A Cooperative Network at the Nuclear Envelope Counteracts LINC-mediated Forces During Oogenesis in

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2023 Jul 12

PMID 37436986

Authors

Chenshu Liu

Rachel Rex

Zoe Lung

John S Wang

Fan Wu

Hyung Jun Kim

Liangyu Zhang

Lydia L Sohn

Abby F Dernburg

Affiliations

Soon will be listed here.

Abstract

Oogenesis involves transduction of mechanical forces from the cytoskeleton to the nuclear envelope (NE). In , oocyte nuclei lacking the single lamin protein LMN-1 are vulnerable to collapse under forces mediated through LINC (linker of nucleoskeleton and cytoskeleton) complexes. Here, we use cytological analysis and in vivo imaging to investigate the balance of forces that drive this collapse and protect oocyte nuclei. We also use a mechano-node-pore sensing device to directly measure the effect of genetic mutations on oocyte nuclear stiffness. We find that nuclear collapse is not a consequence of apoptosis. It is promoted by dynein, which induces polarization of a LINC complex composed of Sad1 and UNC-84 homology 1 (SUN-1) and ZYGote defective 12 (ZYG-12). Lamins contribute to oocyte nuclear stiffness and cooperate with other inner nuclear membrane proteins to distribute LINC complexes and protect nuclei from collapse. We speculate that a similar network may protect oocyte integrity during extended oocyte arrest in mammals.

Citing Articles

Rapid meiotic prophase chromosome movements in Arabidopsis thaliana are linked to essential reorganization at the nuclear envelope.

Cromer L, Tiscareno-Andrade M, Lefranc S, Chambon A, Hurel A, Brogniez M Nat Commun. 2024; 15(1):5964.

PMID: 39013853 PMC: 11252379. DOI: 10.1038/s41467-024-50169-4.

Mechanochemical coupling of MGF mediates periodontal regeneration.

Zhao Y, Zhang S, Cheng B, Feng F, Zhu Y, Liu Y Bioeng Transl Med. 2024; 9(1):e10603.

PMID: 38193124 PMC: 10771565. DOI: 10.1002/btm2.10603.

Split-GFP lamin as a tool for studying LMN-1 dynamics .

Gregory E, Ragle J, Ward J, Starr D MicroPubl Biol. 2023; 2023.

PMID: 38152058 PMC: 10751582. DOI: 10.17912/micropub.biology.001022.

The molecular regulatory mechanisms of meiotic arrest and resumption in Oocyte development and maturation.

Pei Z, Deng K, Xu C, Zhang S Reprod Biol Endocrinol. 2023; 21(1):90.

PMID: 37784186 PMC: 10544615. DOI: 10.1186/s12958-023-01143-0.

References

Wu Y, Umeshima H, Kurisu J, Kengaku M . Nesprins and opposing microtubule motors generate a point force that drives directional nuclear motion in migrating neurons. Development. 2018; 145(5). DOI: 10.1242/dev.158782. View

Davies T, Kim H, Romano Spica N, Lesea-Pringle B, Dumont J, Shirasu-Hiza M . Cell-intrinsic and -extrinsic mechanisms promote cell-type-specific cytokinetic diversity. Elife. 2018; 7. PMC: 6054530. DOI: 10.7554/eLife.36204. View

Bhalla N, Dernburg A . Prelude to a division. Annu Rev Cell Dev Biol. 2008; 24:397-424. PMC: 4435778. DOI: 10.1146/annurev.cellbio.23.090506.123245. View

Chang W, Wang Y, Luxton G, Ostlund C, Worman H, Gundersen G . Imbalanced nucleocytoskeletal connections create common polarity defects in progeria and physiological aging. Proc Natl Acad Sci U S A. 2019; 116(9):3578-3583. PMC: 6397528. DOI: 10.1073/pnas.1809683116. View

Link J, Leubner M, Schmitt J, Gob E, Benavente R, Jeang K . Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic LINC complex formation and function. PLoS Genet. 2014; 10(2):e1004099. PMC: 3937131. DOI: 10.1371/journal.pgen.1004099. View

