Abstract

Immune cells exhibit stimulation-dependent traveling waves in the cortex, much faster than typical cortical actin waves. These waves reflect rhythmic assembly of both actin machinery and peripheral membrane proteins such as F-BAR domain-containing proteins. Combining theory and experiments, we develop a mechanochemical feedback model involving membrane shape changes and F-BAR proteins that render the cortex an interesting dynamical system. We show that such cortical dynamics manifests itself as ultrafast traveling waves of cortical proteins, in which the curvature sensitivity-driven feedback always constrains protein lateral diffusion in wave propagation. The resulting protein wave propagation mainly reflects the spatial gradient in the timing of local protein recruitment from cytoplasm. We provide evidence that membrane undulations accompany these protein waves and potentiate their propagation. Therefore, membrane shape change and protein curvature sensitivity may have underappreciated roles in setting high-speed cortical signal transduction rhythms.

Highlights

  • Immune cells exhibit stimulation-dependent traveling waves in the cortex, much faster than typical cortical actin waves

  • Considering that F-BAR proteins are members of BAR superfamily proteins that can sense and generate membrane curvature[5,6,7,22,23,24,25,26,27,28], we reasoned that these cortical proteins might mediate membrane shape changes that are important to the wave propagation

  • We show that feedback between membrane shape changes and recruitment of curvature sensing proteins can lead to traveling waves, in which propagating membrane undulation accompanies the cortical protein waves

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Summary

Introduction

Immune cells exhibit stimulation-dependent traveling waves in the cortex, much faster than typical cortical actin waves. Our recent findings indicated that membrane shape might play an important role for cortical rhythmic propagation[4]: upon antigen stimulation in immune cells, the actin machinery (e.g., actin, N-WASP, and Cdc42), and F-BAR domain-containing proteins—well known for their sensitivities for membrane curvature5–7—exhibit traveling wave behavior within the ventral cortex. These waves travel as fast as ~1 μm s−1, about 10- to 100-fold higher than previously described ventral actin waves[3,8,9,10,11,12,13,14,15,16]. Curvature sensing may be important in high-speed cortical signal transmission

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