Myosin lever arm directs collective motion on cellular actin network

Rizal Hariadi, Mario Cale, Sivaraj Sivaramakrishnan

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

The molecular motor myosin teams up to drive muscle contraction, membrane traffic, and cell division in biological cells.Myosin function in cells emerges from the interaction of multiple motors tethered to a scaffold, with surrounding actin filaments organized into 3D networks. Despite the importance of myosin function, the influence of intermotor interactions on collective motion remains poorly understood. In this study, we used precisely engineered myosin assemblies to examine emergence in collective myosin movement. We report that tethering multiple myosin VI motors, but not myosin V motors, modifies their movement trajectories on keratocyte actin networks. Single myosin V and VI dimers display similar skewed trajectories, albeit in opposite directions, when traversing the keratocyte actin network. In contrast, tethering myosin VI motors, but not myosin V motors, progressively straightens the trajectories with increasing myosin number. Trajectory shape of multimotor scaffolds positively correlates with the stiffness of the myosin lever arm. Swapping the flexible myosin VI lever arm for the relatively rigid myosin V lever increases trajectory skewness, and vice versa. A simplified model of coupled motor movement demonstrates that the differences in flexural rigidity of the two myosin lever arms is sufficient to account for the differences in observed behavior of groups of myosin V and VI motors. In accordance with this model trajectory, shapes for scaffolds containing both myosin V and VI are dominated by the myosin with a stiffer lever arm. Our findings suggest that structural features unique to each myosin type may confer selective advantages in cellular functions.

Original languageEnglish (US)
Pages (from-to)4091-4096
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number11
DOIs
StatePublished - Mar 18 2014
Externally publishedYes

Fingerprint

Myosins
Myosin Type V
Actins
Muscle Contraction
Actin Cytoskeleton
Cell Communication
Cell Division
myosin VI
Membranes

Keywords

  • Collective decision-making
  • DNA nanotechnology
  • Motor proteins
  • Single molecule biophysics
  • Synthetic biology

ASJC Scopus subject areas

  • General

Cite this

Myosin lever arm directs collective motion on cellular actin network. / Hariadi, Rizal; Cale, Mario; Sivaramakrishnan, Sivaraj.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 11, 18.03.2014, p. 4091-4096.

Research output: Contribution to journalArticle

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