Abstract: Ovarian follicular fluid (FF) is a dynamic environment that changes with the seasons, affecting follicle development, ovulation, and oocyte quality. Cells in the follicles release tiny particles called extracellular vesicles (EVs) containing vital regulatory molecules, such as microRNAs (miRNAs). These miRNAs are pivotal in facilitating communication within the follicles through diverse signaling and information transfer forms. EV-coupled miRNA signaling is implicated to be associated with ovarian function, follicle and oocyte growth and response to various environmental insults. Herein, we investigated how seasonal variations directly influence the ovulatory and anovulatory states of ovarian follicles and how are they associated with follicular fluid EV-coupled miRNA dynamics in horses. Results: Ultrasonographic monitoring and follicular fluid aspiration of preovulatory follicles in horses during the anovulatory (spring: non-breeding) and ovulatory (spring, summer, and fall: breeding) seasons and subsequent EV isolation and miRNA profiling identified significant variation in EV-miRNA cargo content. We identified 97 miRNAs with differential expression among the groups and specific clusters of miRNAs involved in the spring transition (miR-149, -200b, -206, -221, -328, and -615) and peak breeding period (including miR-143, -192, -451, -302b, -100, and let-7c). Bioinformatic analyses showed enrichments in various biological functions, e.g., transcription factor activity, transcription and transcription regulation, nucleic acid binding, sequence-specific DNA binding, p53 signaling, and post-translational modifications. Cluster analyses revealed distinct sets of significantly up- and down-regulated miRNAs associated with spring anovulatory (Cluster 1) and summer ovulation-the peak breeding season (Clusters 4 and 6). Conclusions: The findings from the current study shed light on the dynamics of FF-EV-coupled miRNAs in relation to equine ovulatory and anovulatory seasons, and their roles in understanding the mechanisms involved in seasonal shifts and ovulation during the breeding season warrant further investigation.
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The research explores how seasonal changes affect the small RNA molecules (microRNAs or miRNAs) found in the ovarian follicular fluid of horses. These fluids and their contained miRNAs are essential for the growth and health of ovarian follicles and eggs, and their dynamics change with the seasons.
Research Methodology
The researchers collected follicular fluid from the pre-ovulatory follicles of horses during both the non-breeding and breeding season. The breeding season included the spring, summer and fall months while the non-breeding season was isolated to the spring transition period.
Extracellular vesicles (EVs) were then isolated from this fluid, and the researchers used miRNA profiling to understand how the microRNAs contained within these EVs varied across the seasons. Extracellular vesicles are tiny particles that cells emit containing important molecular information.
Findings
The researchers discovered a significant variation in the types and quantities of microRNAs within EVs depending on the season.
They identified 97 specific microRNAs which were differently expressed, classified into two major clusters. One contained microRNAs predominantly found in the anovulatory, or non-breeding season, and the other consisted of those largely found in the peak breeding season.
Bioinformatic analysis demonstrated that these groups of microRNAs were involved in various biological functions such as transcription regulation, DNA binding and signaling of p53, a protein linked to cell cycle control and apoptosis.
Conclusions
The research provides significant insight into the changing dynamics of microRNAs in the ovarian follicular fluid during different seasons.
It illuminates how these changes can trigger alterations in follicular and egg cell growth, as well as the horse’s breeding capability.
The results warrant further research into the exact mechanisms of these seasonal shifts, to fully understand their implications for reproductive health and breeding in horses.
Cite This Article
APA
Feugang JM, Gad A, Menjivar NG, Ishak GM, Gebremedhn S, Gastal MO, Dlamini NH, Prochazka R, Gastal EL, Tesfaye D.
(2024).
Seasonal influence on miRNA expression dynamics of extracellular vesicles in equine follicular fluid.
J Anim Sci Biotechnol, 15(1), 137.
https://doi.org/10.1186/s40104-024-01097-2
Department of Animal and Dairy Sciences, Mississippi State University, Mississippi State, MS, 39762, USA. j.feugang@msstate.edu.
Gad, Ahmed
Animal Reproduction and Biotechnology Laboratory (ARBL), Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, 80523, USA.
Department of Animal Production, Faculty of Agriculture, Cairo University, Giza, 12613, Egypt.
Menjivar, Nico G
Animal Reproduction and Biotechnology Laboratory (ARBL), Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, 80523, USA.
Ishak, Ghassan M
Department of Surgery and Obstetrics, College of Veterinary Medicine, University of Baghdad, Baghdad, 10011, Iraq.
Animal Science, School of Agricultural Sciences, Southern Illinois University, Carbondale, IL, 62901, USA.
Gebremedhn, Samuel
J.R. Simplot Company, Kuna, ID, 83634, USA.
Gastal, Melba O
Animal Science, School of Agricultural Sciences, Southern Illinois University, Carbondale, IL, 62901, USA.
Dlamini, Notsile H
Department of Animal and Dairy Sciences, Mississippi State University, Mississippi State, MS, 39762, USA.
Prochazka, Radek
Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Liběchov, 27721, Czech Republic.
Gastal, Eduardo L
Animal Science, School of Agricultural Sciences, Southern Illinois University, Carbondale, IL, 62901, USA.
Tesfaye, Dawit
Animal Reproduction and Biotechnology Laboratory (ARBL), Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, 80523, USA.
Grant Funding
58-6066-3-038 / USDA-ARS
5P20GMI03476-19 / NIH MS-INBRE
Conflict of Interest Statement
The authors declare that they have no competing interests.
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