Early cleavage of preimplantation embryos is regulated by tRNAGln-TTG–derived small RNAs present in mature spermatozoa

Chen, Xiaoxu; Zheng, Yi; Lei, Anmin; Zhang, Hanxue; Niu, Huimin; Li, Xueliang; Zhang, Pengfei; Liao, Mingzhi; Lv, Yinghua; Zhu, Zhendong; Pan, Chuanying; Dong, Wuzi; Chen, Hong; Wu, De; Liu, Wansheng; Hamer, Geert; Zeng, Shenming; Zeng, Wenxian

doi:10.1074/jbc.ra120.013003

Cited by 41 publications

(32 citation statements)

References 48 publications

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“…Of note, tRF5s and i-tRFs are the most enriched tsRNA subpopulation in clusters 10–12. Likewise, tRNA-Gln-TTG, which is enriched exclusively in cluster 11, have been shown to participate in the early cleavage of porcine preimplantation embryos [ 76 ] and injection of tRNA-Gly-GCC fragments into zygotes results in slowdown of embryo development [ 30 ].…”

Section: Discussionmentioning

confidence: 99%

Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm

Sellem¹,

Marthey

Rau

et al. 2021

Epigenetics & Chromatin

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Background During epididymal transit, spermatozoa go through several functional maturation steps, resulting from interactions with epididymal secretomes specific to each region. In particular, the sperm membrane is under constant remodeling, with sequential attachment and shedding of various molecules provided by the epididymal lumen fluid and epididymosomes, which also deliver sncRNA cargo to sperm. As a result, the payload of sperm sncRNAs changes during the transit from the epididymis caput to the cauda. This work was designed to study the dynamics of cattle sperm sncRNAs from spermatogenesis to final maturation. Results Comprehensive catalogues of sperm sncRNAs were obtained from testicular parenchyma, epididymal caput, corpus and cauda, as well as ejaculated semen from three Holstein bulls. The primary cattle sncRNA sperm content is markedly remodeled as sperm mature along the epididymis. Expression of piRNAs, which are abundant in testis parenchyma, decreases dramatically at epididymis. Conversely, sperm progressively acquires miRNAs, rsRNAs, and tsRNAs along epididymis, with regional specificities. For instance, miRNAs and tsRNAs are enriched in epididymis cauda and ejaculated sperm, while rsRNA expression peaks at epididymis corpus. In addition, epididymis corpus contains mainly 20 nt long piRNAs, instead of 30 nt in all other locations. Beyond the bulk differences in abundance of sncRNAs classes, K-means clustering was performed to study their spatiotemporal expression profile, highlighting differences in specific sncRNAs and providing insights into their putative biological role at each maturation stage. For instance, Gene Ontology analyses using miRNA targets highlighted enriched processes such as cell cycle regulation, response to stress and ubiquitination processes in testicular parenchyma, protein metabolism in epididymal sperm, and embryonic morphogenesis in ejaculated sperm. Conclusions Our findings confirm that the sperm sncRNAome does not simply reflect a legacy of spermatogenesis. Instead, sperm sncRNA expression shows a remarkable level of plasticity resulting probably from the combination of multiple factors such as loss of the cytoplasmic droplet, interaction with epididymosomes, and more surprisingly, the putative in situ production and/or modification of sncRNAs by sperm. Given the suggested role of sncRNA in epigenetic trans-generational inheritance, our detailed spatiotemporal analysis may pave the way for a study of sperm sncRNAs role in embryo development.

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Section: Discussionmentioning

confidence: 99%

Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm

Sellem¹,

Marthey

Rau

et al. 2021

Epigenetics & Chromatin

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show abstract

“…Processing of the collected semen is of utmost importance since it can surely mix up the different allocations of the small RNAs being detected. Many small RNAs have been explored and detected in the male genital tract and semen, including microRNAs (miRNAs), PIWI-interacting RNAs (piRNAs), YRNA and transfer RNA (tRNA)-derived small RNAs (tsRNAs) [ 136 , 182 , 183 , 184 ]. The most commonly explored small RNAs are the single-stranded 22–24 nucleotides miRNAs, considered important regulators of post-transcriptional gene expression [ 182 , 185 ] and detected in the testicles, spermatozoa, free in the SP and within SP EVs [ 181 ].…”

Section: The Particulate Seminal Plasma: the Most Relevant Component Of Seminal Plasma?mentioning

confidence: 99%

Seminal Plasma: Relevant for Fertility?

