Transcription factors COUP-TFI and COUP-TFII are required for the production of granule cells in the mouse olfactory bulb

Zhou, Xing; Liu, Fang; Tian, Miao; Xu, Zhejun; Liang, Qifei; Wang, Chunyang; Li, Jiwen; Liu, Zhidong; Tang, Ke; He, Miao; Yang, Zhengang

doi:10.1242/dev.115279

Cited by 30 publications

(22 citation statements)

References 60 publications

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“…Immunogen: Tyrosine Hydroxylase purified from PC12 cells). Staining results with this TH antibody in the GL were identical to previous descriptions (Fujiwara & Cave, ; Zhou et al, ).RRID: AB_2201528 Rabbit anti‐parvalbumin (PV) (Swant Cat# PV 25, , dilutions 1:2,000, polyclonal. Immunogen: recombinant rat parvalbumin).…”

Section: Methodssupporting

confidence: 93%

“…ASCL1 was expressed in the progenitors in the SVZ, RMS and the core of the OB in the adult mouse. Staining results of brains sections produced a pattern of ASCL1 immunoreactivity that was identical with previous descriptions (Li et al, ; Xu et al, ; Zhou et al, ).RRID: AB_10709354 Goat anti‐SP8 (Santa Cruz Biotechnology Cat# sc‐104661, , Dilutions 1:1,000, polyclonal. Immunogen: amino acids 491–508 of human Sp8).…”

Section: Methodssupporting

confidence: 93%

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The PROK2/PROKR2 signaling pathway is required for the migration of most olfactory bulb interneurons

Wen

Zhang

et al. 2019

J of Comparative Neurology

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Neural stem cells in the subventricular zone (SVZ) of the lateral ventricle generate new interneurons, which migrate tangentially through the rostral migratory stream (RMS) to the olfactory bulb (OB). The PROK2 (prokineticin 2) and PROKR2 (prokineticin receptor 2) signaling pathway has been identified to cause human Kallmann syndrome, a developmental disease that associates hypogonadism with anosmia (OB developmental defects). However, the identities and properties of PROK2 + and PROKR2 + cells in the SVZ-RMS-OB remain largely unknown. Here we examine the expression patterns of Prok2 and Prokr2 in the SVZ-RMS-OB using Prok2 EGFP transgenic and Prokr2 LacZ/+ knockin mice. Our results show that Prokr2 is expressed in postmitotic immature interneurons in the SVZ-RMS-OB. Prok2 is not expressed in the SVZ, but a few PROK2 + cells are found in the medial part of the RMS; they are not neural progenitors or migrating neuroblasts. In the OB, Prok2 is expressed in a subset of granule cells and tufted cells, but no coexpression of Prok2 and Prokr2 in the OB cells is observed. In Prok2 and Prokr2 mutant mice, severe tangential and radial migration defects of neuroblasts in the SVZ-RMS-OB result in loss of~75% of GABAergic interneurons in the OB. These analyses demonstrate that PROK2/PROKR2 signaling is crucial for the tangential and radial migration of OB interneurons.

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Section: Methodssupporting

confidence: 93%

Section: Methodssupporting

confidence: 93%

The PROK2/PROKR2 signaling pathway is required for the migration of most olfactory bulb interneurons

Wen

Zhang

et al. 2019

J of Comparative Neurology

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“…S13). Among them, several known neuronal TFs, like NEUROD1, NEUROG2, POU3F2, or MYT1L, reconstitute <20% of the P19 program, while other "early" factors, like ASCL1 (Huang et al 2012(Huang et al , 2015, NR2F2 (Zhou et al 2015), or NR4A2 (Park et al 2006) reconstitute >60% (Fig. 6B).…”

Section: Generation Of Comprehensive Ra-driven Signal Transduction Nementioning

confidence: 99%

Reconstructed cell fate–regulatory programs in stem cells reveal hierarchies and key factors of neurogenesis

Mendoza-Parra¹,

Malysheva²,

Saleem³

et al. 2016

Genome Res.

