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Integrative single-cell analysis of transcriptome, DNA methylome and chromatin accessibility in mouse oocytes

ABSTRACT: Oocyte growth is a key step in forming mature eggs that are ready to be fertilized. The states and modifications of chromatin represent critical sources of information for this process. However, the dynamics and interrelations of these chromatin characteristics remain elusive. In this study, we developed an improved scCOOL-seq technique (iscCOOL-seq), which is a multi- omics, single-cell and single-base resolution method with high mapping rates, and explored the chromatin accessibility landscape and its relationship to DNA methylation in growing mouse oocytes. The most dramatic change in chromatin accessibility occurs during oocyte growth initiation, accompanied with prominent transcriptome alterations and an elevated variation in DNA methylation levels among individual oocytes. Unlike CpG islands (CGIs), partially methylated domains (PMDs) are associated with a low density of nucleosome-depleted regions (NDRs) during the whole maturation period. Surprisingly, highly expressed genes are usually associated with NDRs at their transcriptional end sites (TESs). In addition, genes with de novo methylated gene bodies during oocyte maturation are already open at their promoters before oocyte growth initiation. Furthermore, epigenetic and transcription factors that might be involved in oocyte maturation are identified. Our work paves the way for dissecting the complex, yet highly coordinated, epigenetic alterations during mouse oocyte growth and the establishment of totipotency.

ORGANISM(S): Mus musculus

PROVIDER: GSE114822 | GEO | 2018/12/19

REPOSITORIES: GEO

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EXOSC10 sculpts the transcriptome during oocyte growth-to-maturation transition

Project description:Growing mammalian oocytes accumulate substantial amounts of RNA, most of which are degraded during the subsequent maturation stage. The growth-to-maturation transition begins with germinal vesicle breakdown (GVBD, envisioned as nuclear envelope breakdown) and is critical for oocyte quality. However, the concomitant changes in the transcriptome during GVBD as well as the underlying machinery remained unclear. Here, we report that an RNA exosome-associated RNase, EXOSC10, sculpts the transcriptome at multiple level to facilitate the oocyte growth-to-maturation transition. We establish an oocyte-specific knockout of Exosc10 in mice using CRISPR/Cas9 and find female subfertility due to failed GVBD. By performing single oocyte RNA-seq in different ways, we document dysregulated transcriptomes, unsuccessfully processed rRNAs in mutant oocytes, and many up-regulated RNAs that encode proteins important for endomembrane trafficking, meiotic cell cycle and RNA metabolism. EXOSC10-depleted oocytes have impaired endomembrane components including endosome, lysosome, ER and Golgi. In addition, CDK1 fails to be activated possibly due to persistent WEE1 activity, which blocked lamina phosphorylation and disassembly in mutant oocytes. Collectively, we propose that EXOSC10 promotes the growth-to-maturation transition in mouse oocytes by degrading mRNAs that encode growth-phase factors and sculpting the transcriptome to support the maturation phase of oogenesis.

2019-11-30 | GSE141190 | GEO

LSM14B is essential for oocyte meiotic maturation by regulating maternal mRNA storage and clearance

Project description:Fully grown oocytes remain transcriptionally quiescent, yet many maternal mRNAs are synthesized and retained in growing oocytes. We now know that maternal mRNAs are stored in a structure called the mitochondria associated ribonucleoprotein domain (MARDO). But the components and functions of MARDO remain elusive. Here, we found that LSM14B knockout prevents the proper storage and timely clearance of mRNAs (including Cyclin B1, Btg4, and other mRNAs that are translationally activated during meiotic maturation), specifically by disrupting MARDO assembly during oocyte growth and meiotic maturation. With decreased levels of storage and clearance, the LSM14B knockout oocytes failed to enter meiosis II, ultimately resulting in female infertility. Our results demonstrate the function of LSM14B in MARDO assembly, couple the MARDO with mRNA clearance and oocyte meiotic maturation

2023-10-17 | PXD042761 | Pride

PATL2 is a key actor of oocyte maturation whose invalidation causes infertility in women and mice

Project description:The genetic causes of oocyte meiotic deficiency (OMD), a form of primary infertility characterised by the production of immature oocytes, remain largely unexplored. Using whole exome sequencing, we found that 26% of a cohort of 23 subjects with OMD harboured the same homozygous nonsense pathogenic mutation in PATL2, a gene encoding a putative RNA-binding protein. Using Patl2 knockout mice, we confirmed that PATL2 deficiency disturbs oocyte maturation, since oocytes and zygotes exhibit morphological and developmental defects respectively. PATL2's amphibian orthologue is involved in the regulation of oocyte mRNA as a partner of CPEB. However, Patl2's expression profile throughout oocyte development in mice, alongside colocalisation experiments with Cpeb1, Msy2 and Ddx6 (three oocyte RNA-regulators) suggest an original role for Patl2 in Mammals. Accordingly, transcriptomic analysis of oocytes from WT and Patl2-/- animals demonstrated that in the absence of Patl2, expression levels of a select number of highly relevant genes involved in oocyte maturation and early embryonic development are deregulated. In conclusion, PATL2 is a novel actor of mammalian oocyte maturation whose invalidation causes OMD in humans.

