Identification of a small molecule that modifies MglA/SspA interaction and impairs intramacrophage survival of Francisella tularensis

PLoS One. 2013;8(1):e54498. doi: 10.1371/journal.pone.0054498. Epub 2013 Jan 23.

Abstract

The transcription factors MglA and SspA of Francisella tularensis form a heterodimer complex and interact with the RNA polymerase to regulate the expression of the Francisella pathogenicity island (FPI) genes. These genes are essential for this pathogen's virulence and survival within host cells. In this study, we used a small molecule screening to identify quinacrine as a thermal stabilizing compound for F. tularensis SCHU S4 MglA and SspA. A bacterial two-hybrid system was used to analyze the in vivo effect of quinacrine on the heterodimer complex. The results show that quinacrine affects the interaction between MglA and SspA, indicated by decreased β-galactosidase activity. Further in vitro analyses, using size exclusion chromatography, indicated that quinacrine does not disrupt the heterodimer formation, however, changes in the alpha helix content were confirmed by circular dichroism. Structure-guided site-directed mutagenesis experiments indicated that quinacrine makes contact with amino acid residues Y63 in MglA, and K97 in SspA, both located in the "cleft" of the interacting surfaces. In F. tularensis subsp. novicida, quinacrine decreased the transcription of the FPI genes, iglA, iglD, pdpD and pdpA. As a consequence, the intramacrophage survival capabilities of the bacteria were affected. These results support use of the MglA/SspA interacting surface, and quinacrine's chemical scaffold, for the design of high affinity molecules that will function as therapeutics for the treatment of Tularemia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / chemistry*
  • Adhesins, Bacterial / metabolism
  • Bacterial Proteins / antagonists & inhibitors
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism
  • DNA-Directed RNA Polymerases / antagonists & inhibitors
  • DNA-Directed RNA Polymerases / chemistry*
  • DNA-Directed RNA Polymerases / metabolism
  • Francisella tularensis / chemistry
  • Francisella tularensis / drug effects
  • Francisella tularensis / genetics*
  • Francisella tularensis / pathogenicity*
  • Gene Expression Regulation, Bacterial / drug effects*
  • Humans
  • Macrophages / microbiology
  • Molecular Docking Simulation
  • Mutagenesis, Site-Directed
  • Protein Multimerization
  • Protein Structure, Secondary
  • Quinacrine / chemistry*
  • Quinacrine / pharmacology
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / chemistry*
  • Transcription Factors / metabolism
  • Transcription, Genetic / drug effects
  • Virulence
  • beta-Galactosidase / metabolism

Substances

  • Adhesins, Bacterial
  • Bacterial Proteins
  • SspA protein, bacteria
  • Transcription Factors
  • DNA-Directed RNA Polymerases
  • beta-Galactosidase
  • Quinacrine

Grants and funding

This work was supported by a grant from the Institute of Food and Agricultural Sciences, University of Florida. Publication of this article was funded in part by the University of Florida Open Access Publishing Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.