Specific expression of a TRIM-containing factor in ectoderm cells affects the skeletal morphogenetic program of the sea urchin embryo

Cavalieri, Vincenzo; Guarcello, Rosa; Spinelli, Giovanni

doi:10.1242/dev.066480

Cited by 21 publications

(31 citation statements)

References 66 publications

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“…This provides evidence of cross-talk between these two pathways, which function synergistically in other systems (Tomanek et al, 2010). Cavalieri et al (Cavalieri et al, 2011) showed that the tripartite motif-containing protein STRIM1 regulates the expression of fgfa in the ectoderm, but not in PMCs, highlighting the separate control of fgfa expression in these two tissues. STRIM1 also regulates otp in the ectoderm whereas VEGF3 and FGFA do not, suggesting that multiple pathways regulate gene expression in the ectoderm overlying the VLCs.…”

Section: Research Article Growth Factors In Cell Guidancementioning

confidence: 93%

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Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation

2013

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Growth factor signaling pathways provide essential cues to mesoderm cells during gastrulation in many metazoans. Recent studies have implicated the VEGF and FGF pathways in providing guidance and differentiation cues to primary mesenchyme cells (PMCs) during sea urchin gastrulation, although the relative contributions of these pathways and the cell behaviors they regulate are not fully understood. Here, we show that FGF and VEGF ligands are expressed in distinct domains in the embryonic ectoderm of Lytechinus variegatus. We find that PMC guidance is specifically disrupted in Lv-vegf3 morphants and these embryos fail to form skeletal elements. By contrast, PMC migration is unaffected in Lv-fgfa morphants, and well-patterned but shortened skeletal elements form. We use a VEGFR inhibitor, axitinib, to show that VEGF signaling is essential not only for the initial phase of PMC migration (subequatorial ring formation), but also for the second phase (migration towards the animal pole). VEGF signaling is not required, however, for PMC fusion. Inhibition of VEGF signaling after the completion of PMC migration causes significant defects in skeletogenesis, selectively blocking the elongation of skeletal rods that support the larval arms, but not rods that form in the dorsal region of the embryo. Nanostring nCounter analysis of ∼100 genes in the PMC gene regulatory network shows a decrease in the expression of many genes with proven or predicted roles in biomineralization in vegf3 morphants. Our studies lead to a better understanding of the roles played by growth factors in sea urchin gastrulation and skeletogenesis.

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Section: Research Article Growth Factors In Cell Guidancementioning

confidence: 93%

“…We also examined two other genes expressed in the ectoderm that have been shown to play a role in regulating skeletogenesis: otp (Di Bernardo et al, 1999;Cavalieri et al, 2003) and pax2/5/8 (Cavalieri et al, 2011). Lv-pax2/5/8 expression was slightly downregulated in Lv-vegf3 morphants (supplementary material Fig.…”

Section: Research Articlementioning

confidence: 99%

Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation

2013

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“…2J). Thus, the candidate LOF effects are distinct from those produced by knockdown of VEGF/R, Wnt5a, Otp, Pax2/5/8 or FGF, because each of the latter LOFs blocks biomineralization, resulting in larvae that lack skeletons entirely (Di Bernardo et al, 1999;Cavalieri et al, 2003;Duloquin et al, 2007;Rottinger et al, 2008;Cavalieri et al, 2011;AdomakoAnkomah and Ettensohn, 2013;McIntyre et al, 2013). Furthermore, each candidate LOF resulted in perturbed PMC organization at the LG stage (Fig.…”

Section: Sb and Nickel Have Opposite Effects On Ectodermal Specificatmentioning

confidence: 99%

“…These include the tripartite motif-containing protein Strim1, the transcription factors Pax2/5/8 and Otp, the signaling ligands FGF, Wnt5a, VEGF and the TGF-β ligand Univin. These genes are expressed in the ectoderm directly adjacent to sites of active biomineralization and with the exception of Univin, which is specifically required for patterning of the secondary skeletal elements (Piacentino et al, 2015), their loss of function (LOF) blocks skeletogenesis, indicating a role in regulating biomineralization (Di Bernardo et al, 1999;Cavalieri et al, 2003;Duloquin et al, 2007;Rottinger et al, 2008;Cavalieri et al, 2011;Adomako-Ankomah and Ettensohn, 2013). Gene products that specifically regulate primary PMC positioning but not biomineralization, i.e.…”

Section: Introductionmentioning

confidence: 99%

RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins

et al. 2016

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The sea urchin larval skeleton offers a simple model for formation of developmental patterns. The calcium carbonate skeleton is secreted by primary mesenchyme cells (PMCs) in response to largely unknown patterning cues expressed by the ectoderm. To discover novel ectodermal cues, we performed an unbiased RNA-Seq-based screen and functionally tested candidates; we thereby identified several novel skeletal patterning cues. Among these, we show that SLC26a2/7 is a ventrally expressed sulfate transporter that promotes a ventral accumulation of sulfated proteoglycans, which is required for ventral PMC positioning and skeletal patterning. We show that the effects of SLC perturbation are mimicked by manipulation of either external sulfate levels or proteoglycan sulfation. These results identify novel skeletal patterning genes and demonstrate that ventral proteoglycan sulfation serves as a positional cue for sea urchin skeletal patterning.

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“…In the intervening time, subpopulations of primary mesenchyme cells migrate within the blastocoel cavity guided by signals emitted by these regions, settle into two ventrolateral aggregates adjacent to the ectoderm thickenings, and eventually mineralize two skeletal primordia [19][20][21]. At the end of gastrulation, the opening of the larval mouth occurs by bending of the archenteron towards the ventral ectoderm and subsequent fusion of the two epithelia.…”

Section: Introductionmentioning

confidence: 99%

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

Cavalieri

Spinelli

2015

Symmetry

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Abstract:The mechanisms imposing the Dorsal/Ventral (DV) polarity of the early sea urchin embryo consist of a combination of inherited maternal information and inductive interactions among blastomeres. Old and recent studies suggest that a key molecular landmark of DV polarization is the expression of nodal on the future ventral side, in apparent contrast with other metazoan embryos, where nodal is expressed dorsally. A subtle maternally-inherited redox anisotropy, plus some maternal factors such as SoxB1, Univin, and p38-MAPK have been identified as inputs driving the spatially asymmetric transcription of nodal. However, all the mentioned factors are broadly distributed in the embryo as early as nodal transcription occurs, suggesting that repression of the gene in non-ventral territories depends upon negative regulators. Among these, the Hbox12 homeodomain-containing repressor is expressed by prospective dorsal cells, where it acts as a dorsal-specific negative modulator of the p38-MAPK activity. This review provides an overview of the molecular mechanisms governing the establishment of DV polarity in sea urchins, focusing on events taking place in the early embryo. Altogether, these findings provide a framework for future studies aimed to unravel the inceptive mechanisms involved in the DV symmetry breaking.

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Specific expression of a TRIM-containing factor in ectoderm cells affects the skeletal morphogenetic program of the sea urchin embryo

Cited by 21 publications

References 66 publications

Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation

Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation

RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

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