Defective N-sulfation of heparan sulfate proteoglycans limits PDGF-BB binding and pericyte recruitment in vascular development

Genes Dev. 2007 Feb 1;21(3):316-31. doi: 10.1101/gad.398207.

Abstract

During vascular development, endothelial platelet-derived growth factor B (PDGF-B) is critical for pericyte recruitment. Deletion of the conserved C-terminal heparin-binding motif impairs PDGF-BB retention and pericyte recruitment in vivo, suggesting a potential role for heparan sulfate (HS) in PDGF-BB function during vascular development. We studied the participation of HS chains in pericyte recruitment using two mouse models with altered HS biosynthesis. Reduction of N-sulfation due to deficiency in N-deacetylase/N-sulfotransferase-1 attenuated PDGF-BB binding in vitro, and led to pericyte detachment and delayed pericyte migration in vivo. Reduced N-sulfation also impaired PDGF-BB signaling and directed cell migration, but not proliferation. In contrast, HS from glucuronyl C5-epimerase mutants, which is extensively N- and 6-O-sulfated, but lacks 2-O-sulfated L-iduronic acid residues, retained PDGF-BB in vitro, and pericyte recruitment in vivo was only transiently delayed. These observations were supported by in vitro characterization of the structural features in HS important for PDGF-BB binding. We conclude that pericyte recruitment requires HS with sufficiently extended and appropriately spaced N-sulfated domains to retain PDGF-BB and activate PDGF receptor beta (PDGFRbeta) signaling, whereas the detailed sequence of monosaccharide and sulfate residues does not appear to be important for this interaction.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Becaplermin
  • Blood Vessels / embryology*
  • Cell Movement
  • Dimerization
  • Endothelium, Vascular / metabolism
  • Heparan Sulfate Proteoglycans / metabolism*
  • Heparitin Sulfate / metabolism
  • Heparitin Sulfate / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Biological
  • Pericytes / metabolism*
  • Platelet-Derived Growth Factor / metabolism*
  • Protein Binding
  • Protein Processing, Post-Translational / physiology*
  • Proto-Oncogene Proteins c-sis
  • Rhombencephalon / embryology
  • Rhombencephalon / metabolism
  • Sulfates / metabolism*
  • Sulfotransferases / genetics

Substances

  • Heparan Sulfate Proteoglycans
  • Platelet-Derived Growth Factor
  • Proto-Oncogene Proteins c-sis
  • Sulfates
  • Becaplermin
  • Heparitin Sulfate
  • Sulfotransferases
  • heparitin sulfotransferase