A hydro-osmotic coarsening theory of biological cavity formation

Abstract

The blastocoel is a fluid-filled cavity characterizing early embryos at blastula stage. It is commonly described as the result of cell division patterning, but in tightly compacted embryos the mechanism underlying its emergence remains unclear. Based on experimental observations, we discuss an alternative physical model by which a single cavity forms by growth and coarsening of myriad of micrometric lumens interconnected through the intercellular space. Considering explicitly ion and fluid exchanges, we find that cavity formation is primarily controlled by hydraulic fluxes, with a minor influence of osmotic heterogeneities on the dynamics. Performing extensive numerical simulations on 1-dimensional chains of lumens, we show that coarsening is self-similar with a dynamic scaling exponent reminiscent of dewetting films over a large range of ion and water permeability values. Adding active pumping of ions to account for lumen growth largely enriches the dynamics: it prevents from collective collapse and leads to the emergence of a novel coalescence-dominated regime exhibiting a distinct scaling law. Finally, we prove that a spatial bias in pumping may be sufficient to position the final cavity, delineating hence a novel mode of symmetry breaking for tissue patterning. Providing generic testable predictions our hydro-osmotic coarsening theory highlights the essential roles of hydraulic and osmotic flows in development, with expected applications in early embryogenesis and lumenogenesis.

An ex vivo system to study cellular dynamics underlying mouse peri-implantation development

“…Lumen formation has been described as a process analogous to the nucleation of a droplet in a new phase ( Duclut et al., 2019 ), where the competition between a surface- and a bulk term sets a critical radius above which a lumen can grow. In many biological systems, active processes contribute to these terms, i.e., cytoskeleton-generated cellular surface tensions and active pumping of fluid by the cells ( Torres-Sánchez et al., 2021 ; Le Verge-Serandour and Turlier, 2021 ).…”

Pump it up: bioelectric stimulation controls tissue hydrostatic pressure and water transport via electro-inflation

“…3a and b). The basic mechanics of this model are well validated in other approaches and contexts involving lumenized structures, which we built on by newly introducing electromechanical coupling to an external electric field [7,11,[57][58][59][60][61][62][63][64][65]. The full details of our model are thoroughly discussed in our Supporting Information text.…”

Revisiting the relationship between turgor pressure and plant cell growth

“…Such a mechanism has been suggested to play regulatory roles in various organogenic processes (Landrein & Ingram, 2019). It has been established that many plant outer tissues, such as those of the SAM, seed, sepal, stem, and various animal embryonic and tumorous tissues, are pressurized from below by a fluid or another tissue (Dumais & Steele, 2000;Navis & Bagnat, 2015;Beauzamy et al, 2015;Fourquin et al, 2016;Ruiz-Herrero et al, 2017;Robinson & Kuhlemeier, 2018;Tlili et al, 2019;Zhao et al, 2020;McEvoy et al, 2020;Asaoka et al, 2021;Verge-Serandour & Turlier, 2021). The Young-Laplace law, applicable at the cellular level, also applies to this wider, tissular scale.…”