesion organelles expressed on the bacterial envelope, evolutionarily adapted by Escherichia coli strains for the colonization of epithelial linings. Using glycan arrays of the Consortium for Functional Glycomics (CFG), the lectin domains were screened of the fimbrial adhesins F17G and FedF from enterotoxigenic E. coli (ETEC) and of the FimH adhesin from uropathogenic E. coli. This has led to the discovery of a more specific receptor for F17G, GlcNAcb1,3Gal. No significant differences emerged from the glycan binding profiles of the F17G lectin domains from five different E. coli strains. However, strain-dependent amino acid variations, predominantly towards the positively charged arginine, were indicated by sulfate binding in FedF and F17G crystal structures. For FedF, no significant binders could be observed on the CFG glycan array. Hence, a shotgun array was generated from microvilli scrapings of the distal jejunum of a 3-week old piglet about to be weaned. On this array, the blood group A type 1 hexasaccharide emerged as a receptor for the FedF lectin domain and remarkably also for F18-fimbriated E. coli. F17G was found to selectively recognize glycan species with a terminal GlcNAc, typifying intestinal mucins. In conclusion, F17G and FedF recognize long glycan sequences that could only be identified using the shotgun approach. Interestingly, ETEC strains display a large capacity to adapt their fimbrial adhesins to ecological niches via charge-driven interactions, congruent with binding to thick mucosal surfaces displaying an acidic gradient along the intestinal tract.
References
[1]
Kapitany, R.A.; Forsyth, G.W.; Scoot, A.; Mckenzie, S.F.; Worthington, R.W. Isolation and Partial Characterization of 2 Different Heat-Stable Enterotoxins Produced by Bovine and Porcine Strains of Enterotoxigenic Escherichia coli. Infect. Immun. 1979, 26, 173–177.
[2]
Lintermans, P.F.; Pohl, P.; Bertels, A.; Charlier, G.; Vandekerckhove, J.; van Damme, J.; Shoup, J.; Schlicker, C.; Korhonen, T.; de Greve, H.; et al. Characterization and purification of the F17 adhesin on the surface of bovine enteropathogenic and septicemic Escherichia coli. Am. J. Vet. Res. 1988, 49, 1794–1799.
[3]
Hahn, E.; Wild, P.; Schraner, E.M.; Bertschinger, H.U.; Haner, M.; Muller, S.A.; Aebi, U. Structural analysis of F18 fimbriae expressed by porcine toxigenic Escherichia coli. J. Struct. Biol. 2000, 132, 241–250, doi:10.1006/jsbi.2000.4323.
[4]
Choudhury, D.; Thompson, A.; Stojanoff, V.; Langermann, S.; Pinkner, J.; Hultgren, S.J.; Knight, S.D. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 1999, 285, 1061–1066, doi:10.1126/science.285.5430.1061.
[5]
Lintermans, P.; Pohl, P.; Deboeck, F.; Bertels, A.; Schlicker, C.; Vandekerckhove, J.; Vandamme, J.; Vanmontagu, M.; DeGreve, H. Isolation and Nucleotide-Sequence of the F17-A Gene Encoding the Structural Protein of the F-17 Fimbriae in Bovine Entero-Toxigenic Escherichia coli. Infect. Immun. 1988, 56, 1475–1484.
[6]
Lintermans, P.F.; Bertels, A.; Schlicker, C.; Deboeck, F.; Charlier, G.; Pohl, P.; Norgren, M.; Normark, S.; van Montagu, M.; de Greve, H. Identification, characterization, and nucleotide sequence of the F17-G gene, which determines receptor binding of Escherichia coli F17 fimbriae. J. Bacteriol. 1991, 173, 3366–3373.
[7]
Smeds, A.; Hemmann, K.; Jakava-Viljanen, M.; Pelkonen, S.; Imberechts, H.; Palva, A. Characterization of the adhesin of Escherichia coli F18 fimbriae. Infect. Immun. 2001, 69, 7941–7945, doi:10.1128/IAI.69.12.7941-7945.2001.
[8]
Knight, S.D.; Bouckaert, J. Structure, function, and assembly of Type 1 fimbriae. Top. Curr. Chem. 2009, 288, 67–107, doi:10.1007/128_2008_13.
