A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin

Annunziata, Rossella; Arnone, Maria Ina

doi:10.1242/dev.105775

Cited by 37 publications

(40 citation statements)

References 64 publications

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“…Lox morphants are seen to have a disorganized musculature in the foregut region and partial digestive function. Along with Parahox transcription factor, Cdx, circuitry of a GRN for gut regionalization is being uncovered (Annunziata & Arnone, 2014; Annunziata et al, 2014; Cole et al, 2009). What is necessary is to connect those known upstream regulators to the explicit cell behaviors they control.…”

Section: Discussionmentioning

confidence: 99%

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

Martik¹,

McClay²

2017

Mechanisms of Development

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Background Gastrulation is a complex orchestration of movements by cells that are specified early in development. Until now, classical convergent extension was considered to be the main contributor to sea urchin archenteron extension, and the relative contributions of cell divisions were unknown. Active migration of cells along the axis of extension was also not considered as a major factor in invagination. Results Cell transplantations plus live imaging were used to examine endoderm cell morphogenesis during gastrulation at high-resolution in the optically clear sea urchin embryo. The invagination sequence was imaged throughout gastrulation. One of the eight macromeres was replaced by a fluorescently labeled macromere at the 32 cell stage. At gastrulation those patches of fluorescent endoderm cell progeny initially about 4 cells wide, released a column of cells about 2 cells wide early in gastrulation and then often this column narrowed to one cell wide by the end of archenteron lengthening. The primary movement of the column of cells was in the direction of elongation of the archenteron with the narrowing (convergence) occurring as one of the two cells moved ahead of its neighbor. As the column narrowed, the labeled endoderm cells generally remained as a contiguous population of cells, rarely separated by intrusion of a lateral unlabeled cell. This longitudinal cell migration mechanism was assessed quantitatively and accounted for almost 90% of the elongation process. Much of the extension was the contribution of Veg2 endoderm with a minor contribution late in gastrulation by Veg1 endoderm cells. We also analyzed the contribution of cell divisions to elongation. Endoderm cells in Lytechinus variagatus were determined to go through approximately one cell doubling during gastrulation. That doubling occurs without a net increase in cell mass, but the question remained as to whether oriented divisions might contribute to archenteron elongation. We learned that indeed there was a biased orientation of cell divisions along the plane of archenteron elongation, but when the impact of that bias was analyzed quantitatively, it contributed a maximum 15% to the total elongation of the gut. Conclusions The major driver of archenteron elongation in the sea urchin, Lytechinus variagatus, is directed movement of Veg2 endoderm cells as a narrowing column along the plane of elongation. The narrowing occurs as cells in the column converge as they migrate, so that the combination of migration and the angular convergence provide the major component of the lengthening. A minor contributor to elongation is oriented cell divisions that contribute to the lengthening but no more than about 15%.

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Section: Discussionmentioning

confidence: 99%

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

Martik¹,

McClay²

2017

Mechanisms of Development

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“…underlying development (27)(28)(29)(30). It has been shown that FGF signalling is 6 necessary for guiding skeletogenic mesenchymal cell migration and formation 7 of the embryonic skeleton in the sea urchin Paracentrotus lividus (31).…”

Section: Introductionmentioning

confidence: 99%

FGF signalling plays similar roles in development and regeneration of the skeleton in the brittle starAmphiura filiformis

Czarkwiani

Dylus

Carballo

et al. 2019

Preprint

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1 2 Regeneration is an adult developmental process considered to be an 3 epiphenomenon of embryonic development. Although several studies have 4shown that various embryonic genes are expressed during regeneration, 5 there have been no large-scale, direct and functional comparative studies 6 between the development and regeneration of a specific structure in one 7animal. Here, we use the brittle star Amphiura filiformis to characterise the 8 role of the FGF signalling pathway during skeletal development and 9 regeneration. In both processes, we find the ligands expressed in ectodermal 10

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“…Previous gene regulatory studies reveal that endoderm specification is well underway in 24‐h embryos (Peter & Davidson ) and that tripartite gut subdivision occurs past the 24‐h stage (Arenas‐Mena et al . ; Annunziata & Arnone ). When H2A.Z inhibition is triggered in 24‐h embryos, endoderm formation and gastrulation proceeds normally, but tripartite gut subdivision is absent (Fig.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional and post‐transcriptional regulation of histone variant H2A.Z during sea urchin development

et al. 2016

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Histone variant H2A.Z promotes chromatin accessibility at transcriptional regulatory elements and is developmentally regulated in metazoans. We characterize the transcriptional and post-transcriptional regulation of H2A.Z in the purple sea urchin Strongylocentrotus purpuratus. H2A.Z depletion by antisense translation-blocking morpholino oligonucleotides during early development causes developmental collapse, in agreement with its previously demonstrated general role in transcriptional multipotency. During H2A.Z peak expression in 24-h embryos, endogenous H2A.Z 3' UTR sequences stabilize GFP mRNAs relative to those with SV40 3' UTR sequences, although the 3' UTR of H2A.Z does not determine the spatial distribution of H2A.Z transcripts during embryonic and postembryonic development. We elaborated an H2A.Z::GFP BAC reporter that reproduces embryonic H2A.Z expression. Genome-wide chromatin accessibility analysis using ATAC-seq revealed a cis-regulatory module (CRM) that, when deleted, causes a significant decline of the H2A.Z reporter expression. In addition, the mutation of a Sox transcription factor binding site motif and, more strongly, of a Myb motif cause significant decline of reporter gene expression. Our results suggest that an undetermined Myb-family transcription factor controls the transcriptional regulation of H2A.Z.

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A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin

Cited by 37 publications

References 64 publications

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

FGF signalling plays similar roles in development and regeneration of the skeleton in the brittle starAmphiura filiformis

Transcriptional and post‐transcriptional regulation of histone variant H2A.Z during sea urchin development

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