The Chromatin Assembly Factor Complex 1 (CAF1) and 5-Azacytidine (5-AzaC) Affect Cell Motility in Src-transformed Human Epithelial Cells

J Biol Chem. 2017 Jan 6;292(1):172-184. doi: 10.1074/jbc.M116.751024. Epub 2016 Nov 21.

Abstract

Tumor invasion into surrounding stromal tissue is a hallmark of high grade, metastatic cancers. Oncogenic transformation of human epithelial cells in culture can be triggered by activation of v-Src kinase, resulting in increased cell motility, invasiveness, and tumorigenicity and provides a valuable model for studying how changes in gene expression cause cancer phenotypes. Here, we show that epithelial cells transformed by activated Src show increased levels of DNA methylation and that the methylation inhibitor 5-azacytidine (5-AzaC) potently blocks the increased cell motility and invasiveness induced by Src activation. A proteomic screen for chromatin regulators acting downstream of activated Src identified the replication-dependent histone chaperone CAF1 as an important factor for Src-mediated increased cell motility and invasion. We show that Src causes a 5-AzaC-sensitive decrease in both mRNA and protein levels of the p150 (CHAF1A) and p60 (CHAF1B), subunits of CAF1. Depletion of CAF1 in untransformed epithelial cells using siRNA was sufficient to recapitulate the increased motility and invasive phenotypes characteristic of transformed cells without activation of Src. Maintaining high levels of CAF1 by exogenous expression suppressed the increased cell motility and invasiveness phenotypes when Src was activated. These data identify a critical role of CAF1 in the dysregulation of cell invasion and motility phenotypes seen in transformed cells and also highlight an important role for epigenetic remodeling through DNA methylation for Src-mediated induction of cancer phenotypes.

Keywords: Src; cancer biology; cell invasion; cell migration; chromatin; gene expression; proteomics.

MeSH terms

  • Antimetabolites, Antineoplastic / pharmacology
  • Azacitidine / pharmacology*
  • Breast / drug effects
  • Breast / metabolism
  • Breast / pathology*
  • Cell Movement*
  • Cell Transformation, Neoplastic / drug effects
  • Cell Transformation, Neoplastic / metabolism
  • Cell Transformation, Neoplastic / pathology*
  • Cells, Cultured
  • Chromatin Assembly and Disassembly
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology*
  • Female
  • Humans
  • Mass Spectrometry
  • Neoplasm Invasiveness
  • Oncogene Protein pp60(v-src) / genetics
  • Oncogene Protein pp60(v-src) / metabolism*
  • Protein Subunits
  • Proteomics
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Antimetabolites, Antineoplastic
  • CNOT8 protein, human
  • Protein Subunits
  • Transcription Factors
  • Oncogene Protein pp60(v-src)
  • Azacitidine