Department of Chemistry and Biochemistry, University of Tulsa, Tulsa, Oklahoma, United States of America.
Laboratory of Biochemistry and Genetics, National Institutes of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, Maryland, United States of America.
PLoS Genet. 2022 Apr 4;18(4):e1009799. doi: 10.1371/journal.pgen.1009799. eCollection 2022 Apr.
Centrioles are submicron-scale, barrel-shaped organelles typically found in pairs, and play important roles in ciliogenesis and bipolar spindle assembly. In general, successful execution of centriole-dependent processes is highly reliant on the ability of the cell to stringently control centriole number. This in turn is mainly achieved through the precise duplication of centrioles during each S phase. Aberrations in centriole duplication disrupt spindle assembly and cilia-based signaling and have been linked to cancer, primary microcephaly and a variety of growth disorders. Studies aimed at understanding how centriole duplication is controlled have mainly focused on the post-translational regulation of two key components of this pathway: the master regulatory kinase ZYG-1/Plk4 and the scaffold component SAS-6. In contrast, how transcriptional control mechanisms might contribute to this process have not been well explored. Here we show that the chromatin remodeling protein CHD-1 contributes to the regulation of centriole duplication in the C. elegans embryo. Specifically, we find that loss of CHD-1 or inactivation of its ATPase activity can restore embryonic viability and centriole duplication to a strain expressing insufficient ZYG-1 activity. Interestingly, loss of CHD-1 is associated with increases in the levels of two ZYG-1-binding partners: SPD-2, the centriole receptor for ZYG-1 and SAS-6. Finally, we explore transcriptional regulatory networks governing centriole duplication and find that CHD-1 and a second transcription factor, EFL-1/DPL-1 cooperate to down regulate expression of CDK-2, which in turn promotes SAS-6 protein levels. Disruption of this regulatory network results in the overexpression of SAS-6 and the production of extra centrioles.
中心体是亚微米尺度的桶状细胞器,通常成对存在,在纤毛发生和双极纺锤体组装中发挥重要作用。一般来说,中心体依赖性过程的成功执行高度依赖于细胞严格控制中心体数量的能力。这主要是通过每个 S 期中心体的精确复制来实现的。中心体复制异常会破坏纺锤体组装和基于纤毛的信号转导,并与癌症、原发性小头畸形和多种生长障碍有关。旨在了解中心体复制如何受到控制的研究主要集中在该途径的两个关键成分的翻译后调控上:主调控激酶 ZYG-1/Plk4 和支架成分 SAS-6。相比之下,转录控制机制如何有助于这一过程尚未得到很好的探索。在这里,我们表明染色质重塑蛋白 CHD-1 有助于调节线虫胚胎中的中心体复制。具体来说,我们发现 CHD-1 的缺失或其 ATP 酶活性的失活可以恢复胚胎活力和中心体复制到表达不足的 ZYG-1 活性的菌株。有趣的是,CHD-1 的缺失与两种 ZYG-1 结合伴侣的水平增加有关:SPD-2,ZYG-1 和 SAS-6 的中心体受体。最后,我们探索了调节中心体复制的转录调控网络,发现 CHD-1 和另一个转录因子 EFL-1/DPL-1 合作下调 CDK-2 的表达,从而促进 SAS-6 蛋白水平。该调节网络的破坏导致 SAS-6 的过表达和额外中心体的产生。