Analyze Diet
Journal of animal science and biotechnology2024; 15(1); 137; doi: 10.1186/s40104-024-01097-2

Seasonal influence on miRNA expression dynamics of extracellular vesicles in equine follicular fluid.

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.
Publication Date: 2024-10-09 PubMed ID: 39380110PubMed Central: PMC11462823DOI: 10.1186/s40104-024-01097-2Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

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

Publication

ISSN: 1674-9782
NlmUniqueID: 101581293
Country: England
Language: English
Volume: 15
Issue: 1
Pages: 137
PII: 137

Researcher Affiliations

Feugang, Jean M
  • 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.

References

This article includes 102 references
  1. Donadeu F, Watson E. Seasonal changes in ovarian activity: lessons learnt from the horse.. Anim Reprod Sci 2007;100(3–4):225–42.
    pubmed: 17207590
  2. Donadeu F, Pedersen H. Follicle development in mares.. Reprod Domest Anim 2008;43:224–31.
    pubmed: 18638128
  3. Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells.. J Reprod Dev 2012;58(1):44–50.
    pubmed: 22450284
  4. De Rensis F, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the dairy cow—a review.. Theriogenology 2003;60(6):1139–51.
    pubmed: 12935853
  5. Habeeb AA, Osman SF, Teama FEI, Gad AE. The detrimental impact of high environmental temperature on physiological response, growth, milk production, and reproductive efficiency of ruminants.. Trop Anim Health Prod 2023;55(6):388.
    pmc: PMC10620265pubmed: 37910293
  6. Wolfenson D, Thatcher W, Badinga L, Savio J, Meidan R, Lew B. Effect of heat stress on follicular development during the estrous cycle in lactating dairy cattle.. Biol Reprod 1995;52(5):1106–13.
    pubmed: 7626710
  7. Dobson H, Smith R. What is stress, and how does it affect reproduction?. Anim Reprod Sci 2000;60:743–52.
    pubmed: 10844239
  8. Roth Z. Heat stress, the follicle, and its enclosed oocyte: mechanisms and potential strategies to improve fertility in dairy cows.. Reprod Domest Anim 2008;43:238–44.
    pubmed: 18638130
  9. Wilson S, Marion R, Spain J, Spiers D, Keisler D, Lucy M. Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows.. J Dairy Sci 1998;81(8):2124–31.
    pubmed: 9749376
  10. Ju J-C, Jiang S, Tseng J-K, Parks JE, Yang X. Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes.. Theriogenology 2005;64(8):1677–89.
    pubmed: 15951010
  11. Paes V, Vieira L, Correia H, Sa N, Moura A, Sales A. Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus–oocyte complex.. Theriogenology 2016;86(4):994–1003.
    pubmed: 27125691
  12. Ginther OJ. The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women.. Theriogenology 2012;77(5):818–28.
    pubmed: 22115815
  13. Gastal E. Recent advances and new concepts on follicle and endocrine dynamics during the equine periovulatory period.. Anim Reprod 2009;6(1):144–58.
  14. Ginther O, Beg MA, Bergfelt D, Donadeu F, Kot K. Follicle selection in monovular species.. Biol Reprod 2001;65(3):638–47.
    pubmed: 11514323
  15. Ginther O. Folliculogenesis during the transitional period and early ovulatory season in mares.. J Reprod Fertil 1990;90(1):311–20.
    pubmed: 2231551
  16. Ginther O. Reproductive biology of the mare: basic and applied aspects.. J Equine Vet Sci 1992;12(2):71.
  17. Bergfelt D, Ginther O. Embryo loss following GnRH-induced ovulation in anovulatory mares.. Theriogenology 1992;38(1):33–43.
    pubmed: 16727116
  18. Nagy P, Guillaume D, Daels P. Seasonality in mares.. Anim Reprod Sci 2000;60:245–62.
