ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming

Blood. 2005 Jul 1;106(1):216-23. doi: 10.1182/blood-2005-01-0220. Epub 2005 Mar 24.

Abstract

Exosomes are secreted vesicles formed in late endocytic compartments. Immature dendritic cells (DCs) secrete exosomes, which transfer functional major histocompatibility complex (MHC)-peptide complexes to other DCs. Since immature and mature DCs induce different functional T-cell responses (ie, tolerance versus priming), we asked whether DC maturation also influenced the priming abilities of their exosomes. We show that exosomes secreted by lipopolysaccharide (LPS)-treated mature DCs are 50- to 100-fold more potent to induce antigen-specific T-cell activation in vitro than exosomes from immature DCs. In vitro, exosomes from mature DCs transfer to B lymphocytes the ability to prime naive T cells. In vivo, only mature exosomes trigger effector T-cell responses, leading to fast skin graft rejection. Proteomic and biochemical analyses revealed that mature exosomes are enriched in MHC class II, B7.2, intercellular adhesion molecule 1 (ICAM-1), and bear little milk-fat globule-epidermal growth factor-factor VIII (MFG-E8) as compared with immature exosomes. Functional analysis using DC-derived exosomes from knock-out mice showed that MHC class II and ICAM-1 are required for mature exosomes to prime naive T cells, whereas B7.2 and MFG-E8 are dispensable. Therefore, changes in protein composition and priming abilities of exosomes reflect the maturation signals received by DCs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / immunology
  • Antigens, Surface / immunology
  • B7-1 Antigen / immunology
  • B7-2 Antigen
  • CD4-Positive T-Lymphocytes / immunology*
  • Cell Communication / immunology
  • Cell Division / immunology
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Intercellular Adhesion Molecule-1 / genetics*
  • Intercellular Adhesion Molecule-1 / metabolism*
  • Lipopolysaccharides / pharmacology
  • Membrane Glycoproteins / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Microscopy, Electron
  • Milk Proteins / immunology
  • Phagocytosis / immunology
  • Secretory Vesicles / immunology*
  • Secretory Vesicles / metabolism
  • Secretory Vesicles / ultrastructure

Substances

  • Antigens, CD
  • Antigens, Surface
  • B7-1 Antigen
  • B7-2 Antigen
  • Cd86 protein, mouse
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Mfge8 protein, mouse
  • Milk Proteins
  • Intercellular Adhesion Molecule-1