Single-cell transcriptome profiling of the Ciona larval brain

Sharma, Sarthak; Wang, Wei; Stolfi, Alberto

doi:10.1016/j.ydbio.2018.09.023

Cited by 41 publications

(51 citation statements)

References 84 publications

(107 reference statements)

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“…To further probe Dale's principle in chordates, we first analyzed the neuronal population of the tunicate Ciona intestinalis larval brain, identified upon the expression of the neuronal markers Synaptotagmin 1 ( Syt1 ), CUGBP Elav-like family member 3/4/5 ( Celf3/4/5 ), retinaldehyde-binding protein 1 ( Rlbp1 ), among others (Sharma et al, 2019 ). Neurotransmitter expression was assessed and three main cell types were distinguished: GABAergic neurons ( GAD1/2, glutamate decarboxylase 1/2 and VGAT, vesicular GABA transporter ), cholinergic neurons ( VAChT, vesicular acetylcholine transporter and CHAT, acetylcholine transporter ) and glutamatergic neurons ( VGlut, vesicular glutamate transporter ) ( Figure 6A ).…”

Section: Resultsmentioning

confidence: 99%

“…Here, we provide an extensive evaluation of fast-acting neurotransmitters in neurons populating the brain, or simpler neuronal nets, and its conservation across different species: Hydra vulgaris (Siebert et al, 2019 ) , Schmidtea mediterranea (Fincher et al, 2018 ), Caenorhabditis elegans (Cao et al, 2017 ), Drosophila melanogaster (Davie et al, 2018 ; Brunet Avalos et al, 2019 ), Ciona intestinalis (Sharma et al, 2019 ), Danio rerio (Raj et al, 2018 ), Trachemys scripta, Pogona vitticeps (Tosches et al, 2018 ), and Mus musculus (Ximerakis et al, 2019 ) ( Figure 1 ). We extended the analysis of existing cell atlases, initially originated by scRNAseq technologies, by the usage of the user-friendly R package Seurat (Butler et al, 2018 ; Stuart et al, 2019 ) and assessed whether neurons show an overlapping expression of the canonical marker genes commonly used to define neuronal identity: vesicular transporters and enzymes involved in the biosynthesis and transport of neurotransmitters.…”

Section: Introductionmentioning

confidence: 99%

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Single-Cell Transcriptomic Reveals Dual and Multi-Transmitter Use in Neurons Across Metazoans

Avalos

Sprecher

2021

Front. Mol. Neurosci.

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Neurotransmitter expression is widely used as a criterion for classifying neurons. It was initially thought that neurons express a single type of neurotransmitter, a phenomenon commonly recognized as Dale's principle: “one neuron, one transmitter.” Consequently, the expression of a single neurotransmitter should determine stable and distinguishable neuronal characteristics. However, this notion has been largely challenged and increasing evidence accumulates supporting a different scenario: “one neuron, multiple neurotransmitters.” Single-cell transcriptomics provides an additional path to address coexpression of neurotransmitters, by investigating the expression of genes involved in the biosynthesis and transmission of fast-acting neuromodulators. Here, we study neuronal phenotypes based on the expression of neurotransmitters, at single-cell resolution, across different animal species representing distinct clades of the tree of life. We take advantage of several existing scRNAseq datasets and analyze them in light of neurotransmitter plasticity. Our results show that while most neurons appear to predominantly express a single type of neurotransmitter, a substantial number of neurons simultaneously expresses a combination of them, across all animal species analyzed.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Single-Cell Transcriptomic Reveals Dual and Multi-Transmitter Use in Neurons Across Metazoans

Avalos

Sprecher

2021

Front. Mol. Neurosci.

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“…Sequencing data are then compared and clustered into cell types according to the similarity of transcriptomes (Kiselev, Andrews & Hemberg, 2019). Recent scRNA-seq data for C. robusta (Cao et al, 2019;Sharma, Wang & Stolfi, 2019) form a rich resource with which to compare more targeted differential transcriptomes and proteomes for adhesive organs or their adhesive secretions (U. Rothbächer, unpublished data). The scRNAseq approach is compatible with fixed cells, thus minimising detrimental effects on the cell state.…”

Section: Limitations: Important Considerations For 'Omics-based Bioadhesion Studiesmentioning

confidence: 99%

Omics‐based molecular analyses of adhesion by aquatic invertebrates

et al. 2021

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Many aquatic invertebrates are associated with surfaces, using adhesives to attach to the substratum for locomotion, prey capture, reproduction, building or defence. Their intriguing and sophisticated biological glues have been the focus of study for decades. In all but a couple of specific taxa, however, the precise mechanisms by which the bioadhesives stick to surfaces underwater and (in many cases) harden have proved to be elusive. Since the bulk components are known to be based on proteins in most organisms, the opportunities provided by advancing 'omics technologies have revolutionised bioadhesion research. Time-consuming isolation and analysis of single molecules has been either replaced or augmented by the generation of massive data sets that describe the organism's translated genes and proteins. While these new approaches have provided resources and opportunities that have enabled physiological insights and taxonomic comparisons that were not previously possible, they do not provide the complete picture and continued multi-disciplinarity is essential. This review covers the various ways in which 'omics have contributed to our understanding of adhesion by aquatic invertebrates, with new data to illustrate key points. The associated challenges are highlighted and priorities are suggested for future research.

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“…The ascidian larval CNS has been extensively studied in terms of its lineage, molecular mechanisms of development, gene expression patterns and cell types [ 23 , 24 , 25 , 26 , 27 ]. More recently, a larval nervous system connectome has been revealed [ 28 ] and collections of single cell transcriptomics generated [ 29 , 30 , 31 , 32 , 33 ]. Emerging studies are now aiming to annotate each neuron identified in the connectome with the gene expression patterns, including neurotransmitter types, described from in situ hybridization/immunostaining analysis or single cell transcriptomics datasets, as well as to the cell lineage history and ultimately to neuronal function and larval behavior [ 29 , 34 , 35 , 36 , 37 , 38 , 39 ].…”

Section: The Ascidian Larval Cnsmentioning

confidence: 99%

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

Hudson

Yasuo

2021

Genes

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Ascidians are invertebrate chordates and the closest living relative to vertebrates. In ascidian embryos a large part of the central nervous system arises from cells associated with mesoderm rather than ectoderm lineages. This seems at odds with the traditional view of vertebrate nervous system development which was thought to be induced from ectoderm cells, initially with anterior character and later transformed by posteriorizing signals, to generate the entire anterior-posterior axis of the central nervous system. Recent advances in vertebrate developmental biology, however, show that much of the posterior central nervous system, or spinal cord, in fact arises from cells that share a common origin with mesoderm. This indicates a conserved role for bi-potential neuromesoderm precursors in chordate CNS formation. However, the boundary between neural tissue arising from these distinct neural lineages does not appear to be fixed, which leads to the notion that anterior-posterior patterning and neural fate formation can evolve independently.

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Single-cell transcriptome profiling of the Ciona larval brain

Cited by 41 publications

References 84 publications

Single-Cell Transcriptomic Reveals Dual and Multi-Transmitter Use in Neurons Across Metazoans

Single-Cell Transcriptomic Reveals Dual and Multi-Transmitter Use in Neurons Across Metazoans

Omics‐based molecular analyses of adhesion by aquatic invertebrates

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

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