CE30 - Physique de la matière condensée et de la matière diluée

Self-organized wave-like beating of polar filament bundles in a minimal actomyosin system – ActoMyoBeat

Submission summary

Systems comprising large numbers of molecular motors and filaments from the cytoskeleton of biological cells show emergent active behaviors that are not present at the level of individual molecules. These behaviors emphasize the general principle of self-assembly: “more is different”. The ActoMyoBeat research proposal focuses on the emergence of spontaneous mechanical oscillations and traveling waves in active filament bundles. This prototypical example of self-organization is inspired by cilia and flagella, which are motile slender appendages of eukaryotic cells exhibiting regular wave-like beating patterns to propel the cells through the surrounding fluid or generate flow. Cilia and flagella serve essential functions in biology, such as the locomotion of spermatozoids, mucus clearance in bronchial airways, cerebrospinal-fluid flow in brain ventricles, or imposing the left-right asymmetry of the body during embryonic development. Although the flagellar beat has extensively been studied both experimentally and theoretically for many decades, understanding how molecular motors get coordinated to drive and shape periodic bending waves along a filament bundle remains a key open challenge. To tackle this challenge, we present here a bottom-up approach based on a minimal active molecular system comprising polar filaments (actin) and molecular motors (myosin) that self-assembles in vitro into oscillatory polar bundles of filaments, resembling eukaryotic flagellar beating. A better understanding of the interaction between the building blocks of this form of active matter—here actin filaments and myosin—is essential to describe the emergent properties of the beating bundles. As a result, we present a collaborative project between three teams of complementary expertise at the molecular and supramolecular scales and with a demonstrated ability to combine experimental and theoretical approaches.
Our preliminary results strongly suggest that the binding affinity of the motors for the filament bundle is regulated by the bundle shape, resulting in a dynamic interplay between myosin binding (myosin force dipoles and torques affect the shape of the filament bundle) and actin-bundle shape (shape/stresses affects the binding affinity of the motors for actin). Specifically, we plan to investigate (i) how the actin-bundle architecture, including the filament number, density, and length distribution as well as filament cross-linking, affects beating properties, (ii) how varying motor properties affects beating of the actin bundles, (iii) the interplay between myosin-motor localization and actin-filament shape, (iv) the effect of viscous drag by the surrounding fluid and of external localized forces on beating property, and (v) how a beating actin bundle interacts with its environment to generate flow, synchronize with its neighbors, and apply forces that may lead to swimming. Finally, (vi) we aim at integrating our experimental results into a physical description of self-organized beating in active-filament systems.
Overall, the ActoMyoBeat project will shed light on self-assembly of polar–filament bundles and molecular motors. By identifying generic physical principles underlying spontaneous movements and waves in this form of active matter, our research will provide the fundamental groundwork to describe the beating of biological cilia and flagella, as well as motile mechanisms in other cellular systems.

Project coordination

Pascal Martin (Institut Curie)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

IC Institut Curie
IJM Institut Jacques Monod
MPIPKS Max Planck Institute for the Physics of Complex Systems / Division Biolopgical Physics

Help of the ANR 447,508 euros
Beginning and duration of the scientific project: January 2022 - 48 Months

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