N.N. Petrov National Medical Research Center of Oncology, 197758 Saint-Petersburg, Russia.
Veneto Institute of Oncology IOV-IRCCS, 35128 Padua, Italy.
Cells. 2019 Jul 10;8(7):701. doi: 10.3390/cells8070701.
Centrosomes and primary cilia are usually considered as distinct organelles, although both are assembled with the same evolutionary conserved, microtubule-based templates, the centrioles. Centrosomes serve as major microtubule- and actin cytoskeleton-organizing centers and are involved in a variety of intracellular processes, whereas primary cilia receive and transduce environmental signals to elicit cellular and organismal responses. Understanding the functional relationship between centrosomes and primary cilia is important because defects in both structures have been implicated in various diseases, including cancer. Here, we discuss evidence that the animal centrosome evolved, with the transition to complex multicellularity, as a hybrid organelle comprised of the two distinct, but intertwined, structural-functional modules: the centriole/primary cilium module and the pericentriolar material/centrosome module. The evolution of the former module may have been caused by the expanding cellular diversification and intercommunication, whereas that of the latter module may have been driven by the increasing complexity of mitosis and the requirement for maintaining cell polarity, individuation, and adhesion. Through its unique ability to serve both as a plasma membrane-associated primary cilium organizer and a juxtanuclear microtubule-organizing center, the animal centrosome has become an ideal integrator of extracellular and intracellular signals with the cytoskeleton and a switch between the non-cell autonomous and the cell-autonomous signaling modes. In light of this hypothesis, we discuss centrosome dynamics during cell proliferation, migration, and differentiation and propose a model of centrosome-driven microtubule assembly in mitotic and interphase cells. In addition, we outline the evolutionary benefits of the animal centrosome and highlight the hierarchy and modularity of the centrosome biogenesis networks.
中心体和初级纤毛通常被认为是不同的细胞器，尽管它们都是由相同的进化保守的、基于微管的模板——中心粒组装而成的。中心体作为主要的微管和肌动蛋白细胞骨架组织中心，参与多种细胞内过程，而初级纤毛接收和转导环境信号，引发细胞和机体反应。了解中心体和初级纤毛之间的功能关系很重要，因为这两种结构的缺陷与各种疾病有关，包括癌症。在这里，我们讨论了证据表明，动物中心体随着复杂多细胞生物的进化，作为由两个不同但相互交织的结构-功能模块组成的混合细胞器而进化：中心粒/初级纤毛模块和中心粒周围物质/中心体模块。前者模块的进化可能是由于细胞多样化和相互通讯的扩大，而后者模块的进化可能是由于有丝分裂的复杂性增加以及维持细胞极性、个体性和黏附性的需要所驱动的。通过其作为质膜相关初级纤毛组织者和核周微管组织中心的独特能力，动物中心体已成为细胞外和细胞内信号与细胞骨架之间的理想整合者，以及非细胞自主和细胞自主信号模式之间的转换开关。根据这一假设，我们讨论了中心体在细胞增殖、迁移和分化过程中的动态，并提出了一个在有丝分裂和间期中中心体驱动微管组装的模型。此外，我们概述了动物中心体的进化优势，并强调了中心体生物发生网络的层次结构和模块化。
