The HMG box transcription factors Sox1a and Sox1b specify a new class of glycinergic interneuron in the spinal cord of zebrafish embryos

Gerber, Vanessa; Yang, Lixin; Takamiya, Masanari; Ribes, Vanessa; Gourain, Victor; Peravali, Ravindra; Stegmaier, Johannes; Mikut, Ralf; Reischl, Markus; Ferg, Marco; Rastegar, Sepand; Strähle, Uwe

doi:10.1242/dev.172510

Cited by 23 publications

(69 citation statements)

References 55 publications

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“…V2a neurons express the Notch ligand delta-like 4 (Dll4), and V2b neurons express Notch receptors and require Notch signalling for their specification (Peng et al, 2007;Skaggs et al, 2011). Recent evidence in zebrafish has revealed that V2s neurons, which, similar to mammalian V2c neurons, express Sox1 orthologues, require Notch signalling for their generation from a combined postmitotic V2b/s precursor (Gerber et al, 2019). Thus, Notch-dependent cell-cell interactions sequentially subdivide the V2 lineage.…”

Section: Further Diversification Of Neuronal Identitymentioning

confidence: 99%

Establishing neuronal diversity in the spinal cord: a time and a place

2019

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The vertebrate spinal cord comprises multiple functionally distinct neuronal cell types arranged in characteristic positions. During development, these different types of neurons differentiate from transcriptionally distinct neural progenitors that are arrayed in discrete domains along the dorsal-ventral and anterior-posterior axes of the embryonic spinal cord. This organization arises in response to morphogen gradients acting upstream of a gene regulatory network, the architecture of which determines the spatial and temporal pattern of gene expression. In recent years, substantial progress has been made in deciphering the regulatory network that underlies the specification of distinct progenitor and neuronal cell identities. In this Review, we outline how distinct neuronal cell identities are established in response to spatial and temporal patterning systems, and outline novel experimental approaches to study the emergence and function of neuronal diversity in the spinal cord.

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Section: Further Diversification Of Neuronal Identitymentioning

confidence: 99%

Establishing neuronal diversity in the spinal cord: a time and a place

2019

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“…It is unclear whether zebrafish have a homologous V2c population although Sox1a/b is present in the 24 hpf spinal cord and notably also colabels with Gata3 [55]. A possible V2c homolog, referred to as V2s, has been identified as a Sox1a/b+ glycinergic cell type deriving from the V2 domain with long, ipsilateral, caudally projecting axons [56] similar to the V2b-gly neurons described here. However, Gata3 expression was not investigated in V2s neurons, leaving it unclear whether V2s neurons are in fact V2b-gly [56].…”

Section: Discussionmentioning

confidence: 94%

“…A possible V2c homolog, referred to as V2s, has been identified as a Sox1a/b+ glycinergic cell type deriving from the V2 domain with long, ipsilateral, caudally projecting axons [56] similar to the V2b-gly neurons described here. However, Gata3 expression was not investigated in V2s neurons, leaving it unclear whether V2s neurons are in fact V2b-gly [56]. Given the persistent, distinguishing expression of Gata3 in both V2b-gly and V2b-mixed subtypes, our data are consistent with the designation of two subclasses within V2b, not a V2c homolog or additional V2s class.…”

