Autocrine netrin function inhibits glioma cell motility and promotes focal adhesion formation

PLoS One. 2011;6(9):e25408. doi: 10.1371/journal.pone.0025408. Epub 2011 Sep 28.

Abstract

Deregulation of mechanisms that control cell motility plays a key role in tumor progression by promoting tumor cell dissemination. Secreted netrins and their receptors, Deleted in Colorectal Cancer (DCC), neogenin, and the UNC5 homologues, regulate cell and axon migration, cell adhesion, and tissue morphogenesis. Netrin and netrin receptor expression have previously been shown to be disrupted in invasive tumors, including glioblastoma. We determined that the human glioblastoma cell lines U87, U343, and U373 all express neogenin, UNC5 homologues, and netrin-1 or netrin-3, but only U87 cells express DCC. Using transfilter migration assays, we demonstrate DCC-dependent chemoattractant migration of U87 cells up a gradient of netrin-1. In contrast, U343 and U373 cells, which do not express DCC, were neither attracted nor repelled. Ectopic expression of DCC by U343 and U373 cells resulted in these cells becoming competent to respond to a gradient of netrin-1 as a chemoattractant, and also slowed their rate of spontaneous migration. Here, in addition to netrins' well-characterized chemotropic activity, we demonstrate an autocrine function for netrin-1 and netrin-3 in U87 and U373 cells that slows migration. We provide evidence that netrins promote the maturation of focal complexes, structures associated with cell movement, into focal adhesions. Consistent with this, netrin, DCC, and UNC5 homologues were associated with focal adhesions, but not focal complexes. Disrupting netrin or DCC function did not alter cell proliferation or survival. Our findings provide evidence that DCC can slow cell migration, and that neogenin and UNC5 homologues are not sufficient to substitute for DCC function in these cells. Furthermore, we identify a role for netrins as autocrine inhibitors of cell motility that promote focal adhesion formation. These findings suggest that disruption of netrin signalling may disable a mechanism that normally restrains inappropriate cell migration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autocrine Communication* / drug effects
  • Cell Line, Tumor
  • Cell Movement* / drug effects
  • Colorectal Neoplasms / genetics
  • Focal Adhesions / drug effects
  • Focal Adhesions / metabolism*
  • Gene Deletion
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glioma / pathology*
  • Humans
  • Laminin / pharmacology
  • Nerve Growth Factors / deficiency
  • Nerve Growth Factors / genetics
  • Nerve Growth Factors / metabolism*
  • Netrin Receptors
  • Netrin-1
  • Protein Transport / drug effects
  • Receptors, Cell Surface / deficiency
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism
  • Tumor Suppressor Proteins / deficiency
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Laminin
  • NTN1 protein, human
  • Nerve Growth Factors
  • Netrin Receptors
  • Receptors, Cell Surface
  • Tumor Suppressor Proteins
  • laminin 1
  • Netrin-1