The ESCRT machinery directs quality control over inner nuclear membrane architecture

被引:11
作者
Shankar, Raakhee [1 ]
Lettman, Molly M. [1 ]
Whisler, William [1 ]
Frankel, Elisa B. [1 ]
Audhya, Anjon [1 ]
机构
[1] Univ Wisconsin, Dept Biomol Chem, Sch Med & Publ Hlth, Madison, WI 53705 USA
来源
CELL REPORTS | 2022年 / 38卷 / 03期
关键词
ESSENTIAL ROLES; DNA-DAMAGE; ENVELOPE; PROTEIN; HETEROCHROMATIN; SUBUNIT; CHMP7; LOCALIZATION; ORGANIZATION; CENTROSOME;
D O I
10.1016/j.celrep.2021.110263
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
The late-acting endosomal sorting complex required for transport (ESCRT) machinery has been implicated in facilitating the resealing of the nuclear envelope (NE) after mitosis, enabling compartmentalization of the genome away from the cytoplasm. Here, we leverage the stereotypic first division of the C. elegans embryo to identify additional functions of the ESCRT machinery in maintaining the structure of the inner nuclear membrane. Specifically, impaired ESCRT function results in a defect in the pruning of inner nuclear membrane invaginations, which arise normally during NE reformation and expansion. Additionally, in combination with a hypomorphic mutation that interferes with assembly of the underlying nuclear lamina, inhibition of ESCRT function significantly perturbs NE architecture and increases chromosome segregation defects, resulting in penetrant embryonic lethality. Our findings highlight links between ESCRT-mediated inner nuclear membrane remodeling, maintenance of nuclear envelope morphology, and the preservation of the genome during early development.
引用
收藏
页数:19
相关论文
共 82 条
[1]   An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome [J].
Allison, Rachel ;
Lumb, Jennifer H. ;
Fassier, Coralie ;
Connell, James W. ;
Ten Martin, Daniel ;
Seaman, Matthew N. J. ;
Hazan, Jamile ;
Reid, Evan .
JOURNAL OF CELL BIOLOGY, 2013, 202 (03) :527-543
[2]   ESCRT-III mediates budding across the inner nuclear membrane and regulates its integrity [J].
Arii, Jun ;
Watanabe, Mizuki ;
Maeda, Fumio ;
Tokai-Nishizumi, Noriko ;
Chihara, Takahiro ;
Miura, Masayuki ;
Maruzuru, Yuhei ;
Koyanagi, Naoto ;
Kato, Akihisa ;
Kawaguchi, Yasushi .
NATURE COMMUNICATIONS, 2018, 9
[3]   MVB-12, a Fourth Subunit of Metazoan ESCRT-I, Functions in Receptor Downregulation [J].
Audhya, Anjon ;
McLeod, Ian X. ;
Yates, John R., III ;
Oegema, Karen .
PLOS ONE, 2007, 2 (09)
[4]   Ce-emerin and LEM-2: essential roles in Caenorhabditis elegans development, muscle function, and mitosis [J].
Barkan, Rachel ;
Zahand, Adam J. ;
Sharabi, Kfir ;
Lamm, Ayelet T. ;
Feinstein, Naomi ;
Haithcock, Erin ;
Wilson, Katherine L. ;
Liu, Jun ;
Gruenbaum, Yosef .
MOLECULAR BIOLOGY OF THE CELL, 2012, 23 (04) :543-552
[5]   Control of heterochromatin localization and silencing by the nuclear membrane protein Lem2 [J].
Barrales, Ramon Ramos ;
Forn, Marta ;
Georgescu, Paula Raluca ;
Sarkadi, Zsuzsa ;
Braun, Sigurd .
GENES & DEVELOPMENT, 2016, 30 (02) :133-148
[6]   Mitotic Chromosome Mechanics: How Cells Segregate Their Genome [J].
Batty, Paul ;
Gerlich, Daniel W. .
TRENDS IN CELL BIOLOGY, 2019, 29 (09) :717-726
[7]   Evidence for a Nonendosomal Function of the Saccharomyces cerevisiae ESCRT-III-Like Protein Chm7 [J].
Bauer, Iva ;
Brune, Thomas ;
Preiss, Richard ;
Koelling, Ralf .
GENETICS, 2015, 201 (04) :1439-1452
[8]  
Bertin A, 2020, NAT COMMUN, V11, DOI 10.1038/s41467-020-16368-5
[9]   Coaching from the sidelines: the nuclear periphery in genome regulation [J].
Buchwalter, Abigail ;
Kaneshiro, Jeanae M. ;
Hetzer, Martin W. .
NATURE REVIEWS GENETICS, 2019, 20 (01) :39-50
[10]   Active chromatin marks drive spatial sequestration of heterochromatin in C. elegans nuclei [J].
Cabianca, Daphne S. ;
Munoz-Jimenez, Celia ;
Kalck, Veronique ;
Gaidatzis, Dimos ;
Padeken, Jan ;
Seeber, Andrew ;
Askjaer, Peter ;
Gasser, Susan M. .
NATURE, 2019, 569 (7758) :734-+