Thrombospondin-1 (TSP-1), a new bone morphogenetic protein-2 and -4 (BMP-2/4) antagonist identified in pituitary cells

J Biol Chem. 2017 Sep 15;292(37):15352-15368. doi: 10.1074/jbc.M116.736207. Epub 2017 Jul 26.

Abstract

Bone morphogenetic proteins (BMPs) regulate diverse cellular responses during embryogenesis and in adulthood including cell differentiation, proliferation, and death in various tissues. In the adult pituitary, BMPs participate in the control of hormone secretion and cell proliferation, suggesting a potential endocrine/paracrine role for BMPs, but some of the mechanisms are unclear. Here, using a bioactivity test based on embryonic cells (C3H10T1/2) transfected with a BMP-responsive element, we sought to determine whether pituitary cells secrete BMPs or BMP antagonists. Interestingly, we found that pituitary-conditioned medium contains a factor that inhibits action of BMP-2 and -4. Combining surface plasmon resonance and high-resolution mass spectrometry helped pinpoint this factor as thrombospondin-1 (TSP-1). Surface plasmon resonance and co-immunoprecipitation confirmed that recombinant human TSP-1 can bind BMP-2 and -4 and antagonize their effects on C3H10T1/2 cells. Moreover, TSP-1 inhibited the action of serum BMPs. We also report that the von Willebrand type C domain of TSP-1 is likely responsible for this BMP-2/4-binding activity, an assertion based on sequence similarity that TSP-1 shares with the von Willebrand type C domain of Crossveinless 2 (CV-2), a BMP antagonist and member of the chordin family. In summary, we identified for the first time TSP-1 as a BMP-2/-4 antagonist and presented a structural basis for the physical interaction between TSP-1 and BMP-4. We propose that TSP-1 could regulate bioavailability of BMPs, either produced locally or reaching the pituitary via blood circulation. In conclusion, our findings provide new insights into the involvement of TSP-1 in the BMP-2/-4 mechanisms of action.

Keywords: C3H10T1/2 cells; bone morphogenetic protein (BMP); bone morphogenetic protein antagonist; pituitary gland; structural model; surface plasmon resonance (SPR); thrombospondin.

MeSH terms

  • Animals
  • Animals, Inbred Strains
  • Bone Morphogenetic Protein 2 / antagonists & inhibitors*
  • Bone Morphogenetic Protein 2 / blood
  • Bone Morphogenetic Protein 2 / genetics
  • Bone Morphogenetic Protein 2 / metabolism
  • Bone Morphogenetic Protein 4 / antagonists & inhibitors*
  • Bone Morphogenetic Protein 4 / blood
  • Bone Morphogenetic Protein 4 / genetics
  • Bone Morphogenetic Protein 4 / metabolism
  • Cell Line
  • Cells, Cultured
  • Computational Biology
  • Female
  • Genes, Reporter
  • Humans
  • Mice
  • Models, Molecular*
  • Pituitary Gland / cytology
  • Pituitary Gland / metabolism*
  • Protein Interaction Domains and Motifs
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / isolation & purification
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Response Elements*
  • Sequence Homology, Amino Acid
  • Sheep, Domestic
  • Thrombospondin 1 / chemistry
  • Thrombospondin 1 / isolation & purification
  • Thrombospondin 1 / metabolism*

Substances

  • BMP2 protein, human
  • BMP4 protein, human
  • Bone Morphogenetic Protein 2
  • Bone Morphogenetic Protein 4
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Thrombospondin 1
  • thrombospondin-1, human

Associated data

  • PDB/3bk3
  • PDB/3BK3
  • PDB/2H62