Mammalian SWI/SNF chromatin remodeler is essential for reductional meiosis in males

Menon, Debashish U.; Kirsanov, Oleksandr; Geyer, Christopher B.; Magnuson, Terry

doi:10.1038/s41467-021-26828-1

Cited by 19 publications

(19 citation statements)

References 86 publications

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“…In Figure C, most components of the BAF ATPase module, BAF-core, and PBAF-specific were upregulated in the P and D phases, whereas cBAF-specific components presented high expression levels in the L and Z phases. Participation of the PBAF in meiosis rather than cBAF was reported by Menon et al, whose results basically agreed with the abundance changes of PBAF-related components in this study. The Drosha complex, which can initiate miRNA processing, was reported to be an essential factor mediating miRNA production for normal spermatogenesis and male fertility .…”

Section: Resultssupporting

confidence: 93%

Dynamic Responses of Chromosome-Binding Protein Complexes to Meiotic Prophase I of Mouse Spermatocyte

et al. 2022

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Meiotic prophase I (MPI) is the most important event in mammalian meiosis. The status of the chromosome-binding proteins (CBPs) and the corresponding complexes and their functions in MPI have not yet been well scrutinized. Quantitative proteomics focused on MPI-related CBPs was accomplished, in which mouse primary spermatocytes in four different subphases of MPI were collected, and chromosome-enriched proteins were extracted and quantitatively identified. According to a stringent criterion, 1136 CBPs in the MPI subphases were quantified. Looking at the dynamic patterns of CBP abundance in response to MPI progression, the patterns were broadly divided into two groups: high abundance in leptotene and zygotene or that in pachytene and diplotene. Furthermore, 152 such CBPs were regarded as 26 CBP complexes with strict filtration, in which some of these complexes were perceived to be MPI-dependent for the first time. These complexes basically belonged to four functional categories, while their dynamic abundance changes following MPI appeared; the functions of DNA replication decreased; and transcription and synapsis were activated in zygotene, pachytene, and diplotene; in contrast to the traditional prediction, condensin activity weakened in pachytene and diplotene. Profiling of protein complexes thus offered convincing evidence of the importance of CBP complexes in MPI.

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Section: Resultssupporting

confidence: 93%

Dynamic Responses of Chromosome-Binding Protein Complexes to Meiotic Prophase I of Mouse Spermatocyte

et al. 2022

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“…Furthermore, we showed that the SWI/SNF PBAF subcomplex activates genes essential for reductional meiosis and gamete formation (Menon et al, 2021). These data highlight that distinct SWI/SNF subcomplexes govern specific meiotic transitions.…”

Section: Discussionmentioning

confidence: 61%

“…Arid1a WT and Arid1a cKO mice were examined with indirect immunofluorescence (IF). 8-10 μm thick cryosections of testes were prepared using published methods (Menon et al, 2021).…”

Section: Immunofluorescence Staining Of Testis Cryosection and Sperma...mentioning

confidence: 99%

ARID1A governs the silencing of sex-linked transcription during male meiosis in the mouse

Menon

Murcia

Magnuson

2023

Preprint

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We present evidence implicating the BAF (BRG1/BRM Associated Factor) chromatin remodeler in meiotic sex chromosome inactivation (MSCI). By immunofluorescence (IF), the putative BAF DNA binding subunit, ARID1A (AT-rich Interaction Domain 1a), appeared enriched on the male sex chromosomes during diplonema of meiosis I. The germ cell-specific depletion of ARID1A resulted in a pachynema arrest and failure to repress sex-linked genes indicating a defective MSCI. Consistent with this defect, mutant sex chromosomes displayed an abnormal presence of elongating RNA polymerase II coupled with an overall increase in chromatin accessibility detectable by ATAC-seq. By investigating potential mechanisms underlying these anomalies, we identified a role for ARID1A in promoting the preferential enrichment of the histone variant, H3.3, on the sex chromosomes, a known hallmark of MSCI. Without ARID1A, the sex chromosomes appeared depleted of H3.3 at levels resembling autosomes. Higher resolution analyses by CUT&RUN revealed dramatic shifts in sex-linked H3.3 associations from discrete intergenic sites and broader gene-body domains to promoters in response to the loss of ARID1A. Several sex-linked sites displayed ectopic H3.3 occupancy that does not co-localize with DMC1 (DNA Meiotic Recombinase 1). This observation suggests a requirement for ARID1A in DMC1 localization to the asynapsed sex chromatids. We conclude that ARID1A-directed H3.3 localization influences sex chromosome gene regulation and DNA repair during meiosis I.

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“…The overrepresented pathways enriched in testis-specific genes were related to epigenetic regulation, DNA repair, P53 activity regulation, and chromatin organization, which can be explained by the fact that the genes involving meiosis, DNA repair were required in spermiogenesis to produce a large number of sperms [ 39 ] ( Figure 5f ). For example, a gene ARID2 involved in chromatin organization can regulate chromatin organization in metaphase-I spermatocytes, the deletion of which can result in a metaphase-I arrest because of the dysregulation of cell division core genes [ 40 ].…”

Section: Resultsmentioning

confidence: 99%

A comprehensive atlas of epigenetic regulators reveals tissue-specific epigenetic regulation patterns

Wang

Lyu

2022

Epigenetics

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Epigenetic machinery contributes to gene regulation in eukaryotic species. However, the machinery including more than 600 epigenetic regulator (ER) genes responsible for reading, writing, and erasing histone modifications and DNA modifications remains largely uncharacterized across species. We compile a comprehensive list of ERs based on an evolutionary analysis across 23 species, which is the most comprehensive ER list in various species until recently. We further perform comparative transcriptomic analyses across different tissues in humans, mice, as well as other amniote species. We observe a consistent tissue-of-origin expression specificity pattern of duplicated ER genes across species and suggest links between expression specificity and ER gene evolution as well as ER function. Additional analyses further suggest that ER duplication can generate tissue-specific ER genes with the same epigenetic substrates, which may be closely related to their regulatory specificity in tissue development. Our work can serve as a foundation to better comprehend the tissue-specific expression patterns of ER genes from an evolutionary perspective and also the functional implications of ERs in tissue-specific epigenetic regulation.

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Mammalian SWI/SNF chromatin remodeler is essential for reductional meiosis in males

Cited by 19 publications

References 86 publications

Dynamic Responses of Chromosome-Binding Protein Complexes to Meiotic Prophase I of Mouse Spermatocyte

Dynamic Responses of Chromosome-Binding Protein Complexes to Meiotic Prophase I of Mouse Spermatocyte

ARID1A governs the silencing of sex-linked transcription during male meiosis in the mouse

A comprehensive atlas of epigenetic regulators reveals tissue-specific epigenetic regulation patterns

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