    pubmed: 10844199
  19. Ginther O, Gastal E, Gastal M, Beg M. Seasonal influence on equine follicle dynamics.. Anim Reprod 2004;1(1):31–44.
  20. Donadeu F, Schauer S. Differential miRNA expression between equine ovulatory and anovulatory follicles.. Domest Anim Endocrinol 2013;45(3):122–5.
    pubmed: 23932580
  21. Acosta T, Beg MA, Ginther O. Aberrant blood flow area and plasma gonadotropin concentrations during the development of dominant-sized transitional anovulatory follicles in mares.. Biol Reprod 2004;71(2):637–42.
    pubmed: 15084481
  22. Ishak GM, Dutra GA, Gastal GD, Gastal MO, Feugang JM, Gastal EL. Transition to the ovulatory season in mares: an investigation of antral follicle receptor gene expression in vivo.. Mol Reprod Dev 2019;86(12):1832–45.
    pubmed: 31571308
  23. Dutra G, Ishak G, Pechanova O, Pechan T, Peterson D, Jacob J. Seasonal variation in equine follicular fluid proteome.. Reprod Biol Endocrinol 2019;17(1):29.
    pmc: PMC6404268pubmed: 30841911
  24. Ishak GM, Feugang JM, Pechanova O, Pechan T, Peterson DG, Willard ST. Follicular-fluid proteomics during equine follicle development.. Mol Reprod Dev 2022;89(7):298–311.
    pubmed: 35762042
  25. Gebremedhn S, Gad A, Ishak GM, Menjivar NG, Gastal MO, Feugang JM. Dynamics of extracellular vesicle-coupled microRNAs in equine follicular fluid associated with follicle selection and ovulation.. Mol Hum Reprod 2023;29(4):gaad009.
    pmc: PMC10321592pubmed: 36852862
  26. Donadeu FX, Schauer SN, Sontakke SD. Involvement of miRNAs in ovarian follicular and luteal development.. J Endocrinol 2012;215(3):323–34.
    pubmed: 23038794
  27. Li Y, Fang Y, Liu Y, Yang X. MicroRNAs in ovarian function and disorders.. J Ovarian Res 2015;8:51.
    pmc: PMC4522283pubmed: 26232057
  28. Martinez RM, Liang L, Racowsky C, Dioni L, Mansur A, Adir M. Extracellular microRNAs profile in human follicular fluid and IVF outcomes.. Sci Rep 2018;8:17036.
    pmc: PMC6242846pubmed: 30451969
  29. Dalanezi FM, Garcia HDM, de Andrade FR, Franchi FF, Fontes PK, de Souza Castilho AC. Extracellular vesicles of follicular fluid from heat-stressed cows modify the gene expression of in vitro-matured oocytes.. Anim Reprod Sci 2019;205:94–104.
    pubmed: 31060922
  30. Gebremedhn S, Gad A, Aglan HS, Laurincik J, Prochazka R, Salilew-Wondim D. Extracellular vesicles shuttle protective messages against heat stress in bovine granulosa cells.. Sci Rep 2020;10:15824.
    pmc: PMC7519046pubmed: 32978452
  31. Gad A, Joyce K, Menjivar NG, Heredia D, Rojas CS, Tesfaye D. Extracellular vesicle-microRNAs mediated response of bovine ovaries to seasonal environmental changes.. J Ovarian Res 2023;16:101.
    pmc: PMC10207814pubmed: 37221550
  32. Di Pietro C. Exosome-mediated communication in the ovarian follicle.. J Assist Reprod Genet 2016;33:303–11.
    pmc: PMC4785163pubmed: 26814471
  33. Yuan C, Li Z, Zhao Y, Wang X, Chen L, Zhao Z. Follicular fluid exosomes: Important modulator in proliferation and steroid synthesis of porcine granulosa cells.. FASEB J 2021;35(5):e21610.
    pubmed: 33908671
  34. Shao H, Im H, Castro CM, Breakefield X, Weissleder R, Lee H. New technologies for analysis of extracellular vesicles.. Chem Rev 2018;118(4):1917–50.
    pmc: PMC6029891pubmed: 29384376
  35. Yáñez-Mó M, Siljander PRM, Andreu Z, BedinaZavec A, Borràs FE, Buzas EI. Biological properties of extracellular vesicles and their physiological functions.. J Extracell Vesicles 2015;4(1):27066.
    pmc: PMC4433489pubmed: 25979354