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LC-MS of control vs BafA1-treated mouse oocytes during maturation

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2024-02-20 | PXD042769 | Pride

Effects of in vitro maturation on oocyte gene expression

Project description:In vitro oocyte maturation (IVM) holds great promise as a tool for enhancing clinical treatment of infertility, enhancing availability of non human primates for development of disease models, and facilitating endangered species preservation. However, IVM outcomes have remained significantly below success rates obtained using in vivo matured (VVM) oocytes from humans and non human primates. A cDNA array based analysis is presented, comparing the transcriptomes of VVM oocytes with IVM oocytes. We observe a small set of just 59 mRNAs that are differentially expressed between the two cell types. These mRNAs are related to cellular homeostasis, cell-cell interactions including growth factor and hormone stimulation and cell adhesion, and other functions such as mRNA stability and translation. Additionally, we observe in IVM oocytes overexpression of PLAGL1 and MEST, two maternally imprinted genes, indicating a possible interruption or loss of correct epigenetic programming. These results indicate that, under certain IVM conditions, oocytes that are molecularly highly similar to VVM oocytes can be obtained, however the interruption of normal oocyte-somatic cell interactions during the final hours of oocyte maturation may preclude the establishment of full developmental competence. Keywords: oocyte maturation Comparison of in vitro matured MII-stage oocytes (4 biological replicates) with in vivo matured MII-stage oocytes (4 biological replicates)

2009-05-20 | E-GEOD-11895 | biostudies-arrayexpress

Single-cell quantitative proteomic analysis of oocyte maturation revealed high heterogeneities in human in vitro matured oocytes

Project description:In this study we investigated the protein expression patterns during human oocyte in vitro and in vivo maturation (IVO) by single-cell quantitative proteomic analysis of 36 human oocytes. Among 2,094 proteins quantified in 34 oocytes (GV: 11 oocytes, IVM: 12 oocytes, IVO: 11 oocytes), 224 were differential between IVO and GV oocytes during in vivo maturation, and 61 between IVM and IVO oocytes.

2022-08-02 | PXD023366 | Pride

Transcriptional profiling of somatic cells differentiation throughout oocyte competence acquisition in rainbow trout ovarian follicles.

Project description:Somatic cells surrounding the oocyte were sampled at the following stages: developmentally incompetent or poorly competent prophase I oocytes (NC1 oocytes), developmentally competent prophase I oocytes (C1 oocytes), and developmentally competent metaphase II oocytes (C2 oocytes). NC1 samples were collected from late vitellogenic females (LV), C1 samples from post-vitellogenic females (PV), and C2 samples from females undergoing meiotic maturation (Germinal Vesicle Breakdown) Global transcriptional profiling was performed using somatic cells collected from rainbow trout ovarian follicles during in vivo oocyte developmental competence acquisition. Somatic cells were collected at 3 stages of oogenesis: NC1 stage follicles (LV, late vitellogenic, prophase I arrested oocytes, meiotically incompetent and developmentally incompetent, n=6), C1 stage follicles (PV, post-vitellogenic, prophase I arrested oocytes, meiotically competent and developmentally competent, n=16). Ovulatory follicles were also collected during oocyte maturation after in vivo induction (metaphase II arrested oocytes, developmentally fully competent, n=6).

2012-10-14 | E-GEOD-36602 | biostudies-arrayexpress

LSM14B is essential for oocyte meiotic maturation by regulating maternal mRNA storage and clearance

2023-10-15 | GSE231648 | GEO

DIS3L2 clears terminal-uridylated RNA to ensure oocyte maturation and female fertility

Project description:During mammalian oocyte development, transcriptome undergoes accumulation in the oocyte growth phase and elimination in the oocyte maturation phase. At the transition point between growth and maturation, which is the germinal vesicle intact oocyte (GV), terminal uridylation labels RNA for degradation. In our study, we show that a small cohort of RNA are polyadenylated after tail uridylation (defined as uridylated-poly(A) RNA). Upon genetic depletion of DIS3L2 (Dis3l2cKO) in mouse oocytes, uridylated-poly(A) RNA is extensively stabilized and dominates the oocyte transcriptome, which results in increased transcriptome in Dis3l2cKO oocytes. Consequently, Dis3l2cKO female mice are infertile and almost all oocytes are arrested at the GV stage. Uridylated-poly(A) RNA generally has shorter poly(A) tails and lower translation activity. The uridylated-poly(A) RNA in Dis3l2cKO oocytes not only generates from the insufficient RNA degradation, but also comes from the tail dynamics of RNA. Our study demonstrates more possibilities of RNA fates after being terminally uridylated, and highlights the role of DIS3L2 in safeguarding the transcriptome by degrading uridylated-poly(A) RNA.

2022-07-22 | GSE208531 | GEO

Microarray data of prepubertal, peripubertal, and adult oocytes, and from GV and MII oocytes matured in vivo or in vitro

Project description:Expression data from prepubertal, peripubertal, and adult derived mouse oocytes, and from germinal vesicle (GV), in vivo matured, and in vitro matured mouse oocytes. Oocytes derived from prepubertal females, or oocytes matured in vitro, are less developmentally competent compared to adult derived, or in vivo matured, oocytes, indicated by decreased embryonic development. One potential mechanism for decreased developmental potetential in prepubertal or in vitro matured oocytes is inadequate or inappropriate RNA degradation during oocyte maturation (progression from GV to MII). To investigate mechanisms involved in establishing oocyte cytoplasmic maturation and developmental competence, Affymetrix GeneChip microarrays were used. Keywords: Oocyte developmental competence

2010-07-12 | GSE12432 | GEO

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