A cooperative network at the nuclear envelope counteracts LINC-mediated forces during oogenesis in C. elegans

Liu, Chenshu; Rex, Rachel; Lung, Zoe; Wang, John S.; Wu, Fan; Kim, Hyung Jun; Zhang, Liangyu; Sohn, Lydia L.; Dernburg, Abby F.

doi:10.1126/sciadv.abn5709

A cooperative network at the nuclear envelope counteracts LINC-mediated forces during oogenesis in C. elegans

Journal Article · Wed Jul 12 00:00:00 EDT 2023 · Science Advances

DOI:https://doi.org/10.1126/sciadv.abn5709· OSTI ID:2470581

^[1]; ^[2]; Lung, Zoe ^[3]; ^[3]; Wu, Fan ^[3]; ^[2]; ^[1]; ^[2]; ^[4]

University of California, Berkeley, CA (United States); Howard Hughes Medical Institute, Chevy Chase, MD (United States)
University of California, Berkeley, CA (United States)
Howard Hughes Medical Institute, Chevy Chase, MD (United States)
University of California, Berkeley, CA (United States); Howard Hughes Medical Institute, Chevy Chase, MD (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Oogenesis involves transduction of mechanical forces from the cytoskeleton to the nuclear envelope (NE). In Caenorhabditis elegans, 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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470581

Journal Information:: Science Advances, Journal Name: Science Advances Journal Issue: 28 Vol. 9; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (91)

