A hydro-osmotic coarsening theory of biological cavity formation

Abstract

Fluid-filled biological cavities are ubiquitous, but their collective dynamics has remained largely unexplored from a physical perspective. Based on experimental observations in early embryos, we propose a model where a cavity forms through the coarsening of myriad of pressurized micrometric lumens, that interact by ion and fluid exchanges through the intercellular space. Performing extensive numerical simulations, we find that hydraulic fluxes lead to a self-similar coarsening of lumens in time, characterized by a robust dynamic scaling exponent. The collective dynamics is primarily controlled by hydraulic fluxes, which stem from lumen pressures differences and are dampened by water permeation through the membrane. Passive osmotic heterogeneities play, on the contrary, a minor role on cavity formation but active ion pumping can largely modify the coarsening dynamics: it prevents the lumen network from a collective collapse and gives rise to a novel coalescence-dominated regime exhibiting a distinct scaling law. Interestingly, we prove numerically that spatially biasing ion pumping may be sufficient to position the cavity, suggesting a novel mode of symmetry breaking to control tissue patterning. Providing generic testable predictions, our model forms a comprehensive theoretical basis for hydro-osmotic interaction between biological cavities, that shall find wide applications in embryo and tissue morphogenesis.

Spontaneous collapse as a prognostic marker for human blastocysts: a systematic review and meta-analysis

“…The blastocyst stage begins at 4–5 days post-fertilization in humans ( Biggers et al , 1977 ). This is when the sodium pumps in the future trophectoderm cells start to pump sodium into the centre of the embryo, so that the accumulating sodium osmotically draws in water to create a blastocoel cavity ( Biggers et al , 1977 ; Le Verge-Serandour and Turlier, 2021 ; Le Verge-Serandour and Turlier, 2022 ). The growing blastocoel forces the zona pellucida to thin, and the hatching process follows, which is mandatory for implantation to occur ( Cohen et al , 1985 ; Gonzales et al , 1996 ).…”

Shaping epithelial lumina under pressure

“…While we do not believe that any direct active water transporter is known at present, transport, and docking of vesicles to the apical surfaces could contribute to this flux. The physics of the lumen dynamics that arise for imbalanced fluxes, , have been explored, for example, in [ 20 , 40 ].…”

Bioelectric stimulation controls tissue shape and size

“…Investigating the role of externally applied electric fields on ion pumps deserves future work and will be a useful extension of our work. The main ingredients of this model are well validated in other approaches and contexts involving lumenized structures, which we built on by introducing electromechanical coupling to an external electric field 7,16,67,[69][70][71][72][73][74]85,86 (see theory Supplementary Info. for more details).…”