The Zinc Finger Transcription Factor Sp9 Is Required for the Development of Striatopallidal Projection Neurons

Zhang, Qiangqiang; Zhang, Yue; Wang, Chunyang; Xu, Zhejun; Liang, Qifei; An, Lei; Li, Jiwen; Liu, Zhidong; You, Yun; He, Miao; Mao, Ying; Chen, Bin; Xiong, Zhi‐Qi; Rubenstein, John L.R.; Yang, Zhengang

doi:10.1016/j.celrep.2016.06.090

Cited by 60 publications

(98 citation statements)

References 61 publications

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“…Sp9 was reported to be widely expressed in the ganglionic eminences (GEs) and in all striatopallidal MSNs. The expression pattern observed in this study is consistent with that of (Zhang et al, ).…”

Section: Methodssupporting

confidence: 93%

“…SP8 is expressed in the SVZ of the dLGE and dCGE (Ma et al, ) and SP9 is widely expressed in the SVZ of the GE (Guo et al, ; Liu et al, ; Long et al, ; Xu et al, ; Zhang et al, ). In this study, we found SP8/9 were highly co‐expressed in the dCGE SVZ.…”

Section: Discussionmentioning

confidence: 99%

“…Sp8 is widely expressed in the dorsal LGE (dLGE) and dorsal CGE (dCGE) (Ma et al, ), which produce the olfactory bulb (OB) and cortical interneurons, respectively. Sp9 is expressed in the SVZ of the GE (Li et al, ; Xu et al, ; Zhang et al, ). In our previous studies, when Sp8 was conditionally knocked out, we found that there were no significant differences in the number and laminar distribution of CGE‐derived cortical interneurons including RELN + , COUP‐TFII + , and VIP + cells (Ma et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Transcription factors Sp8 and Sp9 regulate the development of caudal ganglionic eminence‐derived cortical interneurons

Song

et al. 2019

J of Comparative Neurology

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Cortical interneurons are derived from the subcortical medial ganglionic eminence (MGE), caudal ganglionic eminence (CGE) and preoptic area (POA). CGE‐derived cortical interneurons, which comprise around 30% of all cortical interneurons, mainly express Htr3a, calretinin (CR), Reelin (RELN) and vasoactive intestinal polypeptide (VIP). In the present study, we show that transcription factors Sp8 and Sp9 are co‐expressed in the subventricular zone (SVZ) of the dorsal CGE. Conditional knockout of Sp8/9 using the Gsx2‐Cre transgenic line results in severe loss of CGE‐derived cortical interneurons. We observed migration defects of Sp8/9 double mutant CGE‐derived cortical interneurons as they had longer leading processes than controls and they ectopically accumulated in the CGE. Dlx5/6‐CIE conditional deletion of Sp8/9 also leads to a significant reduction in the CGE‐derived cortical interneurons. We provide evidence that Sp8/9 coordinately regulate CGE‐derived cortical interneuron development in part through repressing the expression of Pak3, Robo1, and Slit1. Finally, we show that Cxcl14, a member of the CXC chemokine family, is mainly expressed in CGE‐derived interneurons in cortical layers I and II, and its expression is critically dependent on SP8.

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Section: Methodssupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Transcription factors Sp8 and Sp9 regulate the development of caudal ganglionic eminence‐derived cortical interneurons

Song

et al. 2019

J of Comparative Neurology

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“…Studies in recent years have begun to shed light on the molecular genetic mechanisms that control the development of the direct and indirect SPN pathways. In this respect, Ikaros and Sp9 are required for the normal differentiation and survival of the indirect SPNs (Martin-Ibanez et al, 2010; Zhang et al, 2016). Conversely, Ebf1 (Garel et al, 1999; Lobo et al, 2006, 2008) and the LIM homeodomain protein, Isl1 (Ehrman et al, 2013; Lu et al, 2014) have been implicated in the development of the direct pathway (i.e.…”

Section: Introductionmentioning

confidence: 99%

Foxo1 is a downstream effector of Isl1 in direct pathway striatal projection neuron development within the embryonic mouse telencephalon