Nuclear lamins and laminopathies Worman, Howard J. The Journal of Pathology, Vol. 226, Issue 2 https://doi.org/10.1002/path.2999	journal	November 2011
Direct Interaction between Emerin and Lamin A Clements, L.; Manilal, S.; Love, D. R. Biochemical and Biophysical Research Communications, Vol. 267, Issue 3 https://doi.org/10.1006/bbrc.1999.2023	journal	January 2000
Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans Timmons, Lisa; Court, Donald L.; Fire, Andrew Gene, Vol. 263, Issue 1-2 https://doi.org/10.1016/S0378-1119(00)00579-5	journal	January 2001
Genome-wide RNAi screening in Caenorhabditis elegans Kamath, R. Methods, Vol. 30, Issue 4 https://doi.org/10.1016/S1046-2023(03)00050-1	journal	August 2003
A Conserved Checkpoint Pathway Mediates DNA Damage–Induced Apoptosis and Cell Cycle Arrest in C. elegans Gartner, Anton; Milstein, Stuart; Ahmed, Shawn Molecular Cell, Vol. 5, Issue 3 https://doi.org/10.1016/S1097-2765(00)80438-4	journal	March 2000
LINC complexes as regulators of meiosis Burke, Brian Current Opinion in Cell Biology, Vol. 52 https://doi.org/10.1016/j.ceb.2018.01.005	journal	June 2018
Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans MacQueen, Amy J.; Phillips, Carolyn M.; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.034	journal	December 2005
HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis Phillips, Carolyn M.; Wong, Chihunt; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.035	journal	December 2005
SEPA-1 Mediates the Specific Recognition and Degradation of P Granule Components by Autophagy in C. elegans Zhang, Yuxia; Yan, Libo; Zhou, Zhi Cell, Vol. 136, Issue 2 https://doi.org/10.1016/j.cell.2008.12.022	journal	January 2009
Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis Sato, Aya; Isaac, Berith; Phillips, Carolyn M. Cell, Vol. 139, Issue 5 https://doi.org/10.1016/j.cell.2009.10.039	journal	November 2009
C. elegans Screen Identifies Autophagy Genes Specific to Multicellular Organisms Tian, Ye; Li, Zhipeng; Hu, Wanqiu Cell, Vol. 141, Issue 6 https://doi.org/10.1016/j.cell.2010.04.034	journal	June 2010
A High-Resolution C. elegans Essential Gene Network Based on Phenotypic Profiling of a Complex Tissue Green, Rebecca A.; Kao, Huey-Ling; Audhya, Anjon Cell, Vol. 145, Issue 3 https://doi.org/10.1016/j.cell.2011.03.037	journal	April 2011
COSA-1 Reveals Robust Homeostasis and Separable Licensing and Reinforcement Steps Governing Meiotic Crossovers Yokoo, Rayka; Zawadzki, Karl A.; Nabeshima, Kentaro Cell, Vol. 149, Issue 1 https://doi.org/10.1016/j.cell.2012.01.052	journal	March 2012
Catastrophic Nuclear Envelope Collapse in Cancer Cell Micronuclei Hatch, Emily M.; Fischer, Andrew H.; Deerinck, Thomas J. Cell, Vol. 154, Issue 1 https://doi.org/10.1016/j.cell.2013.06.007	journal	July 2013
Direct Visualization Reveals Kinetics of Meiotic Chromosome Synapsis Rog, Ofer; Dernburg, Abby F. Cell Reports, Vol. 10, Issue 10 https://doi.org/10.1016/j.celrep.2015.02.032	journal	March 2015
Mechanism and Regulation of Rapid Telomere Prophase Movements in Mouse Meiotic Chromosomes Lee, Chih-Ying; Horn, Henning F.; Stewart, Colin L. Cell Reports, Vol. 11, Issue 4 https://doi.org/10.1016/j.celrep.2015.03.045	journal	April 2015
A Family of Zinc-Finger Proteins Is Required for Chromosome-Specific Pairing and Synapsis during Meiosis in C. elegans Phillips, Carolyn M.; Dernburg, Abby F. Developmental Cell, Vol. 11, Issue 6 https://doi.org/10.1016/j.devcel.2006.09.020	journal	December 2006
The Nuclear Envelope Protein Matefin/SUN-1 Is Required for Homologous Pairing in C. elegans Meiosis Penkner, Alexandra; Tang, Lois; Novatchkova, Maria Developmental Cell, Vol. 12, Issue 6 https://doi.org/10.1016/j.devcel.2007.05.004	journal	June 2007
Pairing Centers Recruit a Polo-like Kinase to Orchestrate Meiotic Chromosome Dynamics in C. elegans Harper, Nicola C.; Rillo, Regina; Jover-Gil, Sara Developmental Cell, Vol. 21, Issue 5 https://doi.org/10.1016/j.devcel.2011.09.001	journal	November 2011
Transient and Partial Nuclear Lamina Disruption Promotes Chromosome Movement in Early Meiotic Prophase Link, Jana; Paouneskou, Dimitra; Velkova, Maria Developmental Cell, Vol. 45, Issue 2 https://doi.org/10.1016/j.devcel.2018.03.018	journal	April 2018
