Biomimetic niches reveal the minimal cues to trigger apical lumen formation in single hepatocytes

Zhang, Yue; Mets, Richard De; Monzel, Cornelia; Acharya, Vidhyalakshmi; Toh, Pearlyn Jia Ying; Chin, Jasmine Fei Li; Hul, Noémi Van; Ng, Inn Chuan; Yu, Hanry; Ng, Soon Seng; Rashid, S. Tamir; Viasnoff, Virgile

doi:10.1038/s41563-020-0662-3

Cited by 30 publications

(32 citation statements)

References 30 publications

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“…Future studies will be needed to understand what sets robust transcellular fluid accumulation during preimplantation development. The ability of single cells to polarize and inflate a lumen was recently demonstrated in vitro by plating hepatocytes onto CDH1-coated substrates (Zhang et al, 2020). In this study, fluid accumulation in single-celled embryos does not result in the formation of a lumen but in the formation of inflating vacuoles.…”

Section: Discussionmentioning

confidence: 54%

Multiscale analysis of single and double maternal-zygotic Myh9 and Myh10 mutants during mouse preimplantation development

Schliffka

Tortorelli

Özgüç

et al. 2021

eLife

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During the first days of mammalian development, the embryo forms the blastocyst, the structure responsible for implanting the mammalian embryo. Consisting of an epithelium enveloping the pluripotent inner cell mass and a fluid-filled lumen, the blastocyst results from a series of cleavages divisions, morphogenetic movements and lineage specification. Recent studies identified the essential role of actomyosin contractility in driving the cytokinesis, morphogenesis and fate specification leading to the formation of the blastocyst. However, the preimplantation development of contractility mutants has not been characterized. Here, we generated single and double maternal-zygotic mutants of non-muscle myosin II heavy chains (NMHC) to characterize them with multiscale imaging. We find that Myh9 (NMHC II-A) is the major NMHC during preimplantation development as its maternal-zygotic loss causes failed cytokinesis, increased duration of the cell cycle, weaker embryo compaction and reduced differentiation, whereas Myh10 (NMHC II-B) maternal-zygotic loss is much less severe. Double maternal-zygotic mutants for Myh9 and Myh10 show a much stronger phenotype, failing most attempts of cytokinesis. We find that morphogenesis and fate specification are affected but nevertheless carry on in a timely fashion, regardless of the impact of the mutations on cell number. Strikingly, even when all cell divisions fail, the resulting single-celled embryo can initiate trophectoderm differentiation and lumen formation by accumulating fluid in increasingly large vacuoles. Therefore, contractility mutants reveal that fluid accumulation is a cell-autonomous process and that the preimplantation program carries on independently of successful cell division.

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Section: Discussionmentioning

confidence: 54%

Multiscale analysis of single and double maternal-zygotic Myh9 and Myh10 mutants during mouse preimplantation development

Schliffka

Tortorelli

Özgüç

et al. 2021

eLife

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“…The successful opening and shaping of cavities of various topologies (tubes, network of cavities…) during development is essential to organ functions in adult organisms. Lumens appear generally at the non-adhesive side of polarized cells and are called apical [ 1 ], to distinguish them from adhesive contacts of polarized cells called basolateral. Common mechanisms for the formation of apical lumens have been described in various model systems, and include: apical membrane secretion, cavitation by cell apoptosis and paracellular ion transport [ 2 , 3 ].…”

Section: Introductionmentioning

confidence: 99%

A hydro-osmotic coarsening theory of biological cavity formation

Verge-Serandour

Turlier

2021

PLoS Comput Biol

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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.

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“…Common mechanisms for the formation of lumens at the apical side of polarized cells are described in various model systems Sigurbjörnsdóttir et al ( 2014 ), but the emergence of basolateral cavities, also called cysts in tissues, or blastocoels in early embryos, has received much less attention. Apical lumens are facing intrinsically non-adherent cell interfaces Zhang et al ( 2020 ) and are directly sealed at their surface by tight junction proteins Krug et al ( 2014 ), limiting paracellular water leaking from the cavity into the intercellular space, while allowing for the passage of selected ions Narayanan et al ( 2020 ). This may explain why tissues with multiple apical lumens may fail to spontaneously resolve into a single cavity Torkko et al ( 2008 ).…”

Section: Introductionmentioning

confidence: 99%

“…Lumens appear generally at the non-adhesive side of polarized cells and are called apical [1], to distinguish them from adhesive contacts of polarized cells called basolateral. Common mechanisms for the formation of apical lumens have been described in various model systems, and include: apical membrane secretion, cavitation by cell apoptosis and paracellular ion transport [2,3].…”

Section: Introductionmentioning

confidence: 99%

“…It is indeed important to remark that blastocoel-like cavities emerge at the baso-lateral side of polarized cells, that is typically adhesive. They differ hence topologically from apical lumens, that are facing apical -and intrinsically non-adherent-cell interfaces (29,30). Apical lumens are directly sealed at their surface by tight junction proteins (31), limiting paracellular water leaking into the intercellular space, while allowing for the passage of selected ions (32).…”

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confidence: 99%

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A hydro-osmotic coarsening theory of biological cavity formation

Verge-Serandour

Turlier

2020

Preprint

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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.

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Biomimetic niches reveal the minimal cues to trigger apical lumen formation in single hepatocytes

Cited by 30 publications

References 30 publications

Multiscale analysis of single and double maternal-zygotic Myh9 and Myh10 mutants during mouse preimplantation development

Multiscale analysis of single and double maternal-zygotic Myh9 and Myh10 mutants during mouse preimplantation development

A hydro-osmotic coarsening theory of biological cavity formation

A hydro-osmotic coarsening theory of biological cavity formation

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