Molecular Biology of Reproduction and Development Group, Fundació Clínic per a la Recerca Biomèdica, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine, University of Barcelona, Barcelona, Spain.
Reproduction. 2019 Oct;158(4):R113-R123. doi: 10.1530/REP-18-0639.
The paternal contribution to the new individual is not just limited to half the diploid genome. Recent findings have shown that sperm delivers to the oocyte several components, including a complex population of RNAs, which may influence early embryo development and the long-term phenotype of the offspring. Although the majority of sperm RNAs may only represent spermatogenic leftovers with no further function, the male gamete provides a specific set of RNAs to the oocyte that is able to modulate gene expression in the preimplantation embryo. Those sperm transcripts include coding and non-coding RNAs that might either be translated by the oocyte machinery or directly regulate embryo gene expression at the transcriptional or post-transcriptional level. Interestingly, some sperm RNAs seem to be acquired during post-testicular maturation through active communication between sperm and epididymal and seminal exosomes released by the epididymis and the male accessory sex glands, respectively. Exosomes contained in the seminal plasma seem to not only interact with the spermatozoa but also with cells from the female reproductive tract, modulating their gene expression and influencing female immune response triggered by the semen. This review also considers the findings that indicate the role of semen RNAs in preimplantation embryo development and offspring phenotypes. In this regard, different studies supporting the hypothesis of paternal epigenetic inheritance of altered metabolic phenotypes associated with environmental exposures are discussed. Lastly, potential mechanisms that could explain the impact of semen RNAs to both early embryogenesis and paternal epigenetic inheritance are suggested.
父本对新个体的贡献不仅仅局限于二倍体基因组的一半。最近的研究发现,精子向卵母细胞传递了几种成分,包括复杂的 RNA 群体,这些 RNA 可能影响早期胚胎发育和后代的长期表型。尽管大多数精子 RNA 可能仅代表没有进一步功能的精子发生残留物,但雄性配子向卵母细胞提供了一组特定的 RNA,能够调节植入前胚胎的基因表达。这些精子转录本包括编码和非编码 RNA,它们可以被卵母细胞机制翻译,或者直接在转录或转录后水平调节胚胎基因表达。有趣的是,一些精子 RNA 似乎是在睾丸后成熟过程中通过精子与附睾和精囊分别释放的外泌体之间的主动通信获得的。精液中的外泌体不仅与精子相互作用,还与来自女性生殖道的细胞相互作用,调节它们的基因表达,并影响由精液触发的女性免疫反应。这篇综述还考虑了表明精液 RNA 在植入前胚胎发育和后代表型中的作用的研究结果。在这方面,讨论了支持与环境暴露相关的改变的代谢表型的父系表观遗传遗传假说的不同研究。最后,提出了可以解释精液 RNA 对早期胚胎发生和父系表观遗传遗传的影响的潜在机制。