Serotonin receptor 3A controls interneuron migration into the neocortex

Murthy, Sahana; Niquille, Mathieu; Hurni, Nicolas; Limoni, Greta; Frazer, Sarah Louise; Chameau, Pascal; Hooft, Johannes A. van; Vitalis, Tania; Dayer, Alexandre

doi:10.1038/ncomms6524

Cited by 78 publications

(98 citation statements)

References 59 publications

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“…Interestingly, long-lasting alteration in the positioning of reelin+ cortical interneurons was reported. This suggests that 5-HT 3A activation acts as a migratory signal for CGE-derived interneurons and alters definitively the positioning of their subpopulation [189]. A similar conclusion was suggested using SERT:KO animals that showed a specific increase in the migratory speed and positioning of VIP+ interneurons [92].…”

Section: Serotonin and Neuronal Migrationsupporting

confidence: 63%

Sculpting Cerebral Cortex with Serotonin in Rodent and Primate

Vitalis¹,

Verney²

2017

Serotonin - A Chemical Messenger Between All Types of Living Cells

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The mammalian cerebral cortex is critical for sensory and motor integrations and, for higher-order cognitive functions. The construction of mammalian cortical circuits involves the coordinated interplay between cellular processes such as proliferation, migration and differentiation of neural and glial cell subtypes followed by accurate connectivity evolving in complexity in primates. Alteration in cortical development may induce the emergence of various pathological traits and behaviours. Among the large array of factors that regulate the assembly of cortical circuits, serotonin (5-HT) plays important role as a developmental signal that impacts on a broad diversity of cellular processes. 5-HT plays distinct roles during specific sensitive periods and is produced from various sources depending on the perinatal stage. Its roles are mediated by more than fourteen 5-HT receptors that are all G-protein coupled receptors except the ionotropic 5-HT type 3A receptor (5-HT 3A ) mediating rapid neuronal activation. Importantly, 5-HT metabolism and signalling are influenced by numerous epigenetic and genetic factors, including nutrition and gut microbiota, perinatal stress, infection and inflammation. In this review, we will recapitulate some evidences showing that dysregulation of 5-HT homeostasis and 5-HT 3A signalling impairs distinct steps of cortical circuit formation leading to the predisposition of the onset of various psychiatric diseases.

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Section: Serotonin and Neuronal Migrationsupporting

confidence: 63%

Sculpting Cerebral Cortex with Serotonin in Rodent and Primate

Vitalis¹,

Verney²

2017

Serotonin - A Chemical Messenger Between All Types of Living Cells

Self Cite

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“…However, due to the wide expression of those proteins, both in GABAergic interneurons and many other cells, as well as the global nature of the mouse mutants employed, it remains unclear to which extent the effects observed were cell-autonomous or caused by other cortical abnormalities. For GABAergic interneurons derived from the CGE, the serotonin receptor 3A was recently found to play a role in cortical plate invasion (Murthy et al, 2014). Here we showed that MGE-derived interneurons can reach the neocortex in normal numbers in the absence of TCAs, indicating that they do not require this axonal tract for tangential migration from the ventral telencephalon nor for tangential dispersion through the subplate and IZ.…”

Section: Discussionmentioning

confidence: 99%

Thalamo-cortical axons regulate the radial dispersion of neocortical GABAergic interneurons

Zechel

Nakagawa

Ibáñez

2016

eLife

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Neocortical GABAergic interneuron migration and thalamo-cortical axon (TCA) pathfinding follow similar trajectories and timing, suggesting they may be interdependent. The mechanisms that regulate the radial dispersion of neocortical interneurons are incompletely understood. Here we report that disruption of TCA innervation, or TCA-derived glutamate, affected the laminar distribution of GABAergic interneurons in mouse neocortex, resulting in abnormal accumulation in deep layers of interneurons that failed to switch from tangential to radial orientation. Expression of the KCC2 cotransporter was elevated in interneurons of denervated cortex, and KCC2 deletion restored normal interneuron lamination in the absence of TCAs. Disruption of interneuron NMDA receptors or pharmacological inhibition of calpain also led to increased KCC2 expression and defective radial dispersion of interneurons. Thus, although TCAs are not required to guide the tangential migration of GABAergic interneurons, they provide crucial signals that restrict interneuron KCC2 levels, allowing coordinated neocortical invasion of TCAs and interneurons.DOI: http://dx.doi.org/10.7554/eLife.20770.001

