HeliosTranscription Factor Expression Depends onGsx2andDlx1&amp;2Function in Developing Striatal Matrix Neurons

Martín‐Ibáñez, Raquel; Crespo, Empar; Esgleas, Miriam; Urbán, Noelia; Wang, Bei; Waclaw, Ronald R.; Georgopoulos, Katia; Campbell, Kenneth; Vicario‐Abejón, Carlos; Alberch, Jordi; Chan, Susan; Kastner, Philippe; Rubenstein, John L.R.; Canals, Josep M.

doi:10.1089/scd.2011.0607

Cited by 32 publications

(40 citation statements)

References 71 publications

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“…See Table 1 for a list of all primary antibodies used in this study. The rabbit polyclonal chicken ovalbumin upstream promoter transcription factor-interacting protein 2 (CTIP2) antibody used in this study has been shown to recognize specifically deep-layer cortical neurons in developing mouse cerebral cortex (Diaz-Alonso et al, 2012;Hong et al, 2013;Chinn et al, 2015;Liu et al, 2015) and the MSNs of the developing mouse striatum (Martin-Ibanez et al, 2012), both of which have been shown to express CTIP2 in many previous studies (Arlotta et al, 2008;Desplats et al, 2008;Leone et al, 2008;Leyva-Diaz and Lopez-Bendito, 2013). Our immunohistochemical analyses in the developing striatum with this antibody showed a staining pattern of CTIP2 consistent with previous descriptions (Arlotta et al, 2008;Desplats et al, 2008;Martin-Ibanez et al, 2012).…”

Section: Antibody Characterizationsupporting

confidence: 86%

Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum

Hagimoto

Takami

Murakami

et al. 2016

J of Comparative Neurology

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The striatum, the largest nucleus of the basal ganglia controlling motor and cognitive functions, can be characterized by a labyrinthine mosaic organization of striosome/matrix compartments. It is unclear how striosome/matrix mosaic formation is spatially and temporally controlled at the cellular level during striatal development. Here, by combining in vivo electroporation and brain slice cultures, we set up a prospective experimental system in which we differentially labeled striosome and matrix cells from the time of birth and followed their distributions and migratory behaviors. Our results showed that, at an initial stage of striosome/matrix mosaic formation, striosome cells were mostly stationary, whereas matrix cells actively migrated in multiple directions regardless of the presence of striosome cells. The mostly stationary striosome cells were still able to associate to form patchy clusters via attractive interactions. Our results suggest that the restricted migratory capability of striosome cells may allow them to cluster together only when they happen to be located in close proximity to each other and are not separated by actively migrating matrix cells. The way in which the mutidirectionally migrating matrix cells intermingle with the mostly stationary striosome cells may therefore determine the topographic features of striosomes. At later stages, the actively migrating matrix cells began to repulse the patchy clusters of striosomes, presumably enhancing the striosome cluster formation and the segregation and eventual formation of dichotomous homogeneous striosome/matrix compartments. Overall, our study reveals temporally distinct migratory behaviors of striosome/matrix cells, which may underlie the sequential steps of mosaic formation in the developing striatum. J. Comp. Neurol. 525:794-817, 2017. © 2016 Wiley Periodicals, Inc.

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Section: Antibody Characterizationsupporting

confidence: 86%

Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum

Hagimoto

Takami

Murakami

et al. 2016

J of Comparative Neurology

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“…S1" type="url"/>) until P15 peaking at E18.5 (Martín-Ibáñez et al, 2012). He showed preferential expression in D2R-eGFP neurons (mean±s.e.m.…”

Section: Resultsmentioning

confidence: 99%

“…He- expressing cells are derived from radial glial cells, as its expression disappears in Gsx2 knockout mice (Martín-Ibáñez et al, 2012). However, He loss does not compromise the number of the radial glial cell subtypes described elsewhere (Pilz et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Helios expression coordinates the development of a subset of striatopallidal medium spiny neurons

