Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons.

paper Cited Public

Authors: McKinsey, Gabriel L; Lindtner, Susan; Trzcinski, Brett; Visel, Axel; Pennacchio, Len A; Huylebroeck, Danny; Higashi, Yujiro; Rubenstein, John L R
Year: 2013
Journal: Neuron
PMID: 23312518
DOI: 10.1016/j.neuron.2012.11.035
PMCID: PMC3547499

Figure 1

Zfhx1b expression in the MGE is required for interneuron migration at E12.5. (A-C) Zfhx1b RNA expression detected by in situ hybridization in control and conditional Zfhx1b mutant telencephalons. (B) Nkx2.1-Cre. (C) DlxI12b-Cre. Black arrowhead in B shows loss of Zfhx1b expression in the MGE VZ (except dorsal-most MGE). White arrowheads in B and C show loss of Zfhx1b expression in the SVZ of the MGE. X in B shows loss of Zfhx1b expression in the SVZ/MZ of the LGE. (D-P’) Coronal hemisections of the telencephalon comparing gene expression in three rostral-to-caudal planes of section in control (left side) and Zfhx1b Nkx2.1-Cre conditional mutants (right side). (D-F’) Two color immunofluoresence detection of EGFP (green) and NKX2-1 (red). (G,G’) Higher magnification view of two color immunofluoresence detection of EGFP (green) and Nkx2-1 (red) in control (G) and Zfhx1b mutant (G’). Solid white arrowheads show increased numbers of cells that express both EGFP (green) and NKX2-1 (red) in the mutant's LGE/Str. In the wild type cortex, black arrowheads (with white outline) show that cells express EGFP (green) and not NKX2-1. (H-P’) In situ hybridization expression analysis at E12.5 of Nkx2-1 (H-J’) and Lhx6 (K-M’), and at E13.5 of Nkx2-1 (N-P’). Asterisks in (N-P’) show increased numbers of labeled cells in striatum. X in panels (K’-M’) notes the loss of labeled cells in the cortex. Abbreviations: Cx: cortex; e: ectopia in region of the ventral striatum and central nucleus of the amygdala; GP: globus pallidus; LGE: lateral ganglionic eminence; MGE: medial ganglionic eminence; MZ: mantle zone; Str: Striatum; SVZ: subventricular zone; VPd: ventral pallidum; VZ: ventricular zone. Scale bars equal 500μm (A and D), and 300 μm (G).

Figure 2

Zfhx1b expression in the MGE is required for interneuron migration at E15.5. Coronal hemisections of the telencephalon comparing gene expression in three rostral-to-caudal planes of section in control (left side) and Zfhx1b;Nkx2.1-Cre conditional mutants (right side). (A-C’) Two color immunofluoresence detection of EGFP (green) and NKX2-1 (red). (D-U’) In situ hybridization analysis. Nkx2-1 (D-F’), Lhx6 (G-I’), Sox6 (J-L’), Lhx8 (M-O’), NPY (P-R’), Kcnmb4 (S-U’). Asterisks show increased numbers of labeled cells in the striatum. X shows reduced number of labeled cells in cortex. Abbreviations: CGE: caudal ganglionic eminence; Cx: cortex; e: ectopia in region of the ventral striatum and central nucleus of the amygdala; GP: globus pallidus; LGE: lateral ganglionic eminence; MGE: medial ganglionic eminence; MZ: mantle zone; Str: striatum; SVZ: subventricular zone; VPd: ventral pallidum; VZ: ventricular zone. Scale bar equals 500μm (A).

Figure 3

Zfhx1b expression in the SVZ of the MGE is required for interneuron migration at E15.5. Coronal hemisections of the telencephalon comparing gene expression in three rostral-to-caudal planes of section in control (left side) and Zfhx1b DlxI12b-Cre conditional mutants (right side). In situ hybridization analysis of: Nkx2-1 (A-C’), Lhx6 (D-F’), Sox6 (G-I’), Lhx8 (P-R’), NPY (M-O’), Kcnmb4 (P-R’). Asterisks show increased numbers of labeled cells in the striatum. X shows reduced number of Lhx6+ cells in cortex. Abbreviations: CGE: caudal ganglionic eminence; Cx: cortex; e: ectopia in region of the ventral striatum and central nucleus of the amygdala; GP: globus pallidus; LGE: lateral ganglionic eminence; MGE: medial ganglionic eminence; MZ: mantle zone; Str: striatum; SVZ: subventricular zone; VPd: ventral pallidum; VZ: ventricular zone. Scale bar equals 500μm (A).

Figure 4

Zfhx1b expression in the MGE regulates the numbers and fate of postnatal (P0 and P15) cortical and striatal interneurons. Coronal hemisections showing the neocortex (A-F) and the striatum (G-R), comparing gene expression in control (left side) and Zfhx1b;Nkx2.1-Cre conditional mutants (right side). (A, A’, D- F’ G,G’,M,M’) Two color immunofluorescence with anti-EGFP (Cre reporter; green) and interneuron markers (red); other panels show in situ hybridization results. (S) Cell counts, control relative to mutant, of: total Cre-reporter EGFP+ cell numbers in the P0 and P15 cortex (left); of the number of cells that had colocalization of the EGFP Cre-reporter with Sst or PV at P15 (middle); of the total levels of Sst and PV in the P15 cortex (right). (T) Cell counts, control relative to mutant, of: EGFP+ Cre-reporter cells in the P15 striatum (left); of EGFP-colocalization with PV, Sst and nNos in the P15 striatum (middle); of the total numbers of the markers PV, Sst, nNos, NPY, TacR1 and TrkA in the P15 striatum (right). Scale bar equals 500μm (A,D, G and M). *: p<.05; **: p<.01.

