Defective human leukocyte antigen class I-associated antigen presentation caused by a novel beta2-microglobulin loss-of-function in melanoma cells

J Biol Chem. 2006 Jul 7;281(27):18763-73. doi: 10.1074/jbc.M511525200. Epub 2006 Apr 28.

Abstract

The major histocompatibility complex class I molecules consist of three subunits, the 45-kDa heavy chain, the 12-kDa beta(2)-microglobulin (beta(2)m), and an approximately 8-9-residue antigenic peptide. Without beta(2)m, the major histocompatibility complex class I molecules cannot assemble, thereby abolishing their transport to the cell membrane and the subsequent recognition by antigen-specific T cells. Here we report a case of defective antigen presentation caused by the expression of a beta(2)m with a Cys-to-Trp substitution at position 25 (beta(2)m(C25W)). This substitution causes misfolding and degradation of beta(2)m(C25W) but does not result in complete lack of human leukocyte antigen (HLA) class I molecule expression on the surface of melanoma VMM5B cells. Despite HLA class I expression, VMM5B cells are not recognized by HLA class I-restricted, melanoma antigen-specific cytotoxic T lymphocytes even following loading with exogenous peptides or transduction with melanoma antigen-expressing viruses. Lysis of VMM5B cells is restored only following reconstitution with exogenous or endogenous wild-type beta(2)m protein. Together, our results indicate impairment of antigenic peptide presentation because of a dysfunctional beta(2)m and provide a mechanism for the lack of close association between HLA class I expression and susceptibility of tumor cells to cytotoxic T lymphocytes-mediated lysis in malignant diseases.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Antigen Presentation / genetics*
  • Base Sequence
  • Cell Line, Tumor
  • Cytotoxicity, Immunologic
  • Down-Regulation / immunology
  • Gene Expression Regulation, Neoplastic / immunology
  • Genes, MHC Class I / immunology*
  • HLA-A Antigens / genetics*
  • HLA-A Antigens / immunology
  • Humans
  • Melanoma / genetics
  • Melanoma / immunology*
  • Models, Molecular
  • Molecular Sequence Data
  • T-Lymphocytes, Cytotoxic / immunology
  • beta 2-Microglobulin / genetics*
  • beta 2-Microglobulin / immunology

Substances

  • HLA-A Antigens
  • beta 2-Microglobulin