Actomyosin bundles serve as a tension sensor and a platform for ERK activation

• Published in: EMBO reports Vol. 16; no. 2; pp. 250 - 257
• Main Authors: Hirata, Hiroaki, Gupta, Mukund, Vedula, Sri Ram Krishna, Lim, Chwee Teck, Ladoux, Benoit, Sokabe, Masahiro
• Format: Journal Article
• Language: English
• Published: London Blackwell Publishing Ltd 01-02-2015; Nature Publishing Group UK; EMBO Press; BlackWell Publishing Ltd
• Subjects: Actomyosin; Actomyosin - metabolism; Animals; Biochemistry, Molecular Biology; Cell adhesion & migration; Cell Line; Cellular Biology; contractility; Cytoskeleton; EMBO05; EMBO37; Extracellular Signal-Regulated MAP Kinases; Extracellular Signal-Regulated MAP Kinases - metabolism; Fibers; Focal Adhesions; Focal Adhesions - metabolism; Humans; Life Sciences; mechanotransduction; Mechanotransduction, Cellular; Mechanotransduction, Cellular - physiology; Mice; Myosin Type II; Myosin Type II - metabolism; NIH 3T3 Cells; Scientific Report; Scientific Reports; Signal transduction; stress fiber; Stress Fibers; Stress Fibers - metabolism; Substrates; tensile force; Tensile Strength; Tensile Strength - physiology; Tension; tensile force; contractility; mechanotransduction; stress fiber
• ISSN: 1469-221X; 1469-3178
• DOI: 10.15252/embr.201439140

Tensile forces generated by stress fibers drive signal transduction events at focal adhesions. Here, we report that stress fibers per se act as a platform for tension‐induced activation of biochemical signals. The MAP kinase, ERK is activated on stress fibers in a myosin II‐dependent manner. In myosin II‐inhibited cells, uniaxial stretching of cell adhesion substrates restores ERK activation on stress fibers. By quantifying myosin II‐ or mechanical stretch‐mediated tensile forces in individual stress fibers, we show that ERK activation on stress fibers correlates positively with tensile forces acting on the fibers, indicating stress fibers as a tension sensor in ERK activation. Myosin II‐dependent ERK activation is also observed on actomyosin bundles connecting E‐cadherin clusters, thus suggesting that actomyosin bundles, in general, work as a platform for tension‐dependent ERK activation.
Synopsis
This study reveals that individual stress fibers work as a platform for activating ERK in a mechanical tension‐dependent manner.
Activation of ERK on stress fibers, but not its localization, depends on myosin II activity.
External application of tensile force to stress fibers restores ERK activation on stress fibers under inhibition of myosin II.
ERK activation on individual stress fibers increases with the magnitude of tensile forces acting on the fibers.
Graphical Abstract
This study reveals that individual stress fibers work as a platform for activating ERK in a mechanical tension‐dependent manner.