Impairing Otp homeodomain function in oral ectoderm cells affects skeletogenesis in sea urchin embryos

Cavalieri, Vincenzo; Spinelli, Giovanni; Bernardo, Maria Di

doi:10.1016/s0012-1606(03)00317-8

Cited by 38 publications

(39 citation statements)

References 43 publications

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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%

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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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Section: Sb and Nickel Have Opposite Effects On Ectodermal Specificatmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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“…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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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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“…6F,L and data not shown, n>70 for each marker) three transcription factors required for PMC specification (Croce et al, 2001b;Ettensohn et al, 2003;Kurokawa et al, 1999), were unaffected by FGFA morpholinos, suggesting that FGFA signaling participates in regulating PMC differentiation, although not their specification. We then examined the expression of gene markers in the ectoderm, such as otp (Cavalieri et al, 2003; Di 359 RESEARCH ARTICLE FGF signaling in the sea urchin embryo Bernardo et al, 1999), fgfA, pax2/5/8 and pea3, in the FGF morphants. Expression of the homeobox gene otp, which has been implicated previously in skeletogenesis, was largely unaffected (data not shown, n>40) following downregulation of FGFA.…”

Section: Expression Of Fgfa In the Vegetal Hemisphere Is Required Formentioning

confidence: 99%

FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development

et al. 2008

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The sea urchin embryo is emerging as an attractive model to study morphogenetic processes such as directed migration of mesenchyme cells and cell sheet invagination, but surprisingly, few of the genes regulating these processes have yet been characterized. We present evidence that FGFA, the first FGF family member characterized in the sea urchin, regulates directed migration of mesenchyme cells, morphogenesis of the skeleton and gastrulation during early development. We found that at blastula stages, FGFA and a novel putative FGF receptor are expressed in a pattern that prefigures morphogenesis of the skeletogenic mesoderm and that suggests that FGFA is one of the elusive signals that guide migration of primary mesenchyme cells (PMCs). We first show that fgfA expression is correlated with abnormal migration and patterning of the PMCs following treatments that perturb specification of the ectoderm along the oral-aboral and animal-vegetal axes. Specification of the ectoderm initiated by Nodal is required to restrict fgfA to the lateral ectoderm, and in the absence of Nodal, fgfA is expressed ectopically throughout most of the ectoderm. Inhibition of either FGFA, FGFR1 or FGFR2 function severely affects morphogenesis of the skeleton. Furthermore,inhibition of FGFA and FGFR1 signaling dramatically delays invagination of the archenteron, prevents regionalization of the gut and abrogates formation of the stomodeum. We identified several genes acting downstream of fgfAin these processes, including the transcription factors pea3 and pax2/5/8 and the signaling molecule sprouty in the lateral ectoderm and SM30 and SM50 in the primary mesenchyme cells. This study identifies the FGF signaling pathway as an essential regulator of gastrulation and directed cell migration in the sea urchin embryo and as a key player in the gene regulatory network directing morphogenesis of the skeleton.

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Impairing Otp homeodomain function in oral ectoderm cells affects skeletogenesis in sea urchin embryos

Cited by 38 publications

References 43 publications

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

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

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

FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development

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