Figure 5

Dlx1&2 are required for Zfhx1b expression in the SVZ of the subpallium. (A-B’) Coronal hemisections of the telencephalon comparing Zfhx1b expression in Dlx1/+/- and Dlx1/2-/- at E12.5 (A-A’) and E15.5 (B,B’). Note the greatly reduced Zfhx1b expression in the SVZ of the LGE and MGE. X notes reduction in Zfhx1b expression in the SVZ. (C-K) Regulatory elements near Zfhx1b that drive subpallial expression are bound by DLX2 in vivo, and are positively regulated by DLX2. (C) Relative genomic position of two ultraconserved DNA elements near the Human Zfhx1b (Zeb2) locus, #675 (D) and #649 (E) (data from http://genome.ucsc.edu/). (D and E) Genomic alignment of enhancers #675 and #649; each contain a number of conserved consensus homeobox sites (asterisks). (F and G) Base-resolution view of regions with homeobox sites within #649 and #675, which are heavily conserved across vertebrate species and are similar to known DLX2 binding sites (Potter et al., 2008). (H and I) Whole mount E11.5 enhancer-lacZ transgenic mouse embryos that demonstrated lacZ expression (X-Gal staining) in the ganglionic eminences (subpallium) (H’ and I’). (J) Luciferase assay demonstrating DLX2-dependent transcriptional activation (pCAGGS vector) mediated by enhancers #649 and #675 upstream of luciferase (pGL4.23 vector). (K) Blue bars: DLX2 ChIP qPCR assay (N=3) demonstrates anti-DLX2 binding to chromatin from E13.5 ganglionic eminences to subdomains of enhancers #675 and #649 and the positive control (Dlx5/6 enhancer), and not to the negative control region (a non-conserved domain upstream of Dlx2). Red bars: Addition of a DLX2 peptide blocks the anti-DLX2 binding. Abbreviations: Cx: cortex; LGE: lateral ganglionic eminence; Luc. Luciferase; MGE: medial ganglionic eminence; MZ: mantle zone; SP: subpallium; SVZ: subventricular zone, VZ: ventricular zone. Scale bar equals 500μm (A and B). ***: p<.001; n.s. : not significant.

Figure 6

Zfhx1b;Nkx2.1-Cre and Dlx1/2-/- mutants both fail to repress Nkx2-1 and Sox6, lose cortical interneurons, and accumulate MGE cells in their striatum. Coronal hemisections of the E15.5 telencephalon comparing gene expression in three rostral-to-caudal planes of section in controls (left side) and mutants (right side). In situ hybridization analysis of Nkx2-1 (A-C”), Lhx6 (D-F”), Sox6 (G-I”), NPY (J-L”) expression was assessed for control, Zfhx1b;Nkx2.1-Cre mutants and Dlx1/2-/- mutants. Asterisks show increased numbers of labeled cells in the striatum. X shows reduced number of Lhx6+ cells in cortex. Abbreviations: CGE: caudal ganglionic eminence; Cx: cortex; e: ectopia in region of the ventral striatum and central nucleus of the amygdala; GP: globus pallidus; LGE: lateral ganglionic eminence; MGE: medial ganglionic eminence; MZ: mantle zone; Str: striatum; SVZ: subventricular zone; VPd: ventral pallidum; VZ: ventricular zone. Scale bar equals 500μm (A).

Figure 7

cMaf and CXCR7 are highly specific markers of the cortical interneuron lineage that are lost in Zfhx1b conditional mutants and Dlx1/2-/- mutants. Coronal hemisections of the E12.5 (A-F”) and E15.5 (G-L”) telencephalon comparing cMaf (A-C”; G-I”) and CXCR7 (D-F”; J-L”) RNA expression by in situ hybridization in three rostral-to-caudal planes of section in control (left panels), Zfhx1b;Nkx2.1-Cre conditional mutants (middle panels), and Dlx1/2-/- mutants (right panels). X shows reduced/absent cMaf+ or CXCR7+ cells in cortex or ganglionic eminences. Abbreviations: CGE: caudal ganglionic eminence; ChP: choroid plexus; Cx: cortex; LGE Co: LGE corridor; dMGE: dorsal medial ganglionic eminence; vMGE: ventral medial ganglionic eminence; Str: striatum. Scale bars are equal to 500μm (A) and 200uM (M).

