ATM signaling modulates cohesin behavior in meiotic prophase and proliferating cells

Yu, Zhouliang; Kim, Hyung Jun; Dernburg, Abby F.

doi:10.1038/s41594-023-00929-5

ATM signaling modulates cohesin behavior in meiotic prophase and proliferating cells

Journal Article · Mon Mar 06 00:00:00 EST 2023 · Nature Structural & Molecular Biology

DOI:https://doi.org/10.1038/s41594-023-00929-5· OSTI ID:2470954

^[1]; Kim, Hyung Jun ^[2]; ^[1]

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); California Institute for Quantitative Biosciences (QB3), Berkeley, CA (United States)
University of California, Berkeley, CA (United States)

Cohesins are ancient and ubiquitous regulators of chromosome architecture and function, but their diverse roles and regulation remain poorly understood. During meiosis, chromosomes are reorganized as linear arrays of chromatin loops around a cohesin axis. This unique organization underlies homolog pairing, synapsis, double-stranded break induction, and recombination. We report that axis assembly in Caenorhabditis elegans is promoted by DNA-damage response (DDR) kinases that are activated at meiotic entry, even in the absence of DNA breaks. Downregulation of the cohesin-destabilizing factor WAPL-1 by ATM-1 promotes axis association of cohesins containing the meiotic kleisins COH-3 and COH-4. ECO-1 and PDS-5 also contribute to stabilizing axis-associated meiotic cohesins. Further, our data suggest that cohesin-enriched domains that promote DNA repair in mammalian cells also depend on WAPL inhibition by ATM. Thus, DDR and Wapl seem to play conserved roles in cohesin regulation in meiotic prophase and proliferating cells.

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:: 2470954

Journal Information:: Nature Structural & Molecular Biology, Journal Name: Nature Structural & Molecular Biology Journal Issue: 4 Vol. 30; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Rejuvenation of Meiotic Cohesion in Oocytes during Prophase I Is Required for Chiasma Maintenance and Accurate Chromosome Segregation Weng, Katherine A.; Jeffreys, Charlotte A.; Bickel, Sharon E. PLoS Genetics, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pgen.1004607	journal	September 2014
Transition from a meiotic to a somatic-like DNA damage response during the pachytene stage in mouse meiosis Enguita-Marruedo, Andrea; Martín-Ruiz, Marta; García, Eva PLOS Genetics, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pgen.1007439	journal	January 2019
Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation Challa, Kiran; Fajish V., Ghanim; Shinohara, Miki PLOS Genetics, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pgen.1007851	journal	January 2019
Cohesin acetylation and Wapl‐Pds5 oppositely regulate translocation of cohesin along DNA Kanke, Mai; Tahara, Eri; Huis in't Veld, Pim J. The EMBO Journal, Vol. 35, Issue 24 https://doi.org/10.15252/embj.201695756	journal	November 2016
Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins Wutz, Gordana; Várnai, Csilla; Nagasaka, Kota The EMBO Journal, Vol. 36, Issue 24 https://doi.org/10.15252/embj.201798004	journal	October 2017
PDS 5 proteins regulate the length of axial elements and telomere integrity during male mouse meiosis Viera, Alberto; Berenguer, Inés; Ruiz‐Torres, Miguel EMBO reports, Vol. 21, Issue 6 https://doi.org/10.15252/embr.201949273	journal	April 2020
SYP-3 Restricts Synaptonemal Complex Assembly to Bridge Paired Chromosome Axes During Meiosis in Caenorhabditis elegans Smolikov, Sarit; Eizinger, Andreas; Schild-Prufert, Kristina Genetics, Vol. 176, Issue 4 https://doi.org/10.1534/genetics.107.072413	journal	June 2007
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
Synaptonemal Complex Central Region Proteins Promote Localization of Pro-crossover Factors to Recombination Events DuringCaenorhabditis elegansMeiosis Cahoon, Cori K.; Helm, Jacquellyn M.; Libuda, Diana E. Genetics, Vol. 213, Issue 2 https://doi.org/10.1534/genetics.119.302625	journal	October 2019
Involvement of the Cohesin Cofactor PDS5 (SPO76) During Meiosis and DNA Repair in Arabidopsis thaliana Pradillo, Mónica; Knoll, Alexander; Oliver, Cecilia Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01034	journal	December 2015
Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes Severson, Aaron F.; Meyer, Barbara J. eLife, Vol. 3 https://doi.org/10.7554/eLife.03467	journal	August 2014
Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes Crawley, Oliver; Barroso, Consuelo; Testori, Sarah eLife, Vol. 5 https://doi.org/10.7554/eLife.10851	journal	February 2016
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
Eco1-dependent cohesin acetylation anchors chromatin loops and cohesion to define functional meiotic chromosome domains Barton, Rachael E.; Massari, Lucia F.; Robertson, Daniel eLife, Vol. 11 https://doi.org/10.7554/eLife.74447	journal	February 2022

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ATM signaling modulates cohesin behavior in meiotic prophase and proliferating cells

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