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Seasonal variations of extracellular vesicle-coupled microRNAs in equine follicular fluid

ABSTRACT: Ovarian follicular fluid (FF) comprises a dynamic milieu whose composition alters under seasonal variation, influencing follicle development and oocyte developmental competence. Various cell subtypes (e.g. granulosa, theca, and cumulus) produce cell-secreted nanoparticles, coined extracellular vesicles (EVs), which contain bioactive regulatory molecules such as microRNAs (miRNAs) known to mediate intrafollicular communication through various forms of signaling and information transfer. Markedly, the hallmark feature of EVs transferring cellular knowledge propagates their appealing nature as direct indicators of cellular status, albeit homeostasis, dysfunction, or disease. Photoperiod alterations influencing the regulatory content of FF-EVs as downstream modifiers remain largely unknown, particularly in seasonal breeding animals. Here, we aimed to unpack the impacts of seasonal variation on the miRNA expression profiles of FF-EVs in the mare. Equine pre-ovulatory follicles were monitored and aspirated using ultrasound-guided transvaginal techniques to obtain follicular fluids during non-breeding (spring anovulatory, SAN) and breeding seasons (spring ovulatory, SOV; summer, SUM; and fall ovulatory, FOV). 97 miRNAs were found to be differentially expressed between groups. Pairwise comparisons revealed specific clusters, including six miRNAs involved in the spring transition (miR-149-200b-206-221-328-615) and many others dysregulated during that of the summer (miR-143-192451- 302b-100, and let 7c), the peak time point for breeding. Bioinformatic analyses led to unveiling significant enrichments in various biological functions, such as transcription factor activity, transcription and transcription regulation, nucleic acid binding, sequence-specific DNA binding, p53 signaling, and post-translational modifications. Ultimately, the miRNA content of seasonally divergent FF-EVs poses as potentially relevant indicators of intrafollicular mechanisms directing seasonal transitions and their functional regulatory roles in the pre-ovulatory stage, governing subsequent ovulation.

ORGANISM(S): Equus caballus

PROVIDER: GSE249220 | GEO | 2024/10/23

REPOSITORIES: GEO

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Project description:The mammalian follicular development is a well-orchestrated and complex molecular process characterized by sequences of follicular waves that yield the ovulatory follicle. It has been reported that bi-directional communication between the growing oocyte and the surrounding somatic cells is a hallmark of mammalian follicular development, partially mediated by extracellular vesicles (EVs) present in the follicular fluid (FF). Bioactive molecules such as the miRNAs encapsulated in the EVs mediate this communication within the follicular environment. Here, we aimed to decipher the dynamics of the miRNAs in the EVs of equine FF aspirated in vivo during different stages of follicular development. Hence, all follicles ≥6 mm were ablated on Days 10–11 of the estrous cycle (ovulation = Day 0) and the new induced wave was ultrasound-monitored daily until the largest growing follicle for at least three consecutive days was randomly allocated to one of the five groups (n = 8 follicles/group) namely: predeviation (preDEV; 18–20 mm), deviation (DEV; 22–25 mm), postdeviation (postDEV; 26–29 mm), preovulatory (preOV; 30–35 mm), and impending ovulation (IMP; ~40 mm). The FF was collected from each target group by ultrasound-guided transvaginal follicle aspiration. After removal of cells, cellular debris, and larger particles, EVs were isolated from FF groups (4 biological replicates/group; 0.5 mL FF/replicate) using high-speed ultracentrifugation (120,000xg for 70 min). Isolated EVs were characterized using western blot for EV marker proteins, NanoSight Tracking Analysis, and electron microscopy. MiRNA enriched total RNA was isolated from EVs using an Exosomal RNA Isolation kit and small-RNA library preparation and RNAseq (NextSeq500; Illumina) was performed by Novogene Co, Ltd. Approximately 180 known miRNAs were detected in each group with 148 mutually found in all groups. Among the expressed miRNAs, miR-148a, miR-21, miR-192, and miR-99a were the top highly abundant miRNAs in all groups. Cluster analysis exhibited 15 different expression patterns during follicular development. Among these patterns, a group of 23 miRNAs (including miR-106b, miR-199a-5p, and miR-125a-5p) exhibited a stable expression at the preDev until the postDev stage, a significant increase at the preOV stage, and then a significant decrease at the IMP stage. This miRNA cluster has been found to target genes involved in TGF-signaling and endocytosis pathways. Another interesting pattern with 22 miRNAs (including miR-146b-5p, miR-140, and miR-143) exhibited a sharp reduction in their expression from the preDEV until the preOV stage and was predicted to target genes associated with fatty acid biosynthesis, cell cycle, and oocyte meiosis pathways. In contrast, a group of 16 miRNAs (including miR-483, miR-128, and miR-192) gradually increased in expression from preDEV to the postDEV and then downregulated at the preOV stage. This miRNA cluster targets several signaling pathways, including ErbB, thyroid, and estrogen signaling. In conclusion, this study provides greater insights into the stage-specific expression dynamics of the FF EV-miRNAs during equine follicular development, which may play a role in folliculogenesis in mares.

Project description:Perennial ryegrass (Lolium perenne L.) is a major grass species used for forage and turf throughout the world, and gains by conventional breeding have reached a plateau. Perennial ryegrass is an outcrossing, self-incompatible diploid (2n = 2x = 14) with a relatively large genome (4067 Mbp/diploid genome; Evans, G.M., Rees, H., Snell, C.L. and Sun, S. (1972). The relation between nuclear DNA amount and the duration of the mitotic cycle. Chrom. Today, 3, 24–31). Using tissues sourced from active pastures during the peak of the autumn, winter, spring and summer seasons, we analysed the ryegrass transcriptome employing a Serial Analysis of Gene Expression (SAGE™) protocol, with the dual goals of understanding the seasonal changes in perennial ryegrass gene expression and enhancing our ability to select genes for genetic manipulation. A total of 159 002 14-mer SAGE™ tags was sequenced and mapped to the perennial ryegrass DNA database, comprising methyl-filtered (GeneThresher®) and expressed sequence tag (EST) sequences. The analysis of 14 559 unique SAGE™ tags, which were present more than once in our SAGE™ library, revealed 964, 1331, 346 and 131 exclusive transcripts to autumn, winter, spring and summer, respectively. Intriguingly, our analysis of the SAGE™ tags revealed season-specific expression profiles for the small subunit of ribulose-1,5-bisphosphate carboxylase (Rubisco), LprbcS. The transcript level for LprbcS was highest in spring, and then decreased gradually between summer and winter. Five different copies of LprbcS were revealed in ryegrass, with one possibly producing splice variant transcripts. Two highly expressed LprbcS genes were reported, one of which was not active in autumn. Another LprbcS gene showed an inverse expression profile to the autumn inactive LprbcS in a manner to compensate the expression level. Keywords: paddock samples, pasture, perennial ryegrass, Serial Analysis of Gene Expression (SAGE™), season specific expression, monocot

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Seasonal variations of extracellular vesicle-coupled microRNAs in equine follicular fluid

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