Syndecan-1 modulates β-integrin-dependent and interleukin-6-dependent functions in breast cancer cell adhesion, migration, and resistance to irradiation

FEBS J. 2013 May;280(10):2216-27. doi: 10.1111/febs.12111. Epub 2013 Jan 31.

Abstract

Syndecan-1 is a cell surface heparan sulfate proteoglycan with various biological functions relevant to tumor progression and inflammation, including cell-cell adhesion, cell-matrix interaction, and cytokine signaling driving cell proliferation and motility. Syndecan-1 is a prognostic factor in breast cancer, and has a predicitive value for neodadjuvant chemotherapy. It is still poorly understood how syndecan-1 integrates matrix-dependent and cytokine-dependent signaling processes in the tumor microenvironment. Here, we evaluated the potential role of syndecan-1 in modulating matrix-dependent breast cancer cell migration in the presence of interleukin-6, and its potential involvement in resistance to irradiation in vitro. MDA-MB-231 breast cancer cells were transiently transfected with syndecan-1 small interfering RNA or control reagents, and this was followed by stimulation with interleukin-6 or irradiation. Cellular responses were monitored by adhesion, migration and colony formation assays, as well as analysis of cell signaling. Syndecan-1 depletion increased cell adhesion to fibronectin. Increased migration on fibronectin was significantly suppressed by interleukin-6, and GRGDSP peptides inhibited both adhesion and migration. Interleukin-6-induced activation of focal adhesion kinase and reduction of constitutive nuclear factor kappaB signaling were decreased in syndecan-1-deficient cells. Focal adhesion kinase hyperactivation in syndecan-1-depleted cells was associated with dramatically reduced radiation sensitivity. We conclude that loss of syndecan-1 leads to enhanced activation of β1 -integrins and focal adhesion kinase, thus increasing breast cancer cell adhesion, migration, and resistance to irradiation. Syndecan-1 deficiency also attenuates the modulatory effect of the inflammatory microenvironment constituent interleukin-6 on cancer cell migration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blotting, Western
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Adhesion
  • Cell Line, Tumor / radiation effects
  • Cell Migration Assays
  • Cell Movement*
  • Enzyme Activation
  • Female
  • Fibronectins / metabolism
  • Fibronectins / pharmacology
  • Focal Adhesion Kinase 1
  • Humans
  • Integrin alpha5beta1 / metabolism*
  • Interleukin-6 / metabolism
  • Interleukin-6 / pharmacology*
  • NF-kappa B / metabolism
  • Oligopeptides / pharmacology
  • Photons
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Radiation Tolerance*
  • Signal Transduction
  • Syndecan-1 / metabolism*
  • Transfection
  • Tumor Microenvironment
  • Tumor Stem Cell Assay

Substances

  • Fibronectins
  • Integrin alpha5beta1
  • Interleukin-6
  • NF-kappa B
  • Oligopeptides
  • RNA, Small Interfering
  • SDC1 protein, human
  • Syndecan-1
  • glycyl-arginyl-glycyl-aspartyl-seryl-proline
  • Focal Adhesion Kinase 1
  • PTK2 protein, human