Alteration of microbiota antibody‐mediated immune selection contributes to dysbiosis in inflammatory bowel diseases

Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requ...

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Published inEMBO molecular medicine Vol. 14; no. 8; pp. e15386 - n/a
Main Authors Michaud, Eva, Waeckel, Louis, Gayet, Rémi, Goguyer‐Deschaumes, Roman, Chanut, Blandine, Jospin, Fabienne, Bathany, Katell, Monnoye, Magali, Genet, Coraline, Prier, Amelie, Tokarski, Caroline, Gérard, Philippe, Roblin, Xavier, Rochereau, Nicolas, Paul, Stéphane
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 08.08.2022
EMBO Press
Wiley Open Access
John Wiley and Sons Inc
Springer Nature
Subjects
Antibodies
Antigen-antibody complexes
Bacteria
Commensals
Crohn's disease
Dysbacteriosis
EMBO12
EMBO19
EMBO23
Fatty acids
Feces
glycosylation
High-performance liquid chromatography
Human health and pathology
IBD
immunity
Immunoglobulin A
Immunological tolerance
Immunology
Infectious diseases
Inflammatory bowel disease
Inflammatory bowel diseases
Intestinal microflora
Intestine
Life Sciences
M cells
Microbiology and Parasitology
Microbiota
Mucosa
Peyer's patches
Pharmaceutical sciences
Pharmacology
SIgA
Ulcerative colitis
Vaccinology
Virology
microbiota
glycosylation
IBD
immunity
SIgA
immunity Subject Categories Digestive System
Immunology
Microbiology
amp
SIgA microbiota glycosylation IBD immunity Subject Categories Digestive System Immunology Microbiology
Virology &amp
Host Pathogen Interaction
Online AccessGet full text
ISSN1757-4676
1757-4684
1757-4684
DOI10.15252/emmm.202115386

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Abstract Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan–glycan interaction. Here, we asked whether IgA1 and IgA2‐microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC‐purified IgA, we show that reverse‐transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA‐bound microbiota in CD and UC showed distinct IgA1‐ and IgA2‐associated microbiota; the IgA1 + fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti‐glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis. Synopsis IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC. Evidence of a chain of subclass‐dependent functional disparities between CD and UC IgAs affecting antibody glycosylation, transport across epithelia, and affinity, which may interfere in optimal commensal selection to promote dysbiosis While only IgA2 could undergo RT in non‐IBD, IgA1 in CD had the ability to do so and neither IgA1 nor IgA2 were able to in UC. Despite predominant dual IgA1 and IgA2 binding on stool microbiota, CD associates with enriched commensal binding in the IgA1 + fraction, and UC with a marked reduction in IgA overall reactivity Graphical Abstract IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC.
AbstractList Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse-transcytosis, the apical-to-basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan-glycan interaction. Here, we asked whether IgA1 and IgA2-microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLCpurified IgA, we show that reverse-transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA-bound microbiota in CD and UC showed distinct IgA1-and IgA2-associated microbiota; the IgA1 + fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti-glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis.
Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan–glycan interaction. Here, we asked whether IgA1 and IgA2‐microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC‐purified IgA, we show that reverse‐transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA‐bound microbiota in CD and UC showed distinct IgA1‐ and IgA2‐associated microbiota; the IgA1+ fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti‐glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis. Synopsis IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC. Evidence of a chain of subclass‐dependent functional disparities between CD and UC IgAs affecting antibody glycosylation, transport across epithelia, and affinity, which may interfere in optimal commensal selection to promote dysbiosis While only IgA2 could undergo RT in non‐IBD, IgA1 in CD had the ability to do so and neither IgA1 nor IgA2 were able to in UC. Despite predominant dual IgA1 and IgA2 binding on stool microbiota, CD associates with enriched commensal binding in the IgA1+ fraction, and UC with a marked reduction in IgA overall reactivity IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC.
