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The stable brother hiding in the shadow—news on intermediate filaments
Protoplasma ( IF 2.5 ) Pub Date : 2020-08-17 , DOI: 10.1007/s00709-020-01541-w
Peter Nick 1
Affiliation  

The term “cytoskeleton” has been coined, when, from the early 1960s, electron microscopy has revealed filamentous structures that seemed to organise the cytoplasm (“microtubules”, Ledbetter and Porter 1963; “microfilaments”, Kamiya and Kuroda 1966). Onlywith the advent of fluorescencemicroscopy, it was recognised that this skeleton rather represents a very dynamic network, where both microtubules and actin filaments are continuously and rapidly turning over. In contrast, intermediate filaments, the often overlooked third element of the cytoskeleton, are actually closest to that what one could call a “skeleton”. They are described as stable, structural elements that not only maintain the intracellular architecture, for instance by keeping the nucleus in shape, but also sometimes even structure entire tissues, such as skins, feathers or corneous structures. In the walled cells of fungi and plants, this architectural role has been adopted by the cell wall, and this might be the reason, why intermediate filaments apparently were lost during the evolution of these life forms. However, since this third component of the filamentous cytoskeleton has never enjoyed the limelight of scientific attention, it has remained a bit of a terra incognita lurking in the shadow. That the intermediate filaments are merely a stable structure that, once generated, just persists, and is absent from walled plant cells, might be more a kind of dogma rooted in our ignorance, rather than a scientific fact. Two contributions in the current issue, one from the animal and one from the plant field, suggest that we should start to critically question this dogma. The first contribution by Alibardi (2020b) in the current issue investigates the role of specific keratins during the formation of the caruncle of turtles, a juvenile structure on the beak that helps the young animal to hatch from the egg and, therefore, is also referred to as “egg tooth”. Like birds and the primitive mammal Platypus, turtles have replaced their teeth by a corneous layer, a developmental change that is linked with a loss of function for sonic hedgehog, a signalling protein required for dentition. The adult beak of turtles is then formed by so called β-keratins, intermediate filament proteins that differ from the canonical keratins (Alibardi 2020a).While it is clear that the egg-toothmust be composed of keratinous material, because it has to be hard enough to break the egg shell, the molecular composition, and its genesis as well as its transient existence (the egg tooth is shed a few days after hatching, in contrast to the beak), is unknown. Using specific antibodies against intermediate filament keratins, and two turtle-specific β-keratins, the author follows the histological differentiation of the turtle caruncle. He can demonstrate how epidermal cells that are subtended bymaxilla andmandibles proliferate and form placodes that subsequently fuse into the beak, kept together by gap junctions, and forming a corneous epithelium accumulating intermediate filament keratins, complemented later β-keratins to form the corneous beak. This programme is then recapitulated in a constrained region of the corneous layer, starting from local proliferation, accumulation of intermediate filament keratins at the surface, and accumulation of β-keratins in the subtending, large so-called beta cells that are joined by adhesion proteins, such that a hard and stiff structure is formed. This caruncle can then later, once it has fulfilled its function, be shed altogether. The contribution by Utsunomiya et al. (2020) adds a new facet to a controversial debate that had started already in the 1980s: Do plant cells possess intermediate filaments? Since structural support can be maintained by tethering to the solid cell wall, intermediate filaments might be obsolete. Moreover, plant nuclei seem to lack the nuclear lamina that keeps animal nuclei in shape. Nevertheless, antibodies raised against animal intermediate filaments were repeatedly reported to detect fibrillary structures in plant cells that were adjacent to microtubules (Fairbairn et al. 1994; Mizuno 1995), and soluble proteins purified from various plants were able to assemble filamentous structures of around 10 nm in diameter what would qualify them as intermediate filament proteins (for instance Handling Editor: Peter Nick

中文翻译:

藏在暗处的稳哥——中间丝的消息

“细胞骨架”一词是在 1960 年代初期创造的,当时电子显微镜显示似乎组织细胞质的丝状结构(“微管”,Ledbetter 和 Porter 1963;“微丝”,Kamiya 和 Kuroda 1966)。只有随着荧光显微镜的出现,人们才认识到这个骨架反而代表了一个非常动态的网络,其中微管和肌动蛋白丝都在不断地快速翻转。相比之下,中间丝,细胞骨架的第三个元素,经常被忽视,实际上最接近于所谓的“骨架”。它们被描述为稳定的结构元素,不仅维持细胞内结构,例如通过保持细胞核的形状,而且有时甚至构建整个组织,例如皮肤,羽毛或角质结构。在真菌和植物的壁细胞中,细胞壁已经采用了这种结构作用,这可能就是为什么在这些生命形式的进化过程中中间细丝明显丢失的原因。然而,由于丝状细胞骨架的第三个组成部分从未受到科学界的关注,它仍然是潜伏在阴影中的未知领域。中间丝只是一种稳定的结构,一旦产生,就会持续存在,并且在有壁的植物细胞中不存在,这可能更像是一种植根于我们的无知的教条,而不是科学事实。本期杂志中的两个贡献,一个来自动物领域,一个来自植物领域,表明我们应该开始批判性地质疑这一教条。Alibardi (2020b) 在当前问题中的第一个贡献调查了特定角蛋白在海龟肉阜形成过程中的作用,这是喙上的一种幼年结构,有助于幼龟从卵孵化,因此也被称为作为“蛋牙”。像鸟类和原始哺乳动物鸭嘴兽一样,海龟的牙齿被角质层取代,这种发育变化与声波刺猬的功能丧失有关,刺猬是牙列所需的信号蛋白。然后海龟的成年喙由所谓的 β-角蛋白形成,这是一种不同于标准角蛋白的中间丝蛋白 (Alibardi 2020a)。虽然很明显蛋牙必须由角蛋白材料组成,因为它必须很硬足以打破蛋壳,分子组成,它的起源以及它的短暂存在(与喙相反,卵牙在孵化后几天脱落)是未知的。作者使用针对中间丝角蛋白的特异性抗体,以及两种龟特异性β-角蛋白,追踪龟肉瓤的组织学分化。他可以展示由上颌骨和下颌骨包覆的表皮细胞如何增殖并形成基板,基板随后融合到喙中,通过间隙连接保持在一起,并形成积累中间丝状角蛋白的角质上皮,与后来的 β-角蛋白互补形成角质喙。然后在角质层的受限区域重演该程序,从局部增殖开始,中间丝状角蛋白在表面的积累,β-角蛋白在所谓的大β细胞中积累,这些细胞通过粘附蛋白连接,从而形成坚硬的结构。之后,一旦它完成了它的功能,这个肉瘤就可以完全脱落。宇都宫等人的贡献。(2020) 为 1980 年代已经开始的有争议的辩论增加了一个新的方面:植物细胞是否具有中间丝?由于结构支撑可以通过拴在固体细胞壁上来维持,因此中间细丝可能已经过时。此外,植物细胞核似乎缺乏保持动物细胞核形状的核层。然而,反复报道针对动物中间丝产生的抗体可检测与微管相邻的植物细胞中的纤维结构(Fairbairn 等人 1994;Mizuno 1995),
更新日期:2020-08-17
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