ATDC induces an invasive switch in KRAS-induced pancreatic tumorigenesis

Genes Dev. 2015 Jan 15;29(2):171-83. doi: 10.1101/gad.253591.114.

Abstract

The initiation of pancreatic ductal adenocarcinoma (PDA) is linked to activating mutations in KRAS. However, in PDA mouse models, expression of oncogenic mutant KRAS during development gives rise to tumors only after a prolonged latency or following induction of pancreatitis. Here we describe a novel mouse model expressing ataxia telangiectasia group D complementing gene (ATDC, also known as TRIM29 [tripartite motif 29]) that, in the presence of oncogenic KRAS, accelerates pancreatic intraepithelial neoplasia (PanIN) formation and the development of invasive and metastatic cancers. We found that ATDC up-regulates CD44 in mouse and human PanIN lesions via activation of β-catenin signaling, leading to the induction of an epithelial-to-mesenchymal transition (EMT) phenotype characterized by expression of Zeb1 and Snail1. We show that ATDC is up-regulated by oncogenic Kras in a subset of PanIN cells that are capable of invading the surrounding stroma. These results delineate a novel molecular pathway for EMT in pancreatic tumorigenesis, showing that ATDC is a proximal regulator of EMT.

Keywords: epithelial–mesenchymal transition; metastasis; pancreatic ductal adenocarcinoma.

Publication types

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

MeSH terms

  • Animals
  • Carcinoma, Pancreatic Ductal / physiopathology*
  • Disease Models, Animal
  • Epithelial-Mesenchymal Transition / genetics
  • Gene Expression Regulation, Neoplastic
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Hyaluronan Receptors / metabolism
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Mice
  • Mice, Transgenic
  • Neoplasm Invasiveness / genetics
  • Pancreatic Neoplasms / enzymology
  • Pancreatic Neoplasms / physiopathology*
  • Promoter Regions, Genetic / genetics
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • Snail Family Transcription Factors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Zinc Finger E-box-Binding Homeobox 1
  • beta Catenin / metabolism

Substances

  • Homeodomain Proteins
  • Hyaluronan Receptors
  • Kruppel-Like Transcription Factors
  • SNAI1 protein, human
  • Snai1 protein, mouse
  • Snail Family Transcription Factors
  • TRIM29 protein, mouse
  • Transcription Factors
  • ZEB1 protein, mouse
  • Zinc Finger E-box-Binding Homeobox 1
  • beta Catenin
  • Hras protein, mouse
  • Proto-Oncogene Proteins p21(ras)