#	Section	Preview
20	Results — Deleting Zfhx1b in SVZ of the MGE Using DlxI12b-Cre Phenocopies Loss of Zfhx1b function in the VZ (Nkx2.1-Cre) — Postnatal Analysis of cortical and striatal interneuron phenotypes in Nkx2.1-Cre;Zfhx1b mutants	We analyzed postnatal day 0 (P0) and P15 Nkx2.1-Cre;Zfhx1bF/- conditional mutants to better…
21	Results — Deleting Zfhx1b in SVZ of the MGE Using DlxI12b-Cre Phenocopies Loss of Zfhx1b function in the VZ (Nkx2.1-Cre) — Postnatal Analysis of cortical and striatal interneuron phenotypes in Nkx2.1-Cre;Zfhx1b mutants	In the striatum at P0, as we saw at E15.5, there was an increase in the number of cells expressing…
22	Results — Deleting Zfhx1b in SVZ of the MGE Using DlxI12b-Cre Phenocopies Loss of Zfhx1b function in the VZ (Nkx2.1-Cre) — Postnatal Analysis of cortical and striatal interneuron phenotypes in Nkx2.1-Cre;Zfhx1b mutants	As NPY, Sst, and nNos are also expressed in subsets of cortical interneurons, their increased…
23	Results — Deleting Zfhx1b in SVZ of the MGE Using DlxI12b-Cre Phenocopies Loss of Zfhx1b function in the VZ (Nkx2.1-Cre) — Postnatal Analysis of cortical and striatal interneuron phenotypes in Nkx2.1-Cre;Zfhx1b mutants	At P15 the number of mutant cells (EGFP+) was roughly the same as in controls, and they were evenly…
24	Results — Deleting Zfhx1b in SVZ of the MGE Using DlxI12b-Cre Phenocopies Loss of Zfhx1b function in the VZ (Nkx2.1-Cre) — Postnatal Analysis of cortical and striatal interneuron phenotypes in Nkx2.1-Cre;Zfhx1b mutants	Despite the cell death, Zfhx1b conditional mutants at P15 continued to have significantly increased…
25	Results — Deleting Zfhx1b in SVZ of the MGE Using DlxI12b-Cre Phenocopies Loss of Zfhx1b function in the VZ (Nkx2.1-Cre) — Postnatal Analysis of cortical and striatal interneuron phenotypes in Nkx2.1-Cre;Zfhx1b mutants	We also analyzed the gross morphological properties of nNos/NPY/Sst striatal interneurons in the…
26	Results — Zfhx1b Expression Is downstream of Dlx1/2 in the Developing Basal Ganglia	Dlx1 and Dlx2 are necessary for subpallial development, including interneuron migration to the…
27	Results — Zfhx1b Expression Is downstream of Dlx1/2 in the Developing Basal Ganglia	Towards defining the mechanisms that regulate Zfhx1b expression in the developing subpallium, we…
28	Results — Zfhx1b Expression Is downstream of Dlx1/2 in the Developing Basal Ganglia	To test whether Dlx2 can regulate these candidate Zfhx1b enhancers we used a luciferase reporter…
29	Results — Zfhx1b Expression Is downstream of Dlx1/2 in the Developing Basal Ganglia	To determine whether DLX2 directly regulates enhancers 649 or 675, we performed chromatin…
30	Results — Zfhx1b Expression Is downstream of Dlx1/2 in the Developing Basal Ganglia	In summary, we have identified two candidate distant-acting gene regulatory elements whose activity…
31	Results — Dlx1/2-/- Constitutive and Zfhx1b Conditional Mutants Have Similar Changes in Gene Expression Related to Their Defects in Interneuron Migration	As Zfhx1b expression in the subpallial SVZ was greatly reduced in the Dlx1/2 mutants (Figures…
32	Results — Dlx1/2-/- Constitutive and Zfhx1b Conditional Mutants Have Similar Changes in Gene Expression Related to Their Defects in Interneuron Migration	Indeed, changes in Nkx2-1 and Sox6 expression were similar in the Dlx1/2-/- and Zfhx1b mutants.…
33	Results — Dlx1/2-/- Constitutive and Zfhx1b Conditional Mutants Have Similar Changes in Gene Expression Related to Their Defects in Interneuron Migration	Lhx6+ cells are lacking throughout the cortex and increased in the striatum of both the Dlx1/2-/-…
34	Results — RNA Expression Array Analysis Identifies Candidate Mediators of Zfhx1b Function	Towards identifying the molecular mechanisms underlying the Zfhx1b mutant phenotype we used an RNA…
35	Results — RNA Expression Array Analysis Identifies Candidate Mediators of Zfhx1b Function	We were most interested in genes that were altered in both the Nkx2.1-Cre and DlxI12b-Cre Zfhx1b…
36	Results — RNA Expression Array Analysis Identifies Candidate Mediators of Zfhx1b Function	Dlk1 expression was strongly increased in the VZ and SVZ of the MGE in the Nkx2.1-Cre mutant, and…
37	Results — RNA Expression Array Analysis Identifies Candidate Mediators of Zfhx1b Function	Other genes related to Notch-signaling were also identified in the array analysis, including the Id2…
38	Results — RNA Expression Array Analysis Identifies Candidate Mediators of Zfhx1b Function	Expression of Cited1, a p300-binding transcriptional co-activator that promotes signaling in the…
39	Results — RNA Expression Array Analysis Identifies Candidate Mediators of Zfhx1b Function	Expression of genes related to oligodendrogenesis, including Olg1 and GPR17 (Chen et al., 2009; Lu…

