Prolonged antigen persistence within nonterminal late endocytic compartments of antigen-specific B lymphocytes

J Immunol. 2001 Jun 1;166(11):6657-64. doi: 10.4049/jimmunol.166.11.6657.

Abstract

Although Ag-specific B lymphocytes can process Ag and express peptide-class II complexes as little as 1 h after Ag exposure, it requires 3-5 days for the immune system to develop a population of Ag-specific effector CD4 T lymphocytes to interact with these complexes. Presently, it is unclear how B cells maintain the expression of cell surface antigenic peptide-class II complexes until effector CD4 T lymphocytes become available. Therefore, we investigated B cell receptor (BCR)-mediated Ag processing and presentation by normal B lymphocytes to determine whether these cells have a mechanism to prolong the cell surface expression of peptide-class II complexes derived from the processing of cognate AG: Interestingly, after transit of early endocytic compartments, internalized Ag-BCR complexes are delivered to nonterminal late endosomes where they persist for a prolonged period of time. In contrast, Ags internalized via fluid phase endocytosis are rapidly delivered to terminal lysosomes and degraded. Moreover, persisting Ag-BCR complexes within nonterminal late endosomes exhibit a higher degree of colocalization with the class II chaperone HLA-DM/H2-M than with the HLA-DM/H2-M regulator HLA-DO/H2-O. Finally, B cells harboring persistent Ag-BCR complexes exhibit prolonged cell surface expression of antigenic peptide-class II complexes. These results demonstrate that B lymphocytes possess a mechanism for prolonging the intracellular persistence of Ag-BCR complexes within nonterminal late endosomes and suggest that this intracellular Ag persistence allows for the prolonged cell surface expression of peptide-class II complexes derived from the processing of specific AG:

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antigens / metabolism*
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism*
  • Cell Compartmentation / immunology
  • Cell Line
  • Endocytosis / immunology*
  • Epitopes, B-Lymphocyte / metabolism*
  • HLA-D Antigens / metabolism
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Intracellular Fluid / immunology
  • Intracellular Fluid / metabolism
  • Kinetics
  • Macromolecular Substances
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Muramidase / immunology*
  • Muramidase / metabolism*
  • Peptide Fragments / biosynthesis
  • Peptide Fragments / immunology
  • Protein Transport / immunology
  • Subcellular Fractions / immunology
  • Subcellular Fractions / metabolism

Substances

  • Antigens
  • Epitopes, B-Lymphocyte
  • H-2O antigen
  • H2-M antigens
  • HLA-D Antigens
  • HLA-DM antigens
  • HLA-DO antigens
  • Histocompatibility Antigens Class II
  • Macromolecular Substances
  • Peptide Fragments
  • hen egg lysozyme
  • Muramidase