Branching out: Origins of the sea urchin larval skeleton in development and evolution

McIntyre, Daniel C.; Lyons, Deirdre C.; Martik, Megan L.; McClay, David R.

doi:10.1002/dvg.22756

Cited by 54 publications

(44 citation statements)

References 93 publications

(160 reference statements)

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“…3). This is an important conclusion, which argues against a model in which VEGF signaling is the only or the principle mediator of skeletal patterning in sea urchin embryos, as has been previously suggested (Duloquin et al, 2007;Lyons et al, 2011;Adomako-Ankomah and Ettensohn, 2013;McIntyre et al, 2014). Late VEGFR inhibition (via axitinib) blocks secondary skeletogenesis, which has been interpreted as reflecting a block to biomineralization (Adomako-Ankomah and Ettensohn, 2013).…”

Section: Discussionmentioning

confidence: 93%

Late Alk4/5/7 signaling is required for anterior skeletal patterning in sea urchin embryos

2015

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Skeletal patterning in the sea urchin embryo requires a conversation between the skeletogenic primary mesenchyme cells (PMCs) and the overlying pattern-dictating ectoderm; however, our understanding of the molecular basis for this process remains incomplete. Here, we show that TGF-β-receptor signaling is required during gastrulation to pattern the anterior skeleton. To block TGF-β signaling, we used SB431542 (SB43), a specific inhibitor of the TGF-β type I receptor Alk4/5/7. Treatment with SB43 during gastrulation blocks anterior PMC positioning and the formation of the anterior skeleton, but does not perturb general ectoderm specification or development. This is the first example of a signaling event required for patterning of a specific part of the skeleton. Alk4/5/7 inhibition does not prevent the formation of a mouth, although SB43-treated plutei display reduced feeding ability, presumably due to the loss of the structural support for the mouth conferred by the anterior skeleton. Both Univin and Nodal are potential ligands for Alk4/5/7; however, Nodal is unilaterally expressed on only the right side, whereas Univin is bilaterally expressed in the ectoderm adjacent to the anterior skeleton during the relevant time period. Our results demonstrate that Univin is both necessary and sufficient for secondary skeletal development in a control background, consistent with the hypothesis that Univin is a relevant Alk4/5/7 ligand for anterior skeletal patterning. Taken together, our data demonstrate that Alk4/5/7 signaling during gastrulation is required to direct PMCs to the oral hood, and suggest that Univin is a relevant ligand for this signaling event.

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Section: Discussionmentioning

confidence: 93%

Late Alk4/5/7 signaling is required for anterior skeletal patterning in sea urchin embryos

2015

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“…Armstrong, Hardin and McClay later used microsurgical transplants to demonstrated that the nickel-mediated patterning defect was specific to the ectoderm and not the PMCs (Armstrong et al, 1993). Subsequent experiments have confirmed and corroborated these results (reviewed by Adomako-Ankomah and Ettensohn, 2014;McIntyre et al, 2014). Throughout their migration, the PMCs extend thin filopodia that contact the ectoderm (Gustafson and Wolpert, 1999;Miller et al, 1995).…”

Section: Introductionmentioning

confidence: 80%

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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“…Most of the proteins in these clusters were linked to eukaryotic translation initiation factor 3 subunit D (Eif3d), neuron navigator Nav1/2/3, kinesin protein KifC3L2, calcium‐activated potassium channel Kncma1, axonemal dynein Axndhc3h, Cadherin4L, several zinc finger proteins (e.g., Z156, Z35), growth factor receptor (Grb2), and transcription factors (e.g., TFIIB/GTF2b, TfIID, SOX, KEN2, GTF3C5, AP‐1, ELT‐2, KAY; Table S13). The presence of several ophiuroid orthologs of sea urchin embryonic development (Vaughn et al., 2012) and the remarkable resemblance in the expression of regulatory genes between both groups (McIntyre, Lyons, Martik, & McClay, 2014) suggest a similar molecular makeup of their major embryonic territories (i.e., skeletogenic, endomesoderm, and ectoderm; Dylus et al., 2016). Within echinoids, 11,814 orthologous clusters were identified as unique for sea urchins, from which 4,167 were shared among M. franciscanus , S. purpuratus, and L. variegatus (Figure 2c).…”

Section: Resultsmentioning

confidence: 99%

Gene expression profiling during the embryo‐to‐larva transition in the giant red sea urchin Mesocentrotus franciscanus

Gaitán‐Espitía

Hofmann

2017

Ecology and Evolution

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In echinoderms, major morphological transitions during early development are attributed to different genetic interactions and changes in global expression patterns that shape the regulatory program for the specification of embryonic territories. In order more thoroughly to understand these biological and molecular processes, we examined the transcriptome structure and expression profiles during the embryo‐to‐larva transition of a keystone species, the giant red sea urchin Mesocentrotus franciscanus. Using a de novo assembly approach, we obtained 176,885 transcripts from which 60,439 (34%) had significant alignments to known proteins. From these transcripts, ~80% were functionally annotated allowing the identification of ~2,600 functional, structural, and regulatory genes involved in developmental process. Analysis of expression profiles between gastrula and pluteus stages of M. franciscanus revealed 791 differentially expressed genes with 251 GO overrepresented terms. For gastrula, up‐regulated GO terms were mainly linked to cell differentiation and signal transduction involved in cell cycle checkpoints. In the pluteus stage, major GO terms were associated with phosphoprotein phosphatase activity, muscle contraction, and olfactory behavior, among others. Our evolutionary comparative analysis revealed that several of these genes and functional pathways are highly conserved among echinoids, holothuroids, and ophiuroids.

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Branching out: Origins of the sea urchin larval skeleton in development and evolution

Cited by 54 publications

References 93 publications

Late Alk4/5/7 signaling is required for anterior skeletal patterning in sea urchin embryos

Late Alk4/5/7 signaling is required for anterior skeletal patterning in sea urchin embryos

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

Gene expression profiling during the embryo‐to‐larva transition in the giant red sea urchin Mesocentrotus franciscanus

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