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Cell lineages, which shape the body architecture and specify cell functions, derive from the integration of a plethora of cell intrinsic and extrinsic signals. These signals trigger a multiplicity of decisions at several levels to modulate the activity of dynamic gene regulatory networks (GRNs), which ensure both general and cell-specific functions within a given lineage, thereby establishing cell fates. Significant knowledge about these events and the involved key drivers comes from homogeneous cell differentiation models. Even a single chemical trigger, such as the morphogen all-trans retinoic acid (RA), can induce the complex network of gene-regulatory decisions that matures a stem/precursor cell to a particular step within a given lineage. Here we have dissected the GRNs involved in the RA-induced neuronal or endodermal cell fate specification by integrating dynamic RXRA binding, chromatin accessibility, epigenetic promoter epigenetic status, and the transcriptional activity inferred from RNA polymerase II mapping and transcription profiling. Our data reveal how RA induces a network of transcription factors (TFs), which direct the temporal organization of cognate GRNs, thereby driving neuronal/endodermal cell fate specification. Modeling signal transduction propagation using the reconstructed GRNs indicated critical TFs for neuronal cell fate specification, which were confirmed by CRISPR/Cas9-mediated genome editing. Overall, this study demonstrates that a systems view of cell fate specification combined with computational signal transduction models provides the necessary insight in cellular plasticity for cell fate engineering. The present integrated approach can be used to monitor the in vitro capacity of (engineered) cells/tissues to establish cell lineages for regenerative medicine.

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“…In addition, as progenitors divide while migrating, they are continuously exposed to signalling molecules along their paths. COUP-TFI has been shown to be an important regulator of cell migration in vivo during forebrain development (Alfano et al, 2011;Touzot et al, 2016;Tripodi et al, 2004;Zhou et al, 2015), but also in vitro and in cancerous cells (Adam et al, 2000;Boudot et al, 2014;Le Dily et al, 2008). Here, we show that it modulates the correct expression levels of the chemokine receptor gene Cxcr4 during GC neurogenesis and migration.…”

Section: Increased or Decreased Cxcr4 Expression Levels Affect Cell Mmentioning

confidence: 64%

COUP-TFI mitotically regulates production and migration of dentate granule cells and modulates hippocampal CXCR4 expression

et al. 2017

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Development of the dentate gyrus (DG), the primary gateway for hippocampal inputs, spans embryonic and postnatal stages, and involves complex morphogenetic events. We have previously identified the nuclear receptor COUP-TFI as a novel transcriptional regulator in the postnatal organization and function of the hippocampus. Here, we dissect its role in DG morphogenesis by inactivating it in either granule cell progenitors or granule neurons. Loss of COUP-TFI function in progenitors leads to decreased granule cell proliferative activity, precocious differentiation and increased apoptosis, resulting in a severe DG growth defect in adult mice. COUP-TFI-deficient cells express high levels of the chemokine receptor Cxcr4 and migrate abnormally, forming heterotopic clusters of differentiated granule cells along their paths. Conversely, high COUP-TFI expression levels downregulate Cxcr4 expression, whereas increased Cxcr4 expression in wild-type hippocampal cells affects cell migration. Finally, loss of COUP-TFI in postmitotic cells leads to only minor and transient abnormalities, and to normal Cxcr4 expression. Together, our results indicate that COUP-TFI is required predominantly in DG progenitors for modulating expression of the Cxcr4 receptor during granule cell neurogenesis and migration.

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Transcription factors COUP-TFI and COUP-TFII are required for the production of granule cells in the mouse olfactory bulb

Cited by 30 publications

References 60 publications

The PROK2/PROKR2 signaling pathway is required for the migration of most olfactory bulb interneurons

The PROK2/PROKR2 signaling pathway is required for the migration of most olfactory bulb interneurons

Reconstructed cell fate–regulatory programs in stem cells reveal hierarchies and key factors of neurogenesis

COUP-TFI mitotically regulates production and migration of dentate granule cells and modulates hippocampal CXCR4 expression

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