Logics and properties of a genetic regulatory program that drives embryonic muscle development in an echinoderm

Andrikou, Carmen; Pai, Chih-Yu; Su, Yi-Hsien; Arnone, Maria Ina

doi:10.7554/elife.07343

Cited by 48 publications

(45 citation statements)

References 91 publications

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“…In all experiments, as a negative control, embryos were injected with 100 µM of the standard control MASO (oligo end modified with 3′-Carboxyfluorescein, control-fluo MASO, Gene Tools) at equal or greater concentration and compared side-by-side with uninjected and MASO embryos. As for previous experiments (Andrikou et al, 2015) no delay of development or abnormal morphology was observed at any stage in the control-fluo MASO injected embryos (Figure S1). For mRNA injection, Capped synthetic mRNA was made with T3 RNA polymerase using mMESSAGE mMACHINE Kit (Ambion, Austin, USA), subsequently treating the RNA product with DNase I to remove DNA template.…”

Section: Methodssupporting

confidence: 84%

“…Moreover, the same antibody, used in immunohistochemistry assays, identifies the phosphorylated protein in all nuclei of the early blastula (Fig. 4E), while it appears confined at the tip of archenteron of the early gastrula (Andrikou et al, 2015), a region in which the activated form of ERK kinase is strongly expressed (Fernandez-Serra et al, 2004; Rottinger et al, 2004). …”

Section: Resultsmentioning

confidence: 96%

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An Elk transcription factor is required for Runx-dependent survival signaling in the sea urchin embryo

Rizzo

Coffman

Arnone

2016

Developmental Biology

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Elk proteins are Ets family transcription factors that regulate cell proliferation, survival, and differentiation in response to ERK (extracellular-signal regulated kinase)-mediated phosphorylation. Here we report the embryonic expression and function of Sp-Elk, the single Elk gene of the sea urchin Strongylocentrotus purpuratus. Sp-Elk is zygotically expressed throughout the embryo beginning at late cleavage stage, with peak expression occurring at blastula stage. Morpholino antisense-mediated knockdown of Sp-Elk causes blastula-stage developmental arrest and embryo disintegration due to apoptosis, a phenotype that is rescued by wild-type Elk mRNA. Development is also rescued by Elk mRNA encoding a serine to aspartic acid substitution (S402D) that mimics ERK-mediated phosphorylation of a conserved site that enhances DNA binding, but not by Elk mRNA encoding an alanine substitution at the same site (S402A). This demonstrates both that the apoptotic phenotype of the morphants is specifically caused by Elk depletion, and that phosphorylation of serine 402 of Sp-Elk is critical for its anti-apoptotic function. Knockdown of Sp-Elk results in under-expression of several regulatory genes involved in cell fate specification, cell cycle control, and survival signaling, including the transcriptional regulator Sp-Runt-1 and its target Sp-PKC1, both of which were shown previously to be required for cell survival during embryogenesis. Both Sp-Runt-1 and Sp-PKC1 have sequences upstream of their transcription start sites that specifically bind Sp-Elk. These results indicate that Sp-Elk is the signal-dependent activator of a feed-forward gene regulatory circuit, consisting also of Sp-Runt-1 and Sp-PKC1, which actively suppresses apoptosis in the early embryo.

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Section: Methodssupporting

confidence: 84%

Section: Resultsmentioning

confidence: 96%

An Elk transcription factor is required for Runx-dependent survival signaling in the sea urchin embryo

Rizzo

Coffman

Arnone

2016

Developmental Biology

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“…The data presented on O-A polarity in the NSM of Et suggest that multiple regulatory domains unfold at and around the tip of the archenteron as gastrulation proceeds, as is also the case in euechinoids (98), and that these embryonic domains have diverged markedly since the divergence of the two modern echinoid clades.…”

Section: Divergent Regulatory Linkages In the Evolution Of Echinoid Ementioning

confidence: 97%

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

Proc. Natl. Acad. Sci. U.S.A.

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Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral-aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirectdeveloping euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell typebiased alterations.gene regulatory network | echinoderms | sea urchin embryogenesis | embryonic axis specification | echinoids

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“…The set of Pax, bHLH, Six, Eya, Dach, and MADS transcription factors involved in myogenesis is conserved throughout Bilateria. However, the hierarchy of gene interactions has been reshuffled in some bilaterian groups, and some key myogenic factors were lost in some lineages during evolution, such as Pax3/7 in sea urchins (Andrikou et al, 2015). The general consensus is that MRFs play a crucial role in bilaterian muscle specification and differentiation (reviewed in Bentzinger et al, 2012; Andrikou and Arnone, 2015).…”

Section: Molecular Characterization Of Muscles In Cnidariansmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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The ability to perform muscle contractions is one of the most important and distinctive features of eumetazoans. As the sister group to bilaterians, cnidarians (sea anemones, corals, jellyfish, and hydroids) hold an informative phylogenetic position for understanding muscle evolution. Here, we review current knowledge on muscle function, diversity, development, regeneration and evolution in cnidarians. Cnidarian muscles are involved in various activities, such as feeding, escape, locomotion and defense, in close association with the nervous system. This variety is reflected in the large diversity of muscle organizations found in Cnidaria. Smooth epithelial muscle is thought to be the most common type, and is inferred to be the ancestral muscle type for Cnidaria, while striated muscle fibers and non-epithelial myocytes would have been convergently acquired within Cnidaria. Current knowledge of cnidarian muscle development and its regeneration is limited. While orthologs of myogenic regulatory factors such as MyoD have yet to be found in cnidarian genomes, striated muscle formation potentially involves well-conserved myogenic genes, such as twist and mef2. Although satellite cells have yet to be identified in cnidarians, muscle plasticity (e.g., de- and re-differentiation, fiber repolarization) in a regenerative context and its potential role during regeneration has started to be addressed in a few cnidarian systems. The development of novel tools to study those organisms has created new opportunities to investigate in depth the development and regeneration of cnidarian muscle cells and how they contribute to the regenerative process.

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Logics and properties of a genetic regulatory program that drives embryonic muscle development in an echinoderm

Cited by 48 publications

References 91 publications

An Elk transcription factor is required for Runx-dependent survival signaling in the sea urchin embryo

An Elk transcription factor is required for Runx-dependent survival signaling in the sea urchin embryo

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

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