Catalytic mechanism of rhomboid protease GlpG probed by 3,4-dichloroisocoumarin and diisopropyl fluorophosphonate

J Biol Chem. 2012 Jan 27;287(5):3099-107. doi: 10.1074/jbc.M111.310482. Epub 2011 Nov 29.

Abstract

Rhomboid proteases have many important biological functions. Unlike soluble serine proteases such as chymotrypsin, the active site of rhomboid protease, which contains a Ser-His catalytic dyad, is submerged in the membrane and surrounded by membrane-spanning helices. Previous crystallographic analyses of GlpG, a bacterial rhomboid protease, and its complex with isocoumarin have provided insights into the mechanism of the membrane protease. Here, we studied the interaction of GlpG with 3,4-dichloroisocoumarin and diisopropyl fluorophosphonate, both mechanism-based inhibitors for the serine protease, and describe the crystal structure of the covalent adduct between GlpG and diisopropyl fluorophosphonate, which mimics the oxyanion-containing tetrahedral intermediate of the hydrolytic reaction. The crystal structure confirms that the oxyanion is stabilized by the main chain amide of Ser-201 and by the side chains of His-150 and Asn-154. The phosphorylation of the catalytic Ser-201 weakens its interaction with His-254, causing the catalytic histidine to rotate away from the serine. The rotation of His-254 is accompanied by further rearrangement of the side chains of Tyr-205 and Trp-236 within the substrate-binding groove. The formation of the tetrahedral adduct is also accompanied by opening of the L5 cap and movement of transmembrane helix S5 toward S6 in a direction different from that predicted by the lateral gating model. Combining the new structural data with those on the isocoumarin complex sheds further light on the plasticity of the active site of rhomboid membrane protease.

Publication types

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

MeSH terms

  • Bacterial Proteins / antagonists & inhibitors
  • Bacterial Proteins / chemistry*
  • Coumarins / chemistry*
  • Crystallography, X-Ray
  • Isocoumarins
  • Isoflurophate / chemistry*
  • Models, Molecular
  • Peptide Hydrolases / chemistry*
  • Protease Inhibitors / chemistry*
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Providencia / enzymology*

Substances

  • Bacterial Proteins
  • Coumarins
  • Isocoumarins
  • Protease Inhibitors
  • Isoflurophate
  • 3,4-dichloroisocoumarin
  • Peptide Hydrolases

Associated data

  • PDB/3TXT