Super-resolution imaging reveals nucleolar encapsulation by single-stranded DNA

被引:1
作者
Maki, Koichiro [1 ,2 ,3 ,4 ]
Fukute, Jumpei [1 ,3 ]
Adachi, Taiji [1 ,2 ,3 ,4 ]
机构
[1] Kyoto Univ, Inst Life & Med Sci, Lab Biomech, 53 Shogoin Kawahara,Sakyo Ku, Kyoto 6068507, Japan
[2] Kyoto Univ, Grad Sch Engn, Dept Micro Engn, 53 Shogoin Kawahara,Sakyo Ku, Kyoto 6068507, Japan
[3] Kyoto Univ, Grad Sch Biostudies, Dept Mammalian Regulatory Network, 53 Shogoin Kawahara,Sakyo Ku, Kyoto, 6068507, Japan
[4] Kyoto Univ, Grad Sch Med, Dept Med & Med Sci, 53 Shogoin Kawahara,Sakyo Ku, Kyoto 6068507, Japan
基金
日本学术振兴会; 日本科学技术振兴机构;
关键词
Single-stranded DNA; Nucleolus; Nucleus; DNA- protein interaction; In situ imaging; Super-resolution imaging; HISTONE H1; NUCLEAR; GENOME; CHROMATIN; EXPRESSION; DOMAINS; PROTEIN; ACTIN;
D O I
10.1242/jcs.262039
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
In eukaryotic cell nuclei, specific sets of proteins gather in nuclear bodies and facilitate distinct genomic processes. The nucleolus, a nuclear body, functions as a factory for ribosome biogenesis by accumulating constitutive proteins, such as RNA polymerase I and nucleophosmin 1 (NPM1). Although in vitro assays have suggested the importance of liquid-liquid phase separation (LLPS) of constitutive proteins in nucleolar formation, how the nucleolus is structurally maintained with the intranuclear architecture remains unknown. This study revealed that the nucleolus is encapsulated by a single-stranded (ss)DNA-based molecular complex inside the cell nucleus. Super-resolution lattice-structured illumination microscopy (lattice-SIM) showed that there was a high abundance of ssDNA beyond the 'outer shell' of the nucleolus. Nucleolar disruption and the release of NPM1 were caused by in situ digestion of ssDNA, suggesting that ssDNA has a structural role in nucleolar encapsulation. Furthermore, we identified that ssDNA forms a molecular complex with histone H1 for nucleolar encapsulation. Thus, this study illustrates how an ssDNA-based molecular complex upholds the structural integrity of nuclear bodies to coordinate genomic processes such as gene transcription and replication.
引用
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页数:8
相关论文
共 58 条
[1]   Nucleolar RNA polymerase II drives ribosome biogenesis [J].
Abraham, Karan J. ;
Khosraviani, Negin ;
Chan, Janet N. Y. ;
Gorthi, Aparna ;
Samman, Anas ;
Zhao, Dorothy Y. ;
Wang, Miling ;
Bokros, Michael ;
Vidya, Elva ;
Ostrowski, Lauren A. ;
Oshidari, Roxanne ;
Pietrobon, Violena ;
Patel, Parasvi S. ;
Algouneh, Arash ;
Singhania, Rajat ;
Liu, Yupeng ;
Yerlici, V. Talya ;
De Carvalho, Daniel D. ;
Ohh, Michael ;
Dickson, Brendan C. ;
Hakem, Razq ;
Greenblatt, Jack F. ;
Lee, Stephen ;
Bishop, Alexander J. R. ;
Mekhail, Karim .
NATURE, 2020, 585 (7824) :298-+
[2]   Compositional Control of Phase-Separated Cellular Bodies [J].
Banani, Salman F. ;
Rice, Allyson M. ;
Peeples, William B. ;
Lin, Yuan ;
Jain, Saumya ;
Parker, Roy ;
Rosen, Michael K. .
CELL, 2016, 166 (03) :651-663
[3]   Protein Encapsulation Using Complex Coacervates: What Nature Has to Teach Us [J].
Blocher McTigue, Whitney C. ;
Perry, Sarah L. .
SMALL, 2020, 16 (27)
[4]   The linker histone H1.2 is a novel component of the nucleolar organizer regions [J].
Chen, Junjie ;
Teo, Boon Heng Dennis ;
Cai, Yitian ;
Wee, Seng Yin Kelly ;
Lu, Jinhua .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2018, 293 (07) :2358-2369
[5]   Nuclear actin and myosins at a glance [J].
de Lanerolle, Primal .
JOURNAL OF CELL SCIENCE, 2012, 125 (21) :4945-4949
[6]   ssDNA accessibility of Rad51 is regulated by orchestrating multiple RPA dynamics [J].
Ding, Jiawei ;
Li, Xiangting ;
Shen, Jiangchuan ;
Zhao, Yiling ;
Zhong, Shuchen ;
Lai, Luhua ;
Niu, Hengyao ;
Qi, Zhi .
NATURE COMMUNICATIONS, 2023, 14 (01)
[7]   Coexisting Liquid Phases Underlie Nucleolar Subcompartments [J].
Feric, Marina ;
Vaidya, Nilesh ;
Harmon, Tyler S. ;
Mitrea, Diana M. ;
Zhu, Lian ;
Richardson, Tiffany M. ;
Kriwacki, Richard W. ;
Pappu, Rohit V. ;
Brangwynne, Clifford P. .
CELL, 2016, 165 (07) :1686-1697
[8]   A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells [J].
Feric, Marina ;
Brangwynne, Clifford P. .
NATURE CELL BIOLOGY, 2013, 15 (10) :1253-U295
[9]   The nucleolus functions as a phase-separated protein quality control compartment [J].
Frottin, F. ;
Schueder, F. ;
Tiwary, S. ;
Gupta, R. ;
Koerner, R. ;
Schlichthaerle, T. ;
Cox, J. ;
Jungmann, R. ;
Hartl, F. U. ;
Hipp, M. S. .
SCIENCE, 2019, 365 (6451) :342-+
[10]   The nucleolar shell provides anchoring sites for DNA untwisting [J].
Fukute, Jumpei ;
Maki, Koichiro ;
Adachi, Taiji .
COMMUNICATIONS BIOLOGY, 2024, 7 (01)