The multidrug efflux regulator TtgV recognizes a wide range of structurally different effectors in solution and complexed with target DNA: evidence from isothermal titration calorimetry

J Biol Chem. 2005 May 27;280(21):20887-93. doi: 10.1074/jbc.M500783200. Epub 2005 Mar 13.

Abstract

TtgV modulates the expression of the ttgGHI operon, which encodes an efflux pump that extrudes a wide variety of chemicals including mono- and binuclear aromatic hydrocarbons, aliphatic alcohols, and antibiotics of dissimilar chemical structure. Using a 'lacZ fusion to the ttgG promoter, we show that the most efficient in vivo inducers were 1-naphthol, 2,3-dihydroxynaphthalene, 4-nitrotoluene, benzonitrile, and indole. The thermodynamic parameters for the binding of different effector molecules to purified TtgV were determined by isothermal titration calorimetry. For the majority of effectors, the interaction was enthalpy-driven and counterbalance by unfavorable entropy changes. The TtgV-effector dissociation constants were found to vary between 2 and 890 mum. There was a relationship between TtgV affinity for the different effectors and their potential to induce gene expression in vivo, indicating that the effector binding constant is a major determinant for efficient efflux pump gene expression. Equilibrium dialysis and isothermal titration calorimetry studies indicated that a TtgV dimer binds one effector molecule. No evidence for the simultaneous binding of multiple effectors to TtgV was obtained. The binding of TtgV to a 63-bp DNA fragment containing its cognate operator was tight and entropy-driven (K(D) = 2.4 +/- 0.35 nm, DeltaH = 5.5 +/- 0.04 kcal/mol). The TtgV-DNA complex was shown to bind 1-napthol with an affinity comparable with the free soluble TtgV protein, K(D) = 4.8 +/- 0.19 and 3.0 +/- 0.15 mum, respectively. The biological relevance of this finding is discussed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Calorimetry / methods*
  • DNA, Bacterial / metabolism*
  • Escherichia coli / genetics
  • Gene Expression Regulation, Bacterial / drug effects
  • Indoles / metabolism
  • Indoles / pharmacology
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism*
  • Naphthols / metabolism
  • Naphthols / pharmacology
  • Nitriles / metabolism
  • Nitriles / pharmacology
  • Operon / genetics
  • Promoter Regions, Genetic / genetics
  • Protein Binding
  • Pseudomonas putida / chemistry
  • Pseudomonas putida / genetics
  • Recombinant Fusion Proteins
  • Thermodynamics
  • Toluene / analogs & derivatives*
  • Toluene / metabolism
  • Toluene / pharmacology
  • Transcription, Genetic
  • beta-Galactosidase / genetics

Substances

  • Bacterial Proteins
  • DNA, Bacterial
  • Indoles
  • Membrane Transport Proteins
  • Naphthols
  • Nitriles
  • Recombinant Fusion Proteins
  • TtgG protein, Pseudomonas putida
  • TtgH protein, Pseudomonas putida
  • 1-naphthol
  • Toluene
  • indole
  • benzonitrile
  • 4-nitrotoluene
  • beta-Galactosidase
  • 2,3-dihydroxynaphthalene