Volumetric Compression Induces Intracellular Crowding to Control Intestinal Organoid Growth via Wnt/β-Catenin Signaling

Li, Yiwei; Chen, Maorong; Hu, Jijie; Sheng, Ren; Lin, Qirong; He, Xi; Guo, Ming

doi:10.1016/j.stem.2020.09.012

Cited by 73 publications

(51 citation statements)

References 93 publications

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“…In addition, the mechanosensitive ion channel TRPV4 was also found to regulate lung development and stabilize pulmonary vasculature. [ 78 ] Recently, it has also been discovered that volumetric compression can increase the degree of molecular crowding in cells, which promotes Wnt/β‐catenin signaling, [ 79 ] a process that can be used to regulate the development of mouse intestinal organoids, [ 79 ] as well as de‐differentiation of human and mouse adipocytes. [ 80 ] Similar effect has also been observed on YAP/TAZ signaling, [ 81 ] suggesting that this physical mechanism may have a more general regulatory role in development.…”

Section: Molecular Mechanisms Of Mechanosensingmentioning

confidence: 99%

Generation, Transmission, and Regulation of Mechanical Forces in Embryonic Morphogenesis

Sutlive

Xiu

Chen

et al. 2021

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Embryonic morphogenesis is a biological process which depicts shape forming of tissues and organs during development. Unveiling the roles of mechanical forces generated, transmitted, and regulated in cells and tissues through these processes is key to understanding the biophysical mechanisms governing morphogenesis. To this end, it is imperative to measure, simulate, and predict the regulation and control of these mechanical forces during morphogenesis. This article aims to provide a comprehensive review of the recent advances on mechanical properties of cells and tissues, generation of mechanical forces in cells and tissues, the transmission processes of these generated forces during cells and tissues, the tools and methods used to measure and predict these mechanical forces in vivo, in vitro, or in silico, and to better understand the corresponding regulation and control of generated forces. Understanding the biomechanics and mechanobiology of morphogenesis will not only shed light on the fundamental physical mechanisms underlying these concerted biological processes during normal development, but also uncover new information that will benefit biomedical research in preventing and treating congenital defects or tissue engineering and regeneration.

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Section: Molecular Mechanisms Of Mechanosensingmentioning

confidence: 99%

Generation, Transmission, and Regulation of Mechanical Forces in Embryonic Morphogenesis

Sutlive

Xiu

Chen

et al. 2021

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“…Cells integrate cytokine-mediated, chemical and physical stimuli from the extracellular environment to regulate cell fate and function. Even the physical properties of a cell itself, including cortical stiffness 1 , membrane tension 2, 3 and intracellular crowding 4 , are subject to dynamic changes in response to external cues, thereby integrating microenvironmental information into a physiological response 5, 6 . This intricate pattern of regulation is of particular importance during embryogenesis, when pluripotent cells are faced with the complex task of undergoing spatiotemporal lineage specification to generate an entire fetus.…”

Section: Introductionmentioning

confidence: 99%

“…Membrane tension regulates the endocytic uptake of MEK/ERK signaling components and thus somatic cell-fate acquisition 2 . Recently, volumetric compression has been identified as a physical cue to promote self-renewal of intestinal stem cells in organoid cultures 4 , and dedifferentiation of adipocytes 30 , via WNT/β-catenin signaling. Volumetric compression induces molecular crowding, which stabilizes LRP6 signalosome formation and consequently elevates WNT/β-catenin signaling.…”

Section: Introductionmentioning

confidence: 99%

Plakoglobin is a mechanoresponsive regulator of naïve pluripotency

Kohler

Jonghe

Ellermann

et al. 2022

Preprint

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Biomechanical cues are instrumental in guiding embryonic development and cell differentiation. Understanding how these physical stimuli translate into transcriptional programs could provide insight into mechanisms underlying mammalian pre implantation development. Here, we explore this by exerting microenvironmental control over mouse embryonic stem cells (ESCs). Microfluidic encapsulation of ESCs in agarose microgels stabilized the naïve pluripotency network and specifically induced expression of Plakoglobin (Jup), a vertebrate homologue of β-catenin. Indeed, overexpression of Plakoglobin was sufficient to fully re establish the naïve pluripotency gene regulatory network under metastable pluripotency conditions, as confirmed by single cell transcriptome profiling. Finally, we found that in the epiblast, Plakoglobin was exclusively expressed at the blastocyst stage in human and mouse embryos — further strengthening the link between Plakoglobin and naïve pluripotency in vivo. Our work reveals Plakoglobin as a mechanosensitive regulator of naïve pluripotency and provides a paradigm to interrogate the effects of volumetric confinement on cell fate transitions.

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“…Accruing evidence showed that mechanical and physical cues, such as fluid shear stress, static stretch, and magnetic forces, can also contribute to stem cell fate determination ( Clause et al, 2010 ; Marycz et al, 2016 ; Vining and Mooney, 2017 ). A recent study has revealed that extracellular physical cues could transduce into intracellular force to control the intestinal organoid growth and development through Wnt/β-catenin signaling ( Li et al, 2020 ). Particularly, stretch could stimulate neuron growth ( Loverde and Pfister, 2015 ; Breau and Schneider-Maunoury, 2017 ), axon growth ( De Vincentiis et al, 2020 ), and neurite outgrowth ( Higgins et al, 2013 ; Kampanis et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Cyclic Strain and Electrical Co-stimulation Improve Neural Differentiation of Marrow-Derived Mesenchymal Stem Cells

Cheng

Huang

Chen

et al. 2021

Front. Cell Dev. Biol.

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The current study investigated the combinatorial effect of cyclic strain and electrical stimulation on neural differentiation potential of rat bone marrow-derived mesenchymal stem cells (BMSCs) under epidermal growth factor (EGF) and fibroblast growth factor 2 (FGF2) inductions in vitro. We developed a prototype device which can provide cyclic strain and electrical signal synchronously. Using this system, we demonstrated that cyclic strain and electrical co-stimulation promote the differentiation of BMCSs into neural cells with more branches and longer neurites than strain or electrical stimulation alone. Strain and electrical co-stimulation can also induce a higher expression of neural markers in terms of transcription and protein level. Neurotrophic factors and the intracellular cyclic AMP (cAMP) are also upregulated with co-stimulation. Importantly, the co-stimulation further enhances the calcium influx of neural differentiated BMSCs when responding to acetylcholine and potassium chloride (KCl). Finally, the phosphorylation of extracellular-signal-regulated kinase (ERK) 1 and 2 and protein kinase B (AKT) was elevated under co-stimulation treatment. The present work suggests a synergistic effect of the combination of cyclic strain and electrical stimulation on BMSC neuronal differentiation and provides an alternative approach to physically manipulate stem cell differentiation into mature and functional neural cells in vitro.

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Volumetric Compression Induces Intracellular Crowding to Control Intestinal Organoid Growth via Wnt/β-Catenin Signaling

Cited by 73 publications

References 93 publications

Generation, Transmission, and Regulation of Mechanical Forces in Embryonic Morphogenesis

Generation, Transmission, and Regulation of Mechanical Forces in Embryonic Morphogenesis

Plakoglobin is a mechanoresponsive regulator of naïve pluripotency

Cyclic Strain and Electrical Co-stimulation Improve Neural Differentiation of Marrow-Derived Mesenchymal Stem Cells

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