Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species

Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species
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DOI:
10.1073/pnas.1605707113
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发表时间:
2016-05-24
影响因子:
11.1
通讯作者:
Zhuang, Xiaowei
Zhuang, Xiaowei
中科院分区:
综合性期刊1区
文献类型:
--
作者:
He, Jiang;Zhou, Ruobo;Zhuang, Xiaowei

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肌动蛋白、血影蛋白和相关分子在神经元轴突中形成周期性的膜下细胞骨架。为了更好地了解这种膜相关的周期骨架(MPS),重要的是要解决这种结构在不同类型的神经元、不同的亚细胞室和不同的动物物种中的普遍程度。在这里,我们研究了不同类型的神经细胞和胶质细胞中的血影蛋白的组织。我们观察到从小鼠中枢和外周神经系统培养的所有受试神经元类型中都存在MPS,包括来自几个脑区的兴奋性和抑制性神经元,以及感觉神经元和运动神经元。定量分析表明,MPS优先在所有类型的轴突中形成:血影蛋白在所有轴突中呈长程周期性分布,但仅在一小部分树突中出现周期性,典型地以这些树突亚区中孤立的斑块的形式出现。与树突一样,我们也在从啮齿动物组织培养的四种神经胶质细胞的一小部分神经胶质细胞突起中观察到周期性血影蛋白结构的斑块。有趣的是,尽管MPS强烈存在于轴突中,但它在大多数突触前突触中被破坏,但在相当一部分树突棘颈中存在,包括一些从树突突起的突起,在树突中没有观察到这种周期性结构。最后,我们发现,幽灵蛋白能够在各种动物物种的神经元中采用类似的周期性组织,包括线虫、果蝇、家禽、小鼠和智人。
Actin, spectrin, and associated molecules form a periodic, submembrane cytoskeleton in the axons of neurons. For a better understanding of this membrane-associated periodic skeleton (MPS), it is important to address how prevalent this structure is in different neuronal types, different subcellular compartments, and across different animal species. Here, we investigated the organization of spectrin in a variety of neuronal-and glial-cell types. We observed the presence of MPS in all of the tested neuronal types cultured from mouse central and peripheral nervous systems, including excitatory and inhibitory neurons from several brain regions, as well as sensory and motor neurons. Quantitative analyses show that MPS is preferentially formed in axons in all neuronal types tested here: Spectrin shows a long-range, periodic distribution throughout all axons but appears periodic only in a small fraction of dendrites, typically in the form of isolated patches in subregions of these dendrites. As in dendrites, we also observed patches of periodic spectrin structures in a small fraction of glial-cell processes in four types of glial cells cultured from rodent tissues. Interestingly, despite its strong presence in the axonal shaft, MPS is disrupted in most presynaptic boutons but is present in an appreciable fraction of dendritic spine necks, including some projecting from dendrites where such a periodic structure is not observed in the shaft. Finally, we found that spectrin is capable of adopting a similar periodic organization in neurons of a variety of animal species, including Caenorhabditis elegans, Drosophila, Gallus gallus, Mus musculus, and Homo sapiens.