High microbiota reactivity of adult human intestinal IgA requires somatic mutations

J Exp Med. 2020 Nov 2;217(11):e20200275. doi: 10.1084/jem.20200275.

Abstract

The gut is home to the body's largest population of plasma cells. In healthy individuals, IgA is the dominating isotype, whereas patients with inflammatory bowel disease also produce high concentrations of IgG. In the gut lumen, secretory IgA binds pathogens and toxins but also the microbiota. However, the antigen specificity of IgA and IgG for the microbiota and underlying mechanisms of antibody binding to bacteria are largely unknown. Here we show that microbiota binding is a defining property of human intestinal antibodies in both healthy and inflamed gut. Some bacterial taxa were commonly targeted by different monoclonal antibodies, whereas others selectively bound single antibodies. Interestingly, individual human monoclonal antibodies from both healthy and inflamed intestines bound phylogenetically unrelated bacterial species. This microbiota cross-species reactivity did not correlate with antibody polyreactivity but was crucially dependent on the accumulation of somatic mutations. Therefore, our data suggest that a system of affinity-matured, microbiota cross-species-reactive IgA is a common aspect of SIgA-microbiota interactions in the gut.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Antibodies, Monoclonal / genetics*
  • Antibodies, Monoclonal / immunology*
  • Crohn Disease / immunology
  • Crohn Disease / microbiology
  • Crohn Disease / pathology
  • Cross Reactions / genetics
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • Feces / microbiology
  • Gastrointestinal Microbiome / immunology*
  • Humans
  • Immunoglobulin A, Secretory / genetics*
  • Immunoglobulin A, Secretory / immunology*
  • Immunoglobulin G / immunology
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / microbiology*
  • Intestine, Small / immunology
  • Intestine, Small / microbiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Middle Aged
  • Mutation*
  • Tissue Donors
  • Young Adult

Substances

  • Antibodies, Monoclonal
  • DNA-Binding Proteins
  • Immunoglobulin A, Secretory
  • Immunoglobulin G
  • Rag2 protein, mouse