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Research Articles, Development/Plasticity/Repair

Coronin 2B Regulates Neuronal Migration via Rac1-Dependent Multipolar–Bipolar Transition

Yuewen Chen, Zhenyan Xu, Jing Chen, Yue Qiu, Lin Yuan, Peng Liu, Jing Duan, Li Chen and Yu Chen
Journal of Neuroscience 11 January 2023, 43 (2) 211-220; DOI: https://doi.org/10.1523/JNEUROSCI.1087-22.2022
Yuewen Chen
1Chinese Academy of Sciences Key Laboratory of Brain Connectome and Manipulation, Shenzhen Key Laboratory of Translational Research for Brain Diseases, Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences; Shenzhen–Hong Kong Institute of Brain Science–Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China
2Shenzhen College of Advanced Technology, University of Chinese Academy of Sciences, Beijing, 100049, China
3Guangdong Provincial Key Laboratory of Brain Science, Disease and Drug Development, HKUST Shenzhen Research Institute, Shenzhen, 518057, China
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Zhenyan Xu
1Chinese Academy of Sciences Key Laboratory of Brain Connectome and Manipulation, Shenzhen Key Laboratory of Translational Research for Brain Diseases, Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences; Shenzhen–Hong Kong Institute of Brain Science–Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China
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Jing Chen
1Chinese Academy of Sciences Key Laboratory of Brain Connectome and Manipulation, Shenzhen Key Laboratory of Translational Research for Brain Diseases, Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences; Shenzhen–Hong Kong Institute of Brain Science–Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China
2Shenzhen College of Advanced Technology, University of Chinese Academy of Sciences, Beijing, 100049, China
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Yue Qiu
3Guangdong Provincial Key Laboratory of Brain Science, Disease and Drug Development, HKUST Shenzhen Research Institute, Shenzhen, 518057, China
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Lin Yuan
3Guangdong Provincial Key Laboratory of Brain Science, Disease and Drug Development, HKUST Shenzhen Research Institute, Shenzhen, 518057, China
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Peng Liu
3Guangdong Provincial Key Laboratory of Brain Science, Disease and Drug Development, HKUST Shenzhen Research Institute, Shenzhen, 518057, China
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Jing Duan
4Department of Neurology, Shenzhen Children's Hospital, Shenzhen, 518038, China
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Li Chen
4Department of Neurology, Shenzhen Children's Hospital, Shenzhen, 518038, China
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Yu Chen
1Chinese Academy of Sciences Key Laboratory of Brain Connectome and Manipulation, Shenzhen Key Laboratory of Translational Research for Brain Diseases, Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences; Shenzhen–Hong Kong Institute of Brain Science–Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China
2Shenzhen College of Advanced Technology, University of Chinese Academy of Sciences, Beijing, 100049, China
3Guangdong Provincial Key Laboratory of Brain Science, Disease and Drug Development, HKUST Shenzhen Research Institute, Shenzhen, 518057, China
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Abstract

In the developing cortex, excitatory neurons migrate along the radial fibers to their final destinations and build up synaptic connection with each other to form functional circuitry. The shaping of neuronal morphologies by actin cytoskeleton dynamics is crucial for neuronal migration. However, it is largely unknown how the distribution and assembly of the F-actin cytoskeleton are coordinated. In the present study, we found that an actin regulatory protein, coronin 2B, is indispensable for the transition from a multipolar to bipolar morphology during neuronal migration in ICR mice of either sex. Loss of coronin 2B led to heterotopic accumulation of migrating neurons in the intermediate zone along with reduced dendritic complexity and aberrant neuronal activity in the cortical plate. This was accompanied by increased seizure susceptibility, suggesting the malfunction of cortical development in coronin 2B-deficient brains. Coronin 2B knockdown disrupted the distribution of the F-actin cytoskeleton at the leading processes, while the migration defect in coronin 2B-deficient neurons was partially rescued by overexpression of Rac1 and its downstream actin-severing protein, cofilin. Our results collectively reveal the physiological function of coronin 2B during neuronal migration whereby it maintains the proper distribution of activated Rac1 and the F-actin cytoskeleton.

SIGNIFICANCE STATEMENT Deficits in neuronal migration during cortical development result in various neurodevelopmental disorders (e.g., focal cortical dysplasia, periventricular heterotopia, epilepsy, etc.). Most signaling pathways that control neuronal migration process converge to regulate actin cytoskeleton dynamics. Therefore, it is important to understand how actin dynamics is coordinated in the critical processes of neuronal migration. Herein, we report that coronin 2B is a key protein that regulates neuronal migration through its ability to control the distribution of the actin cytoskeleton and its regulatory signaling protein Rac1 during the multipolar–bipolar transition in the intermediate zone, providing insights into the molecular machinery that drives the migration process of newborn neurons.

  • actin cytoskeleton
  • coronin 2B
  • cortical development
  • multipolar–bipolar transition
  • neuronal migration

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The Journal of Neuroscience: 43 (2)
Journal of Neuroscience
Vol. 43, Issue 2
11 Jan 2023
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Coronin 2B Regulates Neuronal Migration via Rac1-Dependent Multipolar–Bipolar Transition
Yuewen Chen, Zhenyan Xu, Jing Chen, Yue Qiu, Lin Yuan, Peng Liu, Jing Duan, Li Chen, Yu Chen
Journal of Neuroscience 11 January 2023, 43 (2) 211-220; DOI: 10.1523/JNEUROSCI.1087-22.2022

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Coronin 2B Regulates Neuronal Migration via Rac1-Dependent Multipolar–Bipolar Transition
Yuewen Chen, Zhenyan Xu, Jing Chen, Yue Qiu, Lin Yuan, Peng Liu, Jing Duan, Li Chen, Yu Chen
Journal of Neuroscience 11 January 2023, 43 (2) 211-220; DOI: 10.1523/JNEUROSCI.1087-22.2022
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Keywords

  • actin cytoskeleton
  • coronin 2B
  • cortical development
  • multipolar–bipolar transition
  • neuronal migration

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