Myosin-10 produces its power-stroke in two phases and moves processively along a single actin filament under low load

Proc Natl Acad Sci U S A. 2014 May 6;111(18):E1833-42. doi: 10.1073/pnas.1320122111. Epub 2014 Apr 21.

Abstract

Myosin-10 is an actin-based molecular motor that participates in essential intracellular processes such as filopodia formation/extension, phagocytosis, cell migration, and mitotic spindle maintenance. To study this motor protein's mechano-chemical properties, we used a recombinant, truncated form of myosin-10 consisting of the first 936 amino acids, followed by a GCN4 leucine zipper motif, to force dimerization. Negative-stain electron microscopy reveals that the majority of molecules are dimeric with a head-to-head contour distance of ∼50 nm. In vitro motility assays show that myosin-10 moves actin filaments smoothly with a velocity of ∼310 nm/s. Steady-state and transient kinetic analysis of the ATPase cycle shows that the ADP release rate (∼13 s(-1)) is similar to the maximum ATPase activity (∼12-14 s(-1)) and therefore contributes to rate limitation of the enzymatic cycle. Single molecule optical tweezers experiments show that under intermediate load (∼0.5 pN), myosin-10 interacts intermittently with actin and produces a power stroke of ∼17 nm, composed of an initial 15-nm and subsequent 2-nm movement. At low optical trap loads, we observed staircase-like processive movements of myosin-10 interacting with the actin filament, consisting of up to six ∼35-nm steps per binding interaction. We discuss the implications of this load-dependent processivity of myosin-10 as a filopodial transport motor.

Keywords: actomyosin; myosin X; myosin-5a; optical trapping; stable single alpha-helix.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / chemistry
  • Actins / physiology*
  • Adenosine Diphosphate / metabolism
  • Amino Acid Sequence
  • Animals
  • Biomechanical Phenomena
  • Cattle
  • In Vitro Techniques
  • Kinetics
  • Microscopy, Electron
  • Microscopy, Fluorescence
  • Models, Biological
  • Models, Molecular
  • Molecular Sequence Data
  • Myosin Heavy Chains / chemistry
  • Myosin Heavy Chains / genetics
  • Myosin Heavy Chains / physiology*
  • Myosin Subfragments / chemistry
  • Myosin Subfragments / genetics
  • Myosin Subfragments / physiology
  • Optical Tweezers
  • Protein Interaction Domains and Motifs
  • Protein Structure, Quaternary
  • Pseudopodia / physiology
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism

Substances

  • Actins
  • Myosin Subfragments
  • Recombinant Fusion Proteins
  • Adenosine Diphosphate
  • Myosin Heavy Chains