Left/right asymmetric collective migration of parapineal cells is mediated by focal FGF signaling activity in leading cells

Roussigné, Myriam; Wei, Lü; Tsingos, Erika; Kuchling, Franz; Alkobtawi, Mansour; Tsalavouta, Matina; Wittbrodt, Joachim; Carl, Michael; Blader, Patrick; Wilson, Stephen W.

doi:10.1073/pnas.1812016115

Cited by 16 publications

(28 citation statements)

References 62 publications

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“…This is supported by our observation that the onset of sox1a expression in the migrating parapineal is asymmetric, starting at the left (leading) side. In accordance with parapineal migration being a collective behaviour (Roussigné et al, 2018), our parapineal transplant experiments suggest that single parapineal cells do not migrate effectively to their final destination but rather stay close to the site of transplantation. However, regardless of the transplant position, left dHb character is nevertheless induced.…”

Section: Discussionsupporting

confidence: 80%

“…It is not clear whether parapineal cells exhibit any heterogeneity regarding their ability to induce left dHb character nor whether direct cell-cell contact is required between the parapineal and the left dHb. A recent study demonstrated focal activation of FGF-signalling in leading cells of the migrating parapineal, indicating that cells possess positional identity within the parapineal (Roussigné et al, 2018). This is supported by our observation that the onset of sox1a expression in the migrating parapineal is asymmetric, starting at the left (leading) side.…”

Section: Discussionmentioning

confidence: 99%

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Sox1a mediates the ability of the parapineal to impart habenular left-right asymmetry

Lekk

Duboc

Faro

et al. 2019

eLife

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Left-right asymmetries in the zebrafish habenular nuclei are dependent upon the formation of the parapineal, a unilateral group of neurons that arise from the medially positioned pineal complex. In this study, we show that both the left and right habenula are competent to adopt left-type molecular character and efferent connectivity upon the presence of only a few parapineal cells. This ability to impart left-sided character is lost in parapineal cells lacking Sox1a function, despite the normal specification of the parapineal itself. Precisely timed laser ablation experiments demonstrate that the parapineal influences neurogenesis in the left habenula at early developmental stages as well as neurotransmitter phenotype and efferent connectivity during subsequent stages of habenular differentiation. These results reveal a tight coordination between the formation of the unilateral parapineal nucleus and emergence of asymmetric habenulae, ensuring that appropriate lateralised character is propagated within left and right-sided circuitry.

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Section: Discussionsupporting

confidence: 80%

Section: Discussionmentioning

confidence: 99%

Sox1a mediates the ability of the parapineal to impart habenular left-right asymmetry

Lekk

Duboc

Faro

et al. 2019

eLife

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“…The last two decades have produced significant progress in understanding the morphogenetic processes that lead to consistent left-right asymmetries within the nervous system 52 , and the mechanisms by which stochastic neuroanatomical asymmetry emerges when normal lateralizing cues are experimentally removed 53 . Moreover, work in Caenorhabditis elegans has provided important insights into the mechanisms that underlie stochastic acquisition of left-right neuronal identity 54 .…”

Section: Discussionmentioning

confidence: 99%

Molecular and cellular determinants of motor asymmetry in zebrafish

2020

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Asymmetries in motor behavior, such as human hand preference, are observed throughout bilateria. However, neural substrates and developmental signaling pathways that impose underlying functional lateralization on a broadly symmetric nervous system are unknown. Here we report that in the absence of overriding visual information, zebrafish larvae show intrinsic lateralized motor behavior that is mediated by a cluster of 60 posterior tuberculum (PT) neurons in the forebrain. PT neurons impose motor bias via a projection through the habenular commissure. Acquisition of left/right identity is disrupted by heterozygous mutations in mosaic eyes and mindbomb, genes that regulate Notch signaling. These results define the neuronal substrate for motor asymmetry in a vertebrate and support the idea that haploinsufficiency for genes in a core developmental pathway destabilizes left/right identity.

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“…With this work, we have provided a small step towards unifying competing views in the literature [16], and hope that others will follow suit. [30] and asymmetry in the brain [38] in zebrafish, Drosophila border cells [31], and in collective migration of organisms. This study has considered collective cell migration, but the question of whether cell states are best described as discrete or continuous arises in many other biological problems.…”

Section: Discussionmentioning

confidence: 99%

Neural crest migration with continuous cell states

Schumacher

2019

Journal of Theoretical Biology

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Models of cranial neural crest cell migration in cell-induced (or self-generated) gradients have included a division of labour into leader and follower migratory states, which undergo chemotaxis and contact guidance, respectively. Despite validated utility of these models through experimental perturbation of migration in the chick embryo and gene expression analysis showing relevant heterogeneity at the single cell level, an often raised question has been whether the discrete cell states are necessary, or if a continuum of cell behaviours offers a functionally equivalent description. Here we argue that this picture is supported by recent single-cell transcriptome data. Motivated by this, we implement two versions of a continuous-state model: (1) signal choice and (2) signal combination. We find that the cell population migrates further than in the discretestate model and than in experimental observations. We further show that the signal combination model, but not the signal choice model, can be successfully adjusted to experimentally plausible regimes by reducing the chemoattractant consumption parameter. Thus we show an equivalently plausible, experimentally motivated, model of neural crest cell migration.

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Left/right asymmetric collective migration of parapineal cells is mediated by focal FGF signaling activity in leading cells

Cited by 16 publications

References 62 publications

Sox1a mediates the ability of the parapineal to impart habenular left-right asymmetry

Sox1a mediates the ability of the parapineal to impart habenular left-right asymmetry

Molecular and cellular determinants of motor asymmetry in zebrafish

Neural crest migration with continuous cell states

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