  36. Gastal EL, Gastal MO, Bergfelt DR, Ginther OJ. Role of diameter differences among follicles in selection of a future dominant follicle in mares.. Biol Reprod 1997;57(6):1320–7.
    pubmed: 9408236
  37. Haag K, Magalhaes-Padilha D, Fonseca G, Wischral A, Gastal M, King S. Quantification, morphology, and viability of equine preantral follicles obtained via the Biopsy Pick-Up method.. Theriogenology 2013;79(4):599–609.
    pubmed: 23260865
  38. Ishak G, Bashir S, Dutra G, Gastal G, Gastal M, Cavinder C. In vivo antral follicle wall biopsy: a new research technique to study ovarian function at the cellular and molecular levels.. Reprod Biol Endocrinol 2018;16:71.
    pmc: PMC6064614pubmed: 30055625
  39. Menjivar NG, Gad A, Gebremedhn S, Ghosh S, Tesfaye D. Granulosa cell-derived extracellular vesicles mitigate the detrimental impact of thermal stress on bovine oocytes and embryos.. Front Cell Dev Biol 2023;11:1142629.
    pmc: PMC10116072pubmed: 37091982
  40. Van Deun J, Mestdagh P, Agostinis P, Akay Ö, Anand S, Anckaert J. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research.. Nat Methods 2017;14(3):228–32.
    pubmed: 28245209
  41. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data.. Genome Biol 2010;11(3):R25.
    pmc: PMC2864565pubmed: 20196867
  42. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing.. J Roy Stat Soc: Ser B (Methodol) 1995;57(1):289–300.
  43. Kumar L, Futschik M. Mfuzz: a software package for soft clustering of microarray data.. Bioinformation 2007;2(1):5–7.
    pmc: PMC2139991pubmed: 18084642
  44. Sticht C, De La Torre C, Parveen A, Gretz N. miRWalk: an online resource for prediction of microRNA binding sites.. PLoS One 2018;13(10):e0206239.
    pmc: PMC6193719pubmed: 30335862
  45. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto Encyclopedia of Genes and Genomes.. Nucleic Acids Res 1999;27(1):29–34.
    pmc: PMC148090pubmed: 9847135
  46. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D. Cytoscape: a software environment for integrated models of biomolecular interaction networks.. Genome Res 2003;13(11):2498–504.
    pmc: PMC403769pubmed: 14597658
  47. Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines.. J Extracell Vesicles 2018;7(1):1535750.
    pmc: PMC6322352pubmed: 30637094
  48. Godakumara K, Dissanayake K, Hasan MM, Kodithuwakku SP, Fazeli A. Role of extracellular vesicles in intercellular communication during reproduction.. Reprod Domest Anim 2022;57:14–21.
    pmc: PMC9796405pubmed: 35837748
  49. Thomou T, Mori MA, Dreyfuss JM, Konishi M, Sakaguchi M, Wolfrum C. Adipose-derived circulating miRNAs regulate gene expression in other tissues.. Nature 2017;542(7642):450–5.
    pmc: PMC5330251pubmed: 28199304
  50. da Silveira JC, Veeramachaneni DNR, Winger QA, Carnevale EM, Bouma GJ. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle.. Biol Reprod 2012;86(3):71.
    pubmed: 22116803
  51. Leung AK, Sharp PA. MicroRNA functions in stress responses.. Mol Cell 2010;40(2):205–15.
    pmc: PMC2996264pubmed: 20965416
  52. Nehammer C, Podolska A, Mackowiak SD, Kagias K, Pocock R. Specific microRNAs regulate heat stress responses in Caenorhabditis elegans.. Sci Rep 2015;5:8866.
    pmc: PMC4352874pubmed: 25746291
  53. Li Q, Yang C, Du J, Zhang B, He Y, Hu Q. Characterization of miRNA profiles in the mammary tissue of dairy cattle in response to heat stress.. BMC Genomics 2018;19:975.
    pmc: PMC6309072pubmed: 30593264
  54. Gebremedhn S, Ali A, Gad A, Prochazka R, Tesfaye D. Extracellular vesicles as mediators of environmental and metabolic stress coping mechanisms during mammalian follicular development.. Front Vet Sci 2020;7:602043.
