Molecular basis for the antiparasitic activity of a mercaptoacetamide derivative that inhibits histone deacetylase 8 (HDAC8) from the human pathogen schistosoma mansoni

J Mol Biol. 2014 Oct 9;426(20):3442-53. doi: 10.1016/j.jmb.2014.03.007. Epub 2014 Mar 20.

Abstract

Schistosomiasis, caused by the parasitic flatworm Schistosoma mansoni and related species, is a tropical disease that affects over 200 million people worldwide. A new approach for targeting eukaryotic parasites is to tackle their dynamic epigenetic machinery that is necessary for the extensive phenotypic changes during the life cycle of the parasite. Recently, we identified S. mansoni histone deacetylase 8 (smHDAC8) as a potential target for antiparasitic therapy. Here, we present results on the investigations of a focused set of HDAC (histone deacetylase) inhibitors on smHDAC8. Besides several active hydroxamates, we identified a thiol-based inhibitor that inhibited smHDAC8 activity in the micromolar range with unexpected selectivity over the human isotype, which has not been observed so far. The crystal structure of smHDAC8 complexed with the thiol derivative revealed that the inhibitor is accommodated in the catalytic pocket, where it interacts with both the catalytic zinc ion and the essential catalytic tyrosine (Y341) residue via its mercaptoacetamide warhead. To our knowledge, this is the first complex crystal structure of any HDAC inhibited by a mercaptoacetamide inhibitor, and therefore, this finding offers a rationale for further improvement. Finally, an ester prodrug of the thiol HDAC inhibitor exhibited antiparasitic activity on cultured schistosomes in a dose-dependent manner.

Keywords: X-ray crystallography; antiparasitic activity; docking; epigenetics; thiol.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antiparasitic Agents / chemistry*
  • Antiparasitic Agents / metabolism
  • Antiparasitic Agents / pharmacology
  • Apoptosis / drug effects
  • Biocatalysis / drug effects
  • Crystallography, X-Ray
  • Helminth Proteins / antagonists & inhibitors
  • Helminth Proteins / chemistry*
  • Helminth Proteins / metabolism
  • Histone Deacetylase Inhibitors / chemistry
  • Histone Deacetylase Inhibitors / metabolism
  • Histone Deacetylase Inhibitors / pharmacology
  • Histone Deacetylases / chemistry*
  • Histone Deacetylases / metabolism
  • Humans
  • Hydroxamic Acids / chemistry
  • Hydroxamic Acids / metabolism
  • Hydroxamic Acids / pharmacology
  • Inhibitory Concentration 50
  • Models, Molecular
  • Molecular Structure
  • Protein Binding
  • Protein Structure, Tertiary
  • Schistosoma mansoni / drug effects
  • Schistosoma mansoni / enzymology*
  • Schistosoma mansoni / physiology
  • Schistosomiasis mansoni / parasitology
  • Thioacetamide / chemistry*
  • Thioacetamide / metabolism
  • Thioacetamide / pharmacology
  • Vorinostat

Substances

  • Antiparasitic Agents
  • Helminth Proteins
  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • Thioacetamide
  • Vorinostat
  • Histone Deacetylases