Mechanical signals regulate and activate SNAIL1 protein to control the fibrogenic response of cancer-associated fibroblasts

J Cell Sci. 2016 May 15;129(10):1989-2002. doi: 10.1242/jcs.180539. Epub 2016 Apr 12.

Abstract

Increased deposition of collagen in extracellular matrix (ECM) leads to increased tissue stiffness and occurs in breast tumors. When present, this increases tumor invasion and metastasis. Precisely how this deposition is regulated and maintained in tumors is unclear. Much has been learnt about mechanical signal transduction in cells, but transcriptional responses and the pathophysiological consequences are just becoming appreciated. Here, we show that the SNAIL1 (also known as SNAI1) protein level increases and accumulates in nuclei of breast tumor cells and cancer-associated fibroblasts (CAFs) following exposure to stiff ECM in culture and in vivo SNAIL1 is required for the fibrogenic response of CAFs when exposed to a stiff matrix. ECM stiffness induces ROCK activity, which stabilizes SNAIL1 protein indirectly by increasing intracellular tension, integrin clustering and integrin signaling to ERK2 (also known as MAPK1). Increased ERK2 activity leads to nuclear accumulation of SNAIL1, and, thus, avoidance of cytosolic proteasome degradation. SNAIL1 also influences the level and activity of YAP1 in CAFs exposed to a stiff matrix. This work describes a mechanism whereby increased tumor fibrosis can perpetuate activation of CAFs to sustain tumor fibrosis and promote tumor metastasis through regulation of SNAIL1 protein level and activity.

Keywords: Extracellular matrix; Fibrosis; Mechanotransduction; SNAIL1.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / pathology
  • Cancer-Associated Fibroblasts / metabolism
  • Cancer-Associated Fibroblasts / pathology
  • Cell Line, Tumor
  • Collagen / metabolism
  • Extracellular Matrix / genetics
  • Extracellular Matrix / metabolism
  • Humans
  • Mitogen-Activated Protein Kinase 1 / genetics*
  • Phosphoproteins / genetics*
  • Signal Transduction
  • Snail Family Transcription Factors / genetics*
  • Transcription Factors
  • YAP-Signaling Proteins
  • rho-Associated Kinases / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • Phosphoproteins
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • Transcription Factors
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Collagen
  • ROCK1 protein, human
  • rho-Associated Kinases
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1