Zhang Y, Yan L, Zhou Z, Yang P, Tian E, Zhang K . SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans. Cell. 2009; 136(2):308-21. DOI: 10.1016/j.cell.2008.12.022. View

Green R, Kao H, Audhya A, Arur S, Mayers J, Fridolfsson H . A high-resolution C. elegans essential gene network based on phenotypic profiling of a complex tissue. Cell. 2011; 145(3):470-82. PMC: 3086541. DOI: 10.1016/j.cell.2011.03.037. View

Kneissig M, Keuper K, de Pagter M, van Roosmalen M, Martin J, Otto H . Micronuclei-based model system reveals functional consequences of chromothripsis in human cells. Elife. 2019; 8. PMC: 6910827. DOI: 10.7554/eLife.50292. View

Haithcock E, Dayani Y, Neufeld E, Zahand A, Feinstein N, Mattout A . Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2005; 102(46):16690-5. PMC: 1283819. DOI: 10.1073/pnas.0506955102. View

10.

McKeon F, Kirschner M, Caput D . Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986; 319(6053):463-8. DOI: 10.1038/319463a0. View

11.

Kim J, Han S, Lei A, Miyano M, Bloom J, Srivastava V . Characterizing cellular mechanical phenotypes with mechano-node-pore sensing. Microsyst Nanoeng. 2018; 4. PMC: 5958920. DOI: 10.1038/micronano.2017.91. View

12.

Yokoo R, Zawadzki K, Nabeshima K, Drake M, Arur S, Villeneuve A . COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 2012; 149(1):75-87. PMC: 3339199. DOI: 10.1016/j.cell.2012.01.052. View

13.

Denais C, Gilbert R, Isermann P, McGregor A, Te Lindert M, Weigelin B . Nuclear envelope rupture and repair during cancer cell migration. Science. 2016; 352(6283):353-8. PMC: 4833568. DOI: 10.1126/science.aad7297. View

14.

Geles K, Adam S . Germline and developmental roles of the nuclear transport factor importin alpha3 in C. elegans. Development. 2001; 128(10):1817-30. DOI: 10.1242/dev.128.10.1817. View

15.

Huelgas-Morales G, Sanders M, Mekonnen G, Tsukamoto T, Greenstein D . Decreased mechanotransduction prevents nuclear collapse in a laminopathy. Proc Natl Acad Sci U S A. 2020; 117(49):31301-31308. PMC: 7733798. DOI: 10.1073/pnas.2015050117. View

16.

Paix A, Folkmann A, Rasoloson D, Seydoux G . High Efficiency, Homology-Directed Genome Editing in Caenorhabditis elegans Using CRISPR-Cas9 Ribonucleoprotein Complexes. Genetics. 2015; 201(1):47-54. PMC: 4566275. DOI: 10.1534/genetics.115.179382. View

17.

Bone C, Tapley E, Gorjanacz M, Starr D . The Caenorhabditis elegans SUN protein UNC-84 interacts with lamin to transfer forces from the cytoplasm to the nucleoskeleton during nuclear migration. Mol Biol Cell. 2014; 25(18):2853-65. PMC: 4161519. DOI: 10.1091/mbc.E14-05-0971. View

18.

Tsatskis Y, Rosenfeld R, Pearson J, Boswell C, Qu Y, Kim K . The NEMP family supports metazoan fertility and nuclear envelope stiffness. Sci Adv. 2020; 6(35):eabb4591. PMC: 7455189. DOI: 10.1126/sciadv.abb4591. View

19.

Rog O, Dernburg A . Direct Visualization Reveals Kinetics of Meiotic Chromosome Synapsis. Cell Rep. 2015; 10(10):1639-1645. PMC: 4565782. DOI: 10.1016/j.celrep.2015.02.032. View

20.

Han M, Wei G, McManus C, Hillier L, Reinke V . Isolated C. elegans germ nuclei exhibit distinct genomic profiles of histone modification and gene expression. BMC Genomics. 2019; 20(1):500. PMC: 6580472. DOI: 10.1186/s12864-019-5893-9. View