A morphogenetic wave in the chick embryo lateral mesoderm generates mesenchymal-epithelial transition through a 3D-rosette intermediate

Asleh, Manar Abboud; Zaher, Mira; Asleh, Jad; Jadon, Julian; Shaulov, Lihi; Yelin, Ronit; Schultheiss, Thomas M.

doi:10.1016/j.devcel.2023.03.017

Cited by 11 publications

(9 citation statements)

References 63 publications

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“…The LPM then undergoes a further MET and dorsoventral subdivision resulting in two distinct epithelial monolayers. This process begins with sheets of transient LPM mesenchyme undergoing a wave of epithelization along the anterior to posterior axis of the embryo (Abboud Asleh et al, 2023). Initially, the ectoderm and endoderm secrete Fibronectin and Laminin to establish basement membranes that allow the LPM mesenchymal cells to become polarized (Abboud Asleh et al, 2023; Gros & Tabin, 2014).…”

Section: Lpm Formation and Metmentioning

confidence: 99%

“…This process begins with sheets of transient LPM mesenchyme undergoing a wave of epithelization along the anterior to posterior axis of the embryo (Abboud Asleh et al, 2023). Initially, the ectoderm and endoderm secrete Fibronectin and Laminin to establish basement membranes that allow the LPM mesenchymal cells to become polarized (Abboud Asleh et al, 2023; Gros & Tabin, 2014). During the process of epithelialization, the LPM mesenchyme arranges in 3D rosettes, which in turn rearrange their internal junctions into opposing sheets of epithelium (Abboud Asleh et al, 2023).…”

Section: Lpm Formation and Metmentioning

confidence: 99%

“…Initially, the ectoderm and endoderm secrete Fibronectin and Laminin to establish basement membranes that allow the LPM mesenchymal cells to become polarized (Abboud Asleh et al, 2023; Gros & Tabin, 2014). During the process of epithelialization, the LPM mesenchyme arranges in 3D rosettes, which in turn rearrange their internal junctions into opposing sheets of epithelium (Abboud Asleh et al, 2023). Through this processes, the LPM undergoes progressive segmentation into the somatic and splanchnic LPM, and produces the embryonic coelom (Funayama, Sato, Matsumoto, Ogura, & Takahashi, 1999).…”

Section: Lpm Formation and Metmentioning

confidence: 99%

“…The transient somatic LPM epithelia displays a columnar morphology with mesoepithelial characteristics. For example, while these cells contain polarized basement and apical membranes distinguished by laminin and F‐actin, respectively (Abboud Asleh et al, 2023; Gros & Tabin, 2014), they do not express typical E‐cadherin cell–cell adhesion molecules, which instead are restricted to epithelial cells of the ectoderm (not including the neural tube) and endoderm (Newton et al, 2022). Instead, the columnar epithelia possess basal vimentin and abundant N‐cadherin (Gros & Tabin, 2014; Newton et al, 2022) suggesting the somatic LPM may not fully transition to an epithelial cell fate, prior to their subsequent re‐EMT.…”

Section: Limb Field Specification and Emtmentioning

confidence: 99%

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Resolving the mechanisms underlying epithelial‐to‐mesenchymal transition of the lateral plate mesoderm

Newton

2023

Genesis

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SummaryFormation of the vertebrate limb buds begins with a localized epithelial‐to‐mesenchymal transition (EMT) of the somatic lateral plate mesoderm (LPM). While the processes that drive proliferation and outgrowth of the limb mesenchyme are well established, the fundamental mechanisms that precede this process and initiate EMT are less understood. In this review, we outline putative drivers of EMT of the LPM, drawing from analyses across a range of vertebrates and developmental models. We detail the expression patterns of key EMT transcriptional regulators in the somatic LPM of the presumptive limb fields, and their potential role in producing a mesenchymal cell fate. These include a putative cooperative role between the EMT inducers PRRX1 and TWIST1, supported by evidence in zebrafish and chicken models but unconfirmed data from mice. As such, additional functional data are required to definitively determine the mechanisms that initiate and drive EMT of the somatic LPM, a critical transition preceding formation of the limb bud mesenchyme.

