Zhou Chuying, Wu You Kure, Ishidate Fumiyoshi, Fujiwara Takahiro K, Kengaku Mineko
Graduate School of Biostudies, Kyoto University, Kyoto, Japan.
Institute for Integrated Cell-Material Science (WPI-iCeMS), Kyoto University, Kyoto, Japan.
J Cell Biol. 2024 Nov 4;223(11). doi: 10.1083/jcb.202405032. Epub 2024 Aug 8.
Nuclear migration is critical for the proper positioning of neurons in the developing brain. It is known that bidirectional microtubule motors are required for nuclear transport, yet the mechanism of the coordination of opposing motors is still under debate. Using mouse cerebellar granule cells, we demonstrate that Nesprin-2 serves as a nucleus-motor adaptor, coordinating the interplay of kinesin-1 and dynein. Nesprin-2 recruits dynein-dynactin-BicD2 independently of the nearby kinesin-binding LEWD motif. Both motor binding sites are required to rescue nuclear migration defects caused by the loss of function of Nesprin-2. In an intracellular cargo transport assay, the Nesprin-2 fragment encompassing the motor binding sites generates persistent movements toward both microtubule minus and plus ends. Nesprin-2 drives bidirectional cargo movements over a prolonged period along perinuclear microtubules, which advance during the migration of neurons. We propose that Nesprin-2 keeps the nucleus mobile by coordinating opposing motors, enabling continuous nuclear transport along advancing microtubules in migrating cells.
核迁移对于发育中的大脑中神经元的正确定位至关重要。已知双向微管马达是核运输所必需的,然而,相反方向马达的协调机制仍在争论中。利用小鼠小脑颗粒细胞,我们证明Nesprin-2作为核-马达适配器,协调驱动蛋白-1和动力蛋白的相互作用。Nesprin-2独立于附近与驱动蛋白结合的LEWD基序招募动力蛋白-动力蛋白激活蛋白-BicD2。两个马达结合位点都是挽救由Nesprin-2功能丧失引起的核迁移缺陷所必需的。在细胞内货物运输试验中,包含马达结合位点的Nesprin-2片段产生朝向微管负端和正端的持续运动。Nesprin-2沿着核周微管在较长时间内驱动双向货物运动,这些微管在神经元迁移过程中向前延伸。我们提出,Nesprin-2通过协调相反方向的马达使细胞核保持移动,从而使迁移细胞中沿着向前延伸的微管进行连续的核运输。