Name	Type
antisense riboprobe local	drug
apoptosis	phenotype
Ascl1	gene
basal ganglia	anatomy
basal telencephalon local	anatomy
Beta-Actin Cre local	drug
Beta-Actin Cre mice local	cohort
blood cells local	anatomy
body weight	phenotype
CAG-CAT-eGFP local	drug
CAG-CAT-EGFP local	drug
CAG:CAT-EGFP local	drug
CAG:CAT-EGFP Cre reporter allele local	drug
CAG-CAT-eGFP mice local	cohort
CALB2	gene
Calbindin (CB) expressing interneurons local	phenotype
Calretinin (CR) expressing interneurons local	phenotype
CASP6 local	gene
Caudal amygdala local	anatomy
caudoventral medial ganglionic eminence local	anatomy
Caudoventral striatum local	anatomy
central amygdala	anatomy
CGE local	anatomy
Chat	gene
cholinergic neurons	phenotype
cholinergic striatal interneuron local	phenotype
cholinergic striatal interneurons local	phenotype
choroid plexus	anatomy
Cited1 local	gene
CITED1 local	gene
Conditional mutant embryos local	cohort
conditional Zfhx1b mutants local	cohort
control	cohort
control littermates local	cohort
corpus callosum	anatomy
cortex	anatomy
cortical interneuron development local	phenotype
cortical interneuron lineage local	phenotype
cortical interneurons fail to be specified local	phenotype
cortical interneuron subtypes local	phenotype
cortical plate	anatomy
Cortical projection neurons local	anatomy
CR+ cells local	phenotype
Cre local	drug
CRE local	drug
CUX2	gene
Cxcr7	gene
defects in differentiation and interneuron migration local	phenotype
developing cortical interneurons local	phenotype
Dlk1	gene
Dlx local	gene
Dlx1	gene
Dlx1/2 local	gene
Dlx1/2-/- local	variant
Dlx1/2-deficient mice local	cohort
Dlx1/2-/- mutant local	cohort
Dlx1/2-/- mutants local	cohort
DLX1/2-/- mutants local	cohort
Dlx2	gene
Dlx5	gene
Dlx5/6-Cre local	drug
DlxI12b-Cre local	cohort
DlxI12b-Cre local	drug
DlxI12b-Cre local	gene
DlxI1/2b-Cre local	drug
DlxI1/2b-Cre allele local	drug
DlxI12b-Cre mutant local	cohort
DlxI1/2b-Cre mutant local	cohort
DlxI12b-Cre Zfhx1b mutants local	cohort
dorsal MGE local	anatomy
dorsal MGE-derived cortical interneurons local	phenotype
Ectopia local	phenotype
eGFP	drug
EGFP+ cells local	phenotype
embryonic basal ganglia local	anatomy
Embryonic brain	anatomy
enhancer 649 local	variant
Enhancer #649 local	variant
enhancer 675 local	variant
Enhancer #675 local	variant
enhancer element local	drug
epilepsy	phenotype
exon 7 local	variant
FGF	drug
Fgf9 local	gene
forebrain	anatomy
Fugene 6	drug
GABA	phenotype
GABAergic cortical interneurons local	phenotype
GABAergic projection neurons local	phenotype
GABAergic striatal interneurons local	anatomy
GABAergic striatal interneurons local	phenotype
ganglionic eminences local	anatomy
Gbx2	gene
globus pallidus	anatomy
Glypicans local	gene
GPC4 local	gene
GPR17 local	gene
hindbrain	anatomy
hippocampal progenitors local	anatomy
Hirschsprung disease local	phenotype
I1/2b-Cre local	drug
Id2 local	gene
Id4 local	gene
ID4 local	gene
immature cortical interneurons local	phenotype
Immature cortical interneurons local	phenotype
immature migrating cortical interneurons local	phenotype
increased striatal TACR1 expression local	phenotype
interneuron	phenotype
interneuron migration	phenotype
Interneuron migration to the cortex local	phenotype
interneuron phenotype local	phenotype
interneuron tangential migration local	phenotype
Isl1	gene
Islet1 local	gene
Kcnmb4	gene
Kctd12 local	gene
LacZ local	drug
lateral ganglionic eminence	anatomy
lateral ganglionic eminence (LGE) local	anatomy
LGE	anatomy
LGE corridor local	anatomy
Lhx6	gene
Lhx6+ cells local	phenotype
Lhx6 expressing interneurons local	phenotype
