Inhibition of tumor cell migration by LD22-4, an N-terminal fragment of 24-kDa FGF2, is mediated by Neuropilin 1

Cancer Res. 2013 Jun 1;73(11):3316-25. doi: 10.1158/0008-5472.CAN-12-3015. Epub 2013 May 10.

Abstract

LD22-4, an 86-amino acid fragment of the basic fibroblast growth factor, is an inhibitor of cell migration. LD22-4 inhibits the migration of various tumor cells, endothelial cells, and fibroblasts in vitro and suppresses tumor growth and angiogenesis in vivo. LD22-4 is effective in the presence of multiple growth factors, either alone or in combination, as well as haptotactic factors. LD22-4 inhibits the rate of malignant gliomas prepared from U87MG cells in an orthotopic mouse model by 90% compared with untreated mice. Using U87MG cells, we identified the LD22-4 membrane receptor as neuropilin 1 (NRP1). The identification of NRP1 as the LD22-4 receptor was based upon mass spectrometric analysis of proteins that bind to LD22-4, immunoprecipitation of an NRP1-LD22-4 complex formed during incubation of LD22-4 with U87MG cells, LD22-4-NRP1 coimmunoprecipitation studies, and binding of LD22-4 to HEK293 cells expressing NRP1. In contrast, NRP1 binding of an inactive mutant of LD22-4 was substantially reduced. As is typical of NRP1-binding proteins, LD22-4 itself binds to heparin and requires heparan sulfate for binding to cells. The addition of heparin to migration assays increased the inhibitory activity of LD22-4. In addition to a heparin-binding region, LD22-4 contains a 5-amino acid C-terminus that matches an NRP1 consensus binding sequence. Thus, direct binding experiments, dependence on heparan sulfate, and the presence of a NRP1 consensus binding sequence indicate that NRP1 is the binding site of LD22-4 and mediates inhibition of cell migration.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Binding Sites
  • Cell Growth Processes / drug effects
  • Cell Movement / drug effects*
  • Female
  • Fibroblast Growth Factor 2 / chemistry
  • Fibroblast Growth Factor 2 / pharmacology*
  • Glioma / drug therapy*
  • Glioma / metabolism
  • Glioma / pathology
  • HEK293 Cells
  • Heparin / chemistry
  • Heparin / metabolism
  • Humans
  • Mice
  • Mice, Nude
  • Neuropilin-1 / antagonists & inhibitors
  • Neuropilin-1 / metabolism*
  • Peptide Fragments / chemistry
  • Peptide Fragments / pharmacology*
  • Protein Binding
  • Xenograft Model Antitumor Assays

Substances

  • Peptide Fragments
  • Fibroblast Growth Factor 2
  • Neuropilin-1
  • Heparin