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PMID: 21454510 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Recognition of gram-positive intestinal bacteria by hybridoma- and colostrum-derived secretory immunoglobulin A is mediated by carbohydrates.

The Journal of biological chemistry ·Vol. 286 ·No. 19 ·2011-05-13 ·Pages 17239-47

Mathias A, Corthésy B

Abstract

Humans live in symbiosis with 10(14) commensal bacteria among which >99% resides in their gastrointestinal tract. The molecular bases pertaining to the interaction between mucosal secretory IgA (SIgA) and bacteria residing in the intestine are not known. Previous studies have demonstrated that commensals are naturally coated by SIgA in the gut lumen. Thus, understanding how natural SIgA interacts with commensal bacteria can provide new clues on its multiple functions at mucosal surfaces. Using fluorescently labeled, nonspecific SIgA or secretory component (SC), we visualized by confocal microscopy the interaction with various commensal bacteria, including Lactobacillus, Bifidobacteria, Escherichia coli, and Bacteroides strains. These experiments revealed that the interaction between SIgA and commensal bacteria involves Fab- and Fc-independent structural motifs, featuring SC as a crucial partner. Removal of glycans present on free SC or bound in SIgA resulted in a drastic drop in the interaction with gram-positive bacteria, indicating the essential role of carbohydrates in the process. In contrast, poor binding of gram-positive bacteria by control IgG was observed. The interaction with gram-negative bacteria was preserved whatever the molecular form of protein partner used, suggesting the involvement of different binding motifs. Purified SIgA and SC from either mouse hybridoma cells or human colostrum exhibited identical patterns of recognition for gram-positive bacteria, emphasizing conserved plasticity between species. Thus, sugar-mediated binding of commensals by SIgA highlights the currently underappreciated role of glycans in mediating the interaction between a highly diverse microbiota and the mucosal immune system.