Lhx8	gene
luciferase	drug
MAF	gene
Mafb local	gene
MafB local	gene
MAFB local	gene
Matrisomes local	anatomy
medial ganglionic eminence	anatomy
medial ganglionic eminence (MGE) local	anatomy
medium spiny neurons	anatomy
mental retardation	phenotype
MGE-derived interneurons local	phenotype
MGE SVZ local	anatomy
migrating cortical interneurons local	phenotype
migration defect of MGE derivatives local	phenotype
MKI67	gene
Mowat-Wilson syndrome local	phenotype
mutants local	cohort
MZ	anatomy
neocortex	anatomy
neocortical neurons local	anatomy
neurological/behavioral phenotypes local	phenotype
Neurotrophin-3 local	gene
NKX2-1	gene
Nkx2.1-Cre local	cohort
Nkx2.1-Cre local	drug
Nkx2.1-Cre local	gene
Nkx2.1-Cre local	variant
Nkx2.1-Cre allele local	drug
Nkx2.1-Cre conditional mutants local	cohort
Nkx2.1-Cre I1/2b-Cre mice local	cohort
Nkx2.1-Cre mutant local	cohort
Nkx2.1-Cre;Zfhx1bF/- conditional mutants local	cohort
Nkx2.1-Cre Zfhx1b mutants local	cohort
Nkx2.1-Cre;Zfhx1b mutants local	cohort
nNos/NPY/Sst striatal interneurons local	phenotype
Nos1	gene
Npn1 local	gene
Npn2 local	gene
NPY	gene
NPY+ cells local	phenotype
NTRK1	gene
Olg1 local	gene
Olg2 local	gene
oligodendrocytes	phenotype
Overproduction of nNos/NPY/Sst interneurons local	phenotype
P0 local	cohort
P15 local	cohort
pallial interneuron local	phenotype
pallial interneurons local	phenotype
pallidal projection neurons local	phenotype
pallium	anatomy
Parvalbumin	gene
Parvalbumin (PV) expressing interneurons local	phenotype
pCAGGS-Dlx2 local	drug
pCAGGs-empty local	drug
pGL4.23-empty local	drug
pGL4.23-enhancer local	drug
pGL4.73 local	drug
POA local	anatomy
postnatal brain	anatomy
preoptic area local	anatomy
Promega Dual-Luciferase Assay Kit local	drug
PV local	phenotype
Pvalb	gene
Renilla luciferase	gene
rostrodorsal medial ganglionic eminence local	anatomy
Sema3 local	gene
Shh	gene
Shh-Cre local	drug
Similar gross morphological properties local	phenotype
SMAD local	gene
Somatostatin (Sst) expressing interneurons local	phenotype
Sox6	gene
Sst	gene
Sst local	phenotype
Sst+ interneurons	phenotype
striatal GABAergic interneuron local	phenotype
striatal GABAergic interneurons local	phenotype
striatal interneurons	phenotype
striatal projection neurons local	phenotype
striatal PV interneurons local	phenotype
striatum	anatomy
Striosomes	anatomy
subpallial ectopia local	phenotype
Subpallial projection neurons local	phenotype
subpallial SVZ local	anatomy
Subpallial SVZ local	anatomy
subpallial telencephalon local	anatomy
subpallial VZ local	anatomy
subpallium	anatomy
substance P	drug
subventricular zone	anatomy
supernumerary cells local	phenotype
SVZ	anatomy
SVZ of MGE local	anatomy
TacR1	gene
tangential migration local	phenotype
Tangential migration local	phenotype
telencephalon	anatomy
TGFβ	drug
Unc5b	gene
ventral MGE local	anatomy
ventral pallidum	anatomy
ventricular zone	anatomy
VZ	anatomy
Wildtype local	cohort
ZEB2	gene
Zfhx1a local	gene
Zfhx1b+/- local	variant
Zfhx1b conditional mutant local	cohort
Zfhx1b conditional mutants local	cohort
Zfhx1b conditional (Nkx2.1-Cre) mutant local	cohort
Zfhx1bF/+ control littermates local	cohort
Zfhx1bF/F local	variant
Zfhx1bF/F mice local	cohort
Zfhx1bF/- mutants local	cohort
Zfhx1b heterozygotes (control) local	cohort
Zfhx1b+/- mice local	cohort
Zfhx1b mutant local	cohort
Zfhx1b_mutant local	cohort
Zfhx1b mutant phenotype local	phenotype
Zfhx1b mutants local	cohort
Zfhx1b mutants local	variant
Zfhx1b-Nkx2.1-Cre mutants local	cohort
Zfhx1b null allele local	variant
Zfhx1b-/- phenotype local	phenotype

