Diversity and functional convergence of small noncoding RNAs in male germ cell differentiation and fertilization

García-López, Jesús; Alonso, Lola; Cárdenas, David B.; Artaza, Haydeé; Hourcade, Juan de Dios; Martínez, Sérgio; Brieño‐Enríquez, Miguel A.; Mazo, Jesús del

doi:10.1261/rna.048215.114

Cited by 56 publications

(69 citation statements)

References 85 publications

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“…Abundant miRNAs reported in mouse, including miR-15c-5p, miR-16a-5p, miR-20a-5p, miR-30b-5p, miR-92a-3p, and miR-93a-5p, were also found in Atlantic salmon sperm in the present study, indicating the enrichment of sperm with diverse types of miRNAs. Among these, miR-20a-5p and miR-93a-5p were expressed highly in mouse spermatozoa compared to spermatogonia with a concomitant decrease in their predicted targets, signal transducer and activator of transcription 3 (Stat3) and phosphatase and tensin homolog (Pten) [43]. miR-202-5p was highly enriched in seminal plasma compared to spermatozoa, which is in line with Sertoli cell accumulation of this miRNA in human [35].…”

Section: Mirna Accumulation In Atlantic Salmon Spermsupporting

confidence: 53%

Heterogenic Origin of Micro RNAs in Atlantic Salmon (Salmo salar) Seminal Plasma

Bizuayehu

Babiak

2020

IJMS

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The origin and contribution of seminal plasma RNAs into the whole semen RNA repertoire are poorly known, frequently being overlooked or neglected. In this study, we used high-throughput sequencing and RT-qPCR to profile microRNA (miRNA) constituents in the whole semen, as well as in fractionated spermatozoa and seminal plasma of Atlantic salmon (Salmo salar). We found 85 differentially accumulated miRNAs between spermatozoa and the seminal plasma. We identified a number of seminal plasma-enriched and spermatozoa-enriched miRNAs. We localized the expression of some miRNAs in juvenile and mature testes. Two abundant miRNAs, miR-92a-3p and miR-202-5p, localized to both spermatogonia and somatic supporting cells in immature testis, and they were also highly abundant in somatic cells in mature testis. miR-15c-5p, miR-30d-5p, miR-93a-5p, and miR-730-5p were detected only in mature testis. miRs 92a-3p, 202-5p, 15c-5p, and 30d-5p were also detected in a juvenile ovary. The RT-qPCR experiment demonstrated lack of correlation in miRNA transcript levels in seminal plasma versus blood plasma. Our results indicate that salmon semen is rich in miRNAs, which are present in both spermatozoa and seminal plasma. Testicular-supporting somatic cells are likely the source of seminal plasma enrichment, whereas blood plasma is unlikely to contribute to the seminal plasma miRNA repertoire.Teleost fishes are the largest group of vertebrates, and their predominant reproductive features, such as a lack of accessory glands in semen production, external fertilization, or spermatozoa activation upon contact with water [10], make them distinct from tetrapods. Virtually, nothing is known about the potential transfer and possible role of paternal RNAs in embryo formation in fish.The whole semen RNAs are found not only in germ cells (spermatozoa) but also in the seminal plasma, where they are bound in protein complexes and encapsulated in microvesicles [11,12]. Seminal plasma is an important constituent of semen and has a vital role in spermatozoa metabolism, survival, and motility. It contains inorganic and organic compounds, proteins, and RNAs [13]. In fish, seminal plasma has been implicated in osmotic balance, proteolytic activities, and fertilization success [14-16]. However, the repertoire, abundance, origin, and functions of seminal plasma RNAs remain unknown in fish.Micro RNAs (miRNAs) are among the RNAs that are present in the sperm of vertebrates. These non-coding RNAs, approximately 22 nucleotides long, function mainly in translational suppression by binding at 3 UTR of mRNA to regulate various biological processes, including spermatogenesis [17]. In mouse, ingression of sperm miRNA to oocytes causes heritable epigenetic change in gene expression [18]. In addition, a sperm-borne miRNA miR-34c is essential for the first cell division [2]. miRNA expression has been characterized in the testes of some teleost fish [19], such as Atlantic halibut Hippoglossus hippoglossus [20], Atlantic cod Gadus morhua [21], yellow catfish Pelteobagrus ful...

