Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation

Immunity. 2013 Mar 21;38(3):581-95. doi: 10.1016/j.immuni.2013.01.009. Epub 2013 Feb 7.

Abstract

CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1(+/gfp) ×Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation / immunology*
  • Antigens, Bacterial / immunology*
  • Antigens, CD / immunology*
  • Antigens, CD / metabolism
  • CD11c Antigen / genetics
  • CD11c Antigen / immunology
  • CD11c Antigen / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • CX3C Chemokine Receptor 1
  • Cell Line, Tumor
  • Cell Movement / immunology
  • Cells, Cultured
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Flow Cytometry
  • Host-Pathogen Interactions / immunology
  • Integrin alpha Chains / immunology*
  • Integrin alpha Chains / metabolism
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Fluorescence, Multiphoton
  • Mucous Membrane / immunology
  • Mucous Membrane / metabolism
  • Mucous Membrane / microbiology
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / immunology
  • Receptors, Chemokine / metabolism
  • Salmonella typhi / immunology
  • Salmonella typhi / physiology
  • Salmonella typhimurium / immunology
  • Salmonella typhimurium / physiology
  • Toll-Like Receptors / immunology
  • Toll-Like Receptors / metabolism

Substances

  • Antigens, Bacterial
  • Antigens, CD
  • CD11c Antigen
  • CX3C Chemokine Receptor 1
  • Cx3cr1 protein, mouse
  • Integrin alpha Chains
  • Luminescent Proteins
  • Receptors, Chemokine
  • Toll-Like Receptors
  • alpha E integrins