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In this knowledge base

Title	Year	PMID
A genome wide association study of fast beta EEG in families of European ancestry.	2017	28040410
Single-Cell Profiling of an In Vitro Model of Human Interneuron Development Reveals Temporal Dynamics of Cell Type Production and Maturation.	2017	28279351

External

Title	Authors	Journal	Year	Link
Aberrant medial ganglionic eminence (MGE) GABAergic neurogenesis contributes to Huntington's disease pathogenesis.	Molero AE et al.	—	2026	→
Modeling Mowat-Wilson syndrome with patient iPSCs reveals transcriptional and phenotypic defects in neural progenitors.	Musante I et al.	—	2026	→
Transcription factor ZEB2 is essential for ureteral smooth muscle cell differentiation.	Kumar S et al.	—	2026	→
Comparing great apes reveals human-specific ZEB2 roles in neural development.	Lee JE et al.	—	2025	→
DNMT1-mediated regulation of somatostatin-positive interneuron migration impacts cortical architecture and function.	Reichard J et al.	—	2025	→
Human stem cell-derived GABAergic interneuron development reveals early emergence of subtype diversity and gradual electrochemical maturation.	Bershteyn M et al.	—	2025	→
Identifying similar populations across independent single cell studies without data integration.	González-Velasco O et al.	—	2025	→
Metastasis and chemoresistance in breast cancer: Crucial function of ZEB1/2 proteins.	Doodmani SM et al.	—	2025	→
Transcriptomic insights into fate choice of pallial versus subpallial GABAergic neurons.	Sun L et al.	—	2025	→
ZEB2 Gene Pathogenic Variants Across Protein-Coding Regions and Impact on Clinical Manifestations: A Review.	Hossain WA et al.	—	2025	→
Developmental trajectories of GABAergic cortical interneurons are sequentially modulated by dynamic <i>FoxG1</i> expression levels.	Miyoshi G et al.	—	2024	→
DLX genes and proteins in mammalian forebrain development.	Rubenstein JL et al.	—	2024	→
DNMT1-Mediated Regulation of Somatostatin-positive Interneuron Migration Impacts Cortical Architecture and Function	Reichard J et al.	—	2024	—
Human pallial MGE-type GABAergic interneuron cell therapy for chronic focal epilepsy.	Bershteyn M et al.	—	2023	→
Interneuron odyssey: molecular mechanisms of tangential migration.	Toudji I et al.	—	2023	→
Neuronal Transplantation for Alzheimer's Disease and Prospects for Generating Exogenic Neurons as a Source of Cells for Implantation.	Strell P et al.	—	2023	→
Single-Cell Transcriptomics Reveals Conserved Regulatory Networks in Human and Mouse Interneuron Development.	Keefe F et al.	—	2023	→
Transcriptional regulation of EMT transcription factors in cancer.	Saitoh M	—	2023	→
Zeb2 DNA-Binding Sites in Neuroprogenitor Cells Reveal Autoregulation and Affirm Neurodevelopmental Defects, Including in Mowat-Wilson Syndrome.	Birkhoff JC et al.	—	2023	→
Genetics behind Cerebral Disease with Ocular Comorbidity: Finding Parallels between the Brain and Eye Molecular Pathology.	Chang KJ et al.	—	2022	→
Interneuron development and dysfunction.	Yang J et al.	—	2022	→
Single cell enhancer activity distinguishes GABAergic and cholinergic lineages in embryonic mouse basal ganglia.	Su-Feher L et al.	—	2022	→
St18 specifies globus pallidus projection neuron identity in MGE lineage.	Nunnelly LF et al.	—	2022	→
Targeting prefrontal cortex GABAergic microcircuits for the treatment of alcohol use disorder.	Fish KN et al.	—	2022	→
Transcriptional heterogeneity of ventricular zone cells in the ganglionic eminences of the mouse forebrain.	Lee DR et al.	—	2022	→
Transcriptional regulation of neuronal identity.	Sousa E et al.	—	2022	→
ZEB2 haploinsufficient Mowat-Wilson syndrome induced pluripotent stem cells show disrupted GABAergic transcriptional regulation and function.	Schuster J et al.	—	2022	→
Further delineation and long-term evolution of electroclinical phenotype in Mowat Wilson Syndrome. A longitudinal study in 40 individuals.	Ricci E et al.	—	2021	→
<i>In vivo</i> Direct Conversion of Astrocytes to Neurons Maybe a Potential Alternative Strategy for Neurodegenerative Diseases.	Wang Y et al.	—	2021	→
MicroRNA miR-215-5p Regulates Doxorubicin-induced Cardiomyocyte Injury by Targeting ZEB2.	Xiong X et al.	—	2021	→
Neurological Phenotype of Mowat-Wilson Syndrome.	Cordelli DM et al.	—	2021	→
The Epigenome in Neurodevelopmental Disorders.	Reichard J et al.	—	2021	→
The Type 3 Deiodinase Is a Critical Modulator of Thyroid Hormone Sensitivity in the Fetal Brain.	Martinez ME et al.	—	2021	→
ZEB2, the Mowat-Wilson Syndrome Transcription Factor: Confirmations, Novel Functions, and Continuing Surprises.	Birkhoff JC et al.	—	2021	→
Zinc Finger Proteins in Neuro-Related Diseases Progression.	Bu S et al.	—	2021	→
Dlx1/2 mice have abnormal enteric nervous system function.	Wright CM et al.	—	2020	→
Dopamine as a growth differentiation factor in the mammalian brain.	Ohira K	—	2020	→
Dysregulation of Hypothalamic Gene Expression and the Oxytocinergic System by Soybean Oil Diets in Male Mice.	Deol P et al.	—	2020	→
EMT-Inducing Transcription Factors, Drivers of Melanoma Phenotype Switching, and Resistance to Treatment.	Tang Y et al.	—	2020	→
