Effector gene expression underlying neuron subtype-specific traits in the Motor Ganglion of Ciona

Gibboney, Susanne; Orvis, Jameson; Kim, Kwantae; Johnson, Christopher; Martínez-Feduchi, Paula; Lowe, Elijah K.; Sharma, Sarthak; Stolfi, Alberto

doi:10.1016/j.ydbio.2019.10.012

Cited by 13 publications

(29 citation statements)

References 107 publications

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“…The sensory vesicle contains two pigmented sense organs, an otolith, anchored in the ventral wall and used for gravity perception, and an ocellus, required for photo-reception [ 24 , 25 , 41 , 42 , 43 ]. The trunk ganglion [ 44 ] is also referred to as the visceral ganglion [ 24 , 45 ] or motor ganglion, since it contains the motor neurons that innervate the tail muscle [ 23 , 28 , 46 , 47 , 48 ]. Here we use the morphology-based term, ‘trunk ganglion’.…”

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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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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“…Two of the primary cell classes in the MG are the MNs and the MGINs, which are marked by the expression of mnx and vsx , respectively (Gibboney et al, 2020). We performed a triple in situ with vsx , mnx and AMPAR to determine which cell classes expressed AMPAR in the MG (Figure 6 D-H).…”

Section: Left-sided Ampa Receptor Expression In the Motor Ganglion Inmentioning

confidence: 99%

Left/right asymmetry disruptions and mirror-image reversals to behavior and brain anatomy inCiona

Mj¹,

Bostwick

A³

et al. 2021

Preprint

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Left-right asymmetries are a common feature of metazoan nervous systems. This is particularly pronounced in the comparatively simple larval central nervous system (CNS) of the tunicate Ciona , whose swimming tadpole larva shows a clear chordate ground plan. While common pathway elements for specifying the left-right axis are found in the chordates, particularly a requirement for Nodal signaling, Ciona differs from its vertebrate cousins by specifying its axis at the neurula stage, rather than at gastrula. Additionally, Ciona , and other ascidians, have a requirement for an intact chorionic membrane for proper left/right specification. We present here results showing that left-right asymmetry disruptions caused by removal of the chorion (dechorionation) are highly variable and present throughout the Ciona larval nervous system. While previous studies have documented disruptions to the conspicuously asymmetric sensory systems in the anterior brain vesicle, we document asymmetries in seemingly symmetric structures such as the posterior brain vesicle and motor ganglion. Moreover, defects caused by dechorionation include misplaced or absent neuron classes, loss of asymmetric gene expression, aberrant synaptic connectivity, and abnormal behaviors. In the motor ganglion, a brain structure that has been equated with the vertebrate hindbrain, we find that despite the apparent left/right symmetric distribution of interneurons and motor neurons, AMPA receptors are expressed exclusively on the left side, which equates with asymmetric swimming behaviors. We also find that within a population of dechorionated larvae, there is a small percentage with apparently normal left-right specification, and approximately equal population with inverted (mirror-image) asymmetry. We present a method based on a behavioral assay for isolating these larvae. When these two classes of larvae (normal and inverted) are assessed in a light dimming assay they display mirror-image behaviors, with normal larvae responding with counterclockwise swims, while inverted larvae respond with clockwise swims.Our findings highlight the importance of left-right specification pathways not only for proper CNS anatomy, but also for correct synaptic connectivity and behavior.

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“…Previous MG neuron transcriptome profiling and a follow up ISH revealed that Saxo (Stabilizer of axonemal microtubules) was expressed in the BTNs, in addition to the ddNs (Gibboney et al, 2020). Saxo is the Ciona ortholog of human SAXO1/SAXO2, formerly FAM154A/FAM154B.…”

Section: Saxo: Stabilizer Of Axonemal Microtubulesmentioning

confidence: 99%

“…A GFP:Saxo fusion when expressed in Ciona was found to localize to centrosomes in BTN precursors (Figure 8c), and to cilia of ependymal cells (Figure 8d), also consistent with a potentially conserved role in microtubule stabilization. Given its expression in both BTNs and ddNs, and given the dynamic repositioning of the Golgi apparatus observed in both these neurons types immediately predicting direction of axon outgrowth (Stolfi et al, 2015;Gibboney et al, 2020), Saxo is one of the more intriguing candidate effectors of neuronal polarization that remain to be functionally characterized.…”

Section: Saxo: Stabilizer Of Axonemal Microtubulesmentioning

confidence: 99%

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Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona

Kim

Gibboney

Razy-Krajka

et al. 2020

Front. Cell Dev. Biol.

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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.

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Effector gene expression underlying neuron subtype-specific traits in the Motor Ganglion of Ciona

Cited by 13 publications

References 107 publications

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

Left/right asymmetry disruptions and mirror-image reversals to behavior and brain anatomy inCiona

Regulation of Neurogenesis by FGF Signaling and Neurogenin in the Invertebrate Chordate Ciona

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