Brg1 promotes both tumor-suppressive and oncogenic activities at distinct stages of pancreatic cancer formation

Genes Dev. 2015 Mar 15;29(6):658-71. doi: 10.1101/gad.256628.114.

Abstract

Pancreatic ductal adenocarcinoma (PDA) develops predominantly through pancreatic intraepithelial neoplasia (PanIN) and intraductal papillary mucinous neoplasm (IPMN) precursor lesions. Pancreatic acinar cells are reprogrammed to a "ductal-like" state during PanIN-PDA formation. Here, we demonstrate a parallel mechanism operative in mature duct cells during which functional cells undergo "ductal retrogression" to form IPMN-PDA. We further identify critical antagonistic roles for Brahma-related gene 1 (Brg1), a catalytic subunit of the SWI/SNF complexes, during IPMN-PDA development. In mature duct cells, Brg1 inhibits the dedifferentiation that precedes neoplastic transformation, thus attenuating tumor initiation. In contrast, Brg1 promotes tumorigenesis in full-blown PDA by supporting a mesenchymal-like transcriptional landscape. We further show that JQ1, a drug that is currently being tested in clinical trials for hematological malignancies, impairs PDA tumorigenesis by both mimicking some and inhibiting other Brg1-mediated functions. In summary, our study demonstrates the context-dependent roles of Brg1 and points to potential therapeutic treatment options based on epigenetic regulation in PDA.

Keywords: Brg1; EMT; IPMN; Kras; dedifferentiation; pancreatic cancer.

Publication types

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

MeSH terms

  • Animals
  • Azepines / pharmacology
  • Azepines / therapeutic use
  • Carcinoma, Pancreatic Ductal / drug therapy
  • Carcinoma, Pancreatic Ductal / physiopathology*
  • Cell Transformation, Neoplastic / drug effects
  • Cell Transformation, Neoplastic / genetics*
  • DNA Helicases / genetics
  • DNA Helicases / metabolism*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Mice
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / physiopathology*
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Triazoles / pharmacology
  • Triazoles / therapeutic use
  • Tumor Cells, Cultured

Substances

  • (+)-JQ1 compound
  • Azepines
  • Nuclear Proteins
  • SOX9 Transcription Factor
  • Sox9 protein, mouse
  • Transcription Factors
  • Triazoles
  • Smarca4 protein, mouse
  • DNA Helicases
  • Hras protein, mouse
  • Proto-Oncogene Proteins p21(ras)