FRA1 controls acinar cell plasticity during murine KrasG12D-induced pancreatic acinar to ductal metaplasia

Dev Cell. 2024 Nov 18;59(22):3025-3042.e7. doi: 10.1016/j.devcel.2024.07.021. Epub 2024 Aug 22.

Abstract

Acinar cells have been proposed as a cell-of-origin for pancreatic ductal adenocarcinoma (PDAC) after undergoing acinar-to-ductal metaplasia (ADM). ADM can be triggered by pancreatitis, causing acinar cells to de-differentiate to a ductal-like state. We identify FRA1 (gene name Fosl1) as the most active transcription factor during KrasG12D acute pancreatitis-mediated injury, and we have elucidated a functional role of FRA1 by generating an acinar-specific Fosl1 knockout mouse expressing KrasG12D. Using a gene regulatory network and pseudotime trajectory inferred from single-nuclei ATAC-seq and bulk RNA sequencing (RNA-seq), we hypothesized a regulatory model of the acinar-ADM-pancreatic intraepithelial neoplasia (PanIN) continuum and experimentally validated that Fosl1 knockout mice are delayed in the onset of ADM and neoplastic transformation. Our study also identifies that pro-inflammatory cytokines, such as granulocyte colony stimulating factor (G-CSF), can regulate FRA1 activity to modulate ADM. Our findings identify that FRA1 is a mediator of acinar cell plasticity and is critical for acinar cell de-differentiation and transformation.

Keywords: FRA1; G-CSF; KRAS; PanIN; acinar-ductal metaplasia; pancreatic ductal adenocarcinoma; pancreatitis.

MeSH terms

  • Acinar Cells* / metabolism
  • Acinar Cells* / pathology
  • Animals
  • Carcinoma, Pancreatic Ductal* / genetics
  • Carcinoma, Pancreatic Ductal* / metabolism
  • Carcinoma, Pancreatic Ductal* / pathology
  • Cell Plasticity* / genetics
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / metabolism
  • Cell Transformation, Neoplastic / pathology
  • Metaplasia* / genetics
  • Metaplasia* / metabolism
  • Metaplasia* / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Pancreas / metabolism
  • Pancreas / pathology
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Pancreatitis / genetics
  • Pancreatitis / metabolism
  • Pancreatitis / pathology
  • Proto-Oncogene Proteins c-fos* / genetics
  • Proto-Oncogene Proteins c-fos* / metabolism
  • Proto-Oncogene Proteins p21(ras)* / genetics
  • Proto-Oncogene Proteins p21(ras)* / metabolism

Substances

  • fos-related antigen 1
  • Proto-Oncogene Proteins c-fos
  • Proto-Oncogene Proteins p21(ras)
  • Hras protein, mouse