Section: Discussionmentioning

confidence: 99%

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

Callahan¹,

Roberts²,

Sengupta³

et al. 2019

Preprint

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10The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, 11 models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal 12 alternation between left and right sides or flexors and extensors. However, recent work has 13shown that inhibition also increases coincident with excitation during contraction. Here, using 14 larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-15 extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines 16 we define two stable subclasses with distinct neurotransmitter and morphological properties. 17These two V2b subclasses make direct synapses onto motor neurons with differential targeting to 18 slower and faster circuits. In vivo, optogenetic suppression of V2b activity leads to increases in 19 locomotor speed. We conclude that V2b neurons exert speed-specific influence over axial motor 20 circuits throughout the rostrocaudal axis. Together, these results indicate a new role for 21 ipsilateral inhibition in speed control. 22 46In-phase inhibition is thought to derive from two spinal interneuron classes, the V1 and V2b 47 populations. The V1 population includes Renshaw cells [15, 16], which provide recurrent 48 inhibition onto motor neurons with potentially significant shunting effects [17]. To date, most 49 analysis of drive from V2b neurons has focused on the shared contributions of V1s and V2bs to 50 reciprocal inhibition governing flexor/extensor alternation in limbed animals [18][19][20]. However, 51 this does not shed light on potential functions of ipsilateral inhibition in gain control for 52 regulation of motor neuron firing during contraction, as opposed to suppression of motor neuron 53 firing during extension. 54 55In-phase inhibition increases in amplitude for faster locomotor movements [10] suggesting a 56 potential role in speed control. Here we investigated whether V2b neurons could indeed provide 57 direct inhibition to motor neurons for speed control, taking advantage of the speed-dependent 58 organization of zebrafish motor circuits [21][22][23]. V2b neurons are good candidates for in-phase 59 gain control because they are exclusively inhibitory in mouse and zebrafish [24] with ipsilateral, 60 descending axons within the spinal cord [18, 25]. They arise from a final progenitor division that 61 produces pairs of V2a and V2b neurons [26]. Given the role of V2a neurons in triggering motor 62 output [27, 28], particularly through speed-specific circuits for titrating levels of motor excitation 63[4, 29-31], it seems plausible that their sister V2b neurons exert an opposing, inhibitory role in 64 speed control. However, the V2b class has not been well characterized at anatomical or 65 neurochemical levels outside of very early development. 66 67 5Here, we define two subclasses of V2b neurons in larval zebrafish based on differential 68 transmitter expression and anatomy, and further show that these neurons directly inhibit a...

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“…Specifically, nkx2.2+/nkx2.9+ progenitors divide both symmetrically and asymmetrically and form KA” cells in zebrafish embryos ( Huang et al, 2012 ). In addition, morpholino knockdown of nkx2.2a , nkx2.2b , and nkx2.9 completely eliminates KA” cells expressing the markers gata2a , gata3 , sox1a , sox1b , tal2 , and gad65/67 in the LFP ( Yang et al, 2010 ; Gerber et al, 2019 ). Furthermore, a subset of KA” cells expressing tal2+/nkx2.2b+ differentiates into sim1+/huC/D+ V3 interneurons, and thus, tal2+/nkx2.2b+ cells are postulated to be p3 neural progenitor cells ( Schäfer et al, 2007 ).…”

Section: Subsets Of Ka/csf-cn Cells Are Differentiated From Differentmentioning

confidence: 99%

“…Gata2a and gata3 belong to the C4 zinc-finger family and are expressed by the V2b, V2s, KA”, and KA’ cells in zebrafish ( Batista et al, 2008 ; Gerber et al, 2019 ; Yang et al, 2010 ). Morpholino knockdown of gata3 eliminates KA’ cell formation ( Yang et al, 2010 ).…”

Section: Transcription Factors Driving the Identities Of Ka/csf-cn Cementioning

confidence: 99%

The Genetic Programs Specifying Kolmer–Agduhr Interneurons

2020

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Kolmer–Agduhr (KA) cells are a subgroup of interneurons positioned adjacent to the neurocoele with cilia on the apical surface protruding into the central canal of the spinal cord. Although KA cells were identified almost a century ago, their development and functions are only beginning to be unfolded. Recent studies have revealed the characteristics of KA cells in greater detail, including their spatial distribution, the timing of their differentiation, and their specification via extrinsic signaling and a unique combination of transcription factors in zebrafish and mouse. Cell lineage-tracing experiments have demonstrated that two subsets of KA cells, named KA’ and KA” cells, differentiate from motoneuronal progenitors and floor-plate precursors, respectively, in both zebrafish and mouse. Although KA’ and KA” cells originate from different progenitors/precursors, they each share a common set of transcription factors. Intriguingly, the combination of transcription factors that promote the acquisition of KA’ cell characteristics differs from those that promote a KA” cell identity. In addition, KA’ and KA” cells exhibit separable neuronal targets and differential responses to bending of the spinal cord. In this review, we summarize what is currently known about the genetic programs defining the identities of KA’ and KA” cell identities. We then discuss how these two subgroups of KA cells are genetically specified.

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The HMG box transcription factors Sox1a and Sox1b specify a new class of glycinergic interneuron in the spinal cord of zebrafish embryos

Cited by 23 publications

References 55 publications

Establishing neuronal diversity in the spinal cord: a time and a place

Establishing neuronal diversity in the spinal cord: a time and a place

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

The Genetic Programs Specifying Kolmer–Agduhr Interneurons

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