The fission yeast ortholog of Coilin, Mug174, forms Cajal body-like nuclear condensates and is essential for cellular quiescence

• Published in: Nucleic acids research Vol. 52; no. 15; pp. 9174 - 9192
• Main Authors: Deng, Xiaoling, Yao, Qinglian, Horvath, Attila, Jiang, Ziling, Zhao, Junjie, Fischer, Tamás, Sugiyama, Tomoyasu
• Format: Journal Article
• Language: English
• Published: England Oxford University Press 27-08-2024
• Subjects: Cell Nucleolus - genetics; Cell Nucleolus - metabolism; Cell Nucleus - metabolism; Coiled Bodies - metabolism; Humans; Hydro-Lyases - genetics; Hydro-Lyases - metabolism; Meiosis - genetics; Methyltransferases; Nuclear Proteins - genetics; Nuclear Proteins - metabolism; RNA and RNA-protein complexes; RNA Splicing; RNA, Small Nuclear - genetics; RNA, Small Nuclear - metabolism; Schizosaccharomyces - genetics; Schizosaccharomyces - metabolism; Schizosaccharomyces pombe Proteins - genetics; Schizosaccharomyces pombe Proteins - metabolism
• ISSN: 0305-1048; 1362-4962; 1362-4962
• DOI: 10.1093/nar/gkae463

Abstract
The Cajal body, a nuclear condensate, is crucial for ribonucleoprotein assembly, including small nuclear RNPs (snRNPs). While Coilin has been identified as an integral component of Cajal bodies, its exact function remains unclear. Moreover, no Coilin ortholog has been found in unicellular organisms to date. This study unveils Mug174 (Meiosis-upregulated gene 174) as the Coilin ortholog in the fission yeast Schizosaccharomyces pombe. Mug174 forms phase-separated condensates in vitro and is often associated with the nucleolus and the cleavage body in vivo. The generation of Mug174 foci relies on the trimethylguanosine (TMG) synthase Tgs1. Moreover, Mug174 interacts with Tgs1 and U snRNAs. Deletion of the mug174+ gene in S. pombe causes diverse pleiotropic phenotypes, encompassing defects in vegetative growth, meiosis, pre-mRNA splicing, TMG capping of U snRNAs, and chromosome segregation. In addition, we identified weak homology between Mug174 and human Coilin. Notably, human Coilin expressed in fission yeast colocalizes with Mug174. Critically, Mug174 is indispensable for the maintenance of and transition from cellular quiescence. These findings highlight the Coilin ortholog in fission yeast and suggest that the Cajal body is implicated in cellular quiescence, thereby preventing human diseases.
Graphical Abstract
Graphical Abstract