FAK loss reduces BRAFV600E-induced ERK phosphorylation to promote intestinal stemness and cecal tumor formation

Elife. 2024 Jun 26:13:RP94605. doi: 10.7554/eLife.94605.

Abstract

BRAFV600E mutation is a driver mutation in the serrated pathway to colorectal cancers. BRAFV600E drives tumorigenesis through constitutive downstream extracellular signal-regulated kinase (ERK) activation, but high-intensity ERK activation can also trigger tumor suppression. Whether and how oncogenic ERK signaling can be intrinsically adjusted to a 'just-right' level optimal for tumorigenesis remains undetermined. In this study, we found that FAK (Focal adhesion kinase) expression was reduced in BRAFV600E-mutant adenomas/polyps in mice and patients. In Vil1-Cre;BRAFLSL-V600E/+;Ptk2fl/fl mice, Fak deletion maximized BRAFV600E's oncogenic activity and increased cecal tumor incidence to 100%. Mechanistically, our results showed that Fak loss, without jeopardizing BRAFV600E-induced ERK pathway transcriptional output, reduced EGFR (epidermal growth factor receptor)-dependent ERK phosphorylation. Reduction in ERK phosphorylation increased the level of Lgr4, promoting intestinal stemness and cecal tumor formation. Our findings show that a 'just-right' ERK signaling optimal for BRAFV600E-induced cecal tumor formation can be achieved via Fak loss-mediated downregulation of ERK phosphorylation.

Keywords: BRAFV600E; EGFR; ERK; FAK; cancer biology; carcinogenesis; mouse.

MeSH terms

  • Animals
  • Carcinogenesis / genetics
  • Carcinogenesis / metabolism
  • Cecal Neoplasms* / genetics
  • Cecal Neoplasms* / metabolism
  • Cecal Neoplasms* / pathology
  • ErbB Receptors / genetics
  • ErbB Receptors / metabolism
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Focal Adhesion Kinase 1* / genetics
  • Focal Adhesion Kinase 1* / metabolism
  • Humans
  • MAP Kinase Signaling System
  • Male
  • Mice
  • Phosphorylation
  • Proto-Oncogene Proteins B-raf* / genetics
  • Proto-Oncogene Proteins B-raf* / metabolism
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism

Substances

  • Proto-Oncogene Proteins B-raf
  • BRAF protein, human
  • Focal Adhesion Kinase 1
  • Extracellular Signal-Regulated MAP Kinases
  • Ptk2 protein, mouse
  • ErbB Receptors
  • Braf protein, mouse
  • PTK2 protein, human
  • Receptors, G-Protein-Coupled

Associated data

  • GEO/GSE266355