Tissue hydraulics: Physics of lumen formation and interaction

Torres-Sánchez, Alejandro; Winter, Max Kerr; Salbreux, Guillaume

doi:10.1016/j.cdev.2021.203724

Cited by 32 publications

(41 citation statements)

References 105 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…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 ).…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2022

View full text Add to dashboard Cite

Summary Upon implantation, mammalian embryos undergo major morphogenesis and key developmental processes such as body axis specification and gastrulation. However, limited accessibility obscures the study of these crucial processes. Here, we develop an ex vivo Matrigel-collagen-based culture to recapitulate mouse development from E4.5 to E6.0. Our system not only recapitulates embryonic growth, axis initiation, and overall 3D architecture in 49% of the cases, but its compatibility with light-sheet microscopy also enables the study of cellular dynamics through automatic cell segmentation. We find that, upon implantation, release of the increasing tension in the polar trophectoderm is necessary for its constriction and invagination. The resulting extra-embryonic ectoderm plays a key role in growth, morphogenesis, and patterning of the neighboring epiblast, which subsequently gives rise to all embryonic tissues. This 3D ex vivo system thus offers unprecedented access to peri-implantation development for in toto monitoring, measurement, and spatiotemporally controlled perturbation, revealing a mechano-chemical interplay between extra-embryonic and embryonic tissues.

show abstract

Section: Methodsmentioning

confidence: 99%

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

et al. 2022

View full text Add to dashboard Cite

show abstract

“…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.…”

Section: A Mechanical Model For Mdck Cysts Inflation In An Electric F...mentioning

confidence: 98%

“…Such ion crowding works to neutralize the surface charge but also increases the concentration of ions around the cyst and triggers the transport of species into the lumen due to electro-osmotic effects, as the concentration of ions in the lumen is lower than in the DDL. Moreover, the electric potential across the epithelium also increases due to ion crowding [66,67], which drives the transport of water across the epithelium via electro-osmosis leading to inflation [60] (Figs. 3c-e, yellow curves).…”

Section: A Mechanical Model For Mdck Cysts Inflation In An Electric F...mentioning

confidence: 99%

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

Shim

Breinyn

Martínez-Calvo

et al. 2022

Preprint

View full text Add to dashboard Cite

Epithelial tissues sheath many organs, separating ‘outside’ from ‘inside’ and exquisitely regulating ion and water transport via electromechanical pumping to maintain homeostatic balance and tissue hydrostatic pressure. While it is becoming increasingly clear that the ionic microenvironment and external electric stimuli can affect epithelial function and behavior, the coupling between electrical perturbation and tissue form remain unclear. We investigated this by combining electrical stimulation with three-dimensional epithelial tissues with hollow ‘lumens’—both kidney cysts and complex intestinal stem cell organoids. Our core finding is that physiological strength electrical stimulation of order 1-3 V/cm (with both direct and alternating currents) can drive powerful and rapid inflation of hollow tissues through a process we call ‘electro-inflation’, inducing a nearly threefold increase in tissue volume and striking asymmetries in tissue form. Electro-inflation is primarily driven by activation of the CFTR ion channel pumping chloride into the tissue, causing water to osmotically flow. This influx generates hydrostatic pressure, and inflation results from a competition between this pressure and cell cytoskeletal tension. We validated these interpretations with computational models connecting ion dynamics in the Diffuse Double Layer around tissues to tissue mechanics. Electro-inflation is a unique biophysical process to study and control complex tissue function.

show abstract

“…Just as cells control their size, the coeloblastula may control the blastocoel size by passive osmotic transport, active ion pumping or mechanical forces [109]. To physically illustrate these effects, we simplify the description of a coeloblastula as a cavity surrounded by a single cellular compartment, that may be viewed as a continuous and sealed epithelial layer (Fig.…”

Section: Polarized Ion Transport and Volume Regulationmentioning

confidence: 99%