Identification of MicroRNAs in Zebrafish Spermatozoa

Zhang, Jing; Jia, Peng; Zeng, Lin; Jin, Yilin; Yuan, Yusheng; Chen, Jieying; Hong, Yunhan; Yi, Meisheng

doi:10.1089/zeb.2015.1115

Cited by 27 publications

(24 citation statements)

References 64 publications

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“…If this feature is extended to other teleost species, it indicates a possible source of bias in all the studies where spermatozoa were meant to be analyzed, but the whole semen was analyzed instead. For example, in a study on zebrafish spermatozoa [24] where whole non-fractionated semen was used instead of purified spermatozoa, the authors reported very high levels of miR-202-5p in spermatozoa, whereas in the present study, it was demonstrated that the seminal plasma, but not spermatozoa, is the source of this miRNA in the semen (Figures 4 and 6).…”

Section: Mirna Heterogeneity In Sperm Fractionscontrasting

confidence: 64%

“…Some of these miRNAs have been associated with male fertility [35,45,46]. Although all top 26 miRNAs identified in zebrafish whole sperm [24] were also found in our dataset, the level of accumulation was dissimilar for some of the miRNAs; for example, miR-22 and miR-122 were among the abundant miRNAs in zebrafish, while they were less abundant in salmon sperm. Thus, it is important to characterize and profile small RNA constituents of various teleost fish to obtain unifying and discriminatory features to understand the role of miRNAs in semen.…”

Section: Mirna Accumulation In Atlantic Salmon Spermmentioning

confidence: 65%

“…Conserved and specific miRNAs were previously characterized in Atlantic salmon [39][40][41] but not in gonads or gametes. Some of the dominant miRNAs in Atlantic salmon semen, such as let-7a, miR-21a, miR-25, miR-26a, miR-128, and miR-202, were found to be abundant in zebrafish whole sperm analysis [24], and let-7a was among the most abundant miRNAs in human semen exosome samples [42], indicating some functional conservation among divergent species. 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.…”

Section: Mirna Accumulation In Atlantic Salmon Spermmentioning

confidence: 97%

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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 Heterogeneity In Sperm Fractionscontrasting

confidence: 64%

Section: Mirna Accumulation In Atlantic Salmon Spermmentioning

confidence: 65%

Section: Mirna Accumulation In Atlantic Salmon Spermmentioning

confidence: 97%

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

Bizuayehu

Babiak

2020

IJMS

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“…However, due to its small size, sequencing of small transcriptome from zebrafish gonads has thus far been restricted to sexually mature organs27 and spermatozoa28 only. To overcome the challenge of distinguishing zebrafish gonads during juvenile stages of development, we have recently established See-Thru-Gonad line29; this line is a hybrid of the zf45Tg30 and nacre transparent (−/−)3132 lines.…”

mentioning

confidence: 99%

Dynamics of miRNA transcriptome during gonadal development of zebrafish

Presslauer

Bizuayehu

Kopp

et al. 2017

Sci Rep

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Studies in non-teleost vertebrates have found microRNAs (miRNAs) to be essential for proper gonadal development. However, comparatively little is known about their role during gonadal development in teleost fishes. So far in zebrafish, a model teleost, transcript profiling throughout gonadal development has not been established because of a tiny size of an organ in juvenile stages and its poor distinguishability from surrounding tissues. We performed small RNA sequencing on isolated gonads of See-Thru-Gonad line, from the undifferentiated state at 3 weeks post fertilization (wpf) to fully mature adults at 24 wpf. We identified 520 gonadal mature miRNAs; 111 of them had significant changes in abundance over time, while 50 miRNAs were either testis- or ovary-enriched significantly in at least one developmental stage. We characterized patterns of miRNA abundance over time including isomiR variants. We identified putative germline versus gonadal somatic miRNAs through differential small RNA sequencing of isolated gametes versus the whole gonads. This report is the most comprehensive analysis of the miRNA repertoire in zebrafish gonads during the sexual development to date and provides an important database from which functional studies can be performed.

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“…En cuanto a los transcritos no codificantes parece ser que, en el caso de mamíferos, el ARN con mayor presencia en el espermatozoide es el mi-ARN, el cual regula la expresión de genes (Hamatani, 2011), preferiblemente uniéndose a los ARNm Introducción por su extremo 3´-UTR (Jia and Zeng, 2015). Se ha determinado que cientos de mi-ARNs están presentes en el espermatozoide humano (Krawetz et al, 2011;Ostermeier et al, 2002), estando algunos de ellos relacionados con el control de la proliferación celular, la apoptosis y el desarrollo embrionario (Wang y Xu 2015).…”

Section: Transcritos Presentes En El Espermatozoide Madurounclassified

Daño en el genoma paterno y reparación embrionaria en peces: efectos en la descendencia = DNA damage in the paternal genome and embryo repair in fish: effects in the progeny

Díez¹

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Zygotic repair of the paternal genome is a key event after fertilization. Spermatozoa accumulate DNA strand breaks during spermatogenesis and can suffer additional damage by different factors, including cryopreservation. Fertilization with DNA damaged spermatozoa (DDS) is considered to promote implantation failures and abortions, but also long-term effects on the progeny that could be related with a defective repair. Base excision repair (BER) pathway is considered the most active in zygotic DNA repair, but healthy oocytes contain enzymes for all repairing pathways. In this study, the effects of the inhibition of the BER pathway in the zygote were analyzed on the progeny obtained after fertilization with differentially DDS. Massive gene expression (GE; 61 657 unique probes) was analyzed after hatching using microarrays. Trout oocytes are easily fertilized with DDS and the high prolificacy allows live progeny to be obtained even with a high rate of abortions. Nevertheless, the zygotic inhibition of Poly (ADP-ribose) polymerase, upstream of BER pathway, resulted in 810 differentially expressed genes (DEGs) after hatching. DEGs are related with DNA repair, apoptosis, telomere maintenance, or growth and development, revealing a scenario of impaired DNA damage signalization and repair. Downregulation of the apoptotic cascade was noticed, suggesting a selection of embryos tolerant to residual DNA damage during embryo development. Our results reveal changes in the progeny from defective repairing zygotes including higher malformations rate, weight gain, longer telomeres, and lower caspase 3/7 activity, whose long-term consequences should be analyzed in depth.

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Identification of MicroRNAs in Zebrafish Spermatozoa

Cited by 27 publications

References 64 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

Dynamics of miRNA transcriptome during gonadal development of zebrafish

Daño en el genoma paterno y reparación embrionaria en peces: efectos en la descendencia = DNA damage in the paternal genome and embryo repair in fish: effects in the progeny

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