Target-selective vertebrate motor axon regeneration depends on interaction with glial cells at a peripheral nerve plexus.

IF 7.8 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY PLoS Biology Pub Date : 2023-08-17 eCollection Date: 2023-08-01 DOI:10.1371/journal.pbio.3002223
Lauren J Walker, Camilo Guevara, Koichi Kawakami, Michael Granato
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Abstract

A critical step for functional recovery from peripheral nerve injury is for regenerating axons to connect with their pre-injury targets. Reestablishing pre-injury target specificity is particularly challenging for limb-innervating axons as they encounter a plexus, a network where peripheral nerves converge, axons from different nerves intermingle, and then re-sort into target-specific bundles. Here, we examine this process at a plexus located at the base of the zebrafish pectoral fin, equivalent to tetrapod forelimbs. Using live cell imaging and sparse axon labeling, we find that regenerating motor axons from 3 nerves coalesce into the plexus. There, they intermingle and sort into distinct branches, and then navigate to their original muscle domains with high fidelity that restores functionality. We demonstrate that this regeneration process includes selective retraction of mistargeted axons, suggesting active correction mechanisms. Moreover, we find that Schwann cells are enriched and associate with axons at the plexus, and that Schwann cell ablation during regeneration causes profound axonal mistargeting. Our data provide the first real-time account of regenerating vertebrate motor axons navigating a nerve plexus and reveal a previously unappreciated role for Schwann cells to promote axon sorting at a plexus during regeneration.

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脊椎动物运动轴突的靶向选择性再生取决于与周围神经丛神经胶质细胞的相互作用。
外周神经损伤后功能恢复的关键步骤是再生轴突,使其与损伤前的目标连接。重建损伤前目标特异性对肢体神经支配轴突来说尤其具有挑战性,因为它们遇到神经丛,即外周神经汇聚的网络,来自不同神经的轴突混合在一起,然后重新分类为目标特异性束。在这里,我们在位于斑马鱼胸鳍底部的神经丛中观察了这个过程,相当于四足前肢。利用活细胞成像和稀疏轴突标记,我们发现来自3条神经的再生运动轴突融合到神经丛中。在那里,它们混合并分类成不同的分支,然后以高保真度导航到它们的原始肌肉域,从而恢复功能。我们证明,这种再生过程包括选择性回缩错误的轴突,这表明了积极的纠正机制。此外,我们发现雪旺细胞富集并与神经丛的轴突结合,再生过程中的雪旺细胞消融会导致严重的轴突定位错误。我们的数据首次实时描述了脊椎动物运动轴突在神经丛中的再生,并揭示了施旺细胞在再生过程中促进神经丛轴突分类的先前未被重视的作用。
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来源期刊
PLoS Biology
PLoS Biology 生物-生化与分子生物学
CiteScore
14.40
自引率
2.00%
发文量
359
审稿时长
3 months
期刊介绍: PLOS Biology is an open-access, peer-reviewed general biology journal published by PLOS, a nonprofit organization of scientists and physicians dedicated to making the world's scientific and medical literature freely accessible. The journal publishes new articles online weekly, with issues compiled and published monthly. ISSN Numbers: eISSN: 1545-7885 ISSN: 1544-9173
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