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PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation

ABSTRACT: This SuperSeries is composed of the SubSeries listed below.

ORGANISM(S): Mus musculus

PROVIDER: GSE221944 | GEO | 2023/12/18

REPOSITORIES: GEO

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PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation.

Project description:Spermatogonial stem cells functionality reside in the slow-cycling and heterogeneous undifferentiated spermatogonia cell population. This pool of cells supports lifelong fertility in adult males by balancing self-renewal and differentiation to produce haploid gametes. However, the molecular mechanisms underpinning long-term stemness of undifferentiated spermatogonia during adulthood remain unclear. Here, we discover that an epigenetic regulator, Polycomb repressive complex 1 (PRC1), shields adult undifferentiated spermatogonia from differentiation, maintains slow cycling, and directs commitment to differentiation during steady-state spermatogenesis in adults. We show that PRC2-mediated H3K27me3 is an epigenetic hallmark of adult undifferentiated spermatogonia. Indeed, spermatogonial differentiation is accompanied by a global loss of H3K27me3. Disruption of PRC1 impairs global H3K27me3 deposition, leading to precocious spermatogonial differentiation. Therefore, PRC1 directs PRC2-H3K27me3 deposition to maintain the self-renewing state of undifferentiated spermatogonia. Importantly, in contrast to its role in other tissue stem cells, PRC1 negatively regulates the cell cycle to maintain slow cycling of undifferentiated spermatogonia. Our findings have implications for how epigenetic regulators can be tuned to regulate the stem cell potential, cell cycle and differentiation to ensure lifelong fertility in adult males.

| S-EPMC10954450 | biostudies-literature

PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation [RNA-seq]

Project description:To understand the functional role of PRC1 in defining the epigenomic and transcriptional landscape in Aundiff, we eliminated PRC1 function in germ cells using Ddx4-Cre to mutate the E3 ubiquitin ligase RNF2 on a background lacking its partially redundant paralog RING1 (RING1A) to create PRC1 conditional knockout (PRC1cKO) mice. We discover a key role of Polycomb complexes in shielding the undifferentiated state of mouse adult spermatogonia. We then performed gene expression profiling analysis using data obtained from RNA-seq of WT, PRC1ctrl and PRC1cKO spermatogonial cells.

2023-12-18 | GSE221943 | GEO

PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation [CUT&Tag, CUT&RUN]

Project description:To understand the functional role of PRC1 in defining the epigenomic and transcriptional landscape in Aundiff, we eliminated PRC1 function in germ cells using Ddx4-Cre to mutate the E3 ubiquitin ligase RNF2 on a background lacking its partially redundant paralog RING1 (RING1A) to create PRC1 conditional knockout (PRC1cKO) mice. We discover a key role of Polycomb complexes in shielding the undifferentiated state of mouse adult spermatogonia. CUT&RUN or CUT&Tag for H2AK119ub, H3K27me3 and H3K4me3 in WT, PRC1ctrl and PRC1cKO spermatogonial cells.

2023-12-18 | GSE221942 | GEO

PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation

Project description:PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation

| PRJNA916889 | ENA

PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation [RNA-seq]

Project description:PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation [RNA-seq]

| PRJNA916896 | ENA

PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation [CUT&Tag, CUT&RUN]

Project description:PRC1 directs PRC2-H3K27me3 deposition to shield adult spermatogonial stem cells from differentiation [CUT&Tag, CUT&RUN]

| PRJNA916894 | ENA

Jarid2 Methylation via the PRC2 Complex Regulates H3K27me3 Deposition during Cell Differentiation.

