Rosetta comparative modeling for library design: Engineering alternative inducer specificity in a transcription factor

Proteins. 2015 Jul;83(7):1327-40. doi: 10.1002/prot.24828. Epub 2015 May 29.

Abstract

Structure-based rational mutagenesis for engineering protein functionality has been limited by the scarcity and difficulty of obtaining crystal structures of desired proteins. On the other hand, when high-throughput selection is possible, directed evolution-based approaches for gaining protein functionalities have been random and fortuitous with limited rationalization. We combine comparative modeling of dimer structures, ab initio loop reconstruction, and ligand docking to select positions for mutagenesis to create a library focused on the ligand-contacting residues. The rationally reduced library requirement enabled conservative control of the substitutions by oligonucleotide synthesis and bounding its size within practical transformation efficiencies (∼ 10(7) variants). This rational approach was successfully applied on an inducer-binding domain of an Acinetobacter transcription factor (TF), pobR, which shows high specificity for natural effector molecule, 4-hydroxy benzoate (4HB), but no native response to 3,4-dihydroxy benzoate (34DHB). Selection for mutants with high transcriptional induction by 34DHB was carried out at the single-cell level under flow cytometry (via green fluorescent protein expression under the control of pobR promoter). Critically, this selection protocol allows both selection for induction and rejection of constitutively active mutants. In addition to gain-of-function for 34DHB induction, the selected mutants also showed enhanced sensitivity and response for 4HB (native inducer) while no sensitivity was observed for a non-targeted but chemically similar molecule, 2-hydroxy benzoate (2HB). This is unique application of the Rosetta modeling protocols for library design to engineer a TF. Our approach extends applicability of the Rosetta redesign protocol into regimes without a priori precision structural information.

Keywords: BLOSUM62; Rosetta; altered specificity; comparative modeling; ligand docking; pobR; protein engineering; transcription factor.

Publication types

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

MeSH terms

  • Acinetobacter / chemistry
  • Acinetobacter / metabolism
  • Amino Acid Sequence
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites
  • Escherichia coli / drug effects
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression
  • Genes, Reporter
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Hydroxybenzoates / chemistry
  • Hydroxybenzoates / pharmacology
  • Ligands
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation*
  • Parabens / chemistry
  • Parabens / pharmacology
  • Peptide Library*
  • Promoter Regions, Genetic / drug effects
  • Protein Binding
  • Protein Engineering / methods*
  • Recombinant Fusion Proteins / chemistry*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Salicylic Acid / chemistry
  • Salicylic Acid / pharmacology
  • Trans-Activators / chemistry*
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription, Genetic

Substances

  • 3,4-dihydroxybenzoate
  • Bacterial Proteins
  • Hydroxybenzoates
  • Ligands
  • Parabens
  • Peptide Library
  • PobR protein, Acinetobacter calcoaceticus
  • Recombinant Fusion Proteins
  • Trans-Activators
  • Green Fluorescent Proteins
  • 4-hydroxybenzoic acid
  • Salicylic Acid