et al. 2017

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Here, we unravel the mechanism of action of the Ikaros family zinc finger protein Helios (He) during the development of striatal medium spiny neurons (MSNs). He regulates the second wave of striatal neurogenesis involved in the generation of striatopallidal neurons, which express dopamine 2 receptor and enkephalin. To exert this effect, He is expressed in neural progenitor cells (NPCs) keeping them in the G1/G0 phase of the cell cycle. Thus, a lack of He results in an increase of S-phase entry and S-phase length of NPCs, which in turn impairs striatal neurogenesis and produces an accumulation of the number of cycling NPCs in the germinal zone (GZ), which end up dying at postnatal stages. Therefore, He−/− mice show a reduction in the number of dorso-medial striatal MSNs in the adult that produces deficits in motor skills acquisition. In addition, overexpression of He in NPCs induces misexpression of DARPP-32 when transplanted in mouse striatum. These findings demonstrate that He is involved in the correct development of a subset of striatopallidal MSNs and reveal new cellular mechanisms for neuronal development.

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“…The zinc finger transcription factors Ikaros and Helios have also been implicated in striatal neuron development downstream of Gsx2 and Dlx genes (46,47). Moreover, Ikaros has been associated with the differentiation of a subpopulation of Enkexpressing striatopallidial neurons (46,48).…”

Section: Significancementioning

confidence: 99%

The LIM homeobox geneIsl1is required for the correct development of the striatonigral pathway in the mouse

Ehrman

Waclaw

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The mammalian striatum controls the output of the basal ganglia via two distinct efferent pathways, the direct (i.e., striatonigral) and the indirect (i.e., striatopallidal) pathways. The LIM homeodomain transcription factor Islet1 (Isl1) is expressed in a subpopulation of striatal progenitors; however, its specific role in striatal development remains unknown. Our genetic fate-mapping results show that Isl1-expressing progenitors give rise to striatal neurons belonging to the striatonigral pathway. Conditional inactivation of Isl1 in the telencephalon resulted in a smaller striatum with fewer striatonigral neurons and reduced projections to the substantia nigra. Additionally, conditional inactivation in the ventral forebrain (including both the telencephalon and diencephalon) revealed a unique role for Isl1 in diencephalic cells bordering the internal capsule for the normal development of the striatonigral pathway involving PlexinD1-Semaphorin 3e (Sema3e) signaling. Finally, Isl1 conditional mutants displayed a hyperlocomotion phenotype, and their locomotor response to psychostimulants was significantly blunted, indicating that the alterations in basal ganglia circuitry contribute to these mutant behaviors.caudate-putamen | direct pathway | indirect pathway T he basal ganglia control many aspects of human behavior, including purposeful movements and appropriate behaviors, that are affected in childhood neurological disorders such as Tourette's syndrome and attention deficit hyperactivity disorder (ADHD) (1, 2). The striatum, also known as the caudate-putamen, represents the major component of the basal ganglia and is central in the processing of cortical information (reviewed in ref.3). Moreover, the striatum controls the output of the basal ganglia through two distinct efferent pathways: the direct (i.e., striatonigral) pathway and the indirect (i.e., striatopallidal) pathway. Both of these projection neuron subtypes use the inhibitory neurotransmitter gamma aminobutyric acid (GABA) (4). In addition to their different axonal targets, these two projection neuron subtypes express distinct neurochemical characteristics. The striatonigral projection neurons contain the neuropeptide substance P and express the dopamine D1 receptor at high levels (5, 6). Conversely, the striatopallidal projection neurons contain the neuropeptide enkephalin and high levels of the dopamine D2 receptor (5, 6). These two efferent pathways functionally oppose each other and thereby provide a balanced output from the basal ganglia (7). This balance is believed to be crucial for normal motor control (8).Striatal-projection neurons are known to derive from the lateral ganglionic eminence (LGE) (9-12) whereas their interneuron counterparts are derived from an adjacent domain, the medial ganglionic eminence (MGE) (11,13,14). Within the LGE, two developmental compartments have been identified: the ventral (v) LGE and the dorsal (d)LGE (15, 16). The vLGE is proposed to be the source of striatal-projection neurons (16) whereas the dLGE is thou...

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HeliosTranscription Factor Expression Depends onGsx2andDlx1&2Function in Developing Striatal Matrix Neurons

Cited by 32 publications

References 71 publications

Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum

Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum

Helios expression coordinates the development of a subset of striatopallidal medium spiny neurons

The LIM homeobox geneIsl1is required for the correct development of the striatonigral pathway in the mouse

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