[9]
Westerlund-Wikstr？m, B.; Korhonen, T.K. Molecular structure of adhesin domains in Escherichia coli fimbriae. Int. J. Med. Microbiol. 2005, 295, 479–486, doi:10.1016/j.ijmm.2005.06.010.
[10]
De Greve, H.; Wyns, L.; Bouckaert, J. Combining sites of bacterial fimbriae. Curr. Opin. Struct. Biol. 2007, 17, 506–512, doi:10.1016/j.sbi.2007.06.011.
[11]
Bouckaert, J.; Mackenzie, J.; de Paz, J.L.; Chipwaza, B.; Choudhury, D.; Zavialov, A.; Mannerstedt, K.; Anderson, J.; Pierard, D.; Wyns, L.; et al. The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol. Microbiol. 2006, 61, 1556–1568, doi:10.1111/j.1365-2958.2006.05352.x.
[12]
Bertin, Y.; Girardeau, J.P.; Darfeuille-Michaud, A.; Contrepois, M. Characterization of 20K fimbria, a new adhesin of septicemic and diarrhea-associated Escherichia coli strains, that belongs to a family of adhesins with N-acetyl d-glucosamine recognition. Infect. Immun. 1996, 64, 332–342.
[13]
Bertin, Y.; Martin, C.; Oswald, E.; Girardeau, J.P. Rapid and specific detection of F17-related pilin and adhesin genes in diarrheic and septicemic Escherichia coli strains by multiplex PCR. J. Clin. Microbiol. 1996, 34, 2921–2928.
[14]
El Mazouari, K.; Oswald, E.; Hernalsteens, J.-P.; Lintermans, P.; de Greve, H. F-17-like fimbriae from an invasive Escherichia coli strain producing cytotoxic necrotizing factor type-2 toxin. Infect. Immun. 1994, 62, 2633–2638.
[15]
Cid, D.; Sanz, R.; Marín, I.; de Greve, H.; Ruis-Santa-Quiteria, J.A.; Amils, R.; de la Fuente, R. Characterization of nonenterotoxigenic Escherichia coli strains producing F17 fimbriae isolated from diarrheic lambs and goat kids. J. Clin. Microbiol. 1999, 37, 1370–1375.
[16]
Buts, L.; Wellens, A.; van Molle, I.; Wyns, L.; Loris, R.; Lahmann, M.; Oscarson, S.; de Greve, H.; Bouckaert, J. Impact of natural variation in bacterial F17G adhesins on crystallization behaviour. Acta Crystallogr. D Biol. Crystallogr. 2005, 61, 1149–1159, doi:10.1107/S0907444905017038.
[17]
Merckel, M.C.; Tanskanen, J.; Edelman, S.; Westerlund-Wikstrom, B.; Korhonen, T.K.; Goldman, A. The structural basis of receptor-binding by Escherichia coli associated with diarrhea and septicemia. J. Mol. Biol. 2003, 331, 897–905, doi:10.1016/S0022-2836(03)00841-6.
[18]
Buts, L.; Bouckaert, J.; de Genst, E.; Loris, R.; Oscarson, S.; Lahmann, M.; Messens, J.; Brosens, E.; Wyns, L.; de Greve, H. The fimbrial adhesin F17-G of enterotoxigenic Escherichia coli has an immunoglobulin-like lectin domain that binds N-acetylglucosamine. Mol. Microbiol. 2003, 49, 705–715.
[19]
Imberechts, H.; Wild, P.; Charlier, G.; DeGreve, H.; Lintermans, P.; Pohl, P. Characterization of F18 fimbrial genes fedE and fedF involved in adhesion and length of enterotoxemic Escherichia coli strain 107/86. Microb. Pathog. 1996, 21, 183–192, doi:10.1006/mpat.1996.0053.
[20]
Blixt, O.; Head, S.; Mondala, T.; Scanlan, C.; Huflejt, M.E.; Alvarez, R.; Bryan, M.C.; Fazio, F.; Calarese, D.; Stevens, J.; et al. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. USA 2004, 101, 17033–17038, doi:10.1073/pnas.0407902101.
[21]
De Boer, A.R.; Hokke, C.H.; Deelder, A.M.; Wuhrer, M. General Microarray Technique for Immobilization and Screening of Natural Glycans. Anal. Chem. 2007, 79, 8107–8113, doi:10.1021/ac071187g.
