Maillard neoglycans as inhibitors for in vitro adhesion of F4+ of enterotoxigenic Escherichia coli to piglet intestinal cells
Abstract
ABSTRACT
Adhesion of enterotoxigenic (ETEC) E. coli to host intestinal cells is mediated by lectin-like fimbriae that bind to specific glycan moieties on the surfaces of enterocytes. To prevent in vitro binding of E. coli F4 fimbriae (F4 ETEC+) to piglet enterocytes, neoglycans were synthesized by the Maillard reaction conjugating lactose (Lac), galacto-oligosaccharides (GOS) or chitin oligosaccharides (Ochit) to porcine serum albumin (PSA). Neoglycans were characterized by SDS-PAGE, intrinsic tryptophan fluorescence and recognition by plant lectins, as well as by F4 ETEC variants. Electrophoretic patterns suggested the binding to PSA of 63, 13 and 2 molecules of Lac, GOS and Ochit, respectively. All neoglycans showed quenching of tryptophan fluorescence consistent with the degree of glycation estimated by SDS-PAGE. Plant lectins recognized the neoglycans according to their specificity, whereas antigenic variants of F4 ETEC (ab, ac and ad) recognized PSA-Ochit and PSA-Lac with higher affinity than that for GOS. The neoglycans partially hindered the ex vivo binding of F4+ ETEC to piglet enterocytes in a dose-dependent manner. The most effective blocking was observed with PSA-Lac that partially inhibited the adhesion of bacteria to enterocytes in a dose dependent manner as quantified by flow cytometry. Increased production of the cytokines IL-6 and TNF-α was observed in response to F4+ ETEC infection of enterocytes and production was reduced in the presence of PSA-Ochit and PSA-GOS. These results suggest that neoglycans synthesized by the Maillard reaction could be useful in the prophylaxis of diarrhea in piglets.
References
Chun SH, Lee HA, Lee KB, Kim SH, Park KY, Lee KW (2016) Effects of glycated whey protein concentrate on proinflammatory cytokine expression and phagocytic activity in RAW264.7 macrophages. Biol Pharm Bull 39:199-206. http://doi.org/10.1248/bpb.b15-00596
Devriendt B, Stuyven E, Verdonck F, Goddeeris BM, Cox E (2010) Enterotoxigenic Escherichia coli (K88) induce proinflammatory responses in porcine intestinal epithelial cells. Dev Comp Immunol 34:1175-1182. http://doi.org/10.1016/j.dci.2010.06.009
Dubreuil JD, Isaacson RE, Schifferli DM (2016) Animal enterotoxigenic Escherichia coli. EcoSal Plus 7: 10.1128/ecosalplus.ESP-0006-2016.
http://doi.org/10.1128/ecosalplus.ESP-0006-2016
Gonzalez-Ortiz G, Hermes RG, Jimenez-Diaz R, Perez JF, Martin-Orue SM (2013) Screening of extracts from natural feed ingredients for their ability to reduce enterotoxigenic Escherichia coli (ETEC) K88 adhesion to porcine intestinal epithelial cell-line IPEC-J2. Vet Microbiol 167:494-499. http://doi.org/10.1016/j.vetmic.2013.07.035
Grange PA, Erickson AK, Levery SB, Francis DH (1999) Identification of an intestinal neutral glycosphingolipid as a phenotype-specific receptor for the K88ad fimbrial adhesin of Escherichia coli. Infect Immun 67:165-172.
Grange PA, Mouricout MA, Levery SB, Francis DH, Erickson AK (2002) Evaluation of receptor binding specificity of Escherichia coli K88 (F4) fimbrial adhesin variants using porcine serum transferrin and glycosphingolipids as model receptors. Infect Immun 70:2336-2343.
Hermes RG, Manzanilla EG, Martin-Orue SM, Perez JF, Klasing KC (2011) Influence of dietary ingredients on in vitro inflammatory response of intestinal porcine epithelial cells challenged by an enterotoxigenic Escherichia coli (K88). Comp Immunol Microbiol Infect Dis 34:479-488. http://doi.org/10.1016/j.cimid.2011.08.006
Ledesma-Osuna AI, Ramos-Clamont G, Vazquez-Moreno L (2008) Characterization of bovine serum albumin glycated with glucose, galactose, and lactose. Acta Biochim Pol 55:491-497.
Ledesma-Osuna AI, Ramos-Clamont G, Guzman-Partida AM, Vazquez-Moreno L (2010) Conjugates of bovine serum albumin with chitin oligosaccharides prepared through the Maillard reaction. J Agric Food Chem 58:12000-12005. http://doi.org/10.1021/jf102869f
Lu S, Yao Y, Meng S, Cheng X, Black DD (2002) Overexpression of apolipoprotein A-IV enhances lipid transport in newborn swine intestinal epithelial cells. J Biol Chem 277:31929-31937. http://doi.org/10.1074/jbc.M201418200
Moonens K, Van den Broeck I, De Kerpel M, Deboeck F, Raymaekers H, Remaut H, De Greve H (2015) Structural and functional insight into the carbohydrate receptor binding of F4 fimbriae-producing enterotoxigenic Escherichia coli. J Biol Chem 290:8409-8419. http://doi.org/10.1074/jbc.M114.618595
Nagy B, Fekete PZ (2005) Enterotoxigenic Escherichia coli in veterinary medicine. Int J Med Microbiol 295:443-454. http://doi.org/10.1016/j.ijmm.2005.07.003
Nishibata T, Tashiro K, Kanahori S, Hashizume C, Kitagawa M, Okuma K, Gordon DT (2009) Comprehensive measurement of total non-digestible carbohydrates in foods by enzymatic-gravimetric method and liquid chromatography. J Agric Food Chem 57:7659-7665. http://doi.org/10.1021/jf9010565
Payne D, O'Reilly M, Williamson D (1993) The K88 fimbrial adhesin of enterotoxigenic Escherichia coli binds to beta 1-linked galactosyl residues in glycosphingolipids. Infect Immun 61:3673-3677.
