Regulation of anterior neurectoderm specification and differentiation by BMP signaling in ascidians

Roure, Agnès; Chowdhury, Rafath; Darras, Sébastien

doi:10.1242/dev.201575

Cited by 9 publications

(40 citation statements)

References 54 publications

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“…This suggested they do not arise from these core Islet+ cells, consistent with their more lateral positions as shown previously by TEM (Zeng et al, 2019b). Furthermore, recently published in situ hybridization data showing presumptive Pou4expressing PN precursors surrounding Islet-expressing cells at late tailbud stage (Roure et al, 2022). Indeed, co-electroporation of Islet reporter and PN-or OC-specific reporter plasmids clearly showed PNs and OCs immediately adjacent to, but distinct from, Islet+ cells (Figure 2D,I).…”

Section: Specification Of Pns and Ocs From Cells That Downregulate Foxgsupporting

confidence: 88%

“…intestinalis Type A) whole-larva single-cell RNA sequencing (scRNAseq) data (Cao et al, 2019) for evidence of the cell types described by transmission electron microscopy (TEM) of the papillae (Zeng et al, 2019b). While a cell cluster annotated as "Palp Sensory Cells" (PSCs) appeared enriched for known markers of ACCs like CryBG (KH.S605.3) and KH.C3.516 (Sharma et al, 2019;Shimeld et al, 2005), genes expressed in other papilla cell types were also enriched in this cluster as well, including Sp6/7/8 (KH.C13.22) (Liu and Satou, 2019;Wagner et al, 2014) and Pou4 (KH.C2.42) (Roure et al, 2022;Sakamoto et al, 2022). Re-analysis and reclustering of these data revealed novel potential markers for these different cell types within the cluster (Supplemental Figure 1A-C, Supplemental Table 1).…”

Section: Identification Of Novel Markers and Reporters For Specific C...mentioning

confidence: 99%

“…Might PNs and OCs be arising from the cells in between (and flanking) the three spots that downregulate Foxg (via repression by Sp6/7/8) and do not go on to express Islet (Figure 6A) (Liu and Satou, 2019;Roure et al, 2022;Wagner et al, 2014)? To test this, we used the MEK (MAPK kinase) inhibitor U0126 to expand Islet expression as previously done (Figure 6A) (Wagner et al, 2014).…”

Section: Specification Of Pns and Ocs From Cells That Downregulate Foxgmentioning

confidence: 99%

“…Previous papilla-specific TALEN knockout of the neuronal transcription factor-encoding gene Pou4 successfully eliminated PNs and the larva's tail resorption response to mechanical stimuli (Sakamoto et al, 2022). Pou4 has been previously implicated in a Myt1-dependent regulatory cascade that specifies the caudal epidermal neurons (CENs) of the tail, from neurogenic midline cells expressing the proneural bHLH transcription factor Ascl.a (KH.L9.13, sometimes called Ascl2 or Ascl.b previously) (Pasini et al, 2006;Roure et al, 2022;Roure and Darras, 2016;Tang et al, 2013;Waki et al, 2015). To precisely visualize the neurogenic cells of the papillae, we performed double (two-color) mRNA in situ hybridization for Ascl.a and Foxg at the midtailbud stage.…”

Section: Pns Are Specified By Common Peripheral Neuron Regulatorsmentioning

confidence: 99%

“…MAPK) signaling also appears to play an important role in this refinement, as treatment with the MEK inhibitor U0126 results in a "U"-shaped band of Islet expression instead of three discrete foci (Figure 1) (Wagner et al, 2014). Similarly, BMP inhibition also causes a similar "Ushape" swath of Foxg/Islet expression, resulting in a single protrusion instead of the normal three, termed the "cyrano" phenotype (Liu et al, 2023;Roure et al, 2022). However, it has not been shown how these early specification events connect to the final cell type diversity and arrangement of the papillae.…”

Section: Introductionmentioning

confidence: 99%

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Specification of distinct cell types in a sensory-adhesive organ for metamorphosis in theCionalarva

Johnson

Razy-Krajka

Zeng

et al. 2023

Preprint

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The papillae of tunicate larvae contribute sensory, adhesive, and metamorphosis-regulating functions that are crucial for the biphasic lifestyle of these marine, non-vertebrate chordates. We have identified additional molecular markers for at least five distinct cell types in the papillae of the model tunicateCiona,allowing us to further study the development of these organs. Using tissue-specific CRISPR/Cas9-mediated mutagenesis and other molecular perturbations, we reveal the roles of key transcription factors and signaling pathways that are important for patterning the papilla territory into a highly organized array of different cell types and shapes. We further test the contributions of different transcription factors and cell types to the production of the adhesive glue that allows for larval attachment during settlement, and to the processes of tail retraction and body rotation during metamorphosis. With this study, we continue working towards connecting gene regulation to cellular functions that control the developmental transition between the motile larva and sessile adult ofCiona.

