Regulation of neurogenesis by FGF signaling and Neurogenin in the invertebrate chordate Ciona
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ABSTRACT:
ORGANISM(S): Ciona robusta
PROVIDER: GSE150913 | GEO | 2020/05/21
REPOSITORIES: GEO
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Project description:Neurogenesis is a complex sequence of cellular processes and behaviors driven by the coordinated expression of conserved effectors. The bipolar tail neurons (BTNs) of Ciona develop according to a highly dynamic, yet highly stereotyped developmental program and thus could serve as an accessible model system for neurogenesis, including underlying cell behaviors like neuronal delamination, migration, and polarized axon outgrowth. Here we investigate both the upstream events that shape BTN neurogenesis through spatiotemporal regulation of the conserved proneural factor Neurog, spatiotemporal, and the gene expression profile of differentiating BTNs downstream of Neurog activity. We show that, although early FGF signaling is required for Neurog expression and BTN specification, Fgf8/17/18 is expressed in tail tip cells at later stages and suppresses sustained Neurog expression in the anterior BTN (aBTN) lineage, such that only one cell (the one furthest from the source of Fgf8/17/18) maintains Neurog expression and becomes a neuron. Curiously, Fgf8/17/18 might not affect neurogenesis of the posterior BTNs (pBTNs), which are in direct contact with the Fgf8/17/18-expressing cells. Finally, to profile gene expression associated with BTN neurogenesis we performed RNAseq of isolated BTN lineage cells in which BTN neurogenesis was enhanced or suppressed by perturbing Neurog function. This allowed us to identify several candidate genes that might play conserved roles in neurogenesis and neuronal migration in other animals, including mammals.
| S-EPMC7324659 | biostudies-literature
Project description:Regulation of neurogenesis by FGF signaling and Neurogenin in the invertebrate chordate Ciona
| PRJNA634076 | ENA
Project description:Gene number can be considered a pragmatic measure of biological complexity, but reliable data is scarce. Estimates for vertebrates are 50-100,000 genes per haploid genome, whereas invertebrate estimates fall below 25,000. We wished to test the hypothesis that the origin of vertebrates coincided with extensive gene creation. A prediction is that gene number will differ sharply between invertebrate and vertebrate members of the chordate phylum. A gene number estimation method requiring limited sequence sampling of genomic DNA was developed and validated by using data for Caenorhabditis elegans. Using the method, we estimated that the invertebrate chordate Ciona intestinalis has 15,500 protein-coding genes (+/-3,700). This number is significantly lower than gene numbers of vertebrate chordates, but similar to those of invertebrates in distantly related phyla. The data indicate that evolution of vertebrates was accompanied by a dramatic increase in protein-coding capacity of the genome.
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Project description:Vertebrate embryos exploit the mutual inhibition between the RA and FGF signalling pathways to coordinate the proliferative elongation of the main body axis with the progressive patterning and differentiation of its neuroectodermal and paraxial mesodermal structures. The evolutionary history of this patterning system is still poorly understood. Here, we investigate the role played by the RA and FGF/MAPK signals during the development of the tail structures in the tunicate Ciona intestinalis, an invertebrate chordate belonging to the sister clade of vertebrates, in which the prototypical chordate body plan is established through very derived morphogenetic processes. Ciona embryos are constituted of few cells and develop according to a fixed lineage; elongation of the tail occurs largely by rearrangement of postmitotic cells; mesoderm segmentation and somitogenesis are absent. We show that in the Ciona embryo, the antagonism of the RA and FGF/MAPK signals is required to control the anteroposterior patterning of the tail epidermis. We also demonstrate that the RA, FGF/MAPK and canonical Wnt pathways control the anteroposterior patterning of the tail peripheral nervous system, and reveal the existence of distinct subpopulations of caudal epidermal neurons with different responsiveness to the RA, FGF/MAPK and canonical Wnt signals. Our data provide the first demonstration that the use of the antagonism between the RA and FGF signals to pattern the main body axis predates the emergence of vertebrates and highlight the evolutionary plasticity of this patterning strategy, showing that in different chordates it can be used to pattern different tissues within the same homologous body region.
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Project description:BACKGROUND:Genomic analysis has upended chordate phylogeny, placing the tunicates as the sister group to the vertebrates. This taxonomic rearrangement raises questions about the emergence of a tunicate/vertebrate ancestor. RESULTS:Characterization of developmental genes uniquely shared by tunicates and vertebrates is one promising approach for deciphering developmental shifts underlying acquisition of novel, ancestral traits. The matrix glycoprotein Fibronectin (FN) has long been considered a vertebrate-specific gene, playing a major instructive role in vertebrate embryonic development. However, the recent computational prediction of an orthologous "vertebrate-like" Fn gene in the genome of a tunicate, Ciona savignyi, challenges this viewpoint suggesting that Fn may have arisen in the shared tunicate/vertebrate ancestor. Here we verify the presence of a tunicate Fn ortholog. Transgenic reporter analysis was used to characterize a Ciona Fn enhancer driving expression in the notochord. Targeted knockdown in the notochord lineage indicates that FN is required for proper convergent extension. CONCLUSIONS:These findings suggest that acquisition of Fn was associated with altered notochord morphogenesis in the vertebrate/tunicate ancestor.
