Synergistic induction of the MUC4 mucin gene by interferon-gamma and retinoic acid in human pancreatic tumour cells involves a reprogramming of signalling pathways

Oncogene. 2005 Sep 8;24(40):6143-54. doi: 10.1038/sj.onc.1208756.

Abstract

The transmembrane mucin, MUC4, is aberrantly expressed with a high incidence in human pancreatic adenocarcinomas and plays an important role in the pathogenesis of the disease. Our recent studies have shown that interferon-gamma (IFNgamma) and retinoic acid (RA) are important regulators of MUC4 in pancreatic tumour cells. Induction of MUC4 by IFNgamma occurs via a novel pathway involving upregulation of the signal transducer and activator of transcription 1 (STAT-1), whereas its stimulation by RA requires mediation by the transforming growth factor beta-2 (TGFbeta-2). In this study, we have investigated the molecular mechanisms underlying the interaction of IFNgamma and RA in MUC4 regulation in pancreatic tumour cells. We demonstrate that these reagents exert a synergistic induction of MUC4. Interestingly, while the upregulation of STAT-1 by IFNgamma is partially inhibited by RA, IFNgamma is shown to repress RA-driven TGFbeta-2 induction, pointing to the involvement of alternative mechanism(s) in IFNgamma-RA synergism. Moreover, a dose-dependent and cooperative induction of MUC4 promoter activity suggests a regulation at the transcriptional level, most likely by STAT-1 and RAR/RXR (RA receptor/retinoic X receptor) or other IFNgamma/RA-induced secondary intermediate effectors. Our findings provide potential mechanisms that may account for the aberrant expression of MUC4 in pancreatic tumour cells and expose a novel molecular mechanism of gene induction, whereby a reprogramming of signalling pathway through alternative route(s) operates during a synergistic interaction of biological modifiers.

Publication types

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

MeSH terms

  • Cell Line, Tumor
  • DNA-Binding Proteins / physiology
  • Drug Synergism
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Interferon-gamma / pharmacology*
  • Mucin-4
  • Mucins / biosynthesis*
  • Mucins / genetics*
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / pathology
  • Receptors, Retinoic Acid / physiology
  • Retinoic Acid Receptor alpha
  • Retinoic Acid Receptor gamma
  • STAT1 Transcription Factor
  • Signal Transduction
  • Trans-Activators / physiology
  • Transcriptional Activation
  • Tretinoin / pharmacology*
  • Up-Regulation

Substances

  • DNA-Binding Proteins
  • MUC4 protein, human
  • Mucin-4
  • Mucins
  • RARA protein, human
  • Receptors, Retinoic Acid
  • Retinoic Acid Receptor alpha
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Trans-Activators
  • Tretinoin
  • Interferon-gamma