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Section: Specification Of Pns and Ocs From Cells That Downregulate Foxgsupporting

confidence: 88%

Section: Identification Of Novel Markers and Reporters For Specific C...mentioning

confidence: 99%

Section: Specification Of Pns and Ocs From Cells That Downregulate Foxgmentioning

confidence: 99%

Section: Pns Are Specified By Common Peripheral Neuron Regulatorsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Specification of distinct cell types in a sensory-adhesive organ for metamorphosis in theCionalarva

Johnson

Razy-Krajka

Zeng

et al. 2023

Preprint

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Highly conserved and extremely evolvable: BMP signalling in secondary axis patterning of Cnidaria and Bilateria

Mörsdorf,

Knabl,

Genikhovich

2024

Dev Genes Evol

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Bilateria encompass the vast majority of the animal phyla. As the name states, they are bilaterally symmetric, that is with a morphologically clear main body axis connecting their anterior and posterior ends, a second axis running between their dorsal and ventral surfaces, and with a left side being roughly a mirror image of their right side. Bone morphogenetic protein (BMP) signalling has widely conserved functions in the formation and patterning of the second, dorso-ventral (DV) body axis, albeit to different extents in different bilaterian species. Whilst initial findings in the fruit fly Drosophila and the frog Xenopus highlighted similarities amongst these evolutionarily very distant species, more recent analyses featuring other models revealed considerable diversity in the mechanisms underlying dorsoventral patterning. In fact, as phylogenetic sampling becomes broader, we find that this axis patterning system is so evolvable that even its core components can be deployed differently or lost in different model organisms. In this review, we will try to highlight the diversity of ways by which BMP signalling controls bilaterality in different animals, some of which do not belong to Bilateria. Future research combining functional analyses and modelling is bound to give us some understanding as to where the limits to the extent of the evolvability of BMP-dependent axial patterning may lie.

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Molecular control of cellulosic fin morphogenesis in ascidians

LANOIZELET,

ELKHOURY YOUHANNA,

DARRAS

2023

Preprint

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The tunicates form a group of filter-feeding marine animals closely related to vertebrates. They share with them a number of features such as a notochord and a dorsal neural tube in the tadpole larvae of ascidians, one of the three groups that make tunicates. However, a number of typical chordate characters have been lost in different branches of tunicates, a diverse and fast-evolving phylum. Consequently, the tunic, a sort of exoskeleton made of extracellular material including cellulose secreted by the epidermis, is the unifying character defining the tunicate phylum. In the larva of ascidians, the tunic differenBates in the tail into a median fin (with dorsal and ventral extended blades) and a caudal fin. Here we have performed experiments in the ascidianPhallusia mammillatato address the molecular control of tunic 3D morphogenesis. We have demonstrated that the tail epidermis medio-lateral paaerning essenBal for peripheral nervous system specificaBon also controls tunic elongaBon into fins. More specifically, when tail epidermis midline idenBty was abolished by BMP signaling inhibiBon, or CRISPR/Cas9 inacBvaBon of the transcripBon factor coding genesMsxorKlf1/2/4/17, median fin did not form. We postulated that this geneBc program should regulate effectors of tunic secreBon. We thus analyzed the expression and regulaBon in different ascidian species of two genes acquired by horizontal gene transfer (HGT) from bacteria,CesAcoding for a cellulose synthase andGh6coding for a cellulase. Although we have uncovered an unexpected dynamic history of these genes in tunicates, and high levels of variability in gene expression and regulaBon among ascidians, we showed thatGh6has a regionalized expression in the epidermis, and that it is a regulator of caudal fin formaBon. Our study consBtutes an important step in the study of the integraBon of HGT-acquired genes into developmental networks, and a cellulose-based morphogenesis of extracellular material in animals.

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Regulation of anterior neurectoderm specification and differentiation by BMP signaling in ascidians

Cited by 9 publications

References 54 publications

Specification of distinct cell types in a sensory-adhesive organ for metamorphosis in theCionalarva

Specification of distinct cell types in a sensory-adhesive organ for metamorphosis in theCionalarva

Highly conserved and extremely evolvable: BMP signalling in secondary axis patterning of Cnidaria and Bilateria

Molecular control of cellulosic fin morphogenesis in ascidians

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