microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy

Belleannée, Clémence; Légaré, Christine; Calvo, Ézéquiel; Thimon, Véronique; Sullivan, Robert

doi:10.1093/humrep/det088

Cited by 67 publications

(54 citation statements)

References 27 publications

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“…Importantly, this epigenome may be altered by a range of environmental insults44. The relatively high degree of overlap documented among reported epididymosome miRNA profiles (Supplementary Tables S4 and S5)1145 strongly suggests that this mode of intercellular communication may be highly conserved across mammalian species. Indeed, notwithstanding limitations imposed by the use of different methodology for miRNA identification (next generation sequencing versus microarray approaches), our mouse epididymosome dataset comprised as many as 88% of the miRNAs that have previously been documented in bovine epididymosomes11 (Supplementary Table S5).…”

Section: Discussionmentioning

confidence: 99%

Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome

Reilly

McLaughlin

Stanger³

et al. 2016

Sci Rep

196

234

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Recent evidence has shown that the sperm epigenome is vulnerable to dynamic modifications arising from a variety of paternal environment exposures and that this legacy can serve as an important determinant of intergenerational inheritance. It has been postulated that such exchange is communicated to maturing spermatozoa via the transfer of small non-protein-coding RNAs (sRNAs) in a mechanism mediated by epididymosomes; small membrane bound vesicles released by the soma of the male reproductive tract (epididymis). Here we confirm that mouse epididymosomes encapsulate an impressive cargo of >350 microRNAs (miRNAs), a developmentally important sRNA class, the majority (~60%) of which are also represented by the miRNA signature of spermatozoa. This includes >50 miRNAs that were found exclusively in epididymal sperm and epididymosomes, but not in the surrounding soma. We also documented substantial changes in the epididymosome miRNA cargo, including significant fold changes in almost half of the miRNAs along the length of the epididymis. Finally, we provide the first direct evidence for the transfer of several prominent miRNA species between mouse epididymosomes and spermatozoa to afford novel insight into a mechanism of intercellular communication by which the sRNA payload of sperm can be selectively modified during their post-testicular maturation.

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Section: Discussionmentioning

confidence: 99%

Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome

Reilly

McLaughlin

Stanger³

et al. 2016

Sci Rep

196

234

View full text Add to dashboard Cite

show abstract

“…Belleannee et al. (92) used a microarray approach to identify known miRNAs in microvesicles isolated from semen. They report 293 miRNAs detected in SE pooled from normal men; in comparison we detected 175 present in all donors, and another 271 in at least one donor.…”

Section: Methodsmentioning

confidence: 99%

Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions

Vojtech

Woo

Hughes

et al. 2014

Nucleic Acids Research

518

478

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Semen contains relatively ill-defined regulatory components that likely aid fertilization, but which could also interfere with defense against infection. Each ejaculate contains trillions of exosomes, membrane-enclosed subcellular microvesicles, which have immunosuppressive effects on cells important in the genital mucosa. Exosomes in general are believed to mediate inter-cellular communication, possibly by transferring small RNA molecules. We found that seminal exosome (SE) preparations contain a substantial amount of RNA from 20 to 100 nucleotides (nts) in length. We sequenced 20–40 and 40–100 nt fractions of SE RNA separately from six semen donors. We found various classes of small non-coding RNA, including microRNA (21.7% of the RNA in the 20–40 nt fraction) as well as abundant Y RNAs and tRNAs present in both fractions. Specific RNAs were consistently present in all donors. For example, 10 (of ∼2600 known) microRNAs constituted over 40% of mature microRNA in SE. Additionally, tRNA fragments were strongly enriched for 5’-ends of 18–19 or 30–34 nts in length; such tRNA fragments repress translation. Thus, SE could potentially deliver regulatory signals to the recipient mucosa via transfer of small RNA molecules.

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“…One can hypothesize that the caput epididymis could be the structure where a massive process of sperm remodeling takes place, in keeping with the notion that the caput epididymis is the most metabolically active region of this organ, and that 70-80% of the total overall protein secretion in the epididymal lumen takes place here [Cornwall 2009]. Moreover, in this context it is interesting to note that the sperm membrane is highly involved in this process in all its regions, and that epididymal fluid [Orgebin-Crist 1967;Bedford 2015] and epididymosomes [Sharma et al 2015;Belleannée et al 2013a;Belleannée et al 2013b] are actively participating in this process. The analysis of the hubs of the system (EMINeM and MC_ EMINeM) (Table 2) gives other interesting views.…”

Section: Node Degreementioning

confidence: 63%

The maturation of murine spermatozoa membranes within the epididymis, a computational biology perspective

Bernabò

Agostino

Ordinelli

et al. 2016

Systems Biology in Reproductive Medicine

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(2016) The maturation of murine spermatozoa membranes within the epididymis, a computational biology perspective, Systems Biology in Reproductive Medicine, 62:5, 299-308, DOI: 10.1080/19396368.2016 To link to this article: https://doi.org/10. 1080/19396368.2016.1205679 To become fertile, mammalian spermatozoa require completing a complex biochemical maturation that begins in the testis and ends within the female oviduct. Here, we paid attention to the events occurring at the membrane level during the epididymal transit. Indeed, in the epididymis, the molecular composition and the physical-chemical proprieties of sperm membranes markedly change, with functional cross talking among the spermatozoa, the epithelium, and the luminal content (particularly the epididymosomes). To study this process, we undertook a biological networks study, representing the involved molecules as nodes and their interactions as links. The analysis of network topology revealed that it has a scale free and small world architecture and it is robust against random failure. That assures a fast and efficient transmission of information and it leads to identifying the molecules exerting a higher level of control on the system, among which cholesterol plays a pivotal role. The reactome enrichment analysis allowed the reconstruction of the biochemical pathways involved in sperm epididymal maturation and STRING analysis permitted the identification of molecular events possibly involved in that process. In conclusion, this approach allows inferring interesting information, thus contributing to the knowledge on this process and suggesting staring points for further research. ARTICLE HISTORY

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microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy

Cited by 67 publications

References 27 publications

Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome

Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome

Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions

The maturation of murine spermatozoa membranes within the epididymis, a computational biology perspective

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