NOTCH, ERK, and SHH signaling respectively control the fate determination of cortical glia and olfactory bulb interneurons

Y Yanjing Gao (State Key Laboratory of Inorganic Synthesis and Preparative Chemistry, College of Chemistry, Jilin University, Qianjin Street 2699, Changchun 130012, P. R. China) M Mengge Sun (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) T Tongye Fu (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) Z Ziwu Wang (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) X Xin Jiang L Lin Yang X Xiaoyi G. Liang (Department of Molecular, Cell and Developmental Biology, University of California Santa Cruz) G Guoping Liu (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) Y Yu Tian F Feihong Yang (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) J Jialin Li Z Zhenmeiyu Li (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) X Xiaosu Li (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) Y Yan You (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) C Chaoqiong Ding (Department of Neurosurgery, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University) Y Yuan Wang T Tong Ma (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) Z Zhuangzhi Zhang (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) Z Zhejun Xu (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University) B Bin Chen Z Zhengang Yang (Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University)

Abstract

During cortical development, radial glial cells (neural stem cells) initially are neurogenic, generating intermediate progenitor cells that exclusively produce glutamatergic pyramidal neurons. Next, radial glial cells generate tripotential intermediate progenitor cells (Tri-IPCs) that give rise to cortical astrocytes and oligodendrocytes, and olfactory bulb interneurons. The molecular mechanisms underlying the transition from cortical neurogenesis to gliogenesis, and the subsequent fate determination of cortical astrocytes, oligodendrocytes, and olfactory bulb interneurons, remain unclear. Here, we report that extracellular signal-regulated kinase (ERK) signaling plays a fundamental role in promoting cortical gliogenesis and the generation of Tri-IPCs. Additionally, sonic hedgehog-smoothened-glioma-associated oncogene homolog (SHH-SMO-GLI) activator signaling has an auxiliary function to ERK during these processes. We further demonstrate that, from Tri-IPCs, NOTCH signaling is crucial for the fate determination of astrocytes, while ERK signaling plays a prominent role in oligodendrocyte fate specification, and SHH signaling is required for the fate determination of olfactory bulb interneurons. We provide evidence suggesting that this mechanism is conserved in both mice and humans. Finally, we propose a unifying principle of mammalian cortical gliogenesis.

Article Details

Volume / Issue Vol. 122, Issue 9
Published March 04, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (21)

Y

Yanjing Gao

State Key Laboratory of Inorganic Synthesis and Preparative Chemistry, College of Chemistry, Jilin University, Qianjin Street 2699, Changchun 130012, P. R. China

M

Mengge Sun

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

T

Tongye Fu

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

Z

Ziwu Wang

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

X

Xin Jiang

L

Lin Yang

X

Xiaoyi G. Liang

Department of Molecular, Cell and Developmental Biology, University of California Santa Cruz

G

Guoping Liu

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

Y

Yu Tian

F

Feihong Yang

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

J

Jialin Li

Z

Zhenmeiyu Li

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

X

Xiaosu Li

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

Y

Yan You

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

C

Chaoqiong Ding

Department of Neurosurgery, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University

Y

Yuan Wang

T

Tong Ma

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

Z

Zhuangzhi Zhang

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

Z

Zhejun Xu

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University

B

Bin Chen

Z

Zhengang Yang

Department of Neurology, Zhongshan Hospital, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Fudan University