    pmc: PMC7710682pubmed: 33330723
  55. Inoue Y, Munakata Y, Shinozawa A, Kawahara-Miki R, Shirasuna K, Iwata H. Prediction of major microRNAs in follicular fluid regulating porcine oocyte development.. J Assist Reprod Genet 2020;37:2569–79.
    pmc: PMC7550524pubmed: 32780318
  56. Di R, He J, Song S, Tian D, Liu Q, Liang X. Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season.. BMC Genomics 2014;15:899.
    pmc: PMC4287553pubmed: 25318541
  57. Zhai M, Xie Y, Liang H, Lei X, Zhao Z. Comparative profiling of differentially expressed microRNAs in estrous ovaries of Kazakh sheep in different seasons.. Gene 2018;664:181–91.
    pubmed: 29704632
  58. Capra E, Lazzari B, Russo M, Kosior MA, Valle GD, Longobardi V. Seasonal effects on miRNA and transcriptomic profile of oocytes and follicular cells in buffalo (Bubalus bubalis).. Sci Rep 2020;10:13557.
    pmc: PMC7419291pubmed: 32782284
  59. Li Y, Deng X, Zeng X, Peng X. The role of Mir-148a in cancer.. J Cancer 2016;7(10):1233–41.
    pmc: PMC4934031pubmed: 27390598
  60. Nagata S, Inoue Y, Sato T, Tanaka K, Shinozawa A, Shirasuna K. Age-associated changes in miRNA profile of bovine follicular fluid.. Reproduction 2022;164(5):195–206.
    pubmed: 35980236
  61. Wei C, Xiang S, Yu Y, Song J, Zheng M, Lian F. MiR-221-3p regulates apoptosis of ovarian granulosa cells via targeting FOXO1 in older women with diminished ovarian reserve (DOR).. Mol Reprod Dev 2021;88(4):251–60.
    pmc: PMC8251591pubmed: 33694202
  62. da Silveira JC, Winger QA, Bouma GJ, Carnevale EM. Effects of age on follicular fluid exosomal microRNAs and granulosa cell transforming growth factor-β signalling during follicle development in the mare.. Reprod Fertil Dev 2015;27(6):897–905.
    pubmed: 25945781
  63. Noferesti SS, Sohel MMH, Hoelker M, Salilew-Wondim D, Tholen E, Looft C. Controlled ovarian hyperstimulation induced changes in the expression of circulatory miRNA in bovine follicular fluid and blood plasma.. J Ovarian Res 2015;8:81.
    pmc: PMC4673782pubmed: 26645573
  64. Hilker RE, Pan B, Zhan X, Li J. MicroRNA-21 enhances estradiol production by inhibiting WT1 expression in granulosa cells.. J Mol Endocrinol 2022;68(1):11–22.
    pubmed: 34665763
  65. Ding Q, Jin M, Kalds P, Meng C, Wang H, Zhong J. Comparison of microRNA profiles in extracellular vesicles from small and large goat follicular fluid.. Animals 2021;11(11):3190.
    pmc: PMC8614480pubmed: 34827922
  66. Dai T, Kang X, Yang C, Mei S, Wei S, Guo X. Integrative analysis of miRNA-mRNA in ovarian granulosa cells treated with kisspeptin in Tan sheep.. Animals 2022;12(21):2989.
    pmc: PMC9656243pubmed: 36359113
  67. Xie L, Li A, Huang W, Zhang X, Miao X. Identification and analysis of miRNAs at different developmental stages in Hu sheep ovaries.. Acta Vet Zootech Sin 2019;50(7):1396–404.
  68. Zhang X, Chen Y, Yang M, Shang J, Xu Y, Zhang L. MiR-21-5p actions at the Smad7 gene during pig ovarian granulosa cell apoptosis.. Anim Reprod Sci 2020;223:106645.
    pubmed: 33217624
  69. Xu G, Hu Y, Yu D, Chen X, Li X, Duan S. Discovery of differentially expressed microRNAs in porcine ovaries with smaller and larger litter size.. Front Genet 2022;13:762124.
    pmc: PMC8864311pubmed: 35222529
  70. Zhang T, Huo S, Wei S, Cui S. miR-21, miR-125b, and let-7b contribute to the involution of atretic follicles and corpus lutea in Tibetan sheep ovaries.. Anim Sci J 2022;93(1):e13756.
    pubmed: 35822516