Project description:Polycomb Group (PcG) proteins maintain transcriptional repression throughout development, mostly by regulating chromatin structure. Polycomb Repressive Complex 2 (PRC2), a component of the Polycomb machinery, is responsible for the methylation of histone H3 lysine 27 (H3K27me2/3). Jarid2 was previously identified as a cofactor of PRC2, regulating PRC2 targeting to chromatin and its enzymatic activity. Deletion of Jarid2 leads to impaired orchestration of gene expression during cell lineage commitment. Here, we reveal an unexpected crosstalk between Jarid2 and PRC2, with Jarid2 being methylated by PRC2. This modification is recognized by the Eed core component of PRC2 and triggers an allosteric activation of PRC2's enzymatic activity. We show that Jarid2 methylation is important to promote PRC2 activity at a locus devoid of H3K27me3 and for the correct deposition of this mark during cell differentiation. Our results uncover a regulation loop where Jarid2 methylation fine-tunes PRC2 activity depending on the chromatin context.

| S-EPMC4352895 | biostudies-literature

RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3.

Project description:Polycomb-repressive complex 1 (PRC1) has a central role in the regulation of heritable gene silencing during differentiation and development. PRC1 recruitment is generally attributed to interaction of the chromodomain of the core protein Polycomb with trimethyl histone H3K27 (H3K27me3), catalyzed by a second complex, PRC2. Unexpectedly we find that RING1B, the catalytic subunit of PRC1, and associated monoubiquitylation of histone H2A are targeted to closely overlapping sites in wild-type and PRC2-deficient mouse embryonic stem cells (mESCs), demonstrating an H3K27me3-independent pathway for recruitment of PRC1 activity. We show that this pathway is mediated by RYBP-PRC1, a complex comprising catalytic subunits of PRC1 and the protein RYBP. RYBP-PRC1 is recruited to target loci in mESCs and is also involved in Xist RNA-mediated silencing, the latter suggesting a wider role in Polycomb silencing. We discuss the implications of these findings for understanding recruitment and function of Polycomb repressors.

| S-EPMC3281992 | biostudies-literature

Abnormal H3K27me3 underlies degenerative spermatogonial stem cells in cryptorchid testis.

Project description:Cryptorchidism is the most frequent congenital defect in newborn males characterized by the absence of the testis from the scrotum. Approximately 90% of individuals with untreated bilateral cryptorchidism exhibit azoospermia due to defective spermatogenesis in the affected testis. Although abnormal spermatogonial stem cell maintenance or differentiation is suggested to cause germ cell degeneration in the cryptorchid testis, the underlying molecular mechanisms remain unclear. Here, we profiled spermatogonial epigenetic landscapes using surgically induced cryptorchid testis in the mouse. We show that cryptorchidism leads to alterations in local, but not global, H3K27me3 and H3K9me3 in undifferentiated spermatogonia. Of these, the loss of H3K27me3 was correlated with activation of developmental and proapoptotic pathway genes that are repressed by the polycomb machinery in germ cells. Cryptorchid spermatogonia exhibit an increase of the H3K27me3 demethylases KDM6A and KMD6B. Furthermore, we reveal that an increased temperature leads to Kdm6a/b upregulation in germline stem cells cultured in vitro. Thus, our study suggests that temperature-dependent histone demethylation may induce mRNA dysregulation due to the partial loss of H3K27me3 in spermatogonia.

| S-EPMC11829757 | biostudies-literature

Variant PCGF1-PRC1 links PRC2 recruitment with differentiation-associated transcriptional inactivation at target genes.

Project description:Polycomb repressive complexes-1 and -2 (PRC1 and 2) silence developmental genes in a spatiotemporal manner during embryogenesis. How Polycomb group (PcG) proteins orchestrate down-regulation of target genes upon differentiation, however, remains elusive. Here, by differentiating embryonic stem cells into embryoid bodies, we reveal a crucial role for the PCGF1-containing variant PRC1 complex (PCGF1-PRC1) to mediate differentiation-associated down-regulation of a group of genes. Upon differentiation cues, transcription is down-regulated at these genes, in association with PCGF1-PRC1-mediated deposition of histone H2AK119 mono-ubiquitination (H2AK119ub1) and PRC2 recruitment. In the absence of PCGF1-PRC1, both H2AK119ub1 deposition and PRC2 recruitment are disrupted, leading to aberrant expression of target genes. PCGF1-PRC1 is, therefore, required for initiation and consolidation of PcG-mediated gene repression during differentiation.

| S-EPMC8429492 | biostudies-literature

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