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Sperm is epigenetically programmed to regulate gene transcription in embryo

ABSTRACT: Using the frog Xenopus laevis as a model system we profile epigenetic features of sperm and spermatid to study how they relate to gene expression in embryos. We observe that sperm is epigenetically programmed to regulate embryonic gene expression. By comparing the development of sperm- and spermatid-derived frog embryos we show that the programming of sperm for successful development relates to its ability to regulate transcription of a set of developmentally important genes. During spermatid maturation into sperm, these genes lose H3K4me2/3 and retain H3K27me3 marks. Experimental removal of these epigenetic marks, at fertilization, deregulates gene expression in the resulting embryos in a paternal chromatin dependent manner. This demonstrates that epigenetic instructions delivered by the sperm at fertilization are required for correct regulation of gene expression in the future embryos. The epigenetic mechanisms of developmental programming revealed here are likely to relate to the mechanisms involved in transgenerational transmission of acquired traits.

ORGANISM(S): Xenopus laevis

PROVIDER: GSE75164 | GEO | 2016/03/22

SECONDARY ACCESSION(S): PRJNA302662

REPOSITORIES: GEO

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Sperm is epigenetically programmed to regulate gene transcription in embryo

Project description:Using the frog Xenopus laevis as a model system we profile epigenetic features of sperm and spermatid to study how they relate to gene expression in embryos. We observe that sperm is epigenetically programmed to regulate embryonic gene expression. By comparing the development of sperm- and spermatid-derived frog embryos we show that the programming of sperm for successful development relates to its ability to regulate transcription of a set of developmentally important genes. During spermatid maturation into sperm, these genes lose H3K4me2/3 and retain H3K27me3 marks. Experimental removal of these epigenetic marks, at fertilization, deregulates gene expression in the resulting embryos in a paternal chromatin dependent manner. This demonstrates that epigenetic instructions delivered by the sperm at fertilization are required for correct regulation of gene expression in the future embryos. The epigenetic mechanisms of developmental programming revealed here are likely to relate to the mechanisms involved in transgenerational transmission of acquired traits. 48 samples, single-ended ChIP-seq libraries from sperm- and spermatid-derived haploid embryos pulling down H3K4me2, H3K4me3, H3K27me3 and H3K9me3, 3 replicates for each histone modification pull-down. 14 samples of both single-ended and pair-ended RNA-seq libraries for sperm- and spermatid-derived embryos. 3 replicates of single-ended RNA-seq libraries for spermatid cells. 22 samples of single-ended RNA-seq form sperm- and spermatid-derived embryos overexpressing Kdm5b 16 samples of single-ended RNA-seq form sperm- and spermatid-derived embryos overexpressing Kdm6b 6 samples of single-ended MNase-seq from sperm and spermatid chromatin 12 samples of MBD-seq from sperm and spermatid chromatin

2016-03-22 | E-GEOD-75164 | biostudies-arrayexpress

Epigenetic homogeneity underlies sperm programming for embryonic transcription

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2020-06-05 | GSE125982 | GEO

Nucleosomal chromatin in the mature sperm of Drosophila melanogaster.

Project description:Nucleosomal chromatin persists in the mature sperm of Drosophila melanogaster. Paternal epigenetic marks of repression and active transcription are found within many genes essential for embryogenesis. These marks are delivered at fertilization and are subsequently maintained in the early embryo.

2015-09-30 | GSE52165 | GEO

Paternally inherited H3K27me3 affects chromatin accessibility in mouse embryos produced by round spermatid injection

Project description:Round spermatid injection (ROSI) results in a lower birth rate than intracytoplasmic sperm injection, which has hampered its clinical application. Inefficient development of ROSI embryos has been attributed to epigenetic abnormalities. However, the chromatin-based mechanism that underpins the low birth rate in ROSI remains to be determined. Here, we show that a repressive histone mark H3K27me3 persists from mouse round spermatids into zygotes in ROSI and that round spermatid-derived H3K27me3 is associated with less accessible chromatin and impaired gene expression in ROSI embryos. These loci are initially marked by H3K27me3 but undergo histone modification remodelling in spermiogenesis, resulting in reduced H3K27me3 in normal spermatozoa. Therefore, the absence of the epigenetic remodelling, presumably mediated by histone turnover during spermiogenesis, leads to dysregulation of chromatin accessibility and transcription in ROSI embryos. Thus, our results unveil a molecular logic, in which chromatin states in round spermatids impinge on chromatin accessibility and transcription in ROSI embryos, highlighting the importance of epigenetic remodelling during spermiogenesis in successful reproduction.

