Activin A binds to perlecan through its pro-region that has heparin/heparan sulfate binding activity

J Biol Chem. 2010 Nov 19;285(47):36645-55. doi: 10.1074/jbc.M110.177865. Epub 2010 Sep 15.

Abstract

Activin A, a member of the transforming growth factor-β family, plays important roles in hormonal homeostasis and embryogenesis. In this study, we produced recombinant human activin A and examined its abilities to bind to extracellular matrix proteins. Recombinant activin A expressed in 293-F cells was purified as complexes of mature dimeric activin A with its pro-region. Among a panel of extracellular matrix proteins tested, recombinant activin A bound to perlecan and agrin, but not to laminins, nidogens, collagens I and IV, fibronectin, and nephronectin. The binding of recombinant activin A to perlecan was inhibited by heparin and high concentrations of NaCl and abolished by heparitinase treatment of perlecan, suggesting that activin A binds to the heparan sulfate chains of perlecan. In support of this possibility, recombinant activin A was capable of directly binding to heparin and heparan sulfate chains. Site-directed mutagenesis of recombinant activin A revealed that clusters of basic amino acid residues, Lys(259)-Lys(263) and Lys(270)-Lys(272), in the pro-region were required for binding to perlecan. Interestingly, deletion of the peptide segment Lys(259)-Gly(277) containing both basic amino acid clusters from the pro-region did not impair the activity of activin A to stimulate Smad-dependent gene expressions, although it completely ablated the perlecan-binding activity. The binding of activin A to basement membrane heparan sulfate proteoglycans through the basic residues in the pro-region was further confirmed by in situ activin A overlay assays using frozen tissue sections. Taken together, the present results indicate that activin A binds to heparan sulfate proteoglycans through its pro-region and thereby regulates its localization within tissues.

MeSH terms

  • Activins / genetics
  • Activins / metabolism*
  • Amino Acid Sequence
  • Animals
  • Blotting, Western
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / metabolism
  • Extracellular Matrix Proteins / metabolism
  • Heparan Sulfate Proteoglycans / metabolism*
  • Heparin / metabolism*
  • Heparitin Sulfate / metabolism*
  • Humans
  • Immunoenzyme Techniques
  • Laminin / metabolism
  • Luciferases / metabolism
  • Membrane Glycoproteins / metabolism
  • Mice
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Protein Binding
  • Recombinant Proteins / metabolism*
  • Sequence Homology, Amino Acid

Substances

  • Extracellular Matrix Proteins
  • Heparan Sulfate Proteoglycans
  • Laminin
  • Membrane Glycoproteins
  • Recombinant Proteins
  • activin A
  • nephronectin
  • nidogen
  • Activins
  • perlecan
  • Heparin
  • Heparitin Sulfate
  • Luciferases