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“…To understand how CGE-derived INs reach their multiple targets, we used the 5HT3aR-GFP mouse transgenic line, previously reported to label the totality of CGE-derived cortical INs in embryos and in adult mice (Inta et al, 2008;Lee et al, 2010;Murthy et al, 2014;Rudy et al, 2011;Vucurovic et al, 2010). Embryonic day (E) 11.5 to E18.5 5HT3aR-GFP + brains were cut in a horizontal plane allowing an overview of all three GE structures in one section (Fig.…”

Section: Identification Of Two Novel Tangentially Cge-derived Paths Imentioning

confidence: 99%

“…Whereas COUP-TFII acts mainly in directing CGE-derived cells to the caudal migratory stream (CMS) (Cai et al, 2013;Kanatani et al, 2008;Yozu et al, 2005), COUP-TFI is required for the correct balance between MGE-and CGE-derived INs in the developing neocortex (Lodato et al, 2011b), but its role in migration is less known. 5HT3aR is expressed in migrating and mature CGE-and POA-derived cells (Lee et al, 2010;Vucurovic et al, 2010) and is cell-autonomously required for the migration and positioning of RLN + INs in the neocortex (Murthy et al, 2014). Finally, SP8 and PROX1 are transcription factors expressed principally in subpopulations of lateral ganglionic eminence (LGE)/CGE-derived cortical INs (Ma et al, 2012;Rubin and Kessaris, 2013;Rudy et al, 2011) and a recent report has demonstrated a crucial role for PROX1 in the embryonic and postnatal acquisition of CGE-derived cortical IN properties (Miyoshi et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

“…The caudal ganglionic eminence (CGE) is responsible for producing lateborn INs (∼30% of all INs) (Miyoshi et al, 2010;Nery et al, 2002;Rudy et al, 2011;Vitalis and Rossier, 2011), which preferentially integrate superficial layers of the neocortex, whereas the POA contributes to a minor pool of cortical INs (Gelman et al, 2009(Gelman et al, , 2011. The serotonergic ionotropic receptor 5HT3aR (HTR3A -Mouse Genome Informatics) is expressed in the neocortex in all CGE-derived GABAergic INs, such as bipolar calretinin (CR; CALB2 -Mouse Genome Informatics)-, vasoactive intestinal peptide (VIP)-, cholecystokinin (CCK)-and reelin (RLN; RELN -Mouse Genome Informatics)-expressing cells, including multipolar or neurogliaform INs expressing neuropeptide Y (NPY), but not in PV-and SSTpositive INs (Murthy et al, 2014;Lee et al, 2010;Vucurovic et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Molecular control of two novel migratory paths for CGE-derived interneurons in the developing mouse brain

et al. 2016

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GABAergic interneurons are highly heterogeneous and originate in the subpallium mainly from the medial (MGE) and caudal (CGE) ganglionic eminences according to a precise temporal sequence. MGE-derived cells disperse dorsally and migrate towards all regions of the cortex, but little is known about how CGE-derived cells reach their targets during development. Here, we unravel the existence of two novel CGE caudo-rostral migratory streams, one located laterally (LMS) and the other one more medially (MMS), that, together with the well-known caudal migratory stream (CMS), contribute to populate the neocortex, hippocampus and amygdala. These paths appear in a precise temporal sequence and express a distinct combination of transcription factors, such as SP8, PROX1, COUP-TFI and COUP-TFII. By inactivating COUP-TFI in developing interneurons, the lateral and medial streams are perturbed and expression of SP8 and COUP-TFII affected. As a consequence, adult mutant neocortices have laminar-specific alterations of distinct cortical interneuron subtypes. Overall, we propose that the existence of spatially and temporally regulated migratory paths in the subpallium contributes to the laminar distribution and specification of distinct interneuron subpopulations in the adult brain.

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Serotonin receptor 3A controls interneuron migration into the neocortex

Cited by 78 publications

References 59 publications

Sculpting Cerebral Cortex with Serotonin in Rodent and Primate

Sculpting Cerebral Cortex with Serotonin in Rodent and Primate

Thalamo-cortical axons regulate the radial dispersion of neocortical GABAergic interneurons

Molecular control of two novel migratory paths for CGE-derived interneurons in the developing mouse brain

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