Cytoplasmic self-organization established by internal lipid membranes in the interplay with either actin or microtubules

Abstract

AbstractCells harbor an intrinsic organization of their components. Specific protein structures, as the centrosome, have been described master regulators of cell organization. In the absence of these key elements, however, cytoplasmic selforganization has nevertheless been observed. Cytoplasmic self-organization was postulated to arise from the interaction of microtubules with molecular motors on lipid membrane surfaces.Here, we show that lipid membranes are capable of organizing both major cytoskeletal systems, microtubules and actin, even if one or the other cytoskeletal system is completely paralyzed. A microfluidic droplet system and Xenopus oocyte extracts enabled us to build an artificial cell and study minimal requirements for cellular self-organization. Mathematical modeling reveals the interaction of lipid membranes with any filament system through molecular motors as a universal principle of cytoplasmic self-organization. Both cytoskeletal systems form mechanisms to establish robust 2-dimensional selforganization and self-centering. Pharmacologic inhibition of the cytoskeletal network systems helps dissect specific contributions of each network in the interplay with lipid membranes with regards to 2- and 3-dimensional organization, time and length scale of cytoplasmic organization and the degree of concentration of the centered elements. While microtubules provide 3-dimensional polarity, actin filaments ensure fast and dense compaction and long-range organization.