MeSH Terms
Amino Acid Motifs Carbohydrates/chemistry Colostrum/immunology,metabolism,microbiology Dimerization Glycoproteins/chemistry Glycosylation Gram-Positive Bacteria/metabolism Humans Hybridomas/metabolism,microbiology Immunoglobulin A, Secretory/metabolism Immunoglobulin Fragments/chemistry Intestines/microbiology Lactobacillus/metabolism Microscopy, Confocal/methods Polysaccharides/chemistry
Chemicals
Carbohydrates Glycoproteins Immunoglobulin A, Secretory Immunoglobulin Fragments Polysaccharides
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Mathias Amandine
R&D Laboratory of the Division of Immunology and Allergy, Centre Hospitalier Universitaire Vaudois, Rue du Bugnon, 1011 Lausanne, Switzerland.
Corthésy Blaise
References (54)
54 references, click to expand
  1. Immunoglobulin transport across polarized epithelial cells.
    Nat Rev Mol Cell Biol. 2002 Dec;3(12):944-55 PMID: 12461560
  2. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo.
    Immunity. 2002 Jul;17(1):107-15 PMID: 12150896
  3. Cell surface of Lactococcus lactis is covered by a protective polysaccharide pellicle.
    J Biol Chem. 2010 Apr 2;285(14):10464-71 PMID: 20106971
  4. Biliary secretory immunoglobulin A is a major constituent of the new group of cholesterol crystal-binding proteins.
    Gastroenterology. 1998 Jul;115(1):129-38 PMID: 9649468
  5. In vivo IgA coating of anaerobic bacteria in human faeces.
    Gut. 1996 Mar;38(3):348-54 PMID: 8675085
  6. Intestinal IgA: novel views on its function in the defence of the largest mucosal surface.
    Gut. 1999 Jan;44(1):2-5 PMID: 9862815
  7. Crystal structure of a mucus-binding protein repeat reveals an unexpected functional immunoglobulin binding activity.
    J Biol Chem. 2009 Nov 20;284(47):32444-53 PMID: 19758995
  8. Infections in bone marrow transplant recipients.
    Semin Hematol. 1984 Apr;21(2):123-40 PMID: 6204385
  9. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system.
    Infect Immun. 1999 Apr;67(4):1992-2000 PMID: 10085047
  10. Characterization of functional oligosaccharide mimics of the Shigella flexneri serotype 2a O-antigen: implications for the development of a chemically defined glycoconjugate vaccine.
    J Immunol. 2006 Feb 1;176(3):1686-94 PMID: 16424198
  11. Secretory immunoglobulin A obtained from pooled human colostrum and milk for oral passive immunization.
    Pediatr Allergy Immunol. 2005 Nov;16(7):574-81 PMID: 16238582
  12. Intimin and the host cell--is it bound to end in Tir(s)?
    Trends Microbiol. 2001 May;9(5):214-8 PMID: 11336837
  13. Secretory component delays the conversion of secretory IgA into antigen-binding competent F(ab')2: a possible implication for mucosal defense.
    J Immunol. 1998 Nov 15;161(10):5445-53 PMID: 9820520
  14. Commensal host-bacterial relationships in the gut.
    Science. 2001 May 11;292(5519):1115-8 PMID: 11352068
  15. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses.
    Clin Exp Allergy. 2009 Dec;39(12):1842-51 PMID: 19735274
  16. Localization of free and bound secretory component in human intestinal epithelial cells. A model for the assembly of secretory IgA.
    J Exp Med. 1974 Mar 1;139(3):629-42 PMID: 4204729
  17. Role of secretory immunoglobulin A and secretory component in the protection of mucosal surfaces.
    Future Microbiol. 2010 May;5(5):817-29 PMID: 20441552
  18. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria.
    Science. 2004 Mar 12;303(5664):1662-5 PMID: 15016999
  19. Covalent homodimers of murine secretory component induced by epitope substitution unravel the capacity of the polymeric Ig receptor to dimerize noncovalently in the absence of IgA ligand.
    J Biol Chem. 1999 Oct 29;274(44):31445-55 PMID: 10531346
  20. Simplified procedure to recover recombinant antigenized secretory IgA to be used as a vaccine vector.
    J Chromatogr B Analyt Technol Biomed Life Sci. 2003 Mar 25;786(1-2):143-51 PMID: 12651010
  21. Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer's patches with restriction to mucosal compartment.
    J Immunol. 2007 Dec 1;179(11):7751-7 PMID: 18025221
  22. Interaction of bifidobacteria with Caco-2 cells-adhesion and impact on expression profiles.
    Int J Food Microbiol. 2006 Jul 1;110(1):62-8 PMID: 16713644
  23. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses.
    Science. 2010 Jun 25;328(5986):1705-9 PMID: 20576892
  24. T cell control of the gut IgA response against commensal bacteria.
    Gut. 2001 Jun;48(6):762-4 PMID: 11358892
  25. Carbohydrate moieties in human secretory component.
    Biochim Biophys Acta. 1999 Sep 14;1434(1):86-93 PMID: 10556562
  26. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin.
    Infect Immun. 1990 Sep;58(9):3073-7 PMID: 2201644
