Secretory IgA N-glycans contribute to the protection against E. coli O55 infection of germ-free piglets
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32973324
PubMed Central
PMC7946640
DOI
10.1038/s41385-020-00345-8
PII: S1933-0219(22)00150-7
Knihovny.cz E-zdroje
- MeSH
- aglutinace MeSH
- Escherichia coli fyziologie MeSH
- glykosylace MeSH
- gnotobiologické modely MeSH
- imunoglobulin A sekreční metabolismus MeSH
- imunoglobuliny - Fab fragmenty metabolismus MeSH
- infekce vyvolané Escherichia coli imunologie MeSH
- jednořetězcové protilátky metabolismus MeSH
- novorozená zvířata MeSH
- odolnost vůči nemocem MeSH
- polysacharidy metabolismus MeSH
- prasata MeSH
- těhotenství MeSH
- zvířata MeSH
- Check Tag
- těhotenství MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- imunoglobulin A sekreční MeSH
- imunoglobuliny - Fab fragmenty MeSH
- jednořetězcové protilátky MeSH
- polysacharidy MeSH
Mucosal surfaces are colonized by highly diverse commensal microbiota. Coating with secretory IgA (SIgA) promotes the survival of commensal bacteria while it inhibits the invasion by pathogens. Bacterial coating could be mediated by antigen-specific SIgA recognition, polyreactivity, and/or by the SIgA-associated glycans. In contrast to many in vitro studies, only a few reported the effect of SIgA glycans in vivo. Here, we used a germ-free antibody-free newborn piglets model to compare the protective effect of SIgA, SIgA with enzymatically removed N-glycans, Fab, and Fc containing the secretory component (Fc-SC) during oral necrotoxigenic E. coli O55 challenge. SIgA, Fab, and Fc-SC were protective, whereas removal of N-glycans from SIgA reduced SIgA-mediated protection as demonstrated by piglets' intestinal histology, clinical status, and survival. In vitro analyses indicated that deglycosylation of SIgA did not reduce agglutination of E. coli O55. These findings highlight the role of SIgA-associated N-glycans in protection. Further structural studies of SIgA-associated glycans would lead to the identification of those involved in the species-specific inhibition of attachment to corresponding epithelial cells.
Department of Microbiology University of Alabama at Birmingham Birmingham AL USA
Department of Surgery University of Alabama at Birmingham Birmingham AL USA
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Rinninella E, et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019;7:1–22. PubMed PMC
Pabst O, Slack E. IgA and the intestinal microbiota: the importance of being specific. Mucosal Immunol. 2020;13:12–21. PubMed PMC
Macpherson AJ, Yilmaz B, Limenitakis JP, Ganal-Vonarburg SC. IgA function in relation to the intestinal microbiota. Annu. Rev. Immunol. 2018;36:359–381. PubMed
Bunker JJ, Bendelac A. IgA responses to microbiota. Immunity. 2018;49:211–224. PubMed PMC
Bunker JJ, et al. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity. 2015;43:541–553. PubMed PMC
Sterlin D, et al. Human IgA binds a diverse array of commensal bacteria. J. Exp. Med. 2020;217:e20181635. PubMed PMC
Mestecky, J. Protective activities of mucosal antibodies. in Mucosal Vaccines 2nd edn (eds. Kiyono, H., Pascual, D. W.) 71–84 (Elsevier, Academic Press, Amsterdam, 2020).
Mestecky J, Russell MW. Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol. Lett. 2009;124:57–62. PubMed PMC
Royle L, et al. Secretory IgA N and O-glycans provide a link between the innate and adaptive immune systems. J. Biol. Chem. 2003;278:20140–20153. PubMed
Mathias A, Corthesy B. N-glycans on secretory component: Mediators of the interaction between secretory IgA and gram-positive commensals sustaining intestinal homeostasis. Gut Microbes. 2011;2:287–293. PubMed
Hooper LV, Gordon JI. Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology. 2001;11:1R–10R. PubMed
Anthony BF, Concepcion NF, Puentes SM, Payne NR. Nonimmune binding of human immunoglobulin A to type II group B streptococci. Infect. Immun. 1990;58:1789–1795. PubMed PMC
Giugliano LG, Ribeiro ST, Vainstein MH, Ulhoa CJ. Free secretory component and lactoferrin of human milk inhibit the adhesion of enterotoxigenic Escherichia coli. J. Med. Microbiol. 1995;42:3–9. PubMed
Perrier C, Sprenger N, Corthesy B. Glycans on secretory component participate in innate protection against mucosal pathogens. J. Biol. Chem. 2006;281:14280–14287. PubMed
Korhonen TK, et al. Escherichia coli fimbriae recognizing sialyl galactosides. J. Bacteriol. 1984;159:762–766. PubMed PMC
Fernandez C, Alarcon-Riquelme ME, Sverremark E. Polyreactive binding of antibodies generated by polyclonal B cell activation. II. Crossreactive and monospecific antibodies can be generated from an identical Ig rearrangement by differential glycosylation. Scand. J. Immunol. 1997;45:240–247. PubMed
Russell, M. W. & Kilian, M. Biological activities of IgA. in Mucosal immunology 4th edn (eds. Mestecky, J., Strober, W., Russell, M. W., Kelsall, B. L., Cheroutre, H., Lambrecht, B. N.) 429-454 (Elsevier, Academic Press, Amsterdam, 2015).
