Pathways accessory to proteasomal proteolysis are less efficient in major histocompatibility complex class I antigen production

J Biol Chem. 2003 Mar 21;278(12):10013-21. doi: 10.1074/jbc.M211221200. Epub 2002 Dec 16.

Abstract

Degradation of cytosolic proteins depends largely on the proteasome, and a fraction of the cleavage products are presented as major histocompatibility complex (MHC) class I-bound ligands at the cell surface of antigen presenting cells. Proteolytic pathways accessory to the proteasome contribute to protein turnover, and their up-regulation may complement the proteasome when proteasomal proteolysis is impaired. Here we show that reduced reliance on proteasomal proteolysis allowed a reduced efficiency of MHC class I ligand production, whereas protein turnover and cellular proliferation were maintained. Using the proteasomal inhibitor adamantane-acetyl-(6-aminohexanoyl)3-(leucinyl)3-vinyl-(methyl)-sulphone, we show that covalent inhibition of all three types of proteasomal beta-subunits (beta(1), beta(2), and beta(5)) was compatible with continued growth in cells that up-regulate accessory proteolytic pathways, which include cytosolic proteases as well as deubiquitinating enzymes. However, under these conditions, we observed poor assembly of H-2D(b) molecules and inhibited presentation of endogenous tumor antigens. Thus, the tight link between protein turnover and production of MHC class I ligands can be broken by enforcing the substitution of the proteasome with alternative proteolytic pathways.

Publication types

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

MeSH terms

  • Animals
  • Antigen Presentation*
  • Cysteine Endopeptidases / physiology*
  • Cytosol / metabolism
  • H-2 Antigens / metabolism
  • Histocompatibility Antigens Class I / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Multienzyme Complexes / physiology*
  • Oligopeptides / pharmacology
  • Proteasome Endopeptidase Complex
  • Sulfones / pharmacology
  • T-Lymphocytes, Cytotoxic / immunology
  • Ubiquitin / metabolism

Substances

  • 4-hydroxy-5-iodo-3-nitrophenylacetyl-leucyl-leucyl-leucinal-vinyl sulfone
  • H-2 Antigens
  • H-2Kb protein, mouse
  • Histocompatibility Antigens Class I
  • Multienzyme Complexes
  • Oligopeptides
  • Sulfones
  • Ubiquitin
  • Cysteine Endopeptidases
  • Proteasome Endopeptidase Complex