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Section: Lpm Formation and Metmentioning

confidence: 99%

Section: Lpm Formation and Metmentioning

confidence: 99%

Section: Lpm Formation and Metmentioning

confidence: 99%

Section: Limb Field Specification and Emtmentioning

confidence: 99%

See 2 more Smart Citations

Resolving the mechanisms underlying epithelial‐to‐mesenchymal transition of the lateral plate mesoderm

Newton

2023

Genesis

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“…The limbs arise through a series of embryological events that begin in the LPM. During embryogenesis, the undifferentiated LPM undergoes dorsoventral subdivision along the anteroposterior axis of the embryo into the somatic and splanchnic LPM cell layers, producing the embryonic coelom 10,11 . In the first stages of limb development, colinear activation of HOX genes along the anterior-posterior axis define the presumptive fore and hindlimb fields within the established somatic LPM 12–15 .…”

Section: Introductionmentioning

confidence: 99%

Heterotopic reduction of forelimb progenitors underpins development of the vestigial emu wing; implications for vertebrate limb evolution

Newton

Williams

Phipson

et al. 2022

Preprint

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Between tetrapods the limbs have undergone considerable remodelling to achieve unique adaptive behaviours. The forelimb is an ideal model for exploring the molecular basis of adaptive limb development, as it shows remarkable structural variation and is accessible for experimental manipulation. Of the most striking alterations to limb shape is the evolution of powered flight in birds. However, subsequently the flightless ratites (Paleognathae) have further evolved multiple instances of wing reductions, each utilizing distinct molecular mechanisms and displaying heterochrony with flighted birds (Neoaves). The emu has evolved a greatly reduced wing, consisted of a single digit. Thus, the emu is an excellent model to comparatively determine the cellular and molecular basis of wing heterochrony. We utilize comparative single cell transcriptomics of the developing forelimb field in the emu and chicken, to identify the source of the emus reduced wing. This was observed to occur via reduced specification and commitment of lateral plate mesoderm limb progenitor cells, which was accompanied by differential gene expression, persisting during limb initiation and outgrowth. These data suggest a progenitor allocation model, whereby altered limb morphologies may be achieved through altered commitment of precursor cells which act as an underlying template for pre- and post-patterning mechanisms.

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Different Biomechanical Cell Behaviors in an Epithelium Drive Collective Epithelial Cell Extrusion

Balasubramaniam,

Jain,

Dang

et al. 2024

Advanced Science

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In vertebrates, many organs, such as the kidney and the mammary gland form ductal structures based on the folding of epithelial sheets. The development of these organs relies on coordinated sorting of different cell lineages in both time and space, through mechanisms that remain largely unclear. Tissues are composed of several cell types with distinct biomechanical properties, particularly at cell‐cell and cell‐substrate boundaries. One hypothesis is that adjacent epithelial layers work in a coordinated manner to shape the tissue. Using in vitro experiments on model epithelial cells, differential expression of atypical Protein Kinase C iota (aPKCi), a key junctional polarity protein, is shown to reinforce cell epithelialization and trigger sorting by tuning cell mechanical properties at the tissue level. In a broader perspective, it is shown that in a heterogeneous epithelial monolayer, in which cell sorting occurs, forces arising from epithelial cell growth under confinement by surrounding cells with different biomechanical properties are sufficient to promote collective cell extrusion and generate emerging 3D organization related to spheroids and buds. Overall, this research sheds light on the role of aPKCi and the biomechanical interplay between distinct epithelial cell lineages in shaping tissue organization, providing insights into the understanding of tissue and organ development.

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A morphogenetic wave in the chick embryo lateral mesoderm generates mesenchymal-epithelial transition through a 3D-rosette intermediate

Cited by 11 publications

References 63 publications

Resolving the mechanisms underlying epithelial‐to‐mesenchymal transition of the lateral plate mesoderm

Resolving the mechanisms underlying epithelial‐to‐mesenchymal transition of the lateral plate mesoderm

Heterotopic reduction of forelimb progenitors underpins development of the vestigial emu wing; implications for vertebrate limb evolution

Different Biomechanical Cell Behaviors in an Epithelium Drive Collective Epithelial Cell Extrusion

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