NFAT-induced histone acetylation relay switch promotes c-Myc-dependent growth in pancreatic cancer cells

Gastroenterology. 2010 Mar;138(3):1189-99.e1-2. doi: 10.1053/j.gastro.2009.10.045. Epub 2009 Nov 6.

Abstract

Background & aims: Induction of immediate early transcription factors (ITF) represents the first transcriptional program controlling mitogen-stimulated cell cycle progression in cancer. Here, we examined the transcriptional mechanisms regulating the ITF protein c-Myc and its role in pancreatic cancer growth in vitro and in vivo.

Methods: Expression of ITF proteins was examined by reverse-transcription polymerase chain reaction and immunoblotting, and its implications in cell cycle progression and growth was determined by flow cytometry and [(3)H]-thymidine incorporation. Intracellular Ca(2+) concentrations, calcineurin activity, and cellular nuclear factor of activated T cells (NFAT) distribution were analyzed. Transcription factor complex formations and promoter regulation were examined by immunoprecipitations, reporter gene assays, and chromatin immunoprecipitation. Using a combination of RNA interference knockdown technology and xenograft models, we analyzed the significance for pancreatic cancer tumor growth.

Results: Serum promotes pancreatic cancer growth through induction of the proproliferative NFAT/c-Myc axis. Mechanistically, serum increases intracellular Ca(2+) concentrations and activates the calcineurin/NFAT pathway to induce c-Myc transcription. NFAT binds to a serum responsive element within the proximal promoter, initiates p300-dependent histone acetylation, and creates a local chromatin structure permissive for the inducible recruitment of Ets-like gene (ELK)-1, a protein required for maximal activation of the c-Myc promoter. The functional significance of this novel pathway was emphasized by impaired c-Myc expression, G1 arrest, and reduced tumor growth upon NFAT depletion in vitro and in vivo.

Conclusions: Our study uncovers a novel mechanism regulating cell growth and identifies the NFAT/ELK complex as modulators of early stages of mitogen-stimulated proliferation in pancreatic cancer cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Adenocarcinoma / genetics
  • Adenocarcinoma / metabolism*
  • Adenocarcinoma / pathology
  • Animals
  • Binding Sites
  • Blotting, Western
  • Calcineurin / metabolism
  • Calcium / metabolism
  • Cell Cycle
  • Cell Line, Tumor
  • Cell Proliferation*
  • Chromatin Assembly and Disassembly*
  • Chromatin Immunoprecipitation
  • Flow Cytometry
  • Histones / metabolism*
  • Humans
  • Immunohistochemistry
  • Male
  • Mice
  • Mice, Nude
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / metabolism*
  • Neoplasm Transplantation
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology
  • Promoter Regions, Genetic
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism*
  • RNA Interference
  • Reverse Transcriptase Polymerase Chain Reaction
  • Serum / metabolism
  • Serum Response Element
  • Signal Transduction
  • Time Factors
  • Transcription, Genetic
  • Transfection
  • ets-Domain Protein Elk-1 / metabolism
  • p300-CBP Transcription Factors / metabolism

Substances

  • ELK1 protein, human
  • Histones
  • MYC protein, human
  • NFATC Transcription Factors
  • NFATC1 protein, human
  • NFATC2 protein, human
  • Proto-Oncogene Proteins c-myc
  • ets-Domain Protein Elk-1
  • p300-CBP Transcription Factors
  • p300-CBP-associated factor
  • Calcineurin
  • Calcium