Gene therapy conversion of striatal astrocytes into GABAergic neurons in mouse models of Huntington's disease.	Wu Z et al.	—	2020	→
Multifaceted actions of Zeb2 in postnatal neurogenesis from the ventricular-subventricular zone to the olfactory bulb.	Deryckere A et al.	—	2020	→
Regeneration of Functional Neurons After Spinal Cord Injury via <i>in situ</i> NeuroD1-Mediated Astrocyte-to-Neuron Conversion.	Puls B et al.	—	2020	→
Successful treatment of drug-resistant status epilepticus in an adult patient with Mowat-Wilson syndrome: A case report.	Nosaki Y et al.	—	2020	→
Targeted chromatin conformation analysis identifies novel distal neural enhancers of ZEB2 in pluripotent stem cell differentiation.	Birkhoff JC et al.	—	2020	→
Zeb2 Is a Regulator of Astrogliosis and Functional Recovery after CNS Injury.	Vivinetto AL et al.	—	2020	→
Zeb2 regulates the balance between retinal interneurons and Müller glia by inhibition of BMP-Smad signaling.	Menuchin-Lasowski Y et al.	—	2020	→
Dlx1/2 are Central and Essential Components in the Transcriptional Code for Generating Olfactory Bulb Interneurons.	Guo T et al.	—	2019	→
Early embryonic NG2 glia are exclusively gliogenic and do not generate neurons in the brain.	Huang W et al.	—	2019	→
Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders.	Sohal VS et al.	—	2019	→
Functional characterization of the ZEB2 regulatory landscape.	Bar Yaacov R et al.	—	2019	→
Mafb and c-Maf Have Prenatal Compensatory and Postnatal Antagonistic Roles in Cortical Interneuron Fate and Function.	Pai EL et al.	—	2019	→
Role of Zeb2/Sip1 in neuronal development.	Epifanova E et al.	—	2019	→
Sleep in Mowat-Wilson Syndrome: a clinical and video-polysomnographic study.	Di Pisa V et al.	—	2019	→
Sp9 Regulates Medial Ganglionic Eminence-Derived Cortical Interneuron Development.	Liu Z et al.	—	2019	→
The Transcription Factor LHX1 Regulates the Survival and Directed Migration of POA-derived Cortical Interneurons.	Symmank J et al.	—	2019	→
Transcription Factors <i>Sp8</i> and <i>Sp9</i> Regulate Medial Ganglionic Eminence-Derived Cortical Interneuron Migration.	Tao G et al.	—	2019	→
Transcription factors Sp8 and Sp9 regulate the development of caudal ganglionic eminence-derived cortical interneurons.	Wei S et al.	—	2019	→
Zinc finger proteins in psychiatric disorders and response to psychotropic medications.	Squassina A et al.	—	2019	→
A Zeb2-miR-200c loop controls midbrain dopaminergic neuron neurogenesis and migration.	Yang S et al.	—	2018	→
Development and Functional Diversification of Cortical Interneurons.	Lim L et al.	—	2018	→
Diverse facets of cortical interneuron migration regulation - Implications of neuronal activity and epigenetics.	Zimmer-Bensch G	—	2018	→
Dlx1 and Dlx2 Promote Interneuron GABA Synthesis, Synaptogenesis, and Dendritogenesis.	Pla R et al.	—	2018	→
Identification of genes regulating GABAergic interneuron maturation.	Fukumoto K et al.	—	2018	→
Peptide Sharing Between Viruses and DLX Proteins: A Potential Cross-Reactivity Pathway to Neuropsychiatric Disorders.	Lucchese G et al.	—	2018	→
SP8 and SP9 coordinately promote D2-type medium spiny neuron production by activating <i>Six3</i> expression.	Xu Z et al.	—	2018	→
Stranger in a Strange Land: Using Heterotopic Transplantations to Study Nature vs Nurture in Brain Development.	Petros TJ	—	2018	→
Transcriptional Regulator ZEB2 Is Essential for Bergmann Glia Development.	He L et al.	—	2018	→
A genome wide association study of fast beta EEG in families of European ancestry.	Meyers JL et al.	—	2017	→
Cortical interneuron development: a tale of time and space.	Hu JS et al.	—	2017	→
Fate determination of cerebral cortical GABAergic interneurons and their derivation from stem cells.	DeBoer EM et al.	—	2017	→
Genetic and activity-dependent mechanisms underlying interneuron diversity.	Wamsley B et al.	—	2017	→
Heterotopic Transplantations Reveal Environmental Influences on Interneuron Diversity and Maturation.	Quattrocolo G et al.	—	2017	→
Language deficits in schizophrenia and autism as related oscillatory connectomopathies: An evolutionary account.	Murphy E et al.	—	2017	→
Neuroimaging findings in Mowat-Wilson syndrome: a study of 54 patients.	Garavelli L et al.	—	2017	→
Radial glia in the ventral telencephalon.	Turrero García M et al.	—	2017	→
Single-Cell Profiling of an In Vitro Model of Human Interneuron Development Reveals Temporal Dynamics of Cell Type Production and Maturation.	Close JL et al.	—	2017	→
Single-cell RNA sequencing identifies distinct mouse medial ganglionic eminence cell types.	Chen YJ et al.	—	2017	→
Sip-1 mutations cause disturbances in the activity of NMDA- and AMPA-, but not kainate receptors of neurons in the cerebral cortex.	Turovskaya MV et al.	—	2017	→
The DNA Methyltransferase 1 (DNMT1) Controls the Shape and Dynamics of Migrating POA-Derived Interneurons Fated for the Murine Cerebral Cortex.	Pensold D et al.	—	2017	→
Transcriptional regulatory dynamics drive coordinated metabolic and neural response to social challenge in mice.	Saul MC et al.	—	2017	→
Transcriptomic and anatomic parcellation of 5-HT<sub>3A</sub>R expressing cortical interneuron subtypes revealed by single-cell RNA sequencing.	Frazer S et al.	—	2017	→