Mechanical phenotyping reveals unique biomechanical responses in retinoic acid-resistant acute promyelocytic leukemia Li, Brian; Maslan, Annie; Kitayama, Sean E. iScience, Vol. 25, Issue 2 https://doi.org/10.1016/j.isci.2022.103772	journal	February 2022
Meiotic recombination and the crossover assurance checkpoint in Caenorhabditis elegans Yu, Zhouliang; Kim, Yumi; Dernburg, Abby F. Seminars in Cell & Developmental Biology, Vol. 54 https://doi.org/10.1016/j.semcdb.2016.03.014	journal	June 2016
Nuclear positioning in migrating fibroblasts Zhu, Ruijun; Liu, Chenshu; Gundersen, Gregg G. Seminars in Cell & Developmental Biology, Vol. 82 https://doi.org/10.1016/j.semcdb.2017.11.006	journal	October 2018
Broken nuclei – lamins, nuclear mechanics, and disease Davidson, Patricia M.; Lammerding, Jan Trends in Cell Biology, Vol. 24, Issue 4 https://doi.org/10.1016/j.tcb.2013.11.004	journal	April 2014
Proteins that associate with lamins: Many faces, many functions Schirmer, Eric C.; Foisner, Roland Experimental Cell Research, Vol. 313, Issue 10 https://doi.org/10.1016/j.yexcr.2007.03.012	journal	June 2007
Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins McKeon, Frank D.; Kirschner, Marc W.; Caput, Daniel Nature, Vol. 319, Issue 6053 https://doi.org/10.1038/319463a0	journal	February 1986
The nuclear lamina is a meshwork of intermediate-type filaments Aebi, Ueli; Cohn, Julie; Buhle, Loren Nature, Vol. 323, Issue 6088 https://doi.org/10.1038/323560a0	journal	October 1986
Characterizing cellular mechanical phenotypes with mechano-node-pore sensing Kim, Junghyun; Han, Sewoon; Lei, Andy Microsystems & Nanoengineering, Vol. 4, Issue 1 https://doi.org/10.1038/micronano.2017.91	journal	March 2018
Systematic functional analysis of the Caenorhabditis elegans genome using RNAi Kamath, Ravi S.; Fraser, Andrew G.; Dong, Yan Nature, Vol. 421, Issue 6920 https://doi.org/10.1038/nature01278	journal	January 2003
Dynein links engulfment and execution of apoptosis via CED-4/Apaf1 in C. elegans Harders, Rikke Hindsgaul; Morthorst, Tine Hørning; Lande, Anna Dippel Cell Death & Disease, Vol. 9, Issue 10 https://doi.org/10.1038/s41419-018-1067-y	journal	September 2018
Mutant lamins cause nuclear envelope rupture and DNA damage in skeletal muscle cells Earle, Ashley J.; Kirby, Tyler J.; Fedorchak, Gregory R. Nature Materials, Vol. 19, Issue 4 https://doi.org/10.1038/s41563-019-0563-5	journal	December 2019
A hydraulic instability drives the cell death decision in the nematode germline Chartier, Nicolas T.; Mukherjee, Arghyadip; Pfanzelter, Julia Nature Physics, Vol. 17, Issue 8 https://doi.org/10.1038/s41567-021-01235-x	journal	May 2021
Depletion of the LINC complex disrupts cytoskeleton dynamics and meiotic resumption in mouse oocytes Luo, Yibo; Lee, In-Won; Jo, Yu-Jin Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep20408	journal	February 2016
Correcting off-axis effects in an on-chip resistive-pulse analyzer Saleh, O. A.; Sohn, L. L. Review of Scientific Instruments, Vol. 73, Issue 12 https://doi.org/10.1063/1.1519932	journal	December 2002
Counting and Sizing of Submicron Particles by the Resistive Pulse Technique DeBlois, R. W.; Bean, C. P. Review of Scientific Instruments, Vol. 41, Issue 7 https://doi.org/10.1063/1.1684724	journal	July 1970
Age-related changes of nuclear architecture inCaenorhabditis elegans Haithcock, Erin; Dayani, Yaron; Neufeld, Ester Proceedings of the National Academy of Sciences, Vol. 102, Issue 46 https://doi.org/10.1073/pnas.0506955102	journal	November 2005
Matefin/SUN-1 is a nuclear envelope receptor for CED-4 during Caenorhabditis elegans apoptosis Tzur, Yonatan B.; Margalit, Ayelet; Melamed-Book, Naomi Proceedings of the National Academy of Sciences, Vol. 103, Issue 36 https://doi.org/10.1073/pnas.0604224103	journal	September 2006
Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement Folker, Eric S.; Östlund, Cecilia; Luxton, G. W. Gant Proceedings of the National Academy of Sciences, Vol. 108, Issue 1 https://doi.org/10.1073/pnas.1000824108	journal	December 2010