Sterlin D, Fadlallah J, Slack E, Gorochov G. The antibody/microbiota interface in health and disease. Mucosal Immunol. 2020;13:3–11. PubMed
Wold AE, Mestecky J, Svanborg Eden C. Agglutination of E. coli by secretory IgA–a result of interaction between bacterial mannose-specific adhesins and immunoglobulin carbohydrate? Monogr. Allergy. 1988;24:307–309. PubMed
Wold AE, et al. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect. Immun. 1990;58:3073–3077. PubMed PMC
Wold AE, Motas C, Svanborg C, Mestecky J. Lectin receptors on IgA isotypes. Scand. J. Immunol. 1994;39:195–201. PubMed
Wold AE, Thorssen M, Hull S, Eden CS. Attachment of Escherichia coli via mannose- or Galα1→4Galβ-containing receptors to human colonic epithelial cells. Infect. Immun. 1988;56:2531–2537. PubMed PMC
Crago SS, Kulhavy R, Prince SJ, Mestecky J. Secretory component of epithelial cells is a surface receptor for polymeric immunoglobulins. J. Exp. Med. 1978;147:1832–1837. PubMed PMC
Schroten H, et al. Fab-independent antiadhesion effects of secretory immunoglobulin A on s-fimbriated Escherichia coli are mediated by sialyloligosaccharides. Infect. Immun. 1998;66:3971–3973. PubMed PMC
Mestecky J, Russell MW, Elson CO. Intestinal IgA: Novel views on its function in the defence of the largest mucosal surface. Gut. 1999;44:2–5. PubMed PMC
Novak J, et al. Heterogeneity of O-glycosylation in the hinge region of human IgA1. Mol. Immunol. 2000;37:1047–1056. PubMed
Takahashi K, et al. Clustered O-glycans of IgA1: defining macro- and microheterogeneity by use of electron capture/transfer dissociation. Mol. Cell. Proteom. 2010;9:2545–2557. PubMed PMC
Franc V, et al. Elucidating heterogeneity of IgA1 hinge-region O-glycosylation by use of maldi-tof/tof mass spectrometry: role of cysteine alkylation during sample processing. J. Proteom. 2013;92:299–312. PubMed PMC
Phalipon A, et al. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity. 2002;17:107–115. PubMed
Sterzl J, Rejnek J, Travnicek J. Impermeability of pig placenta for antibodies. Folia Microbiol. (Praha) 1966;11:7–10. PubMed
Sinkora M, Butler JE. Progress in the use of swine in developmental immunology of B and T lymphocytes. Dev. Comp. Immunol. 2016;58:1–17. PubMed
Trebichavsky I, Dlabac V, Rehakova Z. Effect of peroral anti-bacterial antiserum treatment on intestinal immune parameters of germ-free piglets intragastrically infected with virulent Salmonella typhimurium or enteropathogenic E.coli. Vet. Immunol. Immunopathol. 1999;67:55–65. PubMed
Miller I, Cerna J, Travnicek J, Rejnek J, Kruml J. The role of immune pig colostrum, serum and immunoglobulins IgG, IgM, and IgA, in local intestinal immunity against enterotoxic strain in Escherichia coli O55 in germfree piglets. Folia Microbiol. (Praha) 1975;20:433–438. PubMed
Tlaskalova H, Rejnek J, Travnicek J, Lanc A. The effect of antibodies present in the intestinal tract of germfree piglets on the infection caused by the intravenous administration of the pathogenic strain Escherichia coli O55. Folia Microbiol. (Praha) 1970;15:372–376. PubMed
Rejnek J, Travnicek J, J. K, Sterzl J, Lanc A. Study of the effect of antibodies in the intestinal tract of germ-free baby pigs. Folia Microbiol. (Praha) 1966;13:36–42.
