Small-molecule inhibitor binding to an N-acyl-homoserine lactone synthase

Proc Natl Acad Sci U S A. 2011 Jul 19;108(29):12089-94. doi: 10.1073/pnas.1103165108. Epub 2011 Jul 5.

Abstract

Quorum sensing (QS) controls certain behaviors of bacteria in response to population density. In gram-negative bacteria, QS is often mediated by N-acyl-L-homoserine lactones (acyl-HSLs). Because QS influences the virulence of many pathogenic bacteria, synthetic inhibitors of acyl-HSL synthases might be useful therapeutically for controlling pathogens. However, rational design of a potent QS antagonist has been thwarted by the lack of information concerning the binding interactions between acyl-HSL synthases and their ligands. In the gram-negative bacterium Burkholderia glumae, QS controls virulence, motility, and protein secretion and is mediated by the binding of N-octanoyl-L-HSL (C8-HSL) to its cognate receptor, TofR. C8-HSL is synthesized by the acyl-HSL synthase TofI. In this study, we characterized two previously unknown QS inhibitors identified in a focused library of acyl-HSL analogs. Our functional and X-ray crystal structure analyses show that the first inhibitor, J8-C8, binds to TofI, occupying the binding site for the acyl chain of the TofI cognate substrate, acylated acyl-carrier protein. Moreover, the reaction byproduct, 5'-methylthioadenosine, independently binds to the binding site for a second substrate, S-adenosyl-L-methionine. Closer inspection of the mode of J8-C8 binding to TofI provides a likely molecular basis for the various substrate specificities of acyl-HSL synthases. The second inhibitor, E9C-3oxoC6, competitively inhibits C8-HSL binding to TofR. Our analysis of the binding of an inhibitor and a reaction byproduct to an acyl-HSL synthase may facilitate the design of a new class of QS-inhibiting therapeutic agents.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Butyrolactone / analogs & derivatives*
  • 4-Butyrolactone / metabolism
  • Bacterial Proteins / antagonists & inhibitors*
  • Bacterial Proteins / metabolism
  • Burkholderia / metabolism*
  • Crystallography, X-Ray
  • Fluorescence
  • Homoserine / analogs & derivatives
  • Homoserine / metabolism
  • Lactones / metabolism
  • Protein Binding*
  • Quorum Sensing / physiology*
  • S-Adenosylmethionine / metabolism*
  • Substrate Specificity
  • Transcription Factors / antagonists & inhibitors*
  • Transcription Factors / metabolism

Substances

  • Bacterial Proteins
  • Lactones
  • LuxI protein, Bacteria
  • N-octanoylhomoserine lactone
  • Transcription Factors
  • homoserine lactone
  • Homoserine
  • S-Adenosylmethionine
  • 4-Butyrolactone

Associated data

  • PDB/3P2F
  • PDB/3P2H