  71. Sohel MMH, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C. Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence.. PLoS One 2013;8(11):e78505.
    pmc: PMC3817212pubmed: 24223816
  72. Dehghan Z, Mohammadi-Yeganeh S, Rezaee D, Salehi M. MicroRNA-21 is involved in oocyte maturation, blastocyst formation, and pre-implantation embryo development.. Dev Biol 2021;480:69–77.
    pubmed: 34411594
  73. Gao R, Li Q, Qiu M, Xie S, Sun X, Huang T. Serum exosomal miR-192 serves as a potential detective biomarker for early pregnancy screening in sows.. Anim Biosci 2023;36(9):1336.
    pmc: PMC10472158pubmed: 37170506
  74. Du X, Zhang L, Li X, Pan Z, Liu H, Li Q. TGF-β signaling controls FSHR signaling-reduced ovarian granulosa cell apoptosis through the SMAD4/miR-143 axis.. Cell Death Dis 2016;7(11):e2476–576.
    pmc: PMC5260897pubmed: 27882941
  75. Zhao Y, Pan S, Li Y, Wu X. Exosomal miR-143-3p derived from follicular fluid promotes granulosa cell apoptosis by targeting BMPR1A in polycystic ovary syndrome.. Sci Rep 2022;12:4359.
    pmc: PMC8921316pubmed: 35288625
  76. Jarrett BY, Vanden Brink H, Oldfield AL, Lujan ME. Ultrasound characterization of disordered antral follicle development in women with polycystic ovary syndrome.. J Clin Endocrinol Metab 2020;105(11):e3847–61.
    pmc: PMC7473602pubmed: 32785651
  77. Lu S, Tang Y, Yao R, Xu R, Zhang H, Liu J. E2/ER signaling mediates the meiotic arrest of goat intrafollicular oocytes induced by follicle-stimulating hormone.. J Anim Sci 2023;101:skad351.
    pmc: PMC10630185pubmed: 37925610
  78. Liu W, Xin Q, Wang X, Wang S, Wang H, Zhang W. Estrogen receptors in granulosa cells govern meiotic resumption of pre-ovulatory oocytes in mammals.. Cell Death Dis 2017;8(3):e2662–762.
    pmc: PMC5386574pubmed: 28277543
  79. Zhang X, Zhang L, Shang J, Tao Q, Tian M, Ma Y. Combined microRNAome and transcriptome analysis of follicular phase and luteal phase in porcine ovaries.. Reprod Domest Anim 2019;54(7):1018–25.
    pubmed: 31077469
  80. Andrei D, Nagy RA, van Montfoort A, Tietge U, Terpstra M, Kok K. Differential miRNA expression profiles in cumulus and mural granulosa cells from human pre-ovulatory follicles.. MicroRNA 2019;8(1):61–7.
    pmc: PMC6340152pubmed: 30207252
  81. Martinez RM, Baccarelli AA, Liang L, Dioni L, Mansur A, Adir M. Body mass index in relation to extracellular vesicle–linked microRNAs in human follicular fluid.. Fertil Steril 2019;112(2):387-96. e3.
    pmc: PMC6663626pubmed: 31146888
  82. Hu J, Dong J, Zeng Z, Wu J, Tan X, Tang T. Using exosomal miRNAs extracted from porcine follicular fluid to investigate their role in oocyte development.. BMC Vet Res 2020;16:485.
    pmc: PMC7737261pubmed: 33317549
  83. Song P, Chen X, Zhang P, Zhou Y, Zhou R. miR-200b/MYBL2/CDK1 suppresses proliferation and induces senescence through cell cycle arrest in ovine granulosa cells.. Theriogenology 2023;207:19–30.
    pubmed: 37257219
  84. Yang J, Li X, Cao Y-H, Pokharel K, Hu X-J, Chen Z-H. Comparative mRNA and miRNA expression in European mouflon (Ovis musimon) and sheep (Ovis aries) provides novel insights into the genetic mechanisms for female reproductive success.. Heredity 2019;122(2):172–86.
    pmc: PMC6327046pubmed: 29784930
  85. Tesfaye D, Gebremedhn S, Salilew-Wondim D, Hailay T, Hoelker M, Grosse-Brinkhaus C. MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development.. Reproduction 2018;155(3):R121–35.
    pubmed: 29170163
  86. Zhang D, Lv J, Tang R, Feng Y, Zhao Y, Fei X. Association of exosomal microRNAs in human ovarian follicular fluid with oocyte quality.. Biochem Biophys Res Commun 2021;534:468–73.
