Diversity from similarity: cellular strategies for assigning particular identities to actin filaments and networks

Abstract

The actin cytoskeleton has the particularity of being assembled into many functionally distinct filamentous networks from a common reservoir of monomeric actin. Each of these networks has its own geometrical, dynamical and mechanical properties, because they are capable of recruiting specific families of actin-binding proteins (ABPs), while excluding the others. This review discusses our current understanding of the underlying molecular mechanisms that cells have developed over the course of evolution to segregate ABPs to appropriate actin networks. Segregation of ABPs requires the ability to distinguish actin networks as different substrates for ABPs, which is regulated in three different ways: (1) by the geometrical organization of actin filaments within networks, which promotes or inhibits the accumulation of ABPs; (2) by the identity of the networks' filaments, which results from the decoration of actin filaments with additional proteins such as tropomyosin, from the use of different actin isoforms or from covalent modifications of actin; (3) by the existence of collaborative or competitive binding to actin filaments between two or multiple ABPs. This review highlights that all these effects need to be taken into account to understand the proper localization of ABPs in cells, and discusses what remains to be understood in this field of research.

Cell wound repair requires the coordinated action of linear and branched actin nucleation factors

“…Many diverse cell processes such as cell division, motility, and shape changes require that actin filaments be organized into assemblies of optimized architecture, dynamics, and mechanical attributes to carry out their specific functions properly (Boiero Sanders et al, 2020; Campellone and Welch, 2010; Cheffings et al, 2016; Gautreau et al, 2021; Schwayer et al, 2016). We find that during cell wound repair the proper assembly and function of the actomyosin ring requires both branched and linear actin networks (Fig.…”

Crosstalk between basal extracellular matrix adhesion and building of apical architecture during morphogenesis

“…Finally, we point readers to other reviews that elaborate on specific aspects related to this work (Table 2). Chaudhuri et al, 2020;Khalilgharibi and Mao, 2021;Walma and Yamada, 2020;Fidler et al, 2018;Pastor-Pareja, 2020 Cell-cell andcell-ECM interactions Bachir et al, 2017;Dzamba and DeSimone, 2018;Klapholz and Brown, 2017;Moreno-Layseca et al, 2019;Perez-Vale andPeifer, 2020 Actin-MT interactions Dogterom andKoenderink, 2019;Voelzmann et al, 2017Biomechanics in morphogenesis Gilmour et al, 2017Kindberg et al, 2020;Kirby and Lammerding, 2018;Molnar and Labouesse, 2021;Tsata andBeis, 2020 Microtubules Muroyama andLechler, 2017;Röper, 2020Actin cytoskeleton Alekhina et al, 2017Boiero Sanders et al, 2020;Miao and Blankenship, 2020;Rottner et al, 2017 Tracheal development andbranching Hayashi andKondo, 2018;Öztürk-Çolak et al, 2016a;Ricolo et al, 2021 Dorsal closure Hayes and Solon, 2017;Kiehart et al, 2017…”

Structural basis underlying specific biochemical activities of non-muscle tropomyosin isoforms

“…To fulfill the specific needs of these diverse cellular processes, actin filaments assemble into a variety of structures with different architectures and dynamic properties and produce force through coordinated filament polymerization, as well as by serving as tracks for myosin motor proteins. Actin filaments of the different cytoskeletal structures associate with specific sets of actin-binding proteins, which give rise to distinct properties of actin filaments (Blanchoin et al, 2014; Boiero Sanders et al, 2020). In plants, the functional variety of actin filament structures has been proposed to derive from the presence of a large number of closely related actin isoforms (Gunning et al, 2015a).…”