Evidence for allosteric interactions of antagonist binding to the smoothened receptor

J Pharmacol Exp Ther. 2009 Jun;329(3):995-1005. doi: 10.1124/jpet.109.152090. Epub 2009 Mar 20.

Abstract

The Smoothened receptor (Smo) mediates hedgehog (Hh) signaling critical for development, cell growth, and migration, as well as stem cell maintenance. Aberrant Hh signaling pathway activation has been implicated in a variety of cancers, and small-molecule antagonists of Smo have entered human clinical trials for the treatment of cancer. Here, we report the biochemical characterization of allosteric interactions of agonists and antagonists for Smo. Binding of two radioligands, [(3)H]3-chloro-N-[trans-4-(methylamino)cyclohexyl]-N-{[3-(4-pyridinyl)-phenyl]methyl}-1-benzothiophene-2-carboxamide (SAG-1.3) (agonist) and [(3)H]cyclopamine (antagonist), was characterized using human Smo expressed in human embryonic kidney 293F membranes. We observed full displacement of [(3)H]cyclopamine by all Smo agonist and antagonist ligands examined. N-[(1E)-(3,5-Dimethyl-1-phenyl-1H-pyrazol-4-yl)methylidene]-4-(phenylmethyl)-1-piperazinamine (SANT-1), an antagonist, did not fully inhibit the binding of [(3)H]SAG-1.3. In a functional cell-based beta-lactamase reporter gene assay, SANT-1 and N-[3-(1H-benzimidazol-2-yl)-4-chlorophenyl]-3,4,5-tris(ethyloxy)-benzamide (SANT-2) fully inhibited 3-chloro-4,7-difluoro-N-[trans-4-(methylamino)cyclohexyl]-N-{[3-(4-pyridinyl)phenyl]methyl}-1-benzothiophene-2-carboxamide (SAG-1.5)-induced Hh pathway activation. Detailed "Schild-type" radioligand binding analysis with [(3)H]SAG-1.3 revealed that two structurally distinct Smoothened receptor antagonists, SANT-1 and SANT-2, bound in a manner consistent with that of allosteric modulation. Our mechanism of action characterization of radioligand binding to Smo combined with functional data provides a better understanding of small-molecule interactions with Smo and their influence on the Hh pathway.

MeSH terms

  • Anilides
  • Animals
  • Benzamides / chemistry
  • Benzamides / metabolism
  • Benzimidazoles / chemistry
  • Benzimidazoles / metabolism
  • Binding Sites
  • Binding, Competitive
  • Cell Line
  • Cell Membrane / metabolism
  • Cyclohexylamines / chemistry
  • Cyclohexylamines / metabolism
  • Genes, Reporter / genetics
  • Humans
  • Kinetics
  • Mice
  • Molecular Structure
  • Morpholines / chemistry
  • Morpholines / metabolism
  • NIH 3T3 Cells
  • Piperazines / chemistry
  • Piperazines / metabolism
  • Purines / chemistry
  • Purines / metabolism
  • Pyrazoles / chemistry
  • Pyrazoles / metabolism
  • Pyridines
  • Radioligand Assay
  • Receptors, G-Protein-Coupled / agonists
  • Receptors, G-Protein-Coupled / antagonists & inhibitors*
  • Receptors, G-Protein-Coupled / chemistry
  • Receptors, G-Protein-Coupled / metabolism*
  • Recombinant Proteins / agonists
  • Recombinant Proteins / antagonists & inhibitors
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Smoothened Receptor
  • Thiophenes / chemistry
  • Thiophenes / metabolism
  • Tomatine / analogs & derivatives
  • Tomatine / chemistry
  • Tomatine / metabolism
  • Transfection
  • Veratrum Alkaloids / chemistry
  • Veratrum Alkaloids / metabolism
  • beta-Lactamases / metabolism

Substances

  • Anilides
  • Benzamides
  • Benzimidazoles
  • Cyclohexylamines
  • HhAntag691
  • Morpholines
  • Piperazines
  • Purines
  • Pyrazoles
  • Pyridines
  • Receptors, G-Protein-Coupled
  • Recombinant Proteins
  • SAG compound
  • SANT-1 compound
  • SANT-2 compound
  • SMO protein, human
  • Smoothened Receptor
  • Thiophenes
  • Veratrum Alkaloids
  • tomatidine
  • Tomatine
  • beta-Lactamases
  • purmorphamine
  • cyclopamine