Splichalova A, Splichal I, Sonnenborn U, Rada V. A modified MacConkey agar for selective enumeration of necrotoxigenic E. coli O55 and probiotic E. coli nissle 1917. J. Microbiol. Methods. 2014;104:82–86. PubMed
Mestecky J, Kilian M. Immunoglobulin A (IgA) Methods Enzymol. 1985;116:37–75. PubMed
Kosowska K, et al. The Clostridium ramosum IgA proteinase represents a novel type of metalloendopeptidase. J. Biol. Chem. 2002;277:11987–11994. PubMed
Hughes GJ, Reason AJ, Savoy L, Jaton J, Frutiger-Hughes S. Carbohydrate moieties in human secretory component. Biochim. Biophys. Acta. 1999;1434:86–93. PubMed
Moon HW. Vacuolated villous epithelium of the small intestine of young pigs. Vet. Pathol. 1972;9:3–21. PubMed
Skrzypek T, et al. Gradual disappearance of vacuolated enterocytes in the small intestine of neonatal piglets. J. Physiol. Pharmacol. 2007;58(Suppl 3):87–95. PubMed
Ogra SS, Weintraub D, Ogra PL. Immunologic aspects of human colostrum and milk. III. Fate and absorption of cellular and soluble components in the gastrointestinal tract of the newborn. J. Immunol. 1977;119:245–248. PubMed
Pierce AE, Smith MW. The intestinal absorption of pig and bovine immune lactoglobulin and human serum albumin by the new-born pig. J. Physiol. 1967;190:1–18. PubMed PMC
Yoo EM, Yu LJ, Wims LA, Goldberg D, Morrison SL. Differences in N-glycan structures found on recombinant IgA1 and IgA2 produced in murine myeloma and CHO cell lines. MAbs. 2010;2:320–334. PubMed PMC
Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 2007;25:21–50. PubMed
Davin JC, Senterre J, Mahieu PR. The high lectin-binding capacity of human secretory IgA protects nonspecifically mucosae against environmental antigens. Biol. Neonate. 1991;59:121–125. PubMed
Lee J, Georgiou G. High-affinity IgA against microbial glycans. Nat. Immunol. 2018;19:514–515. PubMed
Butler JE, Sinkora M. The isolator piglet: A model for studying the development of adaptive immunity. Immunol. Res. 2007;39:33–51. PubMed
Werhahn E, Klobasa F, Butler JE. Investigation of some factors which influence the absorption of IgG by the neonatal piglet. Vet. Immunol. Immunopathol. 1981;2:35–51. PubMed
Butler JE, Klobasa F, Werhahn E. The differential localization of IgA, IgM, and IgG in the gut of suckled neonatal piglets. Vet. Immunol. Immunopathol. 1981;2:53–65. PubMed
Butler JE, Wertz N, Sinkora M. Antibody repertoire development in swine. Annu. Rev. Anim. Biosci. 2017;5:255–279. PubMed
Cukrowska B, et al. Isotype and antibody specificity of spontaneously formed immunoglobulins in pig fetuses and germ-free piglets: Production by CD5- B cells. Immunology. 1996;88:611–617. PubMed PMC
Cukrowska B, et al. Polyclonal immunoglobulin response of thymic, hepatic and splenic lymphocytes from fetal, germ-free and conventionally reared pigs to different B-cell activators. Folia Microbiol. (Praha) 1995;40:421–430. PubMed
Firon N, Ofek I, Sharon N. Carbohydrate specificity of the surface lectins of Escherichia coli, Klebsiella pneumoniae, and Salmonella typhimurium. Carbohydr. Res. 1983;120:235–249. PubMed
Adlerberth I, et al. A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line Ht-29. Appl. Environ. Microbiol. 1996;62:2244–2251. PubMed PMC
Gibbins HL, Proctor GB, Yakubov GE, Wilson S, Carpenter GH. SIgA binding to mucosal surfaces is mediated by mucin-mucin interactions. PLoS One. 2015;10:e0119677. PubMed PMC
Plomp R, et al. Comparative glycomics of immunoglobulin A and G from saliva and plasma reveals biomarker potential. Front. Immunol. 2018;9:2436. PubMed PMC
Stepanova K, Sinkora M. Porcine γδ T lymphocytes can be categorized into two functionally and developmentally distinct subsets according to expression of CD2 and level of TCR. J. Immunol. 2013;190:2111–2120. PubMed
Sinkora M, Stepanova K, Sinkorova J. Different anti-CD21 antibodies can be used to discriminate developmentally and functionally different subsets of B lymphocytes in circulation of pigs. Dev. Comp. Immunol. 2013;39:409–418. PubMed
Russell MW, Brown TA, Radl J, Haaijman JJ, Mestecky J. Assay of human IgA subclass antibodies in serum and secretions by means of monoclonal antibodies. J. Immunol. Methods. 1986;87:87–93. PubMed
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta c(t)) method. Methods. 2001;25:402–408. PubMed
Antibody-dependent passive protection of mucosal surfaces