The role of arsenic-thiol interactions in metalloregulation of the ars operon

J Biol Chem. 1996 Apr 19;271(16):9291-7. doi: 10.1074/jbc.271.16.9291.

Abstract

The ars operon of the Escherichia coli plasmid R773 that confers arsenical and antimonial resistance is negatively regulated by the ArsR repressor. ArsR residues Cys-32 and Cys-34 were previously identified as involved in induction by arsenite and antimonite, suggesting coordination between As(III) and the two cysteine thiolates. However, in small molecule thiolate-As(III) complexes, arsenic is frequently three-coordinate. A site-directed mutagenic approach was employed in a search for a third arsenic ligand. ArsR proteins with C32G, C34G, and C32G/C34G substitutions were active repressors, but were not inducible in vivo. In vitro, the altered repressor-ars DNA complexes could not be dissociated by inducers. Alteration of Cys-37 and Ser-43, residues located in or near the putative helix-turn-helix DNA-binding region of the protein, had no effect on the inducibility of the operon. While these results indicated that neither the thiolate of Cys-37 nor the hydroxyl oxygen of Ser-43 is required for induction, they did not eliminate either atom as a potential arsenic ligand. Another approach involved reaction with an alternative inducer, phenylarsine oxide, which can form only two coordinations. Phenylarsine oxide was shown to be as effective as or more effective than arsenite or antimonite in induction in vivo. In vitro, the organic arsenical was more effective than either arsenite or antimonite in dissociating the repressor-promoter complex. Thus, two ArsR-arsenic bonds are sufficient for induction. The interaction of ArsR proteins with As(III) was examined using a phenylarsine oxide affinity resin. ArsR proteins containing any two of the three cysteine residues Cys-32, Cys-34, and Cys-37 bound to the resin. Alteration of any two of the three resulted in loss of binding. Arsenic X-ray absorption spectroscopy of ArsR treated stoichiometrically with arsenite confirmed the average arsenic coordination as AsS3 These results suggest that all three cysteine thiolates are arsenic ligands, but binding to only two, the Cys-32 and Cys-34 thiolates, is required to produce the conformational change that results in release of the repressor from the DNA and induction.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Antimony / pharmacology*
  • Arsenicals / pharmacology*
  • Arsenites / pharmacology*
  • Bacterial Proteins*
  • Base Sequence
  • Cysteine
  • Drug Resistance, Microbial / genetics*
  • Escherichia coli / drug effects
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Escherichia coli Proteins*
  • Gene Expression Regulation, Bacterial
  • Helix-Turn-Helix Motifs*
  • Kinetics
  • Models, Structural
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Oligodeoxyribonucleotides
  • Operon* / drug effects
  • Protein Structure, Secondary
  • R Factors
  • Repressor Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Serine
  • Trans-Activators / biosynthesis
  • Trans-Activators / chemistry
  • Trans-Activators / metabolism*

Substances

  • ArsR protein, E coli
  • Arsenicals
  • Arsenites
  • Bacterial Proteins
  • Escherichia coli Proteins
  • Oligodeoxyribonucleotides
  • Repressor Proteins
  • Trans-Activators
  • oxophenylarsine
  • Serine
  • Antimony
  • Cysteine