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Project description:Cell-matrix adhesion strongly influences developmental signaling. Resulting impacts on cell migration and tissue morphogenesis are well characterized. However, the in vivo impact of adhesion on fate induction remains ambiguous. Here, we employ the invertebrate chordate Ciona intestinalis to delineate an essential in vivo role for matrix adhesion in heart progenitor induction. In Ciona pre-cardiac founder cells, invasion of the underlying epidermis promotes localized induction of the heart progenitor lineage. We found that these epidermal invasions are associated with matrix adhesion along the pre-cardiac cell/epidermal boundary. Through targeted manipulations of RAP GTPase activity, we were able to manipulate pre-cardiac cell-matrix adhesion. Targeted disruption of pre-cardiac cell-matrix adhesion blocked heart progenitor induction. Conversely, increased matrix adhesion generated expanded induction. We were also able to selectively restore cell-matrix adhesion and heart progenitor induction through targeted expression of Ci-Integrin ?2. These results indicate that matrix adhesion functions as a necessary and sufficient extrinsic cue for regional heart progenitor induction. Furthermore, time-lapse imaging suggests that cytokinesis acts as an intrinsic temporal regulator of heart progenitor adhesion and induction. Our findings highlight a potentially conserved role for matrix adhesion in early steps of vertebrate heart progenitor specification.
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Project description:BackgroundThe evolutionary emergence and diversification of the chordates appear to involve dramatic changes in organ morphogenesis along the left/right axis. However, the ancestral chordate mechanism for establishing lateral asymmetry remains ambiguous. Additionally, links between the initial establishment of lateral asymmetry and subsequent asymmetries in organ morphogenesis are poorly characterized.ResultsTo explore asymmetric organ morphogenesis during chordate evolution, we have begun to characterize left/right patterning of the heart and endodermal organs in an invertebrate chordate, Ciona intestinalis. Here, we show that Ciona has a laterally asymmetric, right-sided heart. Our data indicate that cardiac lateral asymmetry requires H+/K+ ion flux, but is independent of Nodal signaling. Our pharmacological inhibitor studies show that ion flux is required for polarization of epidermal cilia and neurula rotation and suggest that ion flux functions synergistically with chorion contact to drive cardiac laterality. Live imaging analysis revealed that larval heart progenitor cells undergo a lateral shift without displaying any migratory behaviors. Furthermore, we find that this passive shift corresponds with the emergence of lateral asymmetry in the endoderm, which is also ion flux dependent.ConclusionsOur data suggest that ion flux promotes laterally asymmetric morphogenesis of the larval endoderm rudiment leading to a passive, Nodal-independent shift in the position of associated heart progenitor cells. These findings help to refine hypotheses regarding ancestral chordate left/right patterning mechanisms and how they have diverged within invertebrate and vertebrate chordate lineages.
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Project description:The major thiol redox buffer glutathione (l-gamma-glutamyl-l-cysteinylglycine, GSH) is central to cell fate determination, and thus, associated metabolic and regulatory pathways are exquisitely sensitive to a wide range of environmental cues. An imbalance of cellular redox homeostasis has emerged as a pathologic hallmark of a diverse range of human gene-environment disorders. Despite the central importance of GSH in cellular homeostasis, underlying genetic regulatory pathways remain poorly defined. This report describes the annotation and expression analysis of genes contributing to GSH homeostasis in the invertebrate chordate Ciona intestinalis. A core pathway comprising 19 genes contributing to the biosynthesis of GSH and its use as both a redox buffer and a conjugate in phase II detoxification as well as known transcriptional regulators were analyzed. These genes exhibit a high level of sequence conservation with corresponding human, rat, and mouse homologs and were expressed constitutively in tissues of adult animals. The GSH biosynthetic genes Gclc and Gclm were also responsive to the prototypical antioxidant tert-butylhydroquinone. The present evidence of a conserved GSH homeostasis pathway in C. intestinalis together with its phylogenetic position as a basal chordate and lifestyle as a filter feeder constantly exposed to natural marine toxins introduces this species as an important animal model for defining molecular mechanisms that potentially underlie genetic susceptibility to environmentally associated stress.
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Project description:3-Hydroxyisoquinolines (ISOs) and their tautomeric isoquinolin-3-ones are heterocycles with attractive biological properties. Here we reported the revisited synthesis of a highly functionalized ISO that showed blue fluorescence and the characterization of its biological properties in an invertebrate animal model, the ascidian Ciona intestinalis. Larvae exposed to ISO at concentrations higher than 1 μM showed an intense fluorescence localized in the cell nuclei of all tissues. Moreover, exposure to ISO interfered with larval ability to swim; this neuromuscular effect was reversible. Overall, these results suggested that ISOs can have promising applications as novel fluorescent dyes of the cell nuclei.
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Project description:We recently showed HMX is expressed in bipolar tail neurons (BTN) in early embryos of Ciona intestinalis. In order to assess the function of the homeobox transcription factor in this cell fate, we used an overexpression strategy. ciHMX was overexpressed in the epidermis, followed by RNAseq of experimental and control embryos. We then looked for differential expression of BTN fate markers, testing if HMX is able to regulate BTN fate determination.
2021-11-26 | GSE141046 | GEO