Frizzled3 Controls Axonal Polarity and Intermediate Target Entry during Striatal Pathway Development

Morello, Francesca; Prasad, Asheeta A.; Rehberg, Kati; Sá, Renata Baptista Vieira de; Antón-Bolaños, Noelia; Leyva-Díaz, Eduardo; Adolfs, Youri; Tissir, Fadel; López‐Bendito, Guillermina; Pasterkamp, R. Jeroen

doi:10.1523/jneurosci.1840-15.2015

Cited by 27 publications

(52 citation statements)

References 70 publications

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“…Our data is also in accordance with evidence showing that abnormalities, such as cell loss or misplacement, at the level of the most caudal parts of the corridor domain or the globus pallidus are associated with severe defects in TCA subpallial pathfinding (involving, in some cases, almost all fibers) [52, 63, 66, 70, 71]. Furthermore, these findings support the scaffolding model of axon guidance that has been proposed for IC guidepost cells [27, 68].…”

Section: Discussionsupporting

confidence: 92%

Semaphorin-Plexin signaling influences early ventral telencephalic development and thalamocortical axon guidance

2017

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BackgroundSensory processing relies on projections from the thalamus to the neocortex being established during development. Information from different sensory modalities reaching the thalamus is segregated into specialized nuclei, whose neurons then send inputs to cognate cortical areas through topographically defined axonal connections.Developing thalamocortical axons (TCAs) normally approach the cortex by extending through the subpallium; here, axonal navigation is aided by distributed guidance cues and discrete cell populations, such as the corridor neurons and the internal capsule (IC) guidepost cells. In mice lacking Semaphorin-6A, axons from the dorsal lateral geniculate nucleus (dLGN) bypass the IC and extend aberrantly in the ventral subpallium. The functions normally mediated by Semaphorin-6A in this system remain unknown, but might depend on interactions with Plexin-A2 and Plexin-A4, which have been implicated in other neurodevelopmental processes.MethodsWe performed immunohistochemical and neuroanatomical analyses of thalamocortical wiring and subpallial development in Sema6a and Plxna2; Plxna4 null mutant mice and analyzed the expression of these genes in relevant structures.ResultsIn Plxna2; Plxna4 double mutants we discovered TCA pathfinding defects that mirrored those observed in Sema6a mutants, suggesting that Semaphorin-6A − Plexin-A2/Plexin-A4 signaling might mediate dLGN axon guidance at subpallial level.In order to understand where and when Semaphorin-6A, Plexin-A2 and Plexin-A4 may be required for proper subpallial TCA guidance, we then characterized their spatiotemporal expression dynamics during early TCA development. We observed that the thalamic neurons whose axons are misrouted in these mutants normally express Semaphorin-6A but not Plexin-A2 or Plexin-A4. By contrast, all three proteins are expressed in corridor cells and other structures in the developing basal ganglia.This finding could be consistent with an hypothetical action of Plexins as guidance signals through Sema6A as a receptor on dLGN axons, and/or with their indirect effect on TCA guidance due to functions in the morphogenesis of subpallial intermediate targets. In support of the latter possibility, we observed that in both Plxna2; Plxna4 and Sema6a mutants some IC guidepost cells abnormally localize in correspondence of the ventral path misrouted TCAs elongate into.ConclusionsThese findings implicate Semaphorin-6A − Plexin-A2/Plexin-A4 interactions in dLGN axon guidance and in the spatiotemporal organization of guidepost cell populations in the mammalian subpallium.Electronic supplementary materialThe online version of this article (doi:10.1186/s13064-017-0083-4) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 92%

Semaphorin-Plexin signaling influences early ventral telencephalic development and thalamocortical axon guidance

2017

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“…Since the striatum does not only contain Islet1 + and Ebf1 + direct projection neurons (dSPN; Ehrman et al, ; Lobo, Karsten, Gray, Geschwind, & Yang, ; Lobo, Yeh, & Yang, ; Lu et al, ) but also Drd2‐EGFP ‐expressing indirect projection neurons (iSPN; Gong et al, ; Morello et al, ), we examined whether the Co and Vms regions contained exclusively dSPN‐like neurons. We observed Drd2‐EGFP+ cells in the Vms and superficial Co at E13.5 (Figure a), which expressed Ctip2 (Figure b–d) and not Ebf1 (Figure e–f).…”