2022-08-22 | GSE196859 | GEO

Mice produced by mitotic reprogramming of sperm injected into haploid parthenogenotes

Project description:Sperm are highly differentiated and the activities that reprogram them for embryonic development during fertilization have historically been considered unique to the oocyte. We here challenge this view and demonstrate that mouse embryos in the mitotic cell cycle can also directly reprogram sperm for full term development. Developmentally incompetent haploid embryos (parthenogenotes) injected with sperm developed to produce healthy offspring at up to 24% of control rates, depending when in the embryonic cell cycle injection took place. This implies that most of the first embryonic cell cycle can be bypassed in sperm genome reprogramming for full development. Remodeling of histones and genomic 5'- methylcytosine and 5'-hydroxymethylcytosine following embryo injection were distinct from remodeling in fertilization and the resulting 2-cell embryos consistently possessed abnormal transcriptomes. These studies demonstrate plasticity in the reprogramming of terminally differentiated sperm nuclei and suggest that different epigenetic pathways or kinetics can establish totipotency. phICSI vs ICSI

2016-07-22 | E-GEOD-60595 | biostudies-arrayexpress

Mice produced by mitotic reprogramming of sperm injected into haploid parthenogenotes

2016-07-22 | GSE60595 | GEO

Epigenetic programming of human sperm

Project description:Epigenetic programming of human sperm

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Tsga8 is required for spermatid morphogenesis and male fertility in mice

Project description:During spermatogenesis, intricate gene expression is coordinately regulated by epigenetic modifiers, which are required for differentiation of spermatogonial stem cells (SSCs) contained among undifferentiated spermatogonia. We previously found that KMT2B conveys H3K4me3 at bivalent and monovalent promoters in undifferentiated spermatogonia. Because these genes are expressed late in spermatogenesis or during embryogenesis, we expect that many of them are potentially programmed by KMT2B for future expression. Here, we show that one of the genes targeted by KMT2B, Tsga8, plays an essential role in spermatid morphogenesis. Loss of Tsga8 in mice leads to male infertility associated with abnormal chromosomal distribution in round spermatids, malformation of elongating spermatid heads and spermiation failure. Tsga8 depletion leads to dysregulation of thousands of genes, including the X chromosome genes that are reactivated in spermatids, and insufficient nuclear condensation accompanied by reductions of TNP1 and PRM1, key factors for histone-to-protamine transition. Intracytoplasmic sperm injection (ICSI) of spermatids rescued the infertility phenotype, suggesting competency of the spermatid genome for fertilization. Thus, Tsga8 is a KMT2B target that is vitally necessary for spermiogenesis and fertility.

2021-04-16 | GSE147805 | GEO

Cohesin and CTCF do not assemble TADs in Xenopus sperm and male pronuclei

Project description:Paternal genomes are compacted during spermiogenesis and de-compacted following fertilization. These processes are fundamental for inheritance but incompletely understood. We analyzed these processes in the frog Xenopus laevis, whose sperm can be assembled into functional pronuclei in egg extracts in vitro. In such extracts, cohesin extrudes DNA into loops, but in vivo cohesin only assembles topologically-associating domains (TADs) at the mid-blastula transition (MBT). Why cohesin assembles TADs only at this stage is unknown. We first analyzed genome architecture in frog sperm and compared it to human and mouse. Our results indicate that sperm genome organization is conserved between frogs and humans and occurs without formation of TADs. TADs can be detected in mouse sperm samples, as reported, but these structures might originate from somatic chromatin contaminations. We therefore discuss the possibility that the absence of TADs might be a general feature of vertebrate sperm. To analyze sperm genome remodeling upon fertilization, we reconstituted male pronuclei in Xenopus egg extracts. In pronuclei, chromatin compartmentalization increases but cohesin does not accumulate at CTCF sites and assemble TADs. However, if pronuclei are formed in the presence of exogenous CTCF, CTCF binds to its consensus sites, cohesin accumulates at these and forms short-range chromatin loops, which are preferentially anchored at CTCF’s N-terminus. These results indicate that TADs are only assembled at MBT because before this stage CTCF sites are not occupied and cohesin only forms short-range chromatin loops.

2023-10-25 | GSE237049 | GEO

Cohesin and CTCF do not assemble TADs in Xenopus sperm and male pronuclei

2023-10-25 | GSE237050 | GEO

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