Waclaw

Ehrman

Merchan-Sala

et al. 2017

Molecular and Cellular Neuroscience

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Recent studies have shown that the LIM-homeodomain transcription factor Isl1 is required for the survival and differentiation of direct pathway striatonigral neurons during embryonic development. The downstream effectors of Isl1 in these processes are presently unknown. We show here that Foxo1, a transcription factor that has been implicated in cell survival, is expressed in striatal projection neurons (SPNs) that derive from the Isl1 lineage (i.e. direct pathway SPNs). Moreover, Isl1 conditional knockouts (cKOs) show a severe loss of Foxo1 expression at E15.5 with a modest recovery by E18.5. Although Foxo1 is enriched in the direct pathway SPNs at embryonic stages, it is expressed in both direct and indirect pathway SPNs at postnatal time points as evidenced by co-localization with EGFP in both Drd1-EGFP and Drd2-EGFP BAC transgenic mice. Foxo1 was not detected in striatal interneurons as marked by the transcription factor Nkx2.1. Conditional knockout of Foxo1 using Dlx5/6-CIE results in reduced expression of the SPN marker Darpp-32, as well as in the direct pathway SPN markers Ebf1 and Zfp521 within the embryonic striatum at E15.5. However, this phenotype improves in the conditional mutants by E18.5. Interestingly, the Foxo family members, Foxo3 and Foxo6, remain expressed at late embryonic stages in the Foxo1 cKOs unlike the Isl1 cKOs where Foxo1/3/6 as well as the Foxo1/3 target Bach2 are all reduced. Taken together, these findings suggest that Foxo-regulated pathways are downstream of Isl1 in the survival and/or differentiation of direct pathway SPNs.

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“…Moreover, Ctip2 and Foxp1 have been shown to be required for the normal differentiation of SPNs (Arlotta et al, ; Bacon et al, ). The zinc finger transcription factor Sp9 is expressed by many subventricular zone cells of the LGE, however, it's expression resolves to the iSPNs at postnatal stages and is required for the proliferation and postnatal survival of this SPN subtype (Zhang et al, ). Conversely, the early B cell factor Ebf1 , is known to be required for the normal development and connectivity of dSPNs, particularly in the matrix compartment (Garel, Marin, Grosschedl, & Charnay, ; Lobo, Karsten, Gray, Geschwind, & Yang, ; Lobo, Yeh, & Yang, ).…”

Section: Introductionmentioning

confidence: 99%

Selective neuronal expression of the SoxE factor, Sox8, in direct pathway striatal projection neurons of the developing mouse brain

Merchan-Sala

Nardini

Waclaw

et al. 2017

J of Comparative Neurology

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The striatum is the major component of the basal ganglia and is well known to play a key role in the control of motor function via balanced output from the indirect (iSPNs) and direct pathway striatal projection neurons (dSPNs). Little is known, however, about the molecular genetic mechanisms that control the formation of the iSPNs versus dSPNs. We show here that the SoxE family member, Sox8, is co-expressed with the dSPN markers, Isl1 and Ebf1, in the developing striatum. Moreover, dSPNs, as marked by Isl1-cre fate map, express Sox8 in the embryonic striatum and Sox8-EGFP BAC transgenic mice specifically reveal the direct pathway axons during development. These EGFP axons are first observed to reach their midbrain target, the substantia nigra pars reticulata (SNr), at E14 in the mouse with a robust connection observed already at birth. The selective expression of EGFP in dSPNs of Sox8-EGFP BAC mice is maintained at postnatal timepoints. Sox8 is known to be expressed in oligodendrocyte precursor cells (OPCs) together with other SoxE factors and we show here that the EGFP signal co-localizes with the OPC markers throughout the brain. Finally, we show that Sox8-EGFP BAC mice can be used to interrogate the altered dSPN development in Isl1 conditional mutants including aberrant axonal projections detected already at embryonic timepoints. Thus, Sox8 represents an early and specific marker of embryonic dSPNs and the Sox8-EGFP BAC transgenic mice are an excellent tool to study the development of basal ganglia circuitry.

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The Zinc Finger Transcription Factor Sp9 Is Required for the Development of Striatopallidal Projection Neurons

Cited by 60 publications

References 61 publications

Transcription factors Sp8 and Sp9 regulate the development of caudal ganglionic eminence‐derived cortical interneurons

Transcription factors Sp8 and Sp9 regulate the development of caudal ganglionic eminence‐derived cortical interneurons

Foxo1 is a downstream effector of Isl1 in direct pathway striatal projection neuron development within the embryonic mouse telencephalon

Selective neuronal expression of the SoxE factor, Sox8, in direct pathway striatal projection neurons of the developing mouse brain

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