Cell-autonomous action of Slit2 in radial migration of cortical projection neurons

Front Mol Neurosci. 2024 Dec 2:17:1505434. doi: 10.3389/fnmol.2024.1505434. eCollection 2024.

Abstract

Neuronal radial migration is a fundamental process for cortical development, the disruption of which causes neurological and psychiatric dysfunctions. SLIT2 plays diverse functions in brain development and is a well-known axon guidance molecule. In this study, we investigated the radial migration of projection neurons in the developing cerebral cortex by in utero knockdown (KD) of Slit2 in mice. KD of Slit2 did not interfere with the neurogenesis and fate-determination but led to the accumulation of the transfected cells in the intermediate zone (IZ), suggesting that the expression of Slit2 is crucial for the radial migration of the cortical neurons. KD of Slit2 hindered the transition of cells from a multipolar to a bipolar shape, which is necessary for glia-guided locomotion. Interestingly, reducing Slit2 did not affect the migration of neighboring untransfected cells, indicating a cell-autonomous action by SLIT2. In addition, the action of SLIT2 KD was mimicked by a dominant negative mutant of ROBO2, a canonical membrane receptor of SLIT2, supporting that SLIT2 acted locally as a secretory molecule. Our results suggest that SLIT2 is indispensable for the radial migration of cortical neurons through an autocrine signaling mechanism.

Keywords: ROBO2; SLIT2; autocrine; cortical development; morphogenesis; neuronal polarization; radial migration.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China grants (32100799), the China Postdoctoral Science Foundation (2020TQ0332 and 2020M681415), Zhejiang Provincial Natural Science Foundation of China under grant no. LQ20H090001, Zhejiang Provincial Medical and Health Science and Technology Project under grant no. 2019KY247, Scientific Research Fund of Wenling Science and Technology Bureau under grant no. 2018C320001, Zhejiang Provincial Program for the Cultivation of New Health Talents under grant no. 2020-187, the Program for the Cultivation of High-Level Innovative Health Talents from the First People's Hospital of Wenling under grant no. 2021-9, and Youth Scientific Research Project of Shanghai Tongji Hospital (TJ1914).