  27. Mechanisms of neonatal mucosal antibody protection.
    J Immunol. 2006 Nov 1;177(9):6256-62 PMID: 17056555
  28. Immunoglobulin coating of faecal bacteria in inflammatory bowel disease.
    Eur J Gastroenterol Hepatol. 2004 Jul;16(7):669-74 PMID: 15201580
  29. Intranasal monoclonal immunoglobulin A against respiratory syncytial virus protects against upper and lower respiratory tract infections in mice.
    Antimicrob Agents Chemother. 1994 Dec;38(12):2785-91 PMID: 7695263
  30. Glycans on secretory component participate in innate protection against mucosal pathogens.
    J Biol Chem. 2006 May 19;281(20):14280-7 PMID: 16543244
  31. Human secretory immunoglobulin A may contribute to biofilm formation in the gut.
    Immunology. 2003 Aug;109(4):580-7 PMID: 12871226
  32. Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces.
    Immunol Lett. 2009 Jun 4;124(2):57-62 PMID: 19524784
  33. Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems.
    J Biol Chem. 2003 May 30;278(22):20140-53 PMID: 12637583
  34. Lack of association of secretory component with IgA in J chain-deficient mice.
    J Immunol. 1996 Jul 15;157(2):750-4 PMID: 8752925
  35. Purification and measurement of secretory IgA in mouse milk.
    J Immunol Methods. 1995 Mar 27;180(2):147-57 PMID: 7714330
  36. Increase in the population of duodenal immunoglobulin A plasmocytes in axenic mice associated with different living or dead bacterial strains of intestinal origin.
    Infect Immun. 1978 Aug;21(2):532-9 PMID: 357289
  37. Antigen binding properties of purified immunoglobulin A and reconstituted secretory immunoglobulin A antibodies.
    J Biol Chem. 1996 Jul 5;271(27):16300-9 PMID: 8663142
  38. Immunoglobulin-mediated agglutination of and biofilm formation by Escherichia coli K-12 require the type 1 pilus fiber.
    Infect Immun. 2004 Apr;72(4):1929-38 PMID: 15039312
  39. Natural polyreactive secretory immunoglobulin A autoantibodies as a possible barrier to infection in humans.
    Infect Immun. 1997 Oct;65(10):3997-4004 PMID: 9316998
  40. Conditioned polarized Caco-2 cell monolayers allow to discriminate for the ability of gut-derived microorganisms to modulate permeability and antigen-induced basophil degranulation.
    Clin Exp Allergy. 2009 Apr;39(4):527-36 PMID: 19178541
  41. In vitro inhibition activity of nisin A, nisin Z, pediocin PA-1 and antibiotics against common intestinal bacteria.
    Lett Appl Microbiol. 2007 Sep;45(3):252-7 PMID: 17718835
  42. Restricted IgA repertoire in both B-1 and B-2 cell-derived gut plasmablasts.
    J Immunol. 2005 Jan 15;174(2):1046-54 PMID: 15634929
  43. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases.
    Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13780-5 PMID: 17699621
  44. Potentiation of polarized intestinal Caco-2 cell responsiveness to probiotics complexed with secretory IgA.
    J Biol Chem. 2010 Oct 29;285(44):33906-13 PMID: 20729211
  45. Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut.
    Infect Immun. 1995 Oct;63(10):3904-13 PMID: 7558298
  46. Location of secretory component on the Fc edge of dimeric IgA1 reveals insight into the role of secretory IgA1 in mucosal immunity.
    Mucosal Immunol. 2009 Jan;2(1):74-84 PMID: 19079336
  47. Protection of the neonate by the innate immune system of developing gut and of human milk.
    Pediatr Res. 2007 Jan;61(1):2-8 PMID: 17211132
  48. Adaptations of intestinal macrophages to an antigen-rich environment.
    Semin Immunol. 2007 Apr;19(2):84-93 PMID: 17055292
  49. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium.
    Infect Immun. 1992 May;60(5):1786-92 PMID: 1373399
  50. Fab-independent antiadhesion effects of secretory immunoglobulin A on S-fimbriated Escherichia coli are mediated by sialyloligosaccharides.
    Infect Immun. 1998 Aug;66(8):3971-3 PMID: 9673289
  51. Monoclonal immunoglobulin A antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shigellosis.
    J Exp Med. 1995 Sep 1;182(3):769-78 PMID: 7544397
  52. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora.
    Science. 2002 Nov 15;298(5597):1424-7 PMID: 12434060
  53. Lactoferrin: structure, function and applications.
    Int J Antimicrob Agents. 2009 Apr;33(4):301.e1-8 PMID: 18842395
  54. The amount of secreted IgA may not determine the secretory IgA coating ratio of gastrointestinal bacteria.
    FEMS Immunol Med Microbiol. 2009 Jul;56(2):185-9 PMID: 19490128
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
DOI
10.1074/jbc.M110.209015
Published
2011-05-13
Epub
2011-00-21
Pages
17239-47
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC3089566
Subset
IM
External Links
PubMed source DOI: 10.1074/jbc.M110.209015 PMC Full Text View journal details
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