The Laboratory of Biochemistry and Genetics, National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, MD 20892, USA.
Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Fetscherstraße 74, 01307 Dresden, Germany.
Curr Biol. 2023 Mar 13;33(5):791-806.e7. doi: 10.1016/j.cub.2022.12.059. Epub 2023 Jan 23.
Centrosomes are cellular structures that nucleate microtubules. At their core is a pair of centrioles that recruit pericentriolar material (PCM). Although centrosomes are considered membraneless organelles, in many cell types, including human cells, centrosomes are surrounded by endoplasmic reticulum (ER)-derived membranes of unknown structure and function. Using volume electron microscopy (vEM), we show that centrosomes in the Caenorhabditis elegans (C. elegans) early embryo are surrounded by a three-dimensional (3D), ER-derived membrane reticulum that we call the centriculum, for centrosome-associated membrane reticulum. The centriculum is adjacent to the nuclear envelope in interphase and early mitosis and fuses with the fenestrated nuclear membrane at metaphase. Centriculum formation is dependent on the presence of an underlying centrosome and on microtubules. Conversely, increasing centriculum size by genetic means led to the expansion of the PCM, increased microtubule nucleation capacity, and altered spindle width. The effect of the centriculum on centrosome function suggests that in the C. elegans early embryo, the centrosome is not membraneless. Rather, it is encased in a membrane meshwork that affects its properties. We provide evidence that the centriculum serves as a microtubule "filter," preventing the elongation of a subset of microtubules past the centriculum. Finally, we propose that the fusion between the centriculum and the nuclear membrane contributes to nuclear envelope breakdown by coupling spindle elongation to nuclear membrane fenestration.
中心体是起始微管的细胞结构。其核心是一对中心粒，能募集中心粒周围物质（PCM）。尽管中心体被认为是无膜细胞器，但在许多细胞类型中，包括人类细胞，中心体被内质网（ER）衍生的膜所包围，这些膜的结构和功能尚不清楚。我们使用体积电子显微镜（vEM）发现，秀丽隐杆线虫（C. elegans）早期胚胎中的中心体被一个三维的、由 ER 衍生的膜网络所包围，我们将其称为 centriculum，即与中心体相关的膜网络。在间期和早期有丝分裂中，centriculum 与核膜相邻，并在中期与有孔核膜融合。centriculum 的形成依赖于中心体的存在和微管。相反，通过遗传手段增加 centriculum 的大小会导致 PCM 的扩大、微管成核能力的增加以及纺锤体宽度的改变。centriculum 对中心体功能的影响表明，在 C. elegans 早期胚胎中，中心体并不是无膜的。相反，它被包裹在一个影响其特性的膜网格中。我们提供的证据表明，centriculum 充当了微管的“过滤器”，阻止了一部分微管延伸到 centriculum 之外。最后，我们提出 centriculum 与核膜的融合通过将纺锤体的延伸与核膜的孔化偶联，有助于核膜的破裂。