Lonardi, E.; Deelder, A.M.; Wuhrer, M.; Balog, C.I. Microarray technology using glycans extracted from natural sources for serum antibody fluorescent detection. Methods Mol. Biol. 2012, 808, 285–302, doi:10.1007/978-1-61779-373-8_20.
[24]
De Kerpel, M.; van Molle, I.; Brys, L.; Wyns, L.; de Greve, H.; Bouckaert, J. N-terminal truncation enables crystallization of the receptor-binding domain of the FedF bacterial adhesin. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2006, 62, 1278–1282, doi:10.1107/S1744309106049281.
[25]
Moonens, K.; Bouckaert, J.; Coddens, A.; Tran, T.; Panjikar, S.; de Kerpel, M.; Cox, E.; Remaut, H.; de Greve, H. Structural insight in histo-blood group binding by the F18 fimbrial adhesin FedF. Mol. Microbiol. 2012, 86, 82–95, doi:10.1111/j.1365-2958.2012.08174.x.
[26]
Wellens, A.; Garofalo, C.; Nguyen, H.; van Gerven, N.; Slattegard, R.; Hernalsteens, J.P.; Wyns, L.; Oscarson, S.; de Greve, H.; Hultgren, S.; et al. Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS One 2008, 3, e2040, doi:10.1371/journal.pone.0002040.
[27]
CFG Functional Glycomics Gateway, Glycan Array Data. Available online: http://www.functionalglycomics.org/glycomics/publicdata/primaryscreen.jsp/ (accessed on 10 September 2010).
[28]
Cirla, A.; McHale, A.R.; Mann, J. Synthesis of analogues of calicheamicin and neocarzinostatin chromophore. Tetrahedron 2004, 60, 4019–4029, doi:10.1016/j.tet.2004.03.021.
[29]
Wang, H.; She, J.; Zhang, L.H.; Ye, X.S. Silver(I) oxide mediated selective monoprotection of diols in pyranosides. J. Org. Chem. 2004, 69, 5774–5777, doi:10.1021/jo0497252.
Garegg, P.J.; Oscarson, S. Synthesis of 6- and 6'-deoxy derivatives of methyl 4-O-a-galactopyranosyl-？-galactopyranoside for studies of inhibition of pyelonephritogenic fimbriated E. coli adhesion to urinary epithelium-cell surfaces. Carbohydr. Res. 1985, 137, 270–275, doi:10.1016/0008-6215(85)85169-7.
[32]
Valdor, J.F.; Mackie, W. Synthesis of a trisaccharide repeating unit related to arabinogalactan-protein (AGP) polysaccharides. J. Carbohydr. Chem. 1997, 16, 429–440, doi:10.1080/07328309708007326.
[33]
Kajihara, Y.; Kodama, H.; Endo, T.; Hashimoto, H. Novel features of acceptor recognition by ？-(1-4)-galactosyltransferase. Carbohydr. Res. 1998, 306, 361–378, doi:10.1016/S0008-6215(97)10093-3.
Wuhrer, M.; Koeleman, C.A.; Hokke, C.H.; Deelder, A.M. Mass spectrometry of proton adducts of fucosylated N-glycans: Fucose transfer between antennae gives rise to misleading fragments. Rapid Commun. Mass Spectrom. 2006, 20, 1747–1754, doi:10.1002/rcm.2509.
[36]
Taganna, J.; de Boer, A.R.; Wuhrer, M.; Bouckaert, J. Glycosylation changes as important factors for the susceptibility to urinary tract infection. Biochem. Soc. Trans. 2011, 39, 349–354, doi:10.1042/BST0390349.
[37]
Dauter, M.; Dauter, Z. Phase determination using halide ions. Methods Mol. Biol. 2007, 364, 149–158.
[38]
Coddens, A.; Diswall, M.; Angstrom, J.; Breimer, M.E.; Goddeeris, B.; Cox, E.; Teneberg, S. Recognition of blood group ABH type 1 determinants by the FedF adhesin of F18-fimbriated Escherichia coli. J. Biol. Chem. 2009, 284, 9713–9726, doi:10.1074/jbc.M807866200.