Imbalanced nucleocytoskeletal connections create common polarity defects in progeria and physiological aging Chang, Wakam; Wang, Yuexia; Luxton, G. W. Gant Proceedings of the National Academy of Sciences, Vol. 116, Issue 9 https://doi.org/10.1073/pnas.1809683116	journal	February 2019
Decreased mechanotransduction prevents nuclear collapse in a Caenorhabditis elegans laminopathy Huelgas-Morales, Gabriela; Sanders, Mark; Mekonnen, Gemechu Proceedings of the National Academy of Sciences, Vol. 117, Issue 49 https://doi.org/10.1073/pnas.2015050117	journal	November 2020
Keratin-like proteins that coisolate with intermediate filaments of BHK-21 cells are nuclear lamins. Goldman, A. E.; Maul, G.; Steinert, P. M. Proceedings of the National Academy of Sciences, Vol. 83, Issue 11 https://doi.org/10.1073/pnas.83.11.3839	journal	June 1986
A dynein independent role of Tctex-1 at the kinetochore Liu, Chenshu; Chuang, Jen-Zen; Sung, Ching-Hwa Cell Cycle, Vol. 14, Issue 9 https://doi.org/10.1080/15384101.2014.1000217	journal	April 2015
A ZYG-12–dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad Zhou, Kang; Rolls, Melissa M.; Hall, David H. Journal of Cell Biology, Vol. 186, Issue 2 https://doi.org/10.1083/jcb.200902101	journal	July 2009
Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis Wynne, David J.; Rog, Ofer; Carlton, Peter M. Journal of Cell Biology, Vol. 196, Issue 1 https://doi.org/10.1083/jcb.201106022	journal	January 2012
Spindle assembly checkpoint proteins regulate and monitor meiotic synapsis in C. elegans Bohr, Tisha; Nelson, Christian R.; Klee, Erin Journal of Cell Biology, Vol. 211, Issue 2 https://doi.org/10.1083/jcb.201409035	journal	October 2015
Accessorizing and anchoring the LINC complex for multifunctionality Chang, Wakam; Worman, Howard J.; Gundersen, Gregg G. Journal of Cell Biology, Vol. 208, Issue 1 https://doi.org/10.1083/jcb.201409047	journal	January 2015
Essential Roles forCaenorhabditis elegansLamin Gene in Nuclear Organization, Cell Cycle Progression, and Spatial Organization of Nuclear Pore Complexes Liu, Jun; Ben-Shahar, Tom Rolef; Riemer, Dieter Molecular Biology of the Cell, Vol. 11, Issue 11 https://doi.org/10.1091/mbc.11.11.3937	journal	November 2000
Dynein pulling forces counteract lamin-mediated nuclear stability during nuclear envelope repair Penfield, Lauren; Wysolmerski, Brian; Mauro, Michael Molecular Biology of the Cell, Vol. 29, Issue 7 https://doi.org/10.1091/mbc.E17-06-0374	journal	April 2018
SUN-1 and ZYG-12, Mediators of Centrosome–Nucleus Attachment, Are a Functional SUN/KASH Pair in Caenorhabditis elegans Minn, Il; Rolls, Melissa M.; Hanna-Rose, Wendy Molecular Biology of the Cell, Vol. 20, Issue 21 https://doi.org/10.1091/mbc.e08-10-1034	journal	November 2009
The Caenorhabditis elegans SUN protein UNC-84 interacts with lamin to transfer forces from the cytoplasm to the nucleoskeleton during nuclear migration Bone, Courtney R.; Tapley, Erin C.; Gorjánácz, Mátyás Molecular Biology of the Cell, Vol. 25, Issue 18 https://doi.org/10.1091/mbc.e14-05-0971	journal	September 2014
Roles for Caenorhabditis elegans rad-51 in Meiosis and in Resistance to Ionizing Radiation During Development Rinaldo, Cinzia; Bazzicalupo, Paolo; Ederle, Sara Genetics, Vol. 160, Issue 2 https://doi.org/10.1093/genetics/160.2.471	journal	February 2002
THE GENETICS OF CAENORHABDITIS ELEGANS Brenner, S. Genetics, Vol. 77, Issue 1 https://doi.org/10.1093/genetics/77.1.71	journal	May 1974
Interaction between Emerin and Nuclear Lamins Sakaki, M.; Koike, H.; Takahashi, N. Journal of Biochemistry, Vol. 129, Issue 2 https://doi.org/10.1093/oxfordjournals.jbchem.a002860	journal	February 2001
Nuclear Lamins Dechat, T.; Adam, S. A.; Taimen, P. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 11 https://doi.org/10.1101/cshperspect.a000547	journal	September 2010
Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans MacQueen, A. J. Genes & Development, Vol. 16, Issue 18 https://doi.org/10.1101/gad.1011602	journal	September 2002
Caenorhabditis elegans ortholog of the p24/p22 subunit, DNC‐3, is essential for the formation of the dynactin complex by bridging DNC‐1/p150^Glued and DNC‐2/dynamitin Terasawa, Masahiro; Toya, Mika; Motegi, Fumio Genes to Cells, Vol. 15, Issue 11 https://doi.org/10.1111/j.1365-2443.2010.01451.x	journal	October 2010