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Section: Mirna Accumulation In Atlantic Salmon Spermsupporting

confidence: 53%

Heterogenic Origin of Micro RNAs in Atlantic Salmon (Salmo salar) Seminal Plasma

Bizuayehu

Babiak

2020

IJMS

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“…Several groups have previously investigated the miRNA contents in sperm, for a variety of organisms such as mouse [50, 64], human [2, 4], bull [58, 65–67], and pig [68]. Despite this cache of sperm miRNA expression information, cross-species comparisons using these existing data would be, as discussed previously, intrinsically unreliable because of differences in methodology [20, 21, 23–27].…”

Section: Resultsmentioning

confidence: 99%

SpermBase: A Database for Sperm-Borne RNA Contents

Schuster

Tang

Xie

et al. 2016

Biology of Reproduction

107

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Since their discovery approximately three decades ago, sperm-borne RNAs, both large/small and coding/noncoding, have been reported in multiple organisms, and some have been implicated in spermatogenesis, early development, and epigenetic inheritance. Despite these advances, isolation, quantification, and annotation of sperm-borne RNAs remain nontrivial. The yields and subspecies of sperm-borne RNAs isolated from sperm can vary drastically depending on the methods used, and no cross-species analyses of sperm RNA contents have ever been conducted using a standardized sperm RNA isolation protocol. To address these issues, we developed a simple RNA isolation method that is applicable to sperm of various species, thus allowing for reliable interspecies comparisons. Based on RNASeq analyses, we established SpermBase (www.spermbase.org), a database dedicated to sperm-borne RNA profiling of multiple species. Currently, SpermBase contains large and small RNA expression data for mouse, rat, rabbit, and human total sperm and sperm heads. By analyzing large and small RNAs for conserved features, we found that many sperm-borne RNA species were conserved across all four species analyzed, and among the conserved small RNAs, sperm-borne tRNA-derived small noncoding RNAs and miRNAs can target a large number of genes known to be critical for early development.

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“…The complexity of non-coding RNA species has also been well characterized in the sperm (Krawetz et al 2011, Peng et al 2012, Jodar et al 2013, García-lópez et al 2015, Pantano et al 2015, and it is now commonly accepted that non-coding RNAs are critical for the process of embryogenesis (Liu et al 2012a, Chen et al 2016a,b, Yuan et al 2016. The miRNA family is the best Reproduction (2017) 153 [785][786][787][788][789][790][791][792][793][794][795][796] www.reproduction-online.org characterized of the small RNA species in sperm.…”

Section: Introductionmentioning

confidence: 99%

Comparative profiling of small RNAs of pig seminal plasma and ejaculated and epididymal sperm

Cai¹,

Wu²,

Shen³

et al. 2017

Reproduction

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The similarities and differences of small RNAs in seminal plasma, epididymal sperm and ejaculated sperm remain largely undefined. We conducted a systematic comparative analysis of small RNA profiles in pig ejaculated sperm, epididymal sperm and seminal plasma and found that the diversity distribution of small RNA species was generally similar, whereas the abundance of small RNAs is dramatically different across the three libraries; miRNAs and small RNAs derived from rRNA, tRNA, small nuclear RNA, 7SK RNA, NRON RNA and cis-regulatory RNA were enriched in the three libraries, but piRNA was absent. A large population of small RNAs from ejaculated sperm are ejaculated sperm specific, and only 8-30% of small RNAs overlapped with those of epididymal sperm or seminal plasma and a small proportion (5-18%) of small RNAs were shared in the three libraries, suggesting that, in addition to the testes, sperm RNAs may also originate from seminal plasma, epididymis as well as other resources. Most miRNAs were co-distributed but differentially expressed across the three libraries, with epididymal sperm exhibiting the highest abundance, followed by ejaculated sperm and seminal plasma. The prediction of target genes of the top 10 highly expressed miRNAs across the three libraries revealed that these miRNAs may be involved in spermatogenesis, zygote development and the interaction between the environment and animals. Our study provides the first description of the similarities and differences of small RNA profiles in ejaculated sperm, epididymal sperm and seminal plasma and indicates that sperm RNA may have origins other than the testes.Reproduction (2017) 153 [785][786][787][788][789][790][791][792][793][794][795][796]

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Diversity and functional convergence of small noncoding RNAs in male germ cell differentiation and fertilization

Cited by 56 publications

References 85 publications

Heterogenic Origin of Micro RNAs in Atlantic Salmon (Salmo salar) Seminal Plasma

Heterogenic Origin of Micro RNAs in Atlantic Salmon (Salmo salar) Seminal Plasma

SpermBase: A Database for Sperm-Borne RNA Contents

Comparative profiling of small RNAs of pig seminal plasma and ejaculated and epididymal sperm

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