Pattern and process during sea urchin gut morphogenesis: The regulatory landscape

Annunziata, Rossella; Perillo, Margherita; Andrikou, Carmen; Cole, Alison G.; Martinez, Pedro; Arnone, Maria Ina

doi:10.1002/dvg.22738

Cited by 67 publications

(54 citation statements)

References 120 publications

(113 reference statements)

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“…SpGataE ( Lee and Davidson, 2004) Howard-Ashby et al, 2006), and SpPtf1a (Annunziata et al, 2013b), was not significantly affected in Xlox knockdown larvae. Finally, this analysis did not reveal any significantly affected signaling molecule-encoding gene, thus leaving unresolved the mechanism mediating Xlox function in the activation of stomach differentiation genes and introducing new possible hypotheses, such as Xlox requirement in the control of posttranslational events, something not testable with the approaches followed so far.…”

Section: A Differential Transcriptomic Analysis For Xlox Morphantsmentioning

confidence: 82%

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

Annunziata

Arnone

2014

Development

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The anteroposterior patterning of the embryonic gut represents one of the most intriguing biological processes in development. A dynamic control of gene transcription regulation and cell movement is perfectly orchestrated to shape a functional gut in distinct specialized parts. Two ParaHox genes, Xlox and Cdx, play key roles in vertebrate and sea urchin gut patterning through molecular mechanisms that are still mostly unclear. Here, we have combined functional analysis methodologies with high-resolution imaging and RNA-seq to investigate Xlox and Cdx regulation and function. We reveal part of the regulatory machinery responsible for the onset of Xlox and Cdx transcription, uncover a Wnt10 signal that mediates Xlox repression in the intestinal cells, and provide evidence of Xlox-and Cdx-mediated control of stomach and intestine differentiation, respectively. Our findings offer a novel mechanistic explanation of how the control of transcription is linked to cell differentiation and morphogenesis for the development of a perfectly organized biological system such as the sea urchin larval gut.

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Section: A Differential Transcriptomic Analysis For Xlox Morphantsmentioning

confidence: 82%

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

Annunziata

Arnone

2014

Development

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“…The digestive tract ends with an anal sphincter. All these sphincters are endodermally derived and contain myosin heavy chain (Annunziata et al, 2013; Burke, 1981; Wessel et al, 1990). These constrictions give the overall gut structure an hourglass-like shape in the larva.…”

Section: Resultsmentioning

confidence: 99%

“…The endogenous alkaline phosphatase was used to assay for differentiated endoderm of the larvae (Annunziata et al, 2013; Drawbridge, 2003; Hinman and Degnan, 1998; Kumano and Nishida, 1998; Nishida and Kumano, 1997; Whittaker, 1990). Three day old larvae were fixed in MOPS-paraformaldehyde based fixative (4% paraformaldehyde, 100 mM MOPS pH 7.0, 2 mM MgSO 4 , 1 mM EGTA, and 0.8 M NaCl) for 10 min at room temperature.…”

Section: Methodsmentioning

confidence: 99%

microRNAs regulate β-catenin of the Wnt signaling pathway in early sea urchin development

Stepicheva

Nigam

Siddam

et al. 2015

Developmental Biology

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Development of complex multicellular organisms requires careful regulation at both transcriptional and post-transcriptional levels. Post-transcriptional gene regulation is in part mediated by a class of non-coding RNAs of 21–25 nucleotides in length known as microRNAs (miRNAs). β-catenin, regulated by the canonical Wnt signaling pathway, has a highly evolutionarily conserved function in patterning early metazoan embryos, in forming the Anterior-Posterior axis, and in establishing the endomesoderm. Using reporter constructs and site-directed mutagenesis, we identified at least three miRNA binding sites within the 3’ untranslated region (3’UTR) of the sea urchin β-catenin. Further, blocking these three miRNA binding sites within the β-catenin 3’UTR to prevent regulation of endogenous β-catenin by miRNAs resulted in a minor increase in β-catenin protein accumulation that is sufficient to induce aberrant gut morphology and circumesophageal musculature. These phenotypes are likely the result of increased transcript levels of Wnt responsive endomesodermal regulatory genes. This study demonstrates the importance of miRNA regulation of β-catenin in early development.

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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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Pattern and process during sea urchin gut morphogenesis: The regulatory landscape

Cited by 67 publications

References 120 publications

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

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

microRNAs regulate β-catenin of the Wnt signaling pathway in early sea urchin development

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

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