Human Pancreatic Tumor Organoids Reveal Loss of Stem Cell Niche Factor Dependence during Disease Progression

Cell Stem Cell. 2018 Mar 1;22(3):454-467.e6. doi: 10.1016/j.stem.2017.12.009. Epub 2018 Jan 11.

Abstract

Despite recent efforts to dissect the inter-tumor heterogeneity of pancreatic ductal adenocarcinoma (PDAC) by determining prognosis-predictive gene expression signatures for specific subtypes, their functional differences remain elusive. Here, we established a pancreatic tumor organoid library encompassing 39 patient-derived PDACs and identified 3 functional subtypes based on their stem cell niche factor dependencies on Wnt and R-spondin. A Wnt-non-producing subtype required Wnt from cancer-associated fibroblasts, whereas a Wnt-producing subtype autonomously secreted Wnt ligands and an R-spondin-independent subtype grew in the absence of Wnt and R-spondin. Transcriptome analysis of PDAC organoids revealed gene-expression signatures that associated Wnt niche subtypes with GATA6-dependent gene expression subtypes, which were functionally supported by genetic perturbation of GATA6. Furthermore, CRISPR-Cas9-based genome editing of PDAC driver genes (KRAS, CDKN2A, SMAD4, and TP53) demonstrated non-genetic acquisition of Wnt niche independence during pancreas tumorigenesis. Collectively, our results reveal functional heterogeneity of Wnt niche independency in PDAC that is non-genetically formed through tumor progression.

Keywords: CRISPR-Cas9; GATA6; Wnt; organoids; pancreatic cancer; stem cell niche.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CRISPR-Cas Systems / genetics
  • Disease Progression*
  • Epithelial Cells / metabolism
  • Fibroblasts / metabolism
  • GATA6 Transcription Factor / metabolism
  • Gene Expression Regulation, Neoplastic
  • Genetic Engineering
  • Humans
  • Ligands
  • Organoids / pathology*
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / pathology*
  • Stem Cell Niche*
  • Wnt Signaling Pathway

Substances

  • GATA6 Transcription Factor
  • Ligands