Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats

Circulation. 1999 Sep 28;100(13):1423-31. doi: 10.1161/01.cir.100.13.1423.

Abstract

Background: Suppression of tumor growth by thrombospondin-1 (TSP-1) has been associated with its ability to inhibit neovascularization. The antiangiogenic activity of TSP-1, as defined by cornea pocket assays, was previously mapped to the amino-terminal portion of the protein within the procollagen region and the type 1 repeats.

Methods and results: We evaluated the specificity and efficacy of different regions of TSP-1 using recombinant fragments of the protein on chorioallantoic membrane (CAM) angiogenesis and endothelial cell proliferation assays. In both assays, fragments containing the second and third type 1 repeats but not the procollagen region inhibited angiogenesis and endothelial cell proliferation. To further define the sequences responsible for the angiostatic effect of TSP-1, we used synthetic peptides. The CAM assay defined 2 sequences that independently suppressed angiogenesis. The amino-terminal end of the type 1 repeats showed higher potency for inhibiting angiogenesis driven by basic fibroblast growth factor (FGF-2), whereas the second region equally blocked angiogenesis driven by either FGF-2 or vascular endothelial growth factor (VEGF). Modifications of the active peptides revealed the specific amino acids required for the inhibitory response. One sequence included the conserved tryptophan residues in the amino-terminal end of the second and third type 1 repeats, and the other involved the amino acids that follow the CSVTCG sequence in the carboxy-terminus of these repeats. Both inhibition in the CAM assay and inhibition of breast tumor xenograft growth in nude mice were independent of the TGF-beta-activating sequence located in the second type 1 repeat.

Conclusions: These results indicate that the type 1 repeats of TSP-1 contain 2 subdomains that may independently inhibit neovascularization. They also identify 2 independent pathways by which TSP-1 can block FGF-2 and VEGF angiogenic signals on endothelial cells.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence / genetics
  • Animals
  • Cell Division / drug effects
  • Chick Embryo
  • Endothelial Growth Factors / antagonists & inhibitors
  • Endothelial Growth Factors / physiology
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / drug effects
  • Extraembryonic Membranes / blood supply
  • Extraembryonic Membranes / drug effects
  • Female
  • Fibroblast Growth Factor 2 / antagonists & inhibitors
  • Fibroblast Growth Factor 2 / physiology
  • Lymphokines / antagonists & inhibitors
  • Lymphokines / physiology
  • Mammary Neoplasms, Animal / pathology
  • Mice
  • Mice, Nude
  • Molecular Sequence Data
  • Neovascularization, Pathologic / prevention & control*
  • Peptide Fragments / genetics
  • Peptide Fragments / pharmacology
  • Recombinant Proteins
  • Repetitive Sequences, Amino Acid
  • Signal Transduction / drug effects
  • Thrombospondin 1 / genetics*
  • Thrombospondin 1 / pharmacology*
  • Transplantation, Heterologous
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors

Substances

  • Endothelial Growth Factors
  • Lymphokines
  • Peptide Fragments
  • Recombinant Proteins
  • Thrombospondin 1
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • Fibroblast Growth Factor 2