High-throughput screen, using time-resolved FRET, yields actin-binding compounds that modulate actin-myosin structure and function

J Biol Chem. 2018 Aug 3;293(31):12288-12298. doi: 10.1074/jbc.RA118.002702. Epub 2018 Jun 4.

Abstract

We have used a novel time-resolved FRET (TR-FRET) assay to detect small-molecule modulators of actin-myosin structure and function. Actin-myosin interactions play crucial roles in the generation of cellular force and movement. Numerous mutations and post-translational modifications of actin or myosin disrupt muscle function and cause life-threatening syndromes. Here, we used a FRET biosensor to identify modulators that bind to the actin-myosin interface and alter the structural dynamics of this complex. We attached a fluorescent donor to actin at Cys-374 and a nonfluorescent acceptor to a peptide containing the 12 N-terminal amino acids of the long isoform of skeletal muscle myosin's essential light chain. The binding site on actin of this acceptor-labeled peptide (ANT) overlaps with that of myosin, as indicated by (a) a similar distance observed in the actin-ANT complex as in the actin-myosin complex and (b) a significant decrease in actin-ANT FRET upon binding myosin. A high-throughput FRET screen of a small-molecule library (NCC, 727 compounds), using a unique fluorescence lifetime readout with unprecedented speed and precision, showed that FRET is significantly affected by 10 compounds in the micromolar range. Most of these "hits" alter actin-activated myosin ATPase and affect the microsecond dynamics of actin detected by transient phosphorescence anisotropy. We conclude that the actin-ANT TR-FRET assay enables detection of pharmacologically active compounds that affect actin structural dynamics and actomyosin function. This assay establishes feasibility for the discovery of allosteric modulators of the actin-myosin interaction, with the ultimate goal of developing therapies for muscle disorders.

Keywords: actin; fluorescence resonance energy transfer (FRET); high-throughput screening (HTS); myosin; peptide.

Publication types

  • Evaluation Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Actins / chemistry*
  • Actins / metabolism*
  • Actomyosin / chemistry
  • Actomyosin / metabolism
  • Adenosine Triphosphatases / chemistry
  • Adenosine Triphosphatases / metabolism
  • Adenosine Triphosphate / chemistry
  • Adenosine Triphosphate / metabolism
  • Animals
  • Anisotropy
  • Fluorescence Resonance Energy Transfer / methods*
  • High-Throughput Screening Assays / methods*
  • Muscle, Skeletal / chemistry
  • Muscle, Skeletal / metabolism
  • Myosins / chemistry*
  • Myosins / metabolism*
  • Protein Binding
  • Rabbits

Substances

  • Actins
  • Adenosine Triphosphate
  • Actomyosin
  • Adenosine Triphosphatases
  • Myosins