Overexpression of the proteasome subunits LMP2, LMP7, and MECL-1, but not PA28 alpha/beta, enhances the presentation of an immunodominant lymphocytic choriomeningitis virus T cell epitope

J Immunol. 2000 Jul 15;165(2):768-78. doi: 10.4049/jimmunol.165.2.768.

Abstract

The proteasome is a large protease complex that generates most of the peptide ligands of MHC class I molecules either in their final form or in the form of N-terminally extended precursors. Upon the stimulation of cells with IFN-gamma, three constitutively expressed subunits of the 20S proteasome are replaced by the inducible subunits LMP2 (low-molecular mass polypeptide 2), LMP7, and MECL-1 (multicatalytic endopeptidase complex-like-1) to form so-called immunoproteasomes. We show in this study that overexpression of these three subunits in triple transfectants led to a marked enhancement in the H-2Ld-restricted presentation of the immunodominant nonameric epitope NP118, which is derived from the nucleoprotein (NP) of lymphocytic choriomeningitis virus. Overexpression of the alpha and beta subunits of the IFN-gamma-inducible proteasome regulator PA28, in contrast, did not have a comparable effect. In vitro, immunoproteasomes as compared with constitutive proteasomes generated higher amounts of 11- and 12-mer fragments containing the NP118 epitope. These are likely to be cytosolic precursors of NP118, as a proline anchor residue in the second position of NP118 may interfere with TAP-mediated transport of the nonameric epitope itself. In conclusion, we provide evidence that up-regulation of the three inducible subunits, LMP2, LMP7, and MECL-1, can result in a marked improvement of Ag presentation and that, depending on the epitope, PA28 and immunoproteasomes may differentially affect Ag processing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / biosynthesis*
  • Adjuvants, Immunologic / genetics
  • Adjuvants, Immunologic / physiology
  • Amino Acid Sequence
  • Animals
  • Antigen Presentation / genetics
  • Antigen Presentation / immunology*
  • Autoantigens
  • Cell Line
  • Cysteine Endopeptidases / biosynthesis*
  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / immunology
  • Cytosol / immunology
  • Cytosol / metabolism
  • Epitopes, T-Lymphocyte / genetics
  • Epitopes, T-Lymphocyte / metabolism*
  • H-2 Antigens / biosynthesis
  • H-2 Antigens / genetics
  • Histocompatibility Antigen H-2D
  • Hybridomas
  • Immunodominant Epitopes / genetics
  • Immunodominant Epitopes / metabolism*
  • Lymphocytic choriomeningitis virus / genetics
  • Lymphocytic choriomeningitis virus / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Molecular Sequence Data
  • Multienzyme Complexes / biosynthesis*
  • Multienzyme Complexes / genetics
  • Multienzyme Complexes / immunology
  • Nucleoproteins / biosynthesis
  • Nucleoproteins / genetics
  • Nucleoproteins / immunology
  • Nucleoproteins / metabolism
  • Peptide Fragments / biosynthesis
  • Peptide Fragments / genetics
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism
  • Proteasome Endopeptidase Complex
  • Protein Biosynthesis*
  • Protein Precursors / biosynthesis
  • Protein Precursors / genetics
  • Proteins / genetics
  • Proteins / immunology
  • Transfection
  • Viral Proteins / biosynthesis
  • Viral Proteins / genetics
  • Viral Proteins / immunology
  • Viral Proteins / metabolism

Substances

  • Adjuvants, Immunologic
  • Autoantigens
  • Epitopes, T-Lymphocyte
  • H-2 Antigens
  • Histocompatibility Antigen H-2D
  • Immunodominant Epitopes
  • Ki antigen
  • Multienzyme Complexes
  • Nucleoproteins
  • Peptide Fragments
  • Protein Precursors
  • Proteins
  • Viral Proteins
  • nucleoprotein peptide 118-126, lymphocytic choriomeningitis virus
  • LMP-2 protein
  • Cysteine Endopeptidases
  • LMP7 protein
  • Proteasome Endopeptidase Complex
  • Psmb10 protein, mouse
  • Psme1 protein, mouse