Association of IFN-gamma signal transduction defects with impaired HLA class I antigen processing in melanoma cell lines

Clin Cancer Res. 2011 May 1;17(9):2668-78. doi: 10.1158/1078-0432.CCR-10-2114. Epub 2011 Jan 19.

Abstract

Purpose: Abnormalities in the constitutive and IFN-γ-inducible HLA class I surface antigen expression of tumor cells is often associated with an impaired expression of components of the antigen processing machinery (APM). Hence, we analyzed whether there exists a link between the IFN-γ signaling pathway, constitutive HLA class I APM component expression, and IFN-γ resistance.

Experimental design: The basal and IFN-γ-inducible expression profiles of HLA class I APM and IFN-γ signal transduction cascade components were assessed in melanoma cells by real-time PCR (RT-PCR), Western blot analysis and/or flow cytometry, the integrity of the Janus activated kinase (JAK) 2 locus by comparative genomic hybridization. JAK2 was transiently overexpressed in JAK2(-) cells. The effect of IFN-γ on the cell growth was assessed by XTT [2,3-bis(2-methoxy-4-nitro-S-sulfophenynl)-H-tetrazolium-5-carboxanilide inner salt] assay.

Results: The analysis of 8 melanoma cell lines linked the IFN-γ unresponsiveness of Colo 857 cells determined by lack of inducibility of HLA class I surface expression on IFN-γ treatment to a deletion of JAK2 on chromosome 9, whereas other IFN-γ signaling pathway components were not affected. In addition, the constitutive HLA class I APM component expression levels were significantly reduced in JAK2(-) cells. Furthermore, JAK2-deficient cells were also resistant to the antiproliferative effect of IFN-γ. Transfection of wild-type JAK2 into JAK2(-) Colo 857 not only increased the basal APM expression but also restored their IFN-γ sensitivity.

Conclusions: Impaired JAK2 expression in melanoma cells leads to reduced basal expression of MHC class I APM components and impairs their IFN-γ inducibility, suggesting that malfunctional IFN-γ signaling might cause HLA class I abnormalities.

Publication types

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

MeSH terms

  • Antigen Presentation / genetics*
  • Cell Line, Tumor
  • Comparative Genomic Hybridization
  • Drug Resistance / genetics
  • Histocompatibility Antigens Class I / immunology
  • Histocompatibility Antigens Class I / metabolism
  • Humans
  • Interferon-gamma / metabolism*
  • Interferon-gamma / pharmacology
  • Janus Kinase 2 / genetics
  • Janus Kinase 2 / metabolism
  • Janus Kinase 2 / physiology
  • Melanoma / genetics*
  • Melanoma / immunology*
  • Melanoma / metabolism
  • Phosphorylation
  • STAT1 Transcription Factor / metabolism
  • Signal Transduction / genetics
  • Skin Neoplasms / genetics*
  • Skin Neoplasms / immunology*
  • Skin Neoplasms / metabolism
  • Transfection

Substances

  • Histocompatibility Antigens Class I
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Interferon-gamma
  • Janus Kinase 2