Hydraulic control of mammalian embryo size and cell fate

Chan, Chii Jou; Costanzo, Maria; Ruiz-Herrero, Teresa; Mönke, Gregor; Petrie, Ryan J.; Bergert, Martin; Diz-Muñoz, Alba; Mahadevan, L.; Hiiragi, Takashi

doi:10.1038/s41586-019-1309-x

Cited by 246 publications

(265 citation statements)

References 36 publications

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“…The advantages of pressure-independent lumen growth remain to be firmly established in an in vivo context. However, we note that this mechanism is predicted to be physically robust and energy efficient relative to pressure-driven growth, which exposes tissues to pressuredriven rupture (Chan et al, 2019;Ruiz-Herrero et al, 2017). Notably, cells in some model systems continue to utilize pressure-independent mechanisms to grow lumens beyond these intermediate stages, for example, by addition of cells or by fusion of smaller lumens (Cerruti et al, 2013;Dumortier et al, 2019).…”

Section: Discussionmentioning

confidence: 92%

“…3i-l). The requirements for the geometric frame scenario are plausible given that cells can actively regulate lumen pressure (Chan et al, 2019;Latorre et al, 2018) and luminal surface area (Fig. 2g).…”

Section: Cells Regulate Both Luminal Pressure and Surface Area To Defmentioning

confidence: 99%

“…To directly test if modulating intraluminal pressure affects lumen shape, we treated MDCK spheroids grown in Matrigel for 3 days and 7 days with small molecules that act to promote or inhibit apical fluid secretion, the V2 receptor agonist 1-desamino-8-D-AVP (ddAVP, 10µM) (Grant et al, 1991) and the Na + /K + ATPase inhibitor ouabain (330 µM) (Chan et al, 2019;Schoner, 2002), respectively. Treatment of MDCK spheroids either ddAVP or ouabain for 4 hours caused lumen cross-sectional area to increase ( Fig.…”

Section: Size-dependent Crossover From Irregular To Spherical Lumensmentioning

confidence: 99%

“…Previous work in MDCK spheroids and other systems has assumed that lumen growth is driven by hydrostatic pressure (Fig. 1a) (Chan et al, 2019;Dasgupta et al, 2018;Latorre et al, 2018;Ruiz-Herrero et al, 2017). In this model, lumen growth is governed by the Young-Laplace equation, which states that the pressure difference (P) between the cells and the lumen is counterbalanced by the surface tension (ɣ) of the lumen surface (apical faces of the cells) and inversely proportional to the lumen radius (r): !"…”

Section: Introductionmentioning

confidence: 99%

“…= $% & . The presence of a pressure gradient is motivated by work that showed that ion channels are critical for lumen formation and expansion in vitro and in vivo (Bagnat et al, 2007;Yap et al, 1993), and by pressure-driven fluctuations in lumen size in some model systems (Chan et al, 2019;Ruiz-Herrero et al, 2017). Importantly, this model predicts that lumen shape must be close to spherical.…”

Section: Introductionmentioning

confidence: 99%

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Physical basis of lumen shape and stability in a simple epithelium

Vasquez

Vachharajani

Garzón-Coral

et al. 2019

Preprint

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A continuous sheet of epithelial cells surrounding a hollow opening, or lumen, defines the basic topology of numerous organs. De novo lumen formation is a central feature of embryonic development whose dysregulation leads to congenital and acquired diseases of the kidney and other organs. While prior work has described the hydrostatic pressure-driven expansion of lumens when they are large, the physical mechanisms that promote the formation and maintenance of small, nascent lumens are less explored. In particular, models that rely solely on pressure-driven expansion face a potential challenge in that the Laplace pressure, which resists lumen expansion, is predicted to scale inversely with lumen radius. We investigated the cellular and physical mechanisms responsible for stabilizing the initial stages of lumen growth using a 3D culture system in which epithelial cells spontaneously form hollow lumens. Our experiments revealed that neither the actomyosin nor microtubule cytoskeletons are required to stabilize lumen geometry, and that a positive intraluminal pressure is not necessary for lumen stability. Instead, our observations are in agreement with a quantitative model in which cells maintain lumen shape due to topological and geometrical factors tied to the establishment of apicobasolateral polarity. We suggest that this model may provide a general physical mechanism for the formation of luminal openings in a variety of physiological contexts. Lumen shapes for small-and intermediate-size MDCK spheroids are inconsistent with a Laplace model of lumen stabilityWe seeded MDCK cells expressing a fluorescent marker for actin filaments (Lifeact-RFP) in the recombinant extracellular matrix Matrigel. Under these culture conditions, MDCK cells spontaneously form hollow spheroids within 24 hours. To obtain high-resolution images of nascent lumens, we imaged young (18-24 hours) spheroids using lattice light sheet microscopy (LLSM). This acquisition method produced images in which the two opposing apical cortices of the lumen are clearly distinguishable and separated by ~200-300 nm (Fig. 1b,c). We infer that cellular apical surfaces are intrinsically non-adherent, as even small fluctuations in cell shape would allow apposing apical surfaces to contact and potentially adhere. This "non-stick" behavior may reflect the enrichment of negatively charged sialoglycoproteins such as