[39]
Meijerink, E.; Neuenschwander, S.; Fries, R.; Dinter, A.; Bertschinger, H.U.; Stranzinger, G.; Vogeli, P. A DNA polymorphism influencing alpha(1,2)fucosyltransferase activity of the pig FUT1 enzyme determines susceptibility of small intestinal epithelium to Escherichia coli F18 adhesion. Immunogenetics 2000, 52, 129–136, doi:10.1007/s002510000263.
[40]
Hung, C.-S.; Bouckaert, J.; Hung, D.L.; Pinkner, J.; Winberg, C.; Defusco, A.; Auguste, C.G.; Strouse, R.; Langermann, S.; Waksman, G.; et al. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 2002, 44, 903–915, doi:10.1046/j.1365-2958.2002.02915.x.
[41]
Mouricout, M.A.; Julien, R.A. Pilus-mediated binding of bovine enterotoxigenic Escherichia coli to calf small intestinal mucins. Infect. Immun. 1987, 55, 1216–1223.
[42]
Stgeme, J.W.; Cutter, D. Evidence That Surface Fibrils Expressed by Haemophilus-Influenzae Type-B Promote Attachment to Human Epithelial-Cells. Mol. Microbiol. 1995, 15, 77–85, doi:10.1111/j.1365-2958.1995.tb02222.x.
Berenson, C.S.; Sayles, K.B.; Huang, J.; Reinhold, V.N.; Garlipp, M.A.; Yohe, H.C. Nontypeable Haemophilus influenzae-binding gangliosides of human respiratory (HEp-2) cells have a requisite lacto/neolacto core structure. FEMS Immunol. Med. Microbiol. 2005, 45, 171–182, doi:10.1016/j.femsim.2005.03.007.
[45]
Mouricout, M.; Milhavet, M.; Durie, C.; Grange, P. Characterization of glycoprotein glycan receptors for Escherichia coli F17 fimbrial lectin. Microb. Pathog. 1995, 18, 297–306, doi:10.1016/S0882-4010(05)80006-3.
[46]
Vercoutter-Edouart, A.S.; Slomianny, M.C.; Dekeyzer-Beseme, O.; Haeuw, J.F.; Michalski, J.C. Glycoproteomics and glycomics investigation of membrane N-glycosylproteins from human colon carcinoma cells. Proteomics 2008, 8, 3236–3256, doi:10.1002/pmic.200800151.
[47]
Salo, H.; Aitio, O.; Ilves, K.; Bencomo, E.; Toivonen, S.; Penttila, L.; Niemela, R.; Salminen, H.; Grabenhorst, E.; Renkonen, R.; et al. Several polylactosamine-modifying glycosyltransferases also use internal GalNAcbeta1-4GlcNAc units of synthetic saccharides as acceptors. Glycobiology 2002, 12, 217–228, doi:10.1093/glycob/12.3.217.
[48]
Dam, T.K.; Brewer, C.F. Lectins as pattern recognition molecules: The effects of epitope density in innate immunity. Glycobiology 2010, 20, 270–279, doi:10.1093/glycob/cwp186.
[49]
Robbe, C.; Capon, C.; Maes, E.; Rousset, M.; Zweibaum, A.; Zanetta, J.P.; Michalski, J.C. Evidence of regio-specific glycosylation in human intestinal mucins: Presence of an acidic gradient along the intestinal tract. J. Biol. Chem. 2003, 278, 46337–46348.
[50]
Robbe, C.; Capon, C.; Coddeville, B.; Michalski, J.C. Diagnostic ions for the rapid analysis by nano-electrospray ionization quadrupole time-of-flight mass spectrometry of O-glycans from human mucins. Rapid Commun. Mass Spectrom. 2004, 18, 412–420, doi:10.1002/rcm.1352.
[51]
Teneberg, S.; Willemsen, P.T.; de Graaf, F.K.; Stenhagen, G.; Pimlott, W.; Jovall, P.A.; Angstrom, J.; Karlsson, K.A. Characterization of gangliosides of epithelial cells of calf small intestine, with special reference to receptor-active sequences for enteropathogenic Escherichia coli K99. J. Biochem. 1994, 116, 560–574.
[52]
Bouckaert, J.; Hamelryck, T.; Wyns, L.; Loris, R. Novel structures of plant lectins and their complexes with carbohydrates. Curr. Opin. Struct. Biol. 1999, 9, 572–577, doi:10.1016/S0959-440X(99)00007-X.
