Tapasin-mediated retention and optimization of peptide ligands during the assembly of class I molecules

J Immunol. 2000 Jul 1;165(1):322-30. doi: 10.4049/jimmunol.165.1.322.

Abstract

The murine class I H-2Kb molecule achieves high level surface expression in tapasin-deficient 721.220 human cells. Compared with their behavior in wild-type cells, Kb molecules expressed on 721.220 cells are more receptive to exogenous peptide, undergo more rapid surface decay, and fail to form macromolecular peptide loading complexes. As a result, they are rapidly transported to the cell surface, reflecting a failure of endoplasmic reticulum retention mechanisms in the absence of loading complex formation. Despite the failure of Kb molecules to colocalize to the TAP and their rapid egress to the cell surface, Kb is still capable of presenting TAP-dependent peptides in the absence of tapasin. Furthermore, pool sequencing of peptides eluted from these molecules revealed strict conservation of their canonical H-2Kb-binding motif. There was a reduction in the total recovery of peptides associated with Kb molecules purified from the surface of tapasin-deficient cells. Comparison of the peptides bound to Kb in the presence and absence of tapasin revealed considerable overlap in peptide repertoire. These results indicate that in the absence of an interaction with tapasin, Kb molecules fail to assemble with calreticulin and TAP, yet they are still capable of acquiring a diverse array of peptides. However, a significant proportion of these peptides appear to be suboptimal, resulting in reduced cell surface stability of Kb complexes. Taken together, the findings indicate that tapasin plays an essential role in the formation of the class I loading complex, which retains class I heterodimers in the endoplasmic reticulum until optimal ligand selection is completed.

MeSH terms

  • Animals
  • Antigen Presentation* / genetics
  • Antiporters / genetics
  • Antiporters / physiology*
  • Calcium-Binding Proteins / metabolism
  • Calreticulin
  • Cell Line, Transformed
  • Egg Proteins / genetics
  • Egg Proteins / metabolism
  • Endoplasmic Reticulum / metabolism
  • H-2 Antigens / biosynthesis
  • H-2 Antigens / genetics
  • H-2 Antigens / metabolism*
  • Humans
  • Hybridomas
  • Immunoglobulins / deficiency
  • Immunoglobulins / genetics
  • Immunoglobulins / physiology*
  • Ligands
  • Membrane Transport Proteins
  • Mice
  • Oligopeptides / metabolism*
  • Ovalbumin / genetics
  • Ovalbumin / metabolism
  • Peptide Fragments
  • Ribonucleoproteins / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Transfection
  • Tumor Cells, Cultured
  • beta 2-Microglobulin / genetics
  • beta 2-Microglobulin / metabolism

Substances

  • Antiporters
  • Calcium-Binding Proteins
  • Calreticulin
  • Egg Proteins
  • H-2 Antigens
  • H-2Kb protein, mouse
  • Immunoglobulins
  • Ligands
  • Membrane Transport Proteins
  • OVA-8
  • Oligopeptides
  • Peptide Fragments
  • Ribonucleoproteins
  • beta 2-Microglobulin
  • tapasin
  • Ovalbumin