Exploring generic principles of compartmentalization in a developmental in vitro model

Abstract

Self-organization of cells into higher-order structures is key for multicellular organisms, e.g. via repetitive replication of template-like founder cells or syncytial energids. Yet, very similar spatial arrangements of cell-like compartments (’protocells’) are also seen in a minimal model system of Xenopus egg extracts in the absence of template structures and chromatin, with dynamic microtubule assemblies driving the self-organization process. Quantifying geometrical features over time, we show here that protocell patterns are highly organized with a spatial arrangement and coarsening dynamics like two-dimensional foams but without the long-range ordering expected for hexagonal patterns. These features remain invariant when enforcing smaller protocells by adding taxol, i.e. patterns are dominated by a single, microtubule-derived length scale. Comparing our data to generic models, we conclude that protocell patterns emerge by simultaneous formation of randomly assembling protocells that grow at a uniform rate towards a frustrated arrangement before fusion of adjacent protocells eventually drives coarsening. The similarity of protocell patterns to arrays of energids and cells in developing organisms, but also to epithelial monolayers, suggests generic mechanical cues to drive self-organized space compartmentalization.

Protein homeostasis from diffusion-dependent control of protein synthesis and degradation

“…Although Xenopus extracts are an in vitro system, they carry out the complex biological functions of an intact Xenopus egg or embryo remarkably faithfully. For example, extracts can self-organize into sheets of cell-like structures whose overall architecture closely resembles that of embryonic blastomeres (Cheng and Ferrell, 2019;Gires et al, 2023;Mitchison and Field, 2021). If supplied with sperm chromatin, extracts can organize a functional nucleus and carry out DNA replication.…”

The nuclear-cytoplasmic ratio controls the cell cycle period in compartmentalized frog egg extract

“…However, the cell encompasses more than just the cytoplasm; subcellular structures also undergo dynamic oscillations during the cell cycle, such as nuclear envelope breakdown and mitotic spindle assembly that have been recapitulated in Xenopus egg extracts (24)(25)(26). Most studies have focused on a specific event or cell cycle stage, either interphase or mitosis.…”