Inner nuclear membrane protein Ima1 is dispensable for intranuclear positioning of centromeres Hiraoka, Yasushi; Maekawa, Hiromi; Asakawa, Haruhiko Genes to Cells, Vol. 16, Issue 10 https://doi.org/10.1111/j.1365-2443.2011.01544.x	journal	September 2011
Mechanical stress accompanied with nuclear rotation is involved in the dormant state of mouse oocytes Nagamatsu, Go; Shimamoto, So; Hamazaki, Nobuhiko Science Advances, Vol. 5, Issue 6 https://doi.org/10.1126/sciadv.aav9960	journal	June 2019
The NEMP family supports metazoan fertility and nuclear envelope stiffness Tsatskis, Yonit; Rosenfeld, Robyn; Pearson, Joel D. Science Advances, Vol. 6, Issue 35 https://doi.org/10.1126/sciadv.abb4591	journal	August 2020
MJL-1 is a nuclear envelope protein required for homologous chromosome pairing and regulation of synapsis during meiosis in C. elegans Kim, Hyung Jun; Liu, Chenshu; Zhang, Liangyu Science Advances, Vol. 9, Issue 6 https://doi.org/10.1126/sciadv.add1453	journal	February 2023
A Conserved Checkpoint Monitors Meiotic Chromosome Synapsis in Caenorhabditis elegans Bhalla, N. Science, Vol. 310, Issue 5754 https://doi.org/10.1126/science.1117468	journal	December 2005
Integrative Analysis of the Caenorhabditis elegans Genome by the modENCODE Project Gerstein, M. B.; Lu, Z. J.; Van Nostrand, E. L. Science, Vol. 330, Issue 6012 https://doi.org/10.1126/science.1196914	journal	December 2010
Nuclear Lamin-A Scales with Tissue Stiffness and Enhances Matrix-Directed Differentiation Swift, Joe; Ivanovska, Irena L.; Buxboim, Amnon Science, Vol. 341, Issue 6149 https://doi.org/10.1126/science.1240104	journal	August 2013
Nuclear envelope rupture and repair during cancer cell migration Denais, Celine M.; Gilbert, Rachel M.; Isermann, Philipp Science, Vol. 352, Issue 6283 https://doi.org/10.1126/science.aad7297	journal	April 2016
Prelude to a Division Bhalla, Needhi; Dernburg, Abby F. Annual Review of Cell and Developmental Biology, Vol. 24, Issue 1 https://doi.org/10.1146/annurev.cellbio.23.090506.123245	journal	November 2008
Nuclear Lamins: Laminopathies and Their Role in Premature Ageing Broers, J. L. V.; Ramaekers, F. C. S.; Bonne, G. Physiological Reviews, Vol. 86, Issue 3 https://doi.org/10.1152/physrev.00047.2005	journal	July 2006
Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2 Ikegami, Kohta; Egelhofer, Thea A.; Strome, Susan Genome Biology, Vol. 11, Issue 12 https://doi.org/10.1186/gb-2010-11-12-r120	journal	January 2010
Pushing the (nuclear) envelope into meiosis Dernburg, Abby F. Genome Biology, Vol. 14, Issue 3 https://doi.org/10.1186/gb-2013-14-3-110	journal	March 2013
Isolated C. elegans germ nuclei exhibit distinct genomic profiles of histone modification and gene expression Han, Mei; Wei, Guifeng; McManus, Catherine E. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5893-9	journal	June 2019
Fertility and Obstetrical Complications in Women withLMNA-Related Familial Partial Lipodystrophy Vantyghem, M. C.; Vincent-Desplanques, D.; Defrance-Faivre, F. The Journal of Clinical Endocrinology & Metabolism, Vol. 93, Issue 6 https://doi.org/10.1210/jc.2007-2521	journal	June 2008
Germline and developmental roles of the nuclear transport factor importin α3 in C. elegans Geles, Kenneth G.; Adam, Stephen A. Development, Vol. 128, Issue 10 https://doi.org/10.1242/dev.128.10.1817	journal	May 2001
Nesprins and opposing microtubule motors generate a point force that drives directional nuclear motion in migrating neurons Wu, You Kure; Umeshima, Hiroki; Kurisu, Junko Development, Vol. 145, Issue 5 https://doi.org/10.1242/dev.158782	journal	March 2018
Src and Wnt signaling regulate dynactin accumulation to the P2-EMS cell border inC. elegansembryos Zhang, Haining; Skop, Ahna R.; White, John G. Journal of Cell Science, Vol. 121, Issue 2 https://doi.org/10.1242/jcs.015966	journal	January 2008
LEM2 is a novel MAN1-related inner nuclear membrane protein associated with A-type lamins Brachner, Andreas; Reipert, Siegfried; Foisner, Roland Journal of Cell Science, Vol. 118, Issue 24 https://doi.org/10.1242/jcs.02701	journal	December 2005
