CTGF/VEGFA-activated Fibroblasts Promote Tumor Migration Through Micro-environmental Modulation

Mol Cell Proteomics. 2018 Aug;17(8):1502-1514. doi: 10.1074/mcp.RA118.000708. Epub 2018 Apr 18.

Abstract

Fibroblast activation is associated with tumor progression and implicated in metastasis, but the initial triggering signals required to kick-start this process remain largely unknown. Because small cancerous lesions share limited physical contact with neighboring fibroblasts, we reasoned the first tumor-derived signal for fibroblast activation should be secreted and diffusible. By pulsed metabolic labeling and click-chemistry based affinity enrichment, we sieved through the ductal carcinoma secretome for potential fibroblast activators. Using immuno-depletion/supplementation assays on various secreted factors, we pinpointed that tumor-secreted CTGF/VEGFA alone is sufficient to activate paired mammary fibroblasts from the same patient via ROCK1 and JunB signaling. Fibroblasts activated in this manner are distinct in morphology, growth, and adopt a highly tumor-like secretion profile, which in turn promotes tumor migration by counteracting oxidative and lactate stress. These findings reveal a profound division-of-labor between normal and cancer cells under the directive of the latter, and allude to potential metastatic prevention through inhibiting local fibroblast activation.

Keywords: Click chemistry; Mass Spectrometry; Metastasis; Secretome; Tumor microenvironment; fibroblast activation; reciprocal signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology*
  • Carcinoma, Ductal, Breast / metabolism
  • Carcinoma, Ductal, Breast / pathology
  • Cell Adhesion
  • Cell Line, Tumor
  • Cell Movement*
  • Connective Tissue Growth Factor / metabolism*
  • Female
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology*
  • Humans
  • Models, Biological
  • Oxidative Stress
  • Signal Transduction
  • Transcription Factors / metabolism
  • Tumor Microenvironment*
  • Vascular Endothelial Growth Factor A / metabolism*
  • rho-Associated Kinases / metabolism

Substances

  • JunB protein, human
  • Transcription Factors
  • Vascular Endothelial Growth Factor A
  • Connective Tissue Growth Factor
  • rho-Associated Kinases