TRIM27/MRTF-B-dependent integrin β1 expression defines leading cells in cancer cell collectives

Cell Rep. 2014 May 22;7(4):1156-67. doi: 10.1016/j.celrep.2014.03.068. Epub 2014 May 1.

Abstract

For collective invasion, cancer cells form cohesive groups comprised of leading cells (LCs) at the forefront and following cells (FCs) at the rear. However, the molecular mechanisms that define LCs and FCs remain elusive. Here, we demonstrated that LCs, but not FCs, upregulated the expression of integrin β1 after the loss of intercellular adhesion. The LC-specific expression of integrin β1 was posttranscriptionally regulated by the TRIM27/MRTF-B complex in response to the loss of intercellular adhesion, thereby regulating the stability and translation of integrin β1 mRNA via microRNA-124 in LCs. Accordingly, depletion of TRIM27 and MRTF-B abrogated the upregulation of integrin β1 in LCs and blocked the invasion of cancer cell groups in vitro and in vivo. Therefore, our findings revealed that the specific function of LCs was defined by intrinsic mechanisms related to the presence of the cell's free surface, providing insights into the regulation of intratumor heterogeneity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism*
  • Cell Adhesion / physiology
  • Cell Line, Tumor
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Disease Models, Animal
  • Female
  • HEK293 Cells
  • Humans
  • Integrin beta1 / biosynthesis*
  • Integrin beta1 / genetics
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Signal Transduction
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Ubiquitin-Protein Ligases
  • Up-Regulation

Substances

  • DNA-Binding Proteins
  • Integrin beta1
  • Nuclear Proteins
  • TRIM27 protein, human
  • Transcription Factors
  • myocardin-related transcription factor B, mouse
  • Trim27 protein, mouse
  • Ubiquitin-Protein Ligases