An excitable Rho GTPase signaling network generates dynamic subcellular contraction patterns

J Cell Biol. 2017 Dec 4;216(12):4271-4285. doi: 10.1083/jcb.201706052. Epub 2017 Oct 20.

Abstract

Rho GTPase-based signaling networks control cellular dynamics by coordinating protrusions and retractions in space and time. Here, we reveal a signaling network that generates pulses and propagating waves of cell contractions. These dynamic patterns emerge via self-organization from an activator-inhibitor network, in which the small GTPase Rho amplifies its activity by recruiting its activator, the guanine nucleotide exchange factor GEF-H1. Rho also inhibits itself by local recruitment of actomyosin and the associated RhoGAP Myo9b. This network structure enables spontaneous, self-limiting patterns of subcellular contractility that can explore mechanical cues in the extracellular environment. Indeed, actomyosin pulse frequency in cells is altered by matrix elasticity, showing that coupling of contractility pulses to environmental deformations modulates network dynamics. Thus, our study reveals a mechanism that integrates intracellular biochemical and extracellular mechanical signals into subcellular activity patterns to control cellular contractility dynamics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Actin Cytoskeleton / ultrastructure
  • Actomyosin / genetics
  • Actomyosin / metabolism
  • Biomechanical Phenomena
  • Cell Line, Tumor
  • Gene Expression Regulation
  • HeLa Cells
  • Humans
  • Mechanotransduction, Cellular*
  • Microtubules / metabolism*
  • Microtubules / ultrastructure
  • Myosins / genetics
  • Myosins / metabolism*
  • Osteoblasts
  • Rho Guanine Nucleotide Exchange Factors / genetics
  • Rho Guanine Nucleotide Exchange Factors / metabolism
  • rho GTP-Binding Proteins / genetics
  • rho GTP-Binding Proteins / metabolism*

Substances

  • ARHGEF2 protein, human
  • Rho Guanine Nucleotide Exchange Factors
  • myosin IXB
  • Actomyosin
  • Myosins
  • rho GTP-Binding Proteins