Section: Resultsmentioning

confidence: 99%

“…However, unlike the latter, which migrate radially to form the striatum (Halliday & Cepko, ; Hamasaki et al, ; Wichterle et al, ), Co neurons migrate tangentially from the LGE into the MGE from E11.5 to E14, where they create a permissive corridor for TCAs in the otherwise non‐permissive MGE (López‐Bendito et al, ). It has been shown that defects in corridor positioning led to abnormal TCAs pathfinding (Bielle, Marcos‐Mondejar, Keita et al, ; Bielle, Marcos‐Mondéjar, Leyva‐Díaz et al, ; Feng et al, ; Morello et al, ; Zhou et al, ). In addition, Co cells not only control TCA internal navigation but also their topographic organization.…”

Section: Introductionmentioning

confidence: 99%

“…Collectively, our results indicate that Co neurons derive from the LGE/CGE and are labelled by Islet1 cre recombination. Notably, the Co domain comprises also cells generated in the Nkx2.1-positive domain (Figure 1c) as well as cells that still express Nkx2.1 (Figure 1i'), which likely correspond to interneurons migrating toward the neocortex or basal ganglia, respectively.Since the striatum does not only contain Islet1 1 and Ebf1 1 direct projection neurons (dSPN;Ehrman et al, 2013;Lobo, Karsten, Gray, Geschwind, & Yang, 2006;Lobo, Yeh, & Yang, 2008;Lu et al, 2014) but also Drd2-EGFP-expressing indirect projection neurons (iSPN;Gong et al, 2003;Morello et al, 2015), we examined whether the Co and Vms regions contained exclusively dSPN-like neurons. We observed Drd2-EGFP1 cells in the Vms and superficial Co at E13.5(Figure 2a), which expressed Ctip2(Figure 2b-d)and not Ebf1(Figure 2e-f).…”

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Tangential migration of corridor guidepost neurons contributes to anxiety circuits

Tinterri

Deck

Keita

et al. 2017

J of Comparative Neurology

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In mammals, thalamic axons are guided internally toward their neocortical target by corridor (Co) neurons that act as axonal guideposts. The existence of Co-like neurons in non-mammalian species, in which thalamic axons do not grow internally, raised the possibility that Co cells might have an ancestral role. Here, we investigated the contribution of corridor (Co) cells to mature brain circuits using a combination of genetic fate-mapping and assays in mice. We unexpectedly found that Co neurons contribute to striatal-like projection neurons in the central extended amygdala. In particular, Co-like neurons participate in specific nuclei of the bed nucleus of the stria terminalis, which plays essential roles in anxiety circuits. Our study shows that Co neurons possess an evolutionary conserved role in anxiety circuits independently from an acquired guidepost function. It furthermore highlights that neurons can have multiple sequential functions during brain wiring and supports a general role of tangential migration in the building of subpallial circuits.

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“…To investigate how dSPN and iSPN are specified, positioned and assembled in the striatum, we searched for specific markers of these two neuronal populations during embryogenesis. To this aim, we took advantage of the BAC transgenic mouse line Drd2-EGFP 52 , which has been widely used to label iSPN in neonates and is expressed embryonically 53,54 . In addition, we crossed R26 mt/mt reporter mice 55 with Islet1 Cre transgenic mice, which mediate Cre-recombination in dSPN from embryonic stages 41,45 .…”

Section: Defining a Molecular Fingerprint Of Embryonic Dorsal Dspnmentioning

confidence: 99%

Active intermixing of indirect and direct neurons builds the striatal mosaic

Tinterri

Mendary

Diana

et al. 2018

Preprint

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The striatum controls behaviors via the activity of direct and indirect pathway projection neurons (dSPN and iSPN) that are intermingled in all compartments.While such mosaic ensures the balanced activity of the two pathways, how it emerges remains largely unknown. Here, we show that both SPN populations are specified embryonically and progressively intermix through multidirectional iSPN migration. Using conditional mutants of the dSPN-specific transcription factor Ebf1, we found that inactivating this gene impaired selective dSPN properties, including axon pathfinding, whereas molecular and functional features of iSPN were preserved. Remarkably, Ebf1 mutation disrupted iSPN/dSPN intermixing, resulting in an uneven distribution. Such architectural defect was selective of the matrix compartment, revealing that intermixing is a parallel process to compartment formation. Our study reveals that, while iSPN/dSPN specification is largely independent, their intermingling emerges from an active migration of iSPN, thereby providing a novel framework for the building of striatal architecture.

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Frizzled3 Controls Axonal Polarity and Intermediate Target Entry during Striatal Pathway Development

Cited by 27 publications

References 70 publications

Semaphorin-Plexin signaling influences early ventral telencephalic development and thalamocortical axon guidance

Semaphorin-Plexin signaling influences early ventral telencephalic development and thalamocortical axon guidance

Tangential migration of corridor guidepost neurons contributes to anxiety circuits

Active intermixing of indirect and direct neurons builds the striatal mosaic

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