Epigenetic inheritance of diet-induced and sperm-borne mitochondrial RNAs
Ontology highlight
ABSTRACT:
PROVIDER: PRJNA1001005 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR25481800_1.fastq.gz | Fastqsanger.gz | |||
| SRR25481800_2.fastq.gz | Fastqsanger.gz | |||
| SRR25481900_1.fastq.gz | Fastqsanger.gz | |||
| SRR25481900_2.fastq.gz | Fastqsanger.gz | |||
| SRR25482000_1.fastq.gz | Fastqsanger.gz |
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Project description:Spermatozoa harbor a complex and environment sensitive pool of small non-coding RNAs (sncRNA)1, which influences offspring development and adult phenotypes1-7. Whether spermatozoa in the epididymis are directly susceptible to environmental cues is not fully understood8. We used two distinct paradigms of preconception acute high fat diet to dissect epididymal vs testicular contributions to the sperm sncRNA pool and offspring health. We show that epididymal spermatozoa, but not developing germ cells, are sensitive to the environment and identify mitochondrial tRNAs and their fragments (mt-tsRNA) as sperm-borne factors. In humans, mt-tsRNAs in spermatozoa correlate with BMI and paternal overweight at conception doubles offspring obesity risk and compromises metabolic health. Sperm sncRNA-seq of mice mutant for genes involved in mitochondrial function, and metabolic phenotyping of their wild-type offspring, suggest that alterations of mt-tsRNAs are downstream of mitochondrial dysfunction. Most importantly, single embryo transcriptomics of genetically hybrid two-cell embryos demonstrated sperm-to-oocyte transfer of mt-tRNAs at fertilisation and implied them in the control of early embryo transcription. Our study supports the importance of paternal health at conception for offspring metabolism, shows that mt-tRNAs are diet-induced and sperm-borne and demonstrates, for the first time in a physiological setting, father-to-offspring transfer of sperm mitochondrial RNAs at fertilization.
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Project description:Purpose: Sperm-borne RNA are particularly sensitive to degradation and methodology-induced bias, thus necessitating the use of a consistent, effective RNA extraction protocol for inter-species comparisons. To this end, we established SpermBase, an RNA expression database consisting of small and large RNA expression data obtained using consistent methodologies. Methods: Total RNA was extracted from total sperm and sperm head samples using an RNA extraction protocol that required only slight, species-specific alterations at the lysis stage. Total RNA was subjected to either RNA-Seq (large RNA) or sncRNA-Seq (small RNA). Results: By using a consistent methodology, we were able to perform a cross-species analysis on the conserved features of large and small sperm-borne RNAs. We identified conserved features in both populations of RNAs in the four mammalian species (i.e., mouse, rabbit, rat, and human) surveyed. Conclusions: Our study demonstrates an effective, near-universal approach to the study of sperm-borne RNAs, and identifies conserved characteristics in the large and small RNA populations of mammalian sperm.
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Project description:Prototypical micro RNAs (miRNAs) are 21~25-base-pair RNAs that regulate differentiation, carcinogenesis and pluripotency by eliminating mRNAs or blocking their translation, processes collectively termed RNA interference (RNAi). RNAi mediated by miRNAs regulates early development in zebrafish, and mouse embryos lacking the miRNA precursor processor, Dicer, are inviable. However, the role of miRNAs during mammalian fertilization is unknown. We here show using microarrays that miRNAs are present in mouse sperm structures that enter the oocyte at fertilization. Sperm contained a broad profile of miRNAs and a subset of potential mRNA targets were expressed in fertilizable, metaphase II (mII) oocytes. Oocytes contained transcripts for the RNAinduced silencing complex (RISC) catalytic subunit, EIF2C3 (formerly AGO3). However, levels of sperm-borne miRNA (measured by quantitative PCR) were apparently low relative to those of unfertilized, mII oocytes, and fertilization did not alter the part of the mII oocyte miRNA landscape that included the most abundant sperm-borne miRNAs. Coinjection of mII oocytes with sperm heads plus anti-miRNAs - to suppress miRNA function - did not perturb pronuclear activation or preimplantation development. Contrastingly, we provide evidence that nuclear transfer by microinjection alters the miRNA profile of enucleated oocytes. These data argue that sperm-borne prototypical miRNAs play a limited role, if any, in mammalian fertilization or early preimplantation development. Keywords: miRNA profiling Seven samples were analyzed for the study.
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Project description:Increasing evidences indicate diet-induced metabolic disorder could be paternally inherited, but the exact sperm epigenetic carrier remains unclear. Here, in a paternal high-fat diet (HFD) mouse model, we revealed that a highly enriched subset of sperm small RNAs (30-34 nt) that derived from the 5’ halves of tRNAs (tsRNAs), exhibit changes in both expression profiles and RNA modifications. Injection of sperm tsRNAs from HFD male but not synthetic tsRNAs lacking RNA modifications, into normal zygotes generated metabolic disorders in the F1 offspring. Injection of HFD sperm tsRNAs derails gene expression in both early embryos and islets of F1 offspring, enriched in metabolic pathways, but unrelated to DNA methylation at CpG-enriched region. Collectively, we uncover sperm tsRNAs as a type of “epigenetic carrier” that mediate intergenerational inheritance of acquired traits.
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Project description:Sperm chromatin retains small amounts of histones, and the chromatin states of sperm mirror gene expression programs of the next generation. It remains largely unknown how paternal epigenetic information is transmitted through sperm chromatin. Here we developed a novel mouse model of paternal epigenetic inheritance in which deposition of Polycomb repressive complex 2 (PRC2) mediated-repressive H3K27me3 is attenuated in the paternal germline. By applying modified methods of assisted reproductive technology, we rescued infertility of mice absent of Polycomb protein SCML2, which is the regulator of germline gene expression through the establishment of H3K27me3 on bivalent promoters with other active marks H3K4me2/3. In F1 males of Scml2-knockout mice, which has wild-type genotype, gene expression is dysregulated in the male germline during spermiogenesis. These dysregulated genes are targets of SCML2-mediated H3K27me3 in mature sperm. Thus, SCML2 mediates intergenerational inheritance of paternal epigenetic information through the regulation of sperm chromatin.
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