Transplantation of GABAergic interneurons for cell-based therapy.	Spatazza J et al.	—	2017	→
Zeb2 is a negative regulator of midbrain dopaminergic axon growth and target innervation.	Hegarty SV et al.	—	2017	→
Zeb2 Regulates Cell Fate at the Exit from Epiblast State in Mouse Embryonic Stem Cells.	Stryjewska A et al.	—	2017	→
Altered expression of developmental regulators of parvalbumin and somatostatin neurons in the prefrontal cortex in schizophrenia.	Volk DW et al.	—	2016	→
Hedgehog signaling promotes basal progenitor expansion and the growth and folding of the neocortex.	Wang L et al.	—	2016	→
In Vivo Neural Tissue Engineering: Cylindrical Biocompatible Hydrogels That Create New Neural Tracts in the Adult Mammalian Brain.	Clark AR et al.	—	2016	→
Language Impairments in ASD Resulting from a Failed Domestication of the Human Brain.	Benítez-Burraco A et al.	—	2016	→
Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain.	Lake BB et al.	—	2016	→
Sip1 regulates the generation of the inner nuclear layer retinal cell lineages in mammals.	Menuchin-Lasowski Y et al.	—	2016	→
Zeb2 recruits HDAC-NuRD to inhibit Notch and controls Schwann cell differentiation and remyelination.	Wu LM et al.	—	2016	→
Chemokine receptors and cortical interneuron dysfunction in schizophrenia.	Volk DW et al.	—	2015	→
Clonally Related Forebrain Interneurons Disperse Broadly across Both Functional Areas and Structural Boundaries.	Mayer C et al.	—	2015	→
Crosstalk between intracellular and extracellular signals regulating interneuron production, migration and integration into the cortex.	Peyre E et al.	—	2015	→
De novo inbred heterozygous Zeb2/Sip1 mutant mice uniquely generated by germ-line conditional knockout exhibit craniofacial, callosal and behavioral defects associated with Mowat-Wilson syndrome.	Takagi T et al.	—	2015	→
Evolutionarily conserved mechanisms for the selection and maintenance of behavioural activity.	Fiore VG et al.	—	2015	→
Genomic perspectives of transcriptional regulation in forebrain development.	Nord AS et al.	—	2015	→
Homeotic Transformations of Neuronal Cell Identities.	Arlotta P et al.	—	2015	→
Osteogenesis and neurogenesis: a robust link also for language evolution.	Boeckx C et al.	—	2015	→
Sip1 downstream Effector ninein controls neocortical axonal growth, ipsilateral branching, and microtubule growth and stability.	Srivatsa S et al.	—	2015	→
The conserved miR-8/miR-200 microRNA family and their role in invertebrate and vertebrate neurogenesis.	Trümbach D et al.	—	2015	→
Zeb2: A multifunctional regulator of nervous system development.	Hegarty SV et al.	—	2015	→
Clonal origins of neocortical interneurons.	Sultan KT et al.	—	2014	→
Complex network-driven view of genomic mechanisms underlying Parkinson's disease: analyses in dorsal motor vagal nucleus, locus coeruleus, and substantia nigra.	Corradini BR et al.	—	2014	→
Decision making during interneuron migration in the developing cerebral cortex.	Guo J et al.	—	2014	→
Differential regulation of microtubule severing by APC underlies distinct patterns of projection neuron and interneuron migration.	Eom TY et al.	—	2014	→
Early developmental disturbances of cortical inhibitory neurons: contribution to cognitive deficits in schizophrenia.	Volk DW et al.	—	2014	→
Genetic programs controlling cortical interneuron fate.	Kessaris N et al.	—	2014	→
Interneuron cell types are fit to function.	Kepecs A et al.	—	2014	→
Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position.	Vogt D et al.	—	2014	→
Loss of Sip1 leads to migration defects and retention of ectodermal markers during lens development.	Manthey AL et al.	—	2014	→
Mechanisms regulating GABAergic neuron development.	Achim K et al.	—	2014	→
Regulation of C. elegans neuronal differentiation by the ZEB-family factor ZAG-1 and the NK-2 homeodomain factor CEH-28.	Ramakrishnan K et al.	—	2014	→
SIP1 expression patterns in brain investigated by generating a SIP1-EGFP reporter knock-in mouse.	Nishizaki Y et al.	—	2014	→
The shape of the human language-ready brain.	Boeckx C et al.	—	2014	→
The spectrum of ZEB2 mutations causing the Mowat-Wilson syndrome in Japanese populations.	Yamada Y et al.	—	2014	→
A sip of GABA for the cerebral cortex.	Tomassy GS et al.	—	2013	→
Epilepsy in Mowat-Wilson syndrome: is it a matter of GABA?	Cordelli DM et al.	—	2013	→
Four amino acids within a tandem QxVx repeat in a predicted extended α-helix of the Smad-binding domain of Sip1 are necessary for binding to activated Smad proteins.	Conidi A et al.	—	2013	→
Interneuron development and epilepsy: early genetic defects cause long-term consequences in seizures and susceptibility.	Powell EM	—	2013	→
Prenatal ontogeny as a susceptibility period for cortical GABA neuron disturbances in schizophrenia.	Volk DW et al.	—	2013	→
Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization.	Smith CJ et al.	—	2013	→
Soluble guanylate cyclase generation of cGMP regulates migration of MGE neurons.	Mandal S et al.	—	2013	→
Subcortical origins of human and monkey neocortical interneurons.	Ma T et al.	—	2013	→
Use of "MGE enhancers" for labeling and selection of embryonic stem cell-derived medial ganglionic eminence (MGE) progenitors and neurons.	Chen YJ et al.	—	2013	→