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Research Articles, Development/Plasticity/Repair

Cenpj Regulates Cilia Disassembly and Neurogenesis in the Developing Mouse Cortex

Wenyu Ding, Qian Wu, Le Sun, Na Clara Pan and Xiaoqun Wang
Journal of Neuroscience 13 March 2019, 39 (11) 1994-2010; DOI: https://doi.org/10.1523/JNEUROSCI.1849-18.2018
Wenyu Ding
1State Key Laboratory of Brain and Cognitive Science, Chinese Academy of Sciences Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China,
2University of Chinese Academy of Sciences, Beijing 100049, China, and
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Qian Wu
1State Key Laboratory of Brain and Cognitive Science, Chinese Academy of Sciences Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China,
2University of Chinese Academy of Sciences, Beijing 100049, China, and
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Le Sun
1State Key Laboratory of Brain and Cognitive Science, Chinese Academy of Sciences Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China,
2University of Chinese Academy of Sciences, Beijing 100049, China, and
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Na Clara Pan
1State Key Laboratory of Brain and Cognitive Science, Chinese Academy of Sciences Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China,
2University of Chinese Academy of Sciences, Beijing 100049, China, and
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Xiaoqun Wang
1State Key Laboratory of Brain and Cognitive Science, Chinese Academy of Sciences Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China,
2University of Chinese Academy of Sciences, Beijing 100049, China, and
3Beijing Institute for Brain Disorders, Beijing 100069, China
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Abstract

Primary cilia are microtubule-based protuberances that project from the eukaryotic cell body to sense the extracellular environment. Ciliogenesis is closely correlated to the cell cycle and defects of cilia are related to human systemic diseases such as primary ciliary dyskinesia. However, the role of ciliogenesis in cortical development remains unclear. Here, we demonstrate that Cenpj, a protein that is required for centriole biogenesis, plays a role in regulating cilium disassembly in vivo. Depletion of Cenpj in neural progenitor cells results in long cilia and abnormal cilia disassembly. Radial glial cells Cenpj depletion exhibit uncompleted cell division, reduced cell proliferation, and increased cell apoptosis in the developing mouse cerebrum cortex, leading to microcephaly. In addition, Cenpj depletion causes long and thin primary cilia and motile cilia in adult neural stem cells and reduced cell proliferation in the subventricular zone. Furthermore, we show that Cenpj regulates cilia disassembly and neurogenesis through Kif2a, a plus-end-directed motor protein. These data collected from mice of both sexes provide insights into how ciliogenesis plays roles in cortical development and how primary microcephaly is induced by Cenpj mutations in humans.

SIGNIFICANCE STATEMENT Autosomal recessive primary microcephaly is a neurodevelopmental disorder with the major symptoms of reduction of circumference of the head, brain volume, and cortex thickness with normal brain architecture in birth. We used conditional Cenpj deletion mice and found that neural progenitor cells (NPCs) exhibited long primary cilia and abnormal cilium appendages. The defective cilium disassembly caused by Cenpj depletion might correlate to reduced cell proliferation, uncompleted cell division, cell apoptosis, and microcephaly in mice. Cenpj also regulates the cilium structure of adult neural stem cells and adult neurogenesis in mice. Additionally, our results illustrate that Cenpj regulates cilia disassembly and neurogenesis through Kif2a, indicating that primary cilia dynamics play a crucial role in NPC mitosis and adult neurogenesis.

  • CenpJ
  • cerebral cortex
  • neurogenesis
  • primary cilia
  • radial glial cell
  • subventricular zone
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The Journal of Neuroscience: 39 (11)
Journal of Neuroscience
Vol. 39, Issue 11
13 Mar 2019
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Cenpj Regulates Cilia Disassembly and Neurogenesis in the Developing Mouse Cortex
Wenyu Ding, Qian Wu, Le Sun, Na Clara Pan, Xiaoqun Wang
Journal of Neuroscience 13 March 2019, 39 (11) 1994-2010; DOI: 10.1523/JNEUROSCI.1849-18.2018

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Cenpj Regulates Cilia Disassembly and Neurogenesis in the Developing Mouse Cortex
Wenyu Ding, Qian Wu, Le Sun, Na Clara Pan, Xiaoqun Wang
Journal of Neuroscience 13 March 2019, 39 (11) 1994-2010; DOI: 10.1523/JNEUROSCI.1849-18.2018
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Keywords

  • CenpJ
  • cerebral cortex
  • neurogenesis
  • primary cilia
  • radial glial cell
  • subventricular zone

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