Samp1 is functionally associated with the LINC complex and A-type lamina networks Gudise, Santhosh; Figueroa, Ricardo A.; Lindberg, Robert Journal of Cell Science, Vol. 124, Issue 12 https://doi.org/10.1242/jcs.078923	journal	June 2011
Samp1 is a component of TAN lines and is required for nuclear movement Borrego-Pinto, J.; Jegou, T.; Osorio, D. S. Journal of Cell Science, Vol. 125, Issue 5 https://doi.org/10.1242/jcs.087049	journal	February 2012
Drosophila emerins control LINC complex localization and transcription to regulate myonuclear position Mandigo, Torrey R.; Turcich, Blake D.; Anderson, Alyssa J. Journal of Cell Science, Vol. 132, Issue 20 https://doi.org/10.1242/jcs.235580	journal	October 2019
Dynein Modifiers in C. elegans: Light Chains Suppress Conditional Heavy Chain Mutants O'Rourke, Sean M.; Dorfman, Marc D.; Carter, J. Clayton PLoS Genetics, Vol. 3, Issue 8 https://doi.org/10.1371/journal.pgen.0030128	journal	August 2007
The Meiotic Nuclear Lamina Regulates Chromosome Dynamics and Promotes Efficient Homologous Recombination in the Mouse Link, Jana; Jahn, Daniel; Schmitt, Johannes PLoS Genetics, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pgen.1003261	journal	January 2013
Analysis of Meiosis in SUN1 Deficient Mice Reveals a Distinct Role of SUN2 in Mammalian Meiotic LINC Complex Formation and Function Link, Jana; Leubner, Monika; Schmitt, Johannes PLoS Genetics, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pgen.1004099	journal	February 2014
Binucleate germ cells in Caenorhabditis elegans are removed by physiological apoptosis Raiders, Stephan A.; Eastwood, Michael D.; Bacher, Meghan PLOS Genetics, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pgen.1007417	journal	July 2018
Efficient Marker-Free Recovery of Custom Genetic Modifications with CRISPR/Cas9 in Caenorhabditis elegans Arribere, Joshua A.; Bell, Ryan T.; Fu, Becky X. H. Genetics, Vol. 198, Issue 3 https://doi.org/10.1534/genetics.114.169730	journal	August 2014
High Efficiency, Homology-Directed Genome Editing in Caenorhabditis elegans Using CRISPR-Cas9 Ribonucleoprotein Complexes Paix, Alexandre; Folkmann, Andrew; Rasoloson, Dominique Genetics, Vol. 201, Issue 1 https://doi.org/10.1534/genetics.115.179382	journal	July 2015
Synaptonemal Complex Components Are Required for Meiotic Checkpoint Function in Caenorhabditis elegans Bohr, Tisha; Ashley, Guinevere; Eggleston, Evan Genetics, Vol. 204, Issue 3 https://doi.org/10.1534/genetics.116.191494	journal	November 2016
Mps2 links Csm4 and Mps3 to form a telomere-associated LINC complex in budding yeast Fan, Jinbo; Jin, Hui; Koch, Bailey A. Life Science Alliance, Vol. 3, Issue 12 https://doi.org/10.26508/lsa.202000824	journal	September 2020
How and Why Chromosomes Interact with the Cytoskeleton during Meiosis Kim, Hyung Jun; Liu, Chenshu; Dernburg, Abby F. Genes, Vol. 13, Issue 5 https://doi.org/10.3390/genes13050901	journal	May 2022
The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors Rog, Ofer; Köhler, Simone; Dernburg, Abby F. eLife, Vol. 6 https://doi.org/10.7554/eLife.21455	journal	January 2017
A compartmentalized signaling network mediates crossover control in meiosis Zhang, Liangyu; Köhler, Simone; Rillo-Bohn, Regina eLife, Vol. 7 https://doi.org/10.7554/eLife.30789	journal	March 2018
Cell-intrinsic and -extrinsic mechanisms promote cell-type-specific cytokinetic diversity Davies, Tim; Kim, Han X.; Romano Spica, Natalia eLife, Vol. 7 https://doi.org/10.7554/eLife.36204	journal	July 2018
Micronuclei-based model system reveals functional consequences of chromothripsis in human cells Kneissig, Maja; Keuper, Kristina; de Pagter, Mirjam S. eLife, Vol. 8 https://doi.org/10.7554/eLife.50292	journal	November 2019
PLK-1 promotes the merger of the parental genome into a single nucleus by triggering lamina disassembly Velez-Aguilera, Griselda; Nkombo Nkoula, Sylvia; Ossareh-Nazari, Batool eLife, Vol. 9 https://doi.org/10.7554/eLife.59510	journal	October 2020

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A cooperative network at the nuclear envelope counteracts LINC-mediated forces during oogenesis in C. elegans

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