Mutant KRas-Induced Mitochondrial Oxidative Stress in Acinar Cells Upregulates EGFR Signaling to Drive Formation of Pancreatic Precancerous Lesions

Cell Rep. 2016 Mar 15;14(10):2325-36. doi: 10.1016/j.celrep.2016.02.029. Epub 2016 Mar 3.

Abstract

The development of pancreatic cancer requires the acquisition of oncogenic KRas mutations and upregulation of growth factor signaling, but the relationship between these is not well established. Here, we show that mutant KRas alters mitochondrial metabolism in pancreatic acinar cells, resulting in increased generation of mitochondrial reactive oxygen species (mROS). Mitochondrial ROS then drives the dedifferentiation of acinar cells to a duct-like progenitor phenotype and progression to PanIN. This is mediated via the ROS-receptive kinase protein kinase D1 and the transcription factors NF-κB1 and NF-κB2, which upregulate expression of the epidermal growth factor, its ligands, and their sheddase ADAM17. In vivo, interception of KRas-mediated generation of mROS reduced the formation of pre-neoplastic lesions. Hence, our data provide insight into how oncogenic KRas interacts with growth factor signaling to induce the formation of pancreatic cancer.

Keywords: Kras; PanIN; growth factor signaling; mitochondria; oxidative stress; pancreatic cancer.

Publication types

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

MeSH terms

  • ADAM17 Protein / metabolism
  • Acinar Cells / cytology
  • Acinar Cells / metabolism*
  • Animals
  • Cells, Cultured
  • Epidermal Growth Factor / metabolism
  • ErbB Receptors / metabolism*
  • Humans
  • Ligands
  • Mice
  • Mitochondria / metabolism*
  • Mutagenesis, Site-Directed
  • NF-kappa B p52 Subunit / metabolism
  • Oxidative Stress*
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Precancerous Conditions
  • Protein Kinase C / metabolism
  • Proto-Oncogene Proteins p21(ras) / antagonists & inhibitors
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • RNA Interference
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Up-Regulation

Substances

  • Ligands
  • NF-kappa B p52 Subunit
  • Reactive Oxygen Species
  • Epidermal Growth Factor
  • protein kinase D
  • EGFR protein, mouse
  • ErbB Receptors
  • Protein Kinase C
  • ADAM17 Protein
  • Hras protein, mouse
  • Proto-Oncogene Proteins p21(ras)