Symmetry Breaking and Emergence of Directional Flows in Minimal Actomyosin Cortices

Abstract

Cortical actomyosin flows, among other mechanisms, scale up spontaneous symmetry breaking and thus play pivotal roles in cell differentiation, division, and motility. According to many model systems, myosin motor-induced local contractions of initially isotropic actomyosin cortices are nucleation points for generating cortical flows. However, the positive feedback mechanisms by which spontaneous contractions can be amplified towards large-scale directed flows remain mostly speculative. To investigate such a process on spherical surfaces, we reconstituted and confined initially isotropic minimal actomyosin cortices to the interfaces of emulsion droplets. The presence of ATP leads to myosin-induced local contractions that self-organize and amplify into directed large-scale actomyosin flows. By combining our experiments with theory, we found that the feedback mechanism leading to a coordinated directional motion of actomyosin clusters can be described as asymmetric cluster vibrations, caused by intrinsic non-isotropic ATP consumption with spatial confinement. We identified fingerprints of vibrational states as the basis of directed motions by tracking individual actomyosin clusters. These vibrations may represent a generic key driver of directed actomyosin flows under spatial confinement in vitro and in living systems.

Actuation of synthetic cells with proton gradients generated by light-harvesting E. coli

“…This is not surprising given that droplets could also not be deformed with cytoskeletal proteins due to their interfacial properties. [17,42] We thus moved to a compartment system which better mimics the mechanical properties of cellular membranes. We produced giant unilamellar lipid vesicles (GUVs) and functionalized them externally with the cholesteroltagged DNA (Figure 4c).…”

Dynamic self-assembly of compartmentalized DNA nanotubes

“…Encapsulated full cytoplasmic extracts are able to generate assembly, disassembly, and contraction of actomyosin networks 8 , 12 , 13 . The inclusion of motor proteins (as well as ATP production and oxygen scavenging) is key to achieve contraction and directed motion 14 . These advances point to exciting opportunities toward harnessing native cytoskeletal systems in synthetic cells.…”

Actin crosslinker competition and sorting drive emergent GUV size-dependent actin network architecture

“…Although open biomimetic platforms such as supported lipid bilayers, lipid-coated beads, and surface of GUVs introduce appropriate boundary conditions for self-assembly of cytoskeletal components into biochemically and mechanically functional networks 14,15,16,17,18,19 , they do not impose and demonstrate the influence of confined environment of the cell on network organization. To this end, protein components have been encapsulated within or attached to inside lipid-coated single emulsion droplets or GUVs 20,21,22,23,24 . Encapsulated microtubule-kinesin networks in droplets, for instance, reorganized into ring-like, cortical, or star-like structures based on droplet size 25,26 .…”

“…Although biomimetic platforms such as supported lipid bilayers [19][20][21] and the surfaces of giant unilamellar vesicles (GUVs) [22][23][24] introduce appropriate boundary conditions for selfassembly of actin network components into biochemically and mechanically functional networks, they do not confine components in the way that a cell does. To address this issue, actin cytoskeletal components have been encapsulated within or attached to the interiors of lipid-coated single emulsion droplets [25][26][27] or GUVs [27][28][29][30] . Studies that reconstitute actin and microtubule networks from purified components have revealed that spatial confinement can change the structures formed [31][32][33][34] .…”