Functional antagonists of sonic hedgehog reveal the importance of the N terminus for activity

J Cell Sci. 1999 Dec:112 ( Pt 23):4405-14. doi: 10.1242/jcs.112.23.4405.

Abstract

During development, sonic hedgehog functions as a morphogen in both a short-range contact-dependent and in a long-range diffusable mode. Here, we show using a panel of sonic hedgehog variants that regions near the N terminus of the protein play a critical role in modulating these functions. In the hedgehog responsive cell line C3H10T1/2, we discovered that not only were some N-terminally truncated variants inactive at eliciting a hedgehog-dependent response, but they competed with the wild-type protein for function and therefore served as functional antagonists. These variants were indistinguishable from wild-type sonic hedgehog in their ability to bind the receptor patched-1, but failed to induce the hedgehog-responsive markers, Gli-1 and Ptc-1, and failed to promote hedgehog-dependent differentiation of the cell line. They also failed to support the adhesion of C3H10T1/2 cells to hedgehog-coated plates under conditions where wild-type sonic hedgehog supported binding. Structure-activity data indicated that the N-terminal cysteine plays a key regulatory role in modulating hedgehog activity. The ability to dissect patched-1 binding from signaling events in C3H10T1/2 cells suggests the presence of unidentified factors that contribute to hedgehog responses.

MeSH terms

  • Alkaline Phosphatase / biosynthesis
  • Alkaline Phosphatase / genetics*
  • Animals
  • Binding Sites
  • Cell Adhesion
  • Cell Line
  • Cell Movement
  • Chick Embryo
  • Cloning, Molecular
  • Embryonic Induction
  • Enzyme Induction
  • Escherichia coli
  • Hedgehog Proteins
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Mice
  • Mice, Transgenic
  • Nervous System / cytology
  • Nervous System / embryology
  • Oncogene Proteins / metabolism
  • Organ Culture Techniques
  • Patched Receptors
  • Patched-1 Receptor
  • Peptide Fragments / chemistry
  • Peptide Fragments / metabolism
  • Pichia
  • Proteins / antagonists & inhibitors
  • Proteins / chemistry*
  • Proteins / genetics
  • Proteins / metabolism*
  • Receptors, Cell Surface
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Sequence Deletion
  • Trans-Activators*
  • beta-Galactosidase / genetics

Substances

  • Hedgehog Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Oncogene Proteins
  • PTCH1 protein, human
  • Patched Receptors
  • Patched-1 Receptor
  • Peptide Fragments
  • Proteins
  • Ptch1 protein, mouse
  • Receptors, Cell Surface
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • SHH protein, human
  • Trans-Activators
  • Alkaline Phosphatase
  • beta-Galactosidase