    pubmed: 33256978
  87. Machtinger R, Rodosthenous RS, Adir M, Mansour A, Racowsky C, Baccarelli AA. Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: an exploratory study.. J Assist Reprod Genet 2017;34:525–33.
    pmc: PMC5401697pubmed: 28188594
  88. Liu Y, Zhou Z, He X, Tao L, Jiang Y, Lan R. Integrated analyses of miRNA-mRNA expression profiles of ovaries reveal the crucial interaction networks that regulate the prolificacy of goats in the follicular phase.. BMC Genomics 2021;22:812.
    pmc: PMC8582148pubmed: 34763659
  89. Yang H, Liu X, Hu G, Xie Y, Lin S, Zhao Z. Identification and analysis of microRNAs-mRNAs pairs associated with nutritional status in seasonal sheep.. Biochem Biophys Res Commun 2018;499(2):321–7.
    pubmed: 29588175
  90. Eisenberg I, Nahmias N, Novoselsky Persky M, Greenfield C, Goldman-Wohl D, Hurwitz A. Elevated circulating micro-ribonucleic acid (miRNA)-200b and miRNA-429 levels in anovulatory women.. Fertil Steril 2017;107(1):269–75.
    pubmed: 27816236
  91. Salas-Huetos A, James ER, Aston KI, Jenkins TG, Carrell DT, Yeste M. The expression of miRNAs in human ovaries, oocytes, extracellular vesicles, and early embryos: a systematic review.. Cells 2019;8(12):1564.
    pmc: PMC6952888pubmed: 31817143
  92. Lázár B, Szabadi NT, Anand M, Tóth R, Ecker A, Urbán M. Effect of miR-302b microRNA inhibition on chicken primordial germ cell proliferation and apoptosis rate.. Genes 2021;13(1):82.
    pmc: PMC8774308pubmed: 35052421
  93. Li X, Zhang W, Fu J, Xu Y, Gu R, Qu R. MicroRNA-451 is downregulated in the follicular fluid of women with endometriosis and influences mouse and human embryonic potential.. Reprod Biol Endocrinol 2019;17:96.
    pmc: PMC6862852pubmed: 31744497
  94. Hasuwa H, Ueda J, Ikawa M, Okabe M. miR-200b and miR-429 function in mouse ovulation and are essential for female fertility.. Science 2013;341(6141):71–3.
    pubmed: 23765281
  95. Sontakke SD, Mohammed BT, McNeilly AS, Donadeu FX. Characterization of microRNAs differentially expressed during bovine follicle development.. Reproduction 2014;148(3):271–83.
    pubmed: 24920665
  96. Assou S, Al-Edani T, Haouzi D, Philippe N, Lecellier C-H, Piquemal D. MicroRNAs: new candidates for the regulation of the human cumulus–oocyte complex.. Hum Reprod 2013;28(11):3038–49.
    pubmed: 23904466
  97. Bhushan L, Kandpal RP. EphB6 receptor modulates micro RNA profile of breast carcinoma cells.. PLoS One 2011;6(7):e22484.
    pmc: PMC3139643pubmed: 21811619
  98. Assou S, Cerecedo D, Tondeur S, Pantesco V, Hovatta O, Klein B. A gene expression signature shared by human mature oocytes and embryonic stem cells.. BMC Genomics 2009;10:10.
    pmc: PMC2628676pubmed: 19128516
  99. Nagaraja AK, Creighton CJ, Yu Z, Zhu H, Gunaratne PH, Reid JG. A link between mir-100 and FRAP1/mTOR in clear cell ovarian cancer.. Mol Endocrinol 2010;24(2):447–63.
    pmc: PMC2817607pubmed: 20081105
  100. Kharazi U, Badalzadeh R. A review on the stem cell therapy and an introduction to exosomes as a new tool in reproductive medicine.. Reprod Biol 2020;20(4):447–59.
    pubmed: 32900639
  101. Machtinger R, Laurent LC, Baccarelli AA. Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation.. Hum Reprod Update 2016;22(2):182–93.
    pmc: PMC4755440pubmed: 26663221
  102. Wei L, Yang X, Gao L, Liang Z, Yu H, Zhang N. Comparison of miRNA landscapes between the human oocytes with or without arrested development.. J Assist Reprod Genet 2022;39(10):2227–37.
    pmc: PMC9596657pubmed: 36129629

Citations

This article has been cited 0 times.