Doublecortin-like kinase is required for cnidocyte development in Nematostella vectensis.

IF 4 3区 生物学 Q1 DEVELOPMENTAL BIOLOGY Neural Development Pub Date : 2024-06-22 DOI:10.1186/s13064-024-00188-0
Johanna E M Kraus, Henriette Busengdal, Yulia Kraus, Harald Hausen, Fabian Rentzsch
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Abstract

The complex morphology of neurons requires precise control of their microtubule cytoskeleton. This is achieved by microtubule-associated proteins (MAPs) that regulate the assembly and stability of microtubules, and transport of molecules and vesicles along them. While many of these MAPs function in all cells, some are specifically or predominantly involved in regulating microtubules in neurons. Here we use the sea anemone Nematostella vectensis as a model organism to provide new insights into the early evolution of neural microtubule regulation. As a cnidarian, Nematostella belongs to an outgroup to all bilaterians and thus occupies an informative phylogenetic position for reconstructing the evolution of nervous system development. We identified an ortholog of the microtubule-binding protein doublecortin-like kinase (NvDclk1) as a gene that is predominantly expressed in neurons and cnidocytes (stinging cells), two classes of cells belonging to the neural lineage in cnidarians. A transgenic NvDclk1 reporter line revealed an elaborate network of neurite-like processes emerging from cnidocytes in the tentacles and the body column. A transgene expressing NvDclk1 under the control of the NvDclk1 promoter suggests that NvDclk1 localizes to microtubules and therefore likely functions as a microtubule-binding protein. Further, we generated a mutant for NvDclk1 using CRISPR/Cas9 and show that the mutants fail to generate mature cnidocytes. Our results support the hypothesis that the elaboration of programs for microtubule regulation occurred early in the evolution of nervous systems.

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维氏线虫的网眼细胞发育需要双皮质素样激酶。
神经元的复杂形态要求对其微管细胞骨架进行精确控制。微管相关蛋白(MAPs)能调节微管的组装和稳定性,以及分子和囊泡沿微管的运输。虽然这些 MAPs 中有许多在所有细胞中都起作用,但有些专门或主要参与调节神经元中的微管。在这里,我们以海葵(Nematostella vectensis)为模式生物,为神经微管调控的早期进化提供新的见解。作为一种刺胞动物,海葵属于所有双脊类动物的外群,因此在重建神经系统发育进化的系统发育中占有重要地位。我们发现了微管结合蛋白双皮质素样激酶(NvDclk1)的一个直向同源基因,该基因主要在神经元和刺细胞(刺细胞)中表达,这两类细胞属于刺胞动物的神经系。转基因 NvDclk1 报告基因株显示,触手和体柱中的刺胞出现了复杂的神经元样过程网络。在 NvDclk1 启动子控制下表达 NvDclk1 的转基因表明,NvDclk1 定位于微管,因此很可能具有微管结合蛋白的功能。此外,我们还利用 CRISPR/Cas9 生成了 NvDclk1 的突变体,结果表明突变体无法生成成熟的刺胞。我们的研究结果支持这样的假设,即微管调控程序的制定发生在神经系统进化的早期。
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来源期刊
Neural Development
Neural Development 生物-发育生物学
CiteScore
6.60
自引率
0.00%
发文量
11
审稿时长
>12 weeks
期刊介绍: Neural Development is a peer-reviewed open access, online journal, which features studies that use molecular, cellular, physiological or behavioral methods to provide novel insights into the mechanisms that underlie the formation of the nervous system. Neural Development aims to discover how the nervous system arises and acquires the abilities to sense the world and control adaptive motor output. The field includes analysis of how progenitor cells form a nervous system during embryogenesis, and how the initially formed neural circuits are shaped by experience during early postnatal life. Some studies use well-established, genetically accessible model systems, but valuable insights are also obtained from less traditional models that provide behavioral or evolutionary insights.
期刊最新文献
Correction: Embryonic development of a centralised brain in coleoid cephalopods. Terminal differentiation precedes functional circuit integration in the peduncle neurons in regenerating Hydra vulgaris. Mapping the cellular expression patterns of vascular endothelial growth factor aa and bb genes and their receptors in the adult zebrafish brain during constitutive and regenerative neurogenesis LRRK2 kinase activity is necessary for development and regeneration in Nematostella vectensis. Correction: scMultiome analysis identifies a single caudal hindbrain compartment in the developing zebrafish nervous system
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