C-myc activation impairs the NF-kappaB and the interferon response: implications for the pathogenesis of Burkitt's lymphoma

Int J Cancer. 2007 Apr 1;120(7):1387-95. doi: 10.1002/ijc.22372.

Abstract

Deregulation of the proto-oncogene c-myc is a key event in the pathogenesis of many tumors. A paradigm is the activation of the c-myc gene by chromosomal translocations in Burkitt lymphoma (BL). Despite expression of a restricted set of Epstein-Barr viral (EBV) antigens, BL cells are not recognized by antigen-specific cytotoxic T cells (CTLs) because of their inability to process and present HLA class I-restricted antigens. In contrast, cells of EBV-driven posttransplant lymphoproliferative disease (PTLD) are recognized and rejected by EBV-specific CTLs. It is not known whether the poor immunogenicity of BL cells is due to nonexpression of viral antigens, overexpression of c-myc, or both. To understand the basis for immune recognition and escape, we have compared the mRNA expression profiles of BL and EBV-immortalized cells (as PTLD model). Among the genes expressed at low level in BL cells, we have identified many genes involved in the NF-kappaB and interferon response that play a pivotal role in antigen presentation and immune recognition. Using a cell line in which EBNA2 and c-myc can be regulated at will, we show that c-MYC negatively regulates STAT1, the central player linking the Type-I and Type-II interferon response. Switching off c-myc expression leads to STAT1 induction through a direct and indirect mechanism involving induction of Type-I interferons. c-MYC thus masks an interferon-inducing activity in these cells. Our findings imply that immune escape of tumor cells is not only a matter of in vivo selection but may be additionally promoted by activation of a cellular oncogene.

Publication types

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

MeSH terms

  • Blotting, Western
  • Burkitt Lymphoma / etiology*
  • Chromatin Immunoprecipitation
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / physiology*
  • Genes, myc / physiology*
  • Humans
  • Interferon-beta / pharmacology*
  • Microarray Analysis
  • NF-kappa B / genetics*
  • Neoplasm Proteins / genetics*
  • Promoter Regions, Genetic
  • Proto-Oncogene Mas
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / metabolism
  • Tumor Cells, Cultured

Substances

  • MAS1 protein, human
  • NF-kappa B
  • Neoplasm Proteins
  • Proto-Oncogene Mas
  • RNA, Messenger
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Interferon-beta