Qadri F, Svennerholm AM, Faruque AS, Sack RB (2005) Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin Microbiol Rev 18:465-483. http://doi.org/10.1128/CMR.18.3.465-483.2005
Sarabia-Sainz AI, Ramos-Clamont G, Winzerling J, Vazquez-Moreno L (2011) Bacterial recognition of thermal glycation products derived from porcine serum albumin with lactose. Acta Biochim Pol 58:95-100.
Sarabia-Sainz HM, Armenta-Ruiz C, Sarabia-Sainz JA-i, Guzmán-Partida AM, Ledesma-Osuna AI, Vázquez-Moreno L, Ramos-Clamont Montfort G (2013) Adhesion of enterotoxigenic Escherichia coli strains to neoglycans synthesized with prebiotic galactooligosaccharides. Food Chemistry 141:2727-2734. http://dx.doi.org/10.1016/j.foodchem.2013.05.040
Sattin S, Bernardi A (2016) Glycoconjugates and glycomimetics as microbial anti-adhesives. Trends Biotechnol 34:483-495. http://doi.org/10.1016/j.tibtech.2016.01.004
Schierack P, Nordhoff M, Pollmann M, Weyrauch KD, Amasheh S, Lodemann U, Jores J, Tachu B, Kleta S, Blikslager A, Tedin K, Wieler LH (2006) Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem Cell Biol 125:293-305. http://doi.org/10.1007/s00418-005-0067-z
Sharon N (2006) Carbohydrates as future anti-adhesion drugs for infectious diseases. Biochim Biophys Acta 1760:527-537. http://doi.org/10.1016/j.bbagen.2005.12.008
Torres DPM, Gonçalves MdPF, Teixeira JA, Rodrigues LR (2010) Galacto-oligosaccharides: Production, properties, applications, and significance as prebiotics. Comprehensive Reviews in Food Science and Food Safety 9:438-454. http://doi.org/10.1111/j.1541-4337.2010.00119.x
Vendrig JC, Coffeng LE, Fink-Gremmels J (2014) Effects of orally administered galacto-oligosaccharides on immunological parameters in foals: a pilot study. BMC Vet Res 10:278. http://doi.org/10.1186/s12917-014-0278-4
Verdonck F, Cox E, Vancaeneghem S, Goddeeris BM (2004) The interaction of F4 fimbriae with porcine enterocytes as analyzed by surface plasmon resonance. FEMS Immunol Med Microbiol 41:243-248. http://doi.org/10.1016/j.femsim.2004.03.009
Verdonck F, Joensuu JJ, Stuyven E, De Meyer J, Muilu M, Pirhonen M, Goddeeris BM, Mast J, Niklander-Teeri V, Cox E (2008) The polymeric stability of the Escherichia coli F4 (K88) fimbriae enhances its mucosal immunogenicity following oral immunization. Vaccine 26:5728-5735. http://doi.org/10.1016/j.vaccine.2008.08.017
Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR (2008) Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharides mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr 88:1438-1446.
Wagener J, Malireddi RK, Lenardon MD, Koberle M, Vautier S, MacCallum DM, Biedermann T, Schaller M, Netea MG, Kanneganti TD, Brown GD, Brown AJ, Gow NA (2014) Fungal chitin dampens inflammation through IL-10 induction mediated by NOD2 and TLR9 activation. PLoS Pathog 10: e1004050. http://doi.org/10.1371/journal.ppat.1004050
Watts RE, Tan CK, Ulett GC, Carey AJ, Totsika M, Idris A, Paton AW, Morona R, Paton JC, Schembri MA (2012) Escherichia coli 83972 expressing a P fimbriae oligosaccharide receptor mimic impairs adhesion of uropathogenic E. coli. J Infect Dis 206:1242-1249. http://doi.org/10.1093/infdis/jis493
Westwood ME, Thornalley PJ (1995) Molecular characteristics of methylglyoxal-modified bovine and human serum albumins. Comparison with glucose-derived advanced glycation end product-modified serum albumins. J Protein Chem 14:359-372.
Wooster TJ, Augustin MA (2006) Beta-lactoglobulin-dextran Maillard conjugates: their effect on interfacial thickness and emulsion stability. J Colloid Interface Sci 303:564-572. http://doi.org/10.1016/j.jcis.2006.07.081
Wu AM, Wu JH, Singh T, Lai LJ, Yang Z, Herp A (2006) Recognition factors of Ricinus communis agglutinin 1 (RCA1). Mol Immunol 43:1700-1715.
http://doi.org/10.1016/j.molimm.2005.09.008
Zhang W, Fang Y, Francis DH (2009) Characterization of the binding specificity of K88ac and K88ad fimbriae of enterotoxigenic Escherichia coli by constructing K88ac/K88ad chimeric FaeG major subunits. Infect Immun 77:699-706. http://doi.org/10.1128/IAI.01165-08
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