Architecture and Connectivity Govern Actin Network Contractility

• Published in: Current biology Vol. 26; no. 5; pp. 616 - 626
• Main Authors: Ennomani, Hajer, Letort, Gaëlle, Guérin, Christophe, Martiel, Jean-Louis, Cao, Wenxiang, Nédélec, François, De La Cruz, Enrique M., Théry, Manuel, Blanchoin, Laurent
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 07.03.2016; Elsevier
• Subjects: Actins - metabolism; Actomyosin - metabolism; Animals; Cellular Biology; Life Sciences; Muscle Contraction; Myosins - metabolism; Rabbits; Network architecture; Actin network contractility; Actomyosin contractility; Cytoskeleton; Micropatterning; Actin filament dynamics
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2015.12.069

Actomyosin contractility plays a central role in a wide range of cellular processes, including the establishment of cell polarity, cell migration, tissue integrity, and morphogenesis during development. The contractile response is variable and depends on actomyosin network architecture and biochemical composition. To determine how this coupling regulates actomyosin-driven contraction, we used a micropatterning method that enables the spatial control of actin assembly. We generated a variety of actin templates and measured how defined actin structures respond to myosin-induced forces. We found that the same actin filament crosslinkers either enhance or inhibit the contractility of a network, depending on the organization of actin within the network. Numerical simulations unified the roles of actin filament branching and crosslinking during actomyosin contraction. Specifically, we introduce the concept of “network connectivity” and show that the contractions of distinct actin architectures are described by the same master curve when considering their degree of connectivity. This makes it possible to predict the dynamic response of defined actin structures to transient changes in connectivity. We propose that, depending on the connectivity and the architecture, network contraction is dominated by either sarcomeric-like or buckling mechanisms. More generally, this study reveals how actin network contractility depends on its architecture under a defined set of biochemical conditions. [Display omitted] •We generated actin architectures that span the diversity of contractile structures•These different actin organizations respond differently to myosin-induced contraction•Actin filament organization and connectivity determine the contractile response•Network contraction is dominated by either sarcomeric-like or buckling mechanisms The composition, organization, and geometry of actomyosin networks influence the production of contractile forces. Ennomani et al. describe how modulating network architecture and composition finely tunes the contractile response and provides a large degree of mechanical adaptation and responsiveness to contractile networks.