Small-molecule modulators of Hedgehog signaling: identification and characterization of Smoothened agonists and antagonists

J Biol. 2002 Nov 6;1(2):10. doi: 10.1186/1475-4924-1-10.

Abstract

Background: The Hedgehog (Hh) signaling pathway is vital to animal development as it mediates the differentiation of multiple cell types during embryogenesis. In adults, Hh signaling can be activated to facilitate tissue maintenance and repair. Moreover, stimulation of the Hh pathway has shown therapeutic efficacy in models of neuropathy. The underlying mechanisms of Hh signal transduction remain obscure, however: little is known about the communication between the pathway suppressor Patched (Ptc), a multipass transmembrane protein that directly binds Hh, and the pathway activator Smoothened (Smo), a protein that is related to G-protein-coupled receptors and is capable of constitutive activation in the absence of Ptc.

Results: We have identified and characterized a synthetic non-peptidyl small molecule, Hh-Ag, that acts as an agonist of the Hh pathway. This Hh agonist promotes cell-type-specific proliferation and concentration-dependent differentiation in vitro, while in utero it rescues aspects of the Hh-signaling defect in Sonic hedgehog-null, but not Smo-null, mouse embryos. Biochemical studies with Hh-Ag, the Hh-signaling antagonist cyclopamine, and a novel Hh-signaling inhibitor Cur61414, reveal that the action of all these compounds is independent of Hh-protein ligand and of the Hh receptor Ptc, as each binds directly to Smo.

Conclusions: Smo can have its activity modulated directly by synthetic small molecules. These studies raise the possibility that Hh signaling may be regulated by endogenous small molecules in vivo and provide potent compounds with which to test the therapeutic value of activating the Hh-signaling pathway in the treatment of traumatic and chronic degenerative conditions.

MeSH terms

  • Animals
  • Antibodies / chemistry
  • Antibodies / pharmacology
  • Antigen-Antibody Complex / chemistry
  • Antigen-Antibody Complex / pharmacology
  • Antigen-Antibody Complex / physiology
  • Binding, Competitive
  • Cell Differentiation / drug effects
  • Cell Line
  • Cell Membrane / metabolism
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Central Nervous System / drug effects
  • Central Nervous System / metabolism
  • Cerebellum / cytology
  • Chick Embryo
  • Embryo, Mammalian / chemistry
  • Embryo, Mammalian / drug effects
  • Embryo, Mammalian / metabolism
  • Female
  • Hedgehog Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins / physiology
  • Mice
  • Mice, Inbred C3H
  • Molecular Structure
  • Neurons / chemistry
  • Neurons / drug effects
  • Neurons / metabolism
  • Organ Culture Techniques
  • Patched Receptors
  • Patched-1 Receptor
  • Peptides
  • Pregnancy
  • Rats
  • Receptors, Cell Surface
  • Receptors, G-Protein-Coupled / agonists*
  • Receptors, G-Protein-Coupled / antagonists & inhibitors*
  • Receptors, G-Protein-Coupled / physiology
  • Signal Transduction / drug effects*
  • Smoothened Receptor
  • Structure-Activity Relationship
  • Trans-Activators / immunology
  • Trans-Activators / metabolism*
  • Trans-Activators / pharmacology
  • Trans-Activators / physiology

Substances

  • Antibodies
  • Antigen-Antibody Complex
  • Hedgehog Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Patched Receptors
  • Patched-1 Receptor
  • Peptides
  • Ptch1 protein, mouse
  • Receptors, Cell Surface
  • Receptors, G-Protein-Coupled
  • SHH protein, human
  • SMO protein, human
  • Smoothened Receptor
  • Trans-Activators