Quantitative Experimental Embryology: A Modern Classical Approach

Busby, Lara; Saunders, Dillan; Nájera, Guillermo Serrano; Steventon, Benjamin

doi:10.3390/jdb10040044

Cited by 3 publications

(4 citation statements)

References 74 publications

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“…However, uncoupling these events in the context of in vivo studies is a major challenge for the field and can be supported by work in vitro where specific developmental processes can be isolated to uncover novel connections between metabolism and developmental cell biology. In many ways, this is continuing an experimental embryology approach, where cut-and-paste biology has enabled the elucidation of the molecular mechanisms that underpin morphogenesis and patterning [ 12 , 29 ].…”

Section: Why Gastruloids?mentioning

confidence: 99%

“…At the time of Child and Morgan, the field lacked an inclusive conceptual framework that could bring their work under a single umbrella to explain dynamic biological processes such as embryonic development. However, with modern technology and conceptual frameworks that bridge multiple scales of biological organisation, we are now in a new era of integration in approaches to developmental biology [ 12 ]. Similar technological advances in the field of metabolism have given rise to the separate field of metabolomics.…”

Section: Introductionmentioning

confidence: 99%

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Gastruloids — a minimalistic model to study complex developmental metabolism

Dingare,

Steventon

2023

Emerging Topics in Life Sciences

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Metabolic networks are well placed to orchestrate the coordination of multiple cellular processes associated with embryonic development such as cell growth, proliferation, differentiation and cell movement. Here, we discuss the advantages that gastruloids, aggregates of mammalian embryonic stem cells that self-assemble a rudimentary body plan, have for uncovering the instructive role of metabolic pathways play in directing developmental processes. We emphasise the importance of using such reductionist systems to link specific pathways to defined events of early mammalian development and their utility for obtaining enough material for metabolomic studies. Finally, we review the ways in which the basic gastruloid protocol can be adapted to obtain specific models of embryonic cell types, tissues and regions. Together, we propose that gastruloids are an ideal system to rapidly uncover new mechanistic links between developmental signalling pathways and metabolic networks, which can then inform precise in vivo studies to confirm their function in the embryo.

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Section: Why Gastruloids?mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Gastruloids — a minimalistic model to study complex developmental metabolism

Dingare,

Steventon

2023

Emerging Topics in Life Sciences

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“…The delayed contribution of heterochronic grafts of tissue from older to younger embryos relative to stage-matched grafts ( Iimura and Pourquié, 2006 ; Tam and Tan, 1992 ) suggests a degree of intrinsic control over axis contribution timing, but the extent to which this is true remains to be understood. In this article, we exploit the rich toolkit provided by experimental embryology ( Busby et al, 2022 ) in conjunction with next-generation sequencing methods and multiplexed staining to investigate the extent to which axial progenitor gene expression and behaviour are intrinsically or extrinsically regulated.…”

Section: Introductionmentioning

confidence: 99%

Intrinsic and extrinsic cues time somite progenitor contribution to the vertebrate primary body axis

Busby,

Serrano Nájera,

Steventon

2024

eLife

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During embryonic development, the timing of events at the cellular level must be coordinated across multiple length scales to ensure the formation of a well-proportioned body plan. This is clear during somitogenesis, where the progenitors must be allocated to the axis over time whilst maintaining a progenitor population for continued elaboration of the body plan. However, the relative importance of intrinsic and extrinsic signals in timing progenitor addition at the single cell level is not yet understood. Heterochronic grafts from older to younger embryos have suggested a level of intrinsic timing whereby later staged cells contribute to more posterior portions of the axis. To determine the precise step at which cells are delayed, we performed single-cell transcriptomic analysis on heterochronic grafts of somite progenitors in the chicken embryo. This revealed a previously undescribed cell state within which heterochronic grafted cells are stalled. The delayed exit of older cells from this state correlates with expression of posterior Hox genes. Using grafting and explant culture, we find that both Hox gene expression and the migratory capabilities of progenitor populations are intrinsically regulated at the population level. However, by grafting varied sizes of tissue, we find that small heterochronic grafts disperse more readily and contribute to more anterior portions of the body axis while still maintaining Hox gene expression. This enhanced dispersion is not replicated in explant culture, suggesting that it is a consequence of interaction between host and donor tissue and thus extrinsic to the donor tissue. Therefore, we demonstrate that the timing of cell dispersion and resulting axis contribution is impacted by a combination of both intrinsic and extrinsic cues.

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“…The delayed contribution of heterochronic grafts of tissue from older to younger embryos relative to stage-matched grafts (Iimura and Pourquie, 2006;Tam and Tan, 1992) suggests a degree of intrinsic control over axis contribution timing, but the extent to which this is true remains to be understood. In this paper, we exploit the rich toolkit provided by experimental embryology (Busby et al, 2022) in conjunction with next-generation sequencing methods and multiplexed staining to investigate the extent to which axial progenitor gene expression and behaviour are intrinsically or extrinsically regulated.…”

Section: Introductionmentioning

confidence: 99%

A population intrinsic timer controlsHoxgene expression and cell dispersion during progenitor addition to the body axis

Busby

Nájera

Steventon

2023

Preprint

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During embryonic development, the timing of events at the cellular level must be coordinated across multiple length scales to ensure the formation of a well-proportioned body plan. This is clear during somitogenesis, where the progenitors must be allocated to the axis over time whilst maintaining a progenitor population for continued elaboration of the body plan. However, the relative importance of intrinsic and extrinsic signals in timing progenitor addition at the single cell level is not yet understood. Heterochronic grafts from older to younger embryos have suggested a level of intrinsic timing whereby later staged cells contribute to more posterior portions of the axis. To determine the precise step at which cells are delayed, we performed single-cell transcriptomic analysis on heterochronic grafts of somite progenitors in the chicken embryo. This revealed a previously undescribed cell state within which heterochronic grafted cells are stalled, post-ingression through the primitive streak. The delayed exit of older cells from this state correlates with expression of posterior Hox genes. Using grafting and explant culture, we find that both Hox gene expression and the migratory capabilities of progenitor populations are intrinsically regulated at the population level. Therefore, we demonstrate that cell dispersion is controlled by a population intrinsic timer to control progenitor addition to the presomitic mesoderm.

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Quantitative Experimental Embryology: A Modern Classical Approach

Cited by 3 publications

References 74 publications

Gastruloids — a minimalistic model to study complex developmental metabolism

Gastruloids — a minimalistic model to study complex developmental metabolism

Intrinsic and extrinsic cues time somite progenitor contribution to the vertebrate primary body axis

A population intrinsic timer controlsHoxgene expression and cell dispersion during progenitor addition to the body axis

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