Convergent repression of Foxp2 3′UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neurons

Clovis, Yoanne; Enard, Wolfgang; Marinaro, Federica; Huttner, Wieland B.; Tonelli, Davide De Pietri

doi:10.1242/dev.078063

Cited by 127 publications

(116 citation statements)

References 89 publications

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“…Therefore, ectopic expression of FoxP2 increased the accumulation of FoxP2-positive cells in the inner layers of the mouse telencephalon. Similar results have also been reported by Tsui et al [2013] and Clovis et al [2012] in the mouse cortex. FoxP1 and FoxP2 are related proteins of the same family with highly homologous protein subdomains [Li et al, 2004].…”

Section: Discussionsupporting

confidence: 91%

FoxP1 Protein Shows Differential Layer Expression in the Parahippocampal Domain among Bird Species

Garcı́a-Calero

2016

Brain Behav Evol

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Different bird orders show diversity in neural capabilities supported by variations in brain morphology. The parahippocampal domain in the medial pallium, together with the hippocampus proper, plays an important role in memory skills. In the present work, we analyze the expression pattern of the FoxP1 protein in the parahippocampal area of four different bird species: the nonvocal learner birds quail and chicken (Galliformes) and two vocal learner birds, i.e. the zebra finch (Passeriformes) and the budgerigar (Psittaciformes), at different developmental and adult stages. We also analyze the expression of the calbindin protein in quails and zebra finches. We observed differences in the FoxP1 parahippocampal layer among bird species. In quails, chickens, and budgerigar, FoxP1 cells were located in the outer layers of the lateral and caudolateral parahippocampal sectors. In contrast, FoxP1 immunoreactive cells appeared in the inner layer of the same sectors in the zebra finch parahippocampal domain. These differences suggest two possibilities: either the FoxP1-positive cells described in quails, chickens, and budgerigars are a different population than the one described in the zebra finch, or there are changes in the pattern of radial migration in the parahippocampal area among birds. In the present study, we show that FoxP1 expression is more similar between quails, chickens, and budgerigars than between budgerigars and zebra finches in the parahippocampal area. This result contrasts with previous data in other telencephalic structures, like the calbindin-positive projection neurons described in the striatum of budgerigars and zebra finches but not in quails and chickens. All of these data point to diversity in the evolution of different morphological characters and, therefore, a mosaic model for telencephalic evolution in birds.

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Section: Discussionsupporting

confidence: 91%

FoxP1 Protein Shows Differential Layer Expression in the Parahippocampal Domain among Bird Species

Garcı́a-Calero

2016

Brain Behav Evol

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“…2B). In addition to these targets, miR-9 in combination with miR-132 suppresses the expression of Foxp2, a transcription factor known to regulate radial migration of cortical projection neurons (Clovis et al, 2012). miRNAs can also regulate the expression of doublecortin (Dcx) -one of the most studied genes in the context of neuronal migration.…”

Section: Migrationmentioning

confidence: 99%

MicroRNAs in neural development: from master regulators to fine-tuners

2017

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The proper formation and function of neuronal networks is required for cognition and behavior. Indeed, pathophysiological states that disrupt neuronal networks can lead to neurodevelopmental disorders such as autism, schizophrenia or intellectual disability. It is wellestablished that transcriptional programs play major roles in neural circuit development. However, in recent years, post-transcriptional control of gene expression has emerged as an additional, and probably equally important, regulatory layer. In particular, it has been shown that microRNAs (miRNAs), an abundant class of small regulatory RNAs, can regulate neuronal circuit development, maturation and function by controlling, for example, local mRNA translation. It is also becoming clear that miRNAs are frequently dysregulated in neurodevelopmental disorders, suggesting a role for miRNAs in the etiology and/or maintenance of neurological disease states. Here, we provide an overview of the most prominent regulatory miRNAs that control neural development, highlighting how they act as 'master regulators' or 'fine-tuners' of gene expression, depending on context, to influence processes such as cell fate determination, cell migration, neuronal polarization and synapse formation.

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“…We now report a similar negative correlation in Bengalese finches (Fig.7B). Thus, singing may promote FoxP2 mRNA degradation, possibly through miRNA regulation (Clovis et al, 2012), or inhibit mRNA synthesis following song onset. In either case, this regulation of FoxP2 takes time, only producing significant decreases 1.5h following song onset in this study (Fig.6).…”

Section: Behavioral Regulation Of Foxp2 In Songbirdsmentioning

confidence: 99%

Expression analysis of the speech-related genes FoxP1 and FoxP2 and their relation to singing behavior in two songbird species

Chen

Heston

Burkett

et al. 2013

Journal of Experimental Biology

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SUMMARYHumans and songbirds are among the rare animal groups that exhibit socially learned vocalizations: speech and song, respectively. These vocal-learning capacities share a reliance on audition and cortico-basal ganglia circuitry, as well as neurogenetic mechanisms. Notably, the transcription factors Forkhead box proteins 1 and 2 (FoxP1, FoxP2) exhibit similar expression patterns in the cortex and basal ganglia of humans and the zebra finch species of songbird, among other brain regions. Mutations in either gene are associated with language disorders in humans. Experimental knock-down of FoxP2 in the basal ganglia song control region Area X during song development leads to imprecise copying of tutor songs. Moreover, FoxP2 levels decrease naturally within Area X when zebra finches sing. Here, we examined neural expression patterns of FoxP1 and FoxP2 mRNA in adult Bengalese finches, a songbird species whose songs exhibit greater sequence complexity and increased reliance on audition for maintaining their quality. We found that FoxP1 and FoxP2 expression in Bengalese finches is similar to that in zebra finches, including strong mRNA signals for both factors in multiple song control nuclei and enhancement of FoxP1 in these regions relative to surrounding brain tissue. As with zebra finches, when Bengalese finches sing, FoxP2 is behaviorally downregulated within basal ganglia Area X over a similar time course, and expression negatively correlates with the amount of singing. This study confirms that in multiple songbird species, FoxP1 expression highlights song control regions, and regulation of FoxP2 is associated with motor control of song.

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Convergent repression of Foxp2 3′UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neurons

Cited by 127 publications

References 89 publications

FoxP1 Protein Shows Differential Layer Expression in the Parahippocampal Domain among Bird Species

FoxP1 Protein Shows Differential Layer Expression in the Parahippocampal Domain among Bird Species

MicroRNAs in neural development: from master regulators to fine-tuners

Expression analysis of the speech-related genes FoxP1 and FoxP2 and their relation to singing behavior in two songbird species

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