Electrostatic control of DNA intersegmental translocation by the ETS transcription factor ETV6

J Biol Chem. 2017 Aug 11;292(32):13187-13196. doi: 10.1074/jbc.M117.792887. Epub 2017 Jun 7.

Abstract

To find their DNA target sites in complex solution environments containing excess heterogeneous DNA, sequence-specific DNA-binding proteins execute various translocation mechanisms known collectively as facilitated diffusion. For proteins harboring a single DNA contact surface, long-range translocation occurs by jumping between widely spaced DNA segments. We have configured biosensor-based surface plasmon resonance to directly measure the affinity and kinetics of this intersegmental jumping by the ETS-family transcription factor ETS variant 6 (ETV6). To isolate intersegmental target binding in a functionally defined manner, we pre-equilibrated ETV6 with excess salmon sperm DNA, a heterogeneous polymer, before exposing the nonspecifically bound protein to immobilized oligomeric DNA harboring a high-affinity ETV6 site. In this way, the mechanism of ETV6-target association could be toggled electrostatically through varying NaCl concentration in the bulk solution. Direct measurements of association and dissociation kinetics of the site-specific complex indicated that 1) freely diffusive binding by ETV6 proceeds through a nonspecific-like intermediate, 2) intersegmental jumping is rate-limited by dissociation from the nonspecific polymer, and 3) dissociation of the specific complex is independent of the history of complex formation. These results show that target searches by proteins with an ETS domain, such as ETV6, whose single DNA-binding domain cannot contact both source and destination sites simultaneously, are nonetheless strongly modulated by intersegmental jumping in heterogeneous site environments. Our findings establish biosensors as a general technique for directly and specifically measuring target site search by DNA-binding proteins via intersegmental translocation.

Keywords: DNA-binding protein; DNA-protein interaction; ETS transcription factor family; surface plasmon resonance (SPR); translocation.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Binding Sites
  • Biosensing Techniques
  • DNA / chemistry
  • DNA / metabolism*
  • DNA, Single-Stranded / chemistry
  • DNA, Single-Stranded / metabolism
  • ETS Motif
  • ETS Translocation Variant 6 Protein
  • Facilitated Diffusion
  • Humans
  • Kinetics
  • Models, Molecular*
  • Nucleotide Motifs
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Polydeoxyribonucleotides / chemistry
  • Polydeoxyribonucleotides / metabolism
  • Protein Conformation
  • Protein Interaction Domains and Motifs
  • Proto-Oncogene Proteins c-ets / chemistry
  • Proto-Oncogene Proteins c-ets / genetics
  • Proto-Oncogene Proteins c-ets / metabolism*
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Repressor Proteins / chemistry
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Response Elements
  • Salmon
  • Static Electricity
  • Surface Plasmon Resonance
  • Thermodynamics

Substances

  • DNA, Single-Stranded
  • Peptide Fragments
  • Polydeoxyribonucleotides
  • Proto-Oncogene Proteins c-ets
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Repressor Proteins
  • DNA

Associated data

  • PDB/4MHG