TOP-2 is differentially required for the proper maintenance of the cohesin subunit REC-8 on meiotic chromosomes in Caenorhabditis elegans spermatogenesis and oogenesis

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Author(s)Rourke, Christine
Author(s)Jaramillo-Lambert, Aimee
Date Accessioned2022-09-01T18:18:15Z
Date Available2022-09-01T18:18:15Z
Publication Date2022-08-11
DescriptionThis is a pre-copyedited, author-produced version of an article accepted for publication in Genetics following peer review. The version of record Christine Rourke, Aimee Jaramillo-Lambert, TOP-2 is differentially required for the proper maintenance of the cohesin subunit REC-8 on meiotic chromosomes in Caenorhabditis elegans spermatogenesis and oogenesis, Genetics, 2022;, iyac120, https://doi.org/10.1093/genetics/iyac120 is available online at: https://doi.org/10.1093/genetics/iyac120. This article will be embargoed until 08/11/2023.en_US
AbstractDuring meiotic prophase I, accurate segregation of homologous chromosomes requires the establishment of chromosomes with a meiosis-specific architecture. The sister chromatid cohesin complex and the enzyme Topoisomerase II (TOP-2) are important components of meiotic chromosome architecture, but the relationship of these proteins in the context of meiotic chromosome segregation is poorly defined. Here, we analyzed the role of TOP-2 in the timely release of the sister chromatid cohesin subunit REC-8 during spermatogenesis and oogenesis of Caenorhabditis elegans. We show that there is a different requirement for TOP-2 in meiosis of spermatogenesis and oogenesis. The loss-of-function mutation top-2(it7) results in premature REC-8 removal in spermatogenesis, but not oogenesis. This correlates with a failure to maintain the HORMA-domain proteins HTP-1 and HTP-2 (HTP-1/2) on chromosome axes at diakinesis and mislocalization of the downstream components that control REC-8 release including Aurora B kinase. In oogenesis, top-2(it7) causes a delay in the localization of Aurora B to oocyte chromosomes but can be rescued through premature activation of the maturation promoting factor via knockdown of the inhibitor kinase WEE-1.3. The delay in Aurora B localization is associated with an increase in the length of diakinesis bivalents and wee-1.3 RNAi mediated rescue of Aurora B localization in top-2(it7) is associated with a decrease in diakinesis bivalent length. Our results imply that the sex-specific effects of TOP-2 on REC-8 release are due to differences in the temporal regulation of meiosis and chromosome structure in late prophase I in spermatogenesis and oogenesis.en_US
SponsorMicroscopy access was supported by grants from the NIH-NIGMS (P20 GM103446), the NSF (IIA-1301765), and the State of Delaware. The LSM880 confocal microscope was acquired with a shared instrumentation grant S10 OD016361. Some strains were provided by the CGC, which is funded by NIH Office of Research Infrastructure Programs (P40 0D010440). This work was supported by National Institutes of Health R03HD098244 and R35GM142524 (AJL). CR was supported by NIH T32GM133395 and a University of Delaware Graduate Scholars Award.en_US
CitationChristine Rourke, Aimee Jaramillo-Lambert, TOP-2 is differentially required for the proper maintenance of the cohesin subunit REC-8 on meiotic chromosomes in Caenorhabditis elegans spermatogenesis and oogenesis, Genetics, 2022;, iyac120, https://doi.org/10.1093/genetics/iyac120en_US
ISSN1943-2631
URLhttps://udspace.udel.edu/handle/19716/31283
Languageen_USen_US
PublisherGeneticsen_US
Keywordstopoisomerase IIen_US
KeywordsTOP-2en_US
KeywordsREC-8en_US
Keywordschromosome segregationen_US
KeywordsCaenorhabditis elegansen_US
Keywordsmeiosisen_US
TitleTOP-2 is differentially required for the proper maintenance of the cohesin subunit REC-8 on meiotic chromosomes in Caenorhabditis elegans spermatogenesis and oogenesisen_US
TypeArticleen_US
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