Structural conservation of ligand binding reveals a bile acid-like signaling pathway in nematodes

J Biol Chem. 2012 Feb 10;287(7):4894-903. doi: 10.1074/jbc.M111.315242. Epub 2011 Dec 14.

Abstract

Bile acid-like molecules named dafachronic acids (DAs) control the dauer formation program in Caenorhabditis elegans through the nuclear receptor DAF-12. This mechanism is conserved in parasitic nematodes to regulate their dauer-like infective larval stage, and as such, the DAF-12 ligand binding domain has been identified as an important therapeutic target in human parasitic hookworm species that infect more than 600 million people worldwide. Here, we report two x-ray crystal structures of the hookworm Ancylostoma ceylanicum DAF-12 ligand binding domain in complex with DA and cholestenoic acid (a bile acid-like metabolite), respectively. Structure analysis and functional studies reveal key residues responsible for species-specific ligand responses of DAF-12. Furthermore, DA binds to DAF-12 mechanistically and is structurally similar to bile acids binding to the mammalian bile acid receptor farnesoid X receptor. Activation of DAF-12 by cholestenoic acid and the cholestenoic acid complex structure suggest that bile acid-like signaling pathways have been conserved in nematodes and mammals. Together, these results reveal the molecular mechanism for the interplay between parasite and host, provide a structural framework for DAF-12 as a promising target in treating nematode parasitism, and provide insight into the evolution of gut parasite hormone-signaling pathways.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Ancylostoma / chemistry*
  • Ancylostoma / genetics
  • Ancylostoma / metabolism
  • Ancylostomiasis / metabolism
  • Ancylostomiasis / therapy
  • Animals
  • Bile Acids and Salts / chemistry*
  • Bile Acids and Salts / genetics
  • Bile Acids and Salts / metabolism
  • Cholestenes / chemistry*
  • Cholestenes / metabolism
  • Crystallography, X-Ray
  • Helminth Proteins / chemistry*
  • Helminth Proteins / genetics
  • Helminth Proteins / metabolism
  • Mammals
  • Receptors, Cytoplasmic and Nuclear / chemistry*
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Structural Homology, Protein

Substances

  • Bile Acids and Salts
  • Cholestenes
  • Helminth Proteins
  • Receptors, Cytoplasmic and Nuclear
  • cholestenoic acid