Abstract Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan–glycan interaction. Here, we asked whether IgA1 and IgA2‐microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC‐purified IgA, we show that reverse‐transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA‐bound microbiota in CD and UC showed distinct IgA1‐ and IgA2‐associated microbiota; the IgA1+ fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti‐glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis.
Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse-transcytosis, the apical-to-basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan-glycan interaction. Here, we asked whether IgA1 and IgA2-microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC-purified IgA, we show that reverse-transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA-bound microbiota in CD and UC showed distinct IgA1- and IgA2-associated microbiota; the IgA1+ fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti-glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis.Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse-transcytosis, the apical-to-basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan-glycan interaction. Here, we asked whether IgA1 and IgA2-microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC-purified IgA, we show that reverse-transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA-bound microbiota in CD and UC showed distinct IgA1- and IgA2-associated microbiota; the IgA1+ fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti-glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis.
Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan–glycan interaction. Here, we asked whether IgA1 and IgA2‐microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC‐purified IgA, we show that reverse‐transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA‐bound microbiota in CD and UC showed distinct IgA1‐ and IgA2‐associated microbiota; the IgA1+ fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti‐glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis.
Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan–glycan interaction. Here, we asked whether IgA1 and IgA2‐microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC‐purified IgA, we show that reverse‐transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA‐bound microbiota in CD and UC showed distinct IgA1‐ and IgA2‐associated microbiota; the IgA1 + fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti‐glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis. Synopsis IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC. Evidence of a chain of subclass‐dependent functional disparities between CD and UC IgAs affecting antibody glycosylation, transport across epithelia, and affinity, which may interfere in optimal commensal selection to promote dysbiosis While only IgA2 could undergo RT in non‐IBD, IgA1 in CD had the ability to do so and neither IgA1 nor IgA2 were able to in UC. Despite predominant dual IgA1 and IgA2 binding on stool microbiota, CD associates with enriched commensal binding in the IgA1 + fraction, and UC with a marked reduction in IgA overall reactivity Graphical Abstract IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC.
Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the apical‐to‐basal transport of IgA2 immune complexes via M cells of gut Peyer's patches. As such, the maintenance of a diverse gut microbiota requires broad affinity IgA and glycan–glycan interaction. Here, we asked whether IgA1 and IgA2‐microbiota interactions might be involved in dysbiosis induction during inflammatory bowel diseases. Using stool HPLC‐purified IgA, we show that reverse‐transcytosis is abrogated in ulcerative colitis (UC) while it is extended to IgA1 in Crohn's disease (CD). 16S RNA sequencing of IgA‐bound microbiota in CD and UC showed distinct IgA1‐ and IgA2‐associated microbiota; the IgA1 + fraction of CD microbiota was notably enriched in beneficial commensals. These features were associated with increased IgA anti‐glycan reactivity in CD and an opposite loss of reactivity in UC. Our results highlight previously unknown pathogenic properties of IgA in IBD that could support dysbiosis. IBD (both CD and UC) is characterized by dysbiosis and altered immune pathways that lead to and sustain prolonged inflammation in the gut. As IgA are the main drivers of commensal selection in the healthy gut, this study aimed at assessing subclass‐related structure and functions of IgA in both CD and UC.
