Downregulation of extraembryonic tension controls body axis formation in avian embryos

Kunz, Daniele; Wang, Anfu; Chan, Chon U; Pritchard, Robyn H.; Wang, Wenyu; Gallo, Filomena; Bradshaw, Charles R.; Terenzani, Elisa; Müller, Karin H.; Huang, Yan Yan Shery; Xiong, Fengzhu

doi:10.1038/s41467-023-38988-3

Cited by 9 publications

(2 citation statements)

References 63 publications

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“…Ex ovo culture was performed using a modified EC culture 41 protocol as described 42 . For in ovo operations, egg shells were windowed with surgical scissors after removing some albumen.…”

Section: Methodsmentioning

confidence: 99%

Differential tissue deformability underlies shape divergence of the embryonic brain and spinal cord under fluid pressure

McLaren,

Xue,

Ding

et al. 2024

Preprint

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An expanded brain enables the complex behaviours of vertebrates that promote their adaptation in diverse ecological niches. Initial morphological differences between the brain and spinal cord emerge as the antero-posteriorly patterned neural plate folds to form the neural tube during embryonic development. Following neural tube closure, a dramatic expansion of the brain diverges its shape from the spinal cord, setting their distinct morphologies for further development. How the brain and the spinal cord expand differentially remains unclear. Here, using the chicken embryo as a model, we show that the hindbrain expands through dorsal tissue thinning under a positive hydrostatic pressure from the neural tube lumen while the dorsal spinal cord shape resists the same pressure. Using magnetic droplets and atomic force microscopy, we reveal that the dorsal tissue in the hindbrain is more fluid than in the spinal cord. The dorsal hindbrain harbours more migratory neural crest cells and exhibits reduced apical actin and a disorganised laminin matrix compared to the dorsal spinal cord. Blocking the activity of neural crest-associated matrix metalloproteinases inhibited dorsal tissue thinning, leading to abnormal brain morphology. Transplanting early dorsal hindbrain cells to the spinal cord was sufficient to create a region with expanded brain-like morphology including a thinned-out roof. Our findings open new questions in vertebrate head evolution and neural tube defects, and suggest a general role of mechanical pre-pattern in creating shape differences in epithelial tubes.

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“…Ex ovo culture was performed using a modified EC culture 41 protocol as described 42 . For in ovo operations, egg shells were windowed with surgical scissors after removing some albumen.…”

Section: Methodsmentioning

confidence: 99%

Differential tissue deformability underlies shape divergence of the embryonic brain and spinal cord under fluid pressure

McLaren,

Xue,

Ding

et al. 2024

Preprint

Self Cite

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“…We found that the pulled embryos show a longer, darker PSM with unchanged width while the neighbouring neural tube and notochord show a narrower tissue 12 (Figure 2D). This suggests that extension of the mesenchymal pPSM leads to a decrease in cell density, whereas extension of the epithelial axial structures causes tissue narrowing, mimicking their respective normal, active modes (expansion of the pPSM and convergent extension of the axial tissues, respectively) of elongation 2,3,9,18 . We measured the medial-lateral cell density gradient across the PD-pPSM transition area using the fluorescence intensity and found that the gradient is steeper in pulled embryos (Figure 2E).…”

Section: Mechanical Perturbations Alter Body Axis Length and Ppsm Cel...mentioning

confidence: 99%

Cell density couples tissue mechanics to control the elongation speed of the body axis

Lu,

Vidigueira,

Jie

et al. 2024

Preprint

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The vertebrate body forms by progressive addition and segmentation of tissues in an anterior to posterior direction. The posterior presomitic mesoderm (pPSM), which receives new cells from the tailbud, produces an expansive force that drives axis elongation (1,2,3). Elongation moves an FGF gradient that controls the boundary placement of new segments in conjunction with the oscillatory genes of the segmentation clock (4). As the period of the segmentation clock is insensitive to body size (5,6) or elongation progress (7,8), the number and size consistency of segments depend on stable, robust elongation. How elongation speed is constrained remains unknown. Here we utilised modeling and tissue force microscopy (9) on chicken embryos to show that cell density of the pPSM dynamically modulates elongation speed in a negative feedback loop. Elongation alters the cell density in the pPSM, which in turn controls progenitor cell influx through the mechanical coupling of body axis tissues. This enables responsive cell dynamics in over- and under-elongated axes that consequently self-adjust speed to achieve long-term robustness in axial length. Our simulations and experiments further suggest that cell density and activity under FGF signalling act synergistically to drive elongation. Our work supports a simple mechanism of morphogenetic speed control where the cell density relates negatively to progress, and positively to force generation.

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From signalling to form: the coordination of neural tube patterning

Frith,

Briscoe,

Boezio

2024

Current Topics in Developmental Biology

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Downregulation of extraembryonic tension controls body axis formation in avian embryos

Cited by 9 publications

References 63 publications

Differential tissue deformability underlies shape divergence of the embryonic brain and spinal cord under fluid pressure

Differential tissue deformability underlies shape divergence of the embryonic brain and spinal cord under fluid pressure

Cell density couples tissue mechanics to control the elongation speed of the body axis

From signalling to form: the coordination of neural tube patterning

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