Rodriguez‐Martinez

Martı́nez

Calvete

et al. 2021

IJMS

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Seminal plasma (SP), the non-cellular component of semen, is a heterogeneous composite fluid built by secretions of the testis, the epididymis and the accessory sexual glands. Its composition, despite species-specific anatomical peculiarities, consistently contains inorganic ions, specific hormones, proteins and peptides, including cytokines and enzymes, cholesterol, DNA and RNA—the latter often protected within epididymis- or prostate-derived extracellular vesicles. It is beyond question that the SP participates in diverse aspects of sperm function pre-fertilization events. The SP also interacts with the various compartments of the tubular genital tract, triggering changes in gene function that prepares for an eventual successful pregnancy; thus, it ultimately modulates fertility. Despite these concepts, it is imperative to remember that SP-free spermatozoa (epididymal or washed ejaculated) are still fertile, so this review shall focus on the differences between the in vivo roles of the SP following semen deposition in the female and those regarding additions of SP on spermatozoa handled for artificial reproduction, including cryopreservation, from artificial insemination to in vitro fertilization. This review attempts, including our own results on model animal species, to critically summarize the current knowledge of the reproductive roles played by SP components, particularly in our own species, which is increasingly affected by infertility. The ultimate goal is to reconcile the delicate balance between the SP molecular concentration and their concerted effects after temporal exposure in vivo. We aim to appraise the functions of the SP components, their relevance as diagnostic biomarkers and their value as eventual additives to refine reproductive strategies, including biotechnologies, in livestock models and humans.

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“…Of note, sncRNA in the range 18-26 nt also contain short piRNAs, rsRNAs and tsRNA, which may also be involved in the observed phenotype. In this respect, some tsRNA peaking at epididymis cauda or ejaculated sperm in cattle have also been shown to contribute to early cleavage of porcine preimplantation embryos (Chen et al 2020) and injection of tRNA-Gly-GCC fragments into zygotes results in slowdown of embryo development (Sharma et al 2016).…”

Section: Deregulation Of Sncrnas Related To Spermatogenesis Impairs Fertilitymentioning

confidence: 99%

Sperm-borne sncRNAs: potential biomarkers for semen fertility?

Sellem¹,

Jammes

Schibler³

2021

Reprod. Fertil. Dev.

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Semen infertility or sub-fertility, whether in humans or livestock species, remains a major concern for clinicians and technicians involved in reproduction. Indeed, they can cause tragedies in human relationships or have a dramatic overall negative impact on the sustainability of livestock breeding. Understanding and predicting semen fertility issues is therefore crucial and quality control procedures as well as biomarkers have been proposed to ensure sperm fertility. However, their predictive values appeared to be too limited and additional relevant biomarkers are still required to diagnose sub-fertility efficiently. During the last decade, the study of molecular mechanisms involved in spermatogenesis and sperm maturation highlighted the regulatory role of a variety of small non-coding RNAs (sncRNAs) and led to the discovery that sperm sncRNAs comprise both remnants from spermatogenesis and post-testicular sncRNAs acquired through interactions with extracellular vesicles along epididymis. This has led to the hypothesis that sncRNAs may be a source of relevant biomarkers, associated either with sperm functionality or embryo development. This review aims at providing a synthetic overview of the current state of knowledge regarding implication of sncRNA in spermatogenesis defects and their putative roles in sperm maturation and embryo development, as well as exploring their use as fertility biomarkers.

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Early cleavage of preimplantation embryos is regulated by tRNAGln-TTG–derived small RNAs present in mature spermatozoa

Cited by 41 publications

References 48 publications

Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm

Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm

Seminal Plasma: Relevant for Fertility?

Sperm-borne sncRNAs: potential biomarkers for semen fertility?

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