Author Rochereau, Nicolas
Genet, Coraline
Paul, Stéphane
Bathany, Katell
Gérard, Philippe
Monnoye, Magali
Jospin, Fabienne
Tokarski, Caroline
Chanut, Blandine
Gayet, Rémi
Waeckel, Louis
Prier, Amelie
Michaud, Eva
Goguyer‐Deschaumes, Roman
Roblin, Xavier
AuthorAffiliation 3 Micalis Institute, INRAE, AgroParisTech Université Paris‐Saclay Jouy‐en‐Josas France
4 Inserm UMR 1098 Right Université Bourgogne Franche‐Comté Besançon France
2 Chimie et Biologie des Membranes et des Nano‐objets (UMR 5248) Université de Bordeaux, CNRS, Bordeaux INP Pessac France
1 CIRI – Centre International de Recherche en Infectiologie, Team GIMAP, Univ Lyon, Université Claude Bernard Lyon 1, Inserm, U1111, CNRS, UMR530, CIC 1408 Vaccinology Saint‐Etienne France
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– name: 4 Inserm UMR 1098 Right Université Bourgogne Franche‐Comté Besançon France
– name: 3 Micalis Institute, INRAE, AgroParisTech Université Paris‐Saclay Jouy‐en‐Josas France
– name: 2 Chimie et Biologie des Membranes et des Nano‐objets (UMR 5248) Université de Bordeaux, CNRS, Bordeaux INP Pessac France
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  givenname: Eva
  surname: Michaud
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  organization: CIRI – Centre International de Recherche en Infectiologie, Team GIMAP (Saint-Etienne), Université Claude Bernard Lyon 1, Inserm, U1111, CNRS, UMR5308, CIC Inserm 1408 Vaccinology
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  givenname: Rémi
  surname: Gayet
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  organization: CIRI – Centre International de Recherche en Infectiologie, Team GIMAP (Saint-Etienne), Université Claude Bernard Lyon 1, Inserm, U1111, CNRS, UMR5308
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  surname: Goguyer‐Deschaumes
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– sequence: 5
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  surname: Chanut
  fullname: Chanut, Blandine
  organization: CIRI – Centre International de Recherche en Infectiologie, Team GIMAP (Saint-Etienne), Université Claude Bernard Lyon 1, Inserm, U1111, CNRS, UMR5308
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  givenname: Fabienne
  surname: Jospin
  fullname: Jospin, Fabienne
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– sequence: 7
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  surname: Bathany
  fullname: Bathany, Katell
  organization: Chimie et Biologie des Membranes et des Nano‐objets (UMR 5248), Université de Bordeaux, CNRS, Bordeaux INP
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  orcidid: 0000-0001-9521-0067
  surname: Gérard
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  surname: Roblin
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  surname: Paul
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  email: stephane.paul@chu-st-etienne.fr
  organization: CIRI – Centre International de Recherche en Infectiologie, Team GIMAP (Saint-Etienne), Université Claude Bernard Lyon 1, Inserm, U1111, CNRS, UMR5308
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Issue 8
Keywords microbiota
glycosylation
IBD
immunity
SIgA
immunity Subject Categories Digestive System
Immunology
Microbiology
amp
SIgA microbiota glycosylation IBD immunity Subject Categories Digestive System Immunology Microbiology
Virology &amp
Host Pathogen Interaction
Language English
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Attribution: http://creativecommons.org/licenses/by
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Snippet Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the...
Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse-transcytosis, the...
Abstract Human secretory immunoglobulins (SIg) A1 and SIgA2 guide mucosal responses toward tolerance or inflammation, notably through reverse‐transcytosis, the...
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wiley
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StartPage e15386
SubjectTerms Antibodies
Antigen-antibody complexes
Bacteria
Commensals
Crohn's disease
Dysbacteriosis
EMBO12
EMBO19
EMBO23
Fatty acids
Feces
glycosylation
High-performance liquid chromatography
Human health and pathology
IBD
immunity
Immunoglobulin A
Immunological tolerance
Immunology
Infectious diseases
Inflammatory bowel disease
Inflammatory bowel diseases
Intestinal microflora
Intestine
Life Sciences
M cells
Microbiology and Parasitology
Microbiota
Mucosa
Peyer's patches
Pharmaceutical sciences
Pharmacology
SIgA
Ulcerative colitis
Vaccinology
Virology
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  providerName: Wiley-Blackwell
Title Alteration of microbiota antibody‐mediated immune selection contributes to dysbiosis in inflammatory bowel diseases
URI https://link.springer.com/article/10.15252/emmm.202115386
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Femmm.202115386
https://www.proquest.com/docview/2699600129
https://www.proquest.com/docview/2685039319
https://hal.science/hal-04871841
https://pubmed.ncbi.nlm.nih.gov/PMC9358401
https://doaj.org/article/412ce5dad93d49a68a3f2f1a2bf9f560
Volume 14
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