Rapid Assembly of A Polar Network Architecture Drives Efficient Actomyosin Contractility

Vlad Costache, Sorbonne Université
Serena Prigent Garcia, Sorbonne Université
Camille N. Plancke, Sorbonne Université
Jing Li, Purdue University
Simon Begnaud, Sorbonne Université
Shashi Kumar Suman, Sorbonne Université
Anne-Cécile Reymann, Université de Strasbourg
Taeyoon Kim, Purdue University
François B. Robin, Sorbonne Université

This is the publisher's version of Costache V, Prigent Garcia S, Plancke CN, Li J, Begnaud S, Suman SK, Reymann AC, Kim T, Robin FB. Rapid assembly of a polar network architecture drives efficient actomyosin contractility. Cell Rep. 2022 May 31;39(9):110868. doi: 10.1016/j.celrep.2022.110868

Abstract

Actin network architecture and dynamics play a central role in cell contractility and tissue morphogenesis. RhoA-driven pulsed contractions are a generic mode of actomyosin contractility, but the mechanisms underlying how their specific architecture emerges and how this architecture supports the contractile function of the network remain unclear. Here we show that, during pulsed contractions, the actin network is assembled by two subpopulations of formins: a functionally inactive population (recruited) and formins actively participating in actin filament elongation (elongating). We then show that elongating formins assemble a polar actin network, with barbed ends pointing out of the pulse. Numerical simulations demonstrate that this geometry favors rapid network contraction. Our results show that formins convert a local RhoA activity gradient into a polar network architecture, causing efficient network contractility, underlying the key function of kinetic controls in the assembly and mechanics of cortical network architectures.