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Section: Discussionmentioning

confidence: 92%

Section: Cells Regulate Both Luminal Pressure and Surface Area To Defmentioning

confidence: 99%

Section: Size-dependent Crossover From Irregular To Spherical Lumensmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Physical basis of lumen shape and stability in a simple epithelium

Vasquez

Vachharajani

Garzón-Coral

et al. 2019

Preprint

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Heterogeneous Structural Color Microfibers for Cardiomyocytes Tug‐of‐War

Chen

Guo

et al. 2020

Adv Funct Materials

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Cellular mechanics are of great significance in biological functions and have stimulated the development of various techniques to detect and analyze it. Here, a novel heterogeneous structural color microfiber designed for dynamic cardiac mechanics sensing is presented. The microfiber is fabricated by the programmed injection microfluidic spinning method, which achieves the alternative injection of different solutions and generates axial heterogeneous components. This microfiber contains non‐close‐packed colloidal arrays for quantitative optical sensing and bioactive methacrylated gelatin (GelMA) for cardiac culture. When the cultivated cardiomyocytes recover autonomous beating cycles, the structural color section would be stretch and exhibits synchronous stretch cycles with dynamic color variation and wavelength shifts, which transforms microcosmic cell‐generated force into macroscopic optical signals. In addition, the single‐cell‐level mechanics detecting platform can be achieved by tuning the size and diameter of the heterogeneous structural color microfibers. These features contribute to the heterogeneous structural color microfiber to be an ideal platform for biomedical fields.

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Bio‐assembling Macro‐Scale, Lumenized Airway Tubes of Defined Shape via Multi‐Organoid Patterning and Fusion

et al. 2021

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Epithelial, stem‐cell derived organoids are ideal building blocks for tissue engineering, however, scalable and shape‐controlled bio‐assembly of epithelial organoids into larger and anatomical structures is yet to be achieved. Here, a robust organoid engineering approach, Multi‐Organoid Patterning and Fusion (MOrPF), is presented to assemble individual airway organoids of different sizes into upscaled, scaffold‐free airway tubes with predefined shapes. Multi‐Organoid Aggregates (MOAs) undergo accelerated fusion in a matrix‐depleted, free‐floating environment, possess a continuous lumen, and maintain prescribed shapes without an exogenous scaffold interface. MOAs in the floating culture exhibit a well‐defined three‐stage process of inter‐organoid surface integration, luminal material clearance, and lumina connection. The observed shape stability of patterned MOAs is confirmed by theoretical modelling based on organoid morphology and the physical forces involved in organoid fusion. Immunofluorescent characterization shows that fused MOA tubes possess an unstratified epithelium consisting mainly of tracheal basal stem cells. By generating large, shape‐controllable organ tubes, MOrPF enables upscaled organoid engineering towards integrated organoid devices and structurally complex organ tubes.

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Hydraulic control of mammalian embryo size and cell fate

Cited by 246 publications

References 36 publications

Physical basis of lumen shape and stability in a simple epithelium

Physical basis of lumen shape and stability in a simple epithelium

Heterogeneous Structural Color Microfibers for Cardiomyocytes Tug‐of‐War

Bio‐assembling Macro‐Scale, Lumenized Airway Tubes of Defined Shape via Multi‐Organoid Patterning and Fusion

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