Cell surface fluctuations regulate early embryonic lineage sorting

Yanagida, Akira; Corujo-Simon, Elena; Revell, Christopher; Sahu, Preeti Ranjan; Stirparo, Giuliano Giuseppe; Aspalter, Irene M.; Winkel, Alex; Peters, Ruby; Belly, Henry De; Cassani, Davide A. D.; Achouri, Sarra; Blumenfeld, Raphaël; Franze, Kristian; Hannezo, Édouard; Paluch, Ewa K.; Nichols, Jennifer; Chalut, Kevin J.

doi:10.1016/j.cell.2022.03.015

Cited by 11 publications

(13 citation statements)

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“…3d). The existence of such active stresses due to the contractile tension at the cell cortex and the myosin activity is well documented [12,[44][45][46]. In our simulations we find that as the cells continuously push and pull on their neighbors by generating active stresses, the less elastic cells are able to deform more, exchange neighbors at a higher rate (Fig.…”

supporting

confidence: 71%

Differential elasticity in lineage segregation of embryonic stem cells

Ritter

Lejnse

Barooji

et al. 2022

Preprint

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The question of what guides lineage segregation is central to development, where cellular differentiation leads to segregated cell populations destined for specialized functions. Here, using optical tweezers measurements of mouse embryonic stem cells (mESCs), we reveal a mechanical mechanism based on differential elasticity in the second lineage segregation of the embryonic inner cell mass into epiblast (EPI) cells - that will develop into the fetus - and primitive endoderm (PrE) - which will form extraembryonic structures such as the yolk sac. Remarkably, we find that these mechanical differences already occur during priming and not just after a cell has committed to differentiation. Specifically, we show that the mESCs are highly elastic compared to any other reported cell type and that the PrE cells are significantly more elastic than EPI-primed cells. Using a model of two cell types differing only in elasticity we show that differential elasticity alone can lead to segregation between cell types, suggesting that the mechanical attributes of the cells contribute to the segregation process. Our findings present differential elasticity as a previously unknown mechanical contributor to the lineage segregation during the embryo morphogenesis.

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supporting

confidence: 71%

Differential elasticity in lineage segregation of embryonic stem cells

Ritter

Lejnse

Barooji

et al. 2022

Preprint

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“…The outcome of cell sorting has been modelled previously by considering cell-specific differences in interfacial energies maximizing the most energetically favourable cell interfaces 15,[33][34][35][36] . Disparity in interfacial energy was considered to reflect adhesion differences, with cadherins being the best-characterized effectors 1,37 , as espoused in the differential adhesion hypothesis (DAH) 33,38 .…”

Section: Nature Cell Biologymentioning

confidence: 99%

Stem cell-derived synthetic embryos self-assemble by exploiting cadherin codes and cortical tension

et al. 2022

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Mammalian embryos sequentially differentiate into trophectoderm and an inner cell mass, the latter of which differentiates into primitive endoderm and epiblast. Trophoblast stem (TS), extraembryonic endoderm (XEN) and embryonic stem (ES) cells derived from these three lineages can self-assemble into synthetic embryos, but the mechanisms remain unknown. Here, we show that a stem cell-specific cadherin code drives synthetic embryogenesis. The XEN cell cadherin code enables XEN cell sorting into a layer below ES cells, recapitulating the sorting of epiblast and primitive endoderm before implantation. The TS cell cadherin code enables TS cell sorting above ES cells, resembling extraembryonic ectoderm clustering above epiblast following implantation. Whereas differential cadherin expression drives initial cell sorting, cortical tension consolidates tissue organization. By optimizing cadherin code expression in different stem cell lines, we tripled the frequency of correctly formed synthetic embryos. Thus, by exploiting cadherin codes from different stages of development, lineage-specific stem cells bypass the preimplantation structure to directly assemble a postimplantation embryo.

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“…14). In mammalian embryos, differential cell surface fluctuations reportedly account for the lineage sorting of the primitive endoderm from the epiblast 37 . The primitive endoderm displays higher surface fluctuations than the epiblast.…”

Section: Resultsmentioning

confidence: 99%

Spatiotemporal dynamics of zygotic genome activation in basal chordates revealed by interspecific hybrids

Wei

Zhang

Leng

et al. 2022

Preprint

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Zygotic genome activation (ZGA), a universal process in early embryogenesis that occurs during the maternal-to-zygotic transition, involves reprogramming in the zygotic nucleus that initiates global transcription. In recent decades, knowledge of this process has been acquired from research on various model organisms; however, a consensus explanation of the mechanism underlying the process, especially in relation to housekeeping gene reactivation, is lacking. Here, we used hybrids derived from two ascidian species (Ciona robusta and C. savignyi), which diverged >120 Mya with significant divergence among most orthologous genes, to symmetrically document the unique dynamics of ZGA in urochordates. We found two co-ordinated waves of ZGA, representing early developmental and housekeeping gene reactivation, during the 8-cell to 110-cell stage. Comparative analysis revealed the regulatory connection between maternal and zygotic genes as well as allelic-specific expression in a species-rather than parental-related manner, which was attributed to the divergence of cis-regulatory elements. Single-cell RNA sequencing revealed that spatial differential reactivation of paternal housekeeping genes was significantly correlated with the mechanical property of each cell type. These findings potentially provide a new system for understanding the evolution and adaptation of strategies regulating ZGA in basal chordates.

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Cell surface fluctuations regulate early embryonic lineage sorting

Cited by 11 publications

References 0 publications

Differential elasticity in lineage segregation of embryonic stem cells

Differential elasticity in lineage segregation of embryonic stem cells

Stem cell-derived synthetic embryos self-assemble by exploiting cadherin codes and cortical tension

Spatiotemporal dynamics of zygotic genome activation in basal chordates revealed by interspecific hybrids

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