MicroRNAs Associated with the Quality of Follicular Fluids Affect Oocyte and Early Embryonic Development

Overview

Journal Reprod Med Biol

Specialty Biology

Date 2024 Jan 19

PMID 38239486

Authors

Sogo Aoki

Yuki Inoue

Shunsuke Hara

Jun Itou

Koumei Shirasuna

Hisataka Iwata

Affiliations

Soon will be listed here.

Abstract

Purpose: Oocyte and embryo quality differs significantly among individuals. Follicular fluid (FF) is a solo environment of oocyte maturation and may flux into the oviduct. Supplementation of in vitro maturation (IVM) and culture (IVC) medium with extracellular vesicles of FFs supports oocyte maturation and embryonic development. We addressed a hypothesis that miRNA profiles in FFs are crucial background of oocyte maturation and embryonic development.

Methods: FFs were collected from the ovaries of individual cows, and the FFs were classified into Good or Poor FF based on the developmental rate to the blastocyst stage of enclosed oocytes. miRNAs associated with the Good FFs were explored using small RNA sequencing. In addition, FFs were classified using the concentration of Good-FF-associated miRNAs. These classified FFs or miRNA were added to the IVM or IVC mediums.

Results: Supplementation of IVM and IVC medium with Good FF improved embryonic development. Good FFs contained miR-151-3p and miR-425-5p at a high concentration compared with those in Poor FFs. FFs selected by the concentration of miR-151-3p and miR-425-5p improved oocyte maturation and embryonic development. Supplementation of IVM or IVC medium with either miR-151-3p or miR-425-5p improved embryonic development to the blastocyst stage.

Conclusion: miRNAs were associated with the Good FFs determined oocyte maturation and embryonic development.

Citing Articles

Extracellular Vesicles From Follicular Fluid in Infertile Women: Size, Morphology and miRNA Content Analysis.

Ducarre S, Chiechio R, Moulin G, Butera E, Dupont A, Penno C J Extracell Biol. 2025; 4(3):e70041.

PMID: 40052100 PMC: 11881956. DOI: 10.1002/jex2.70041.

Construction and Analysis of miRNA-mRNA Interaction Network in Ovarian Tissue of Wanxi White Geese Across Different Breeding Stages.

Li R, Wang Y, Xie F, Tong X, Li X, Ren M Animals (Basel). 2024; 14(22).

PMID: 39595311 PMC: 11591532. DOI: 10.3390/ani14223258.

From follicle to blastocyst: microRNA-34c from follicular fluid-derived extracellular vesicles modulates blastocyst quality.

Benedetti C, Pavani K, Gansemans Y, Azari-Dolatabad N, Pascottini O, Peelman L J Anim Sci Biotechnol. 2024; 15(1):104.

PMID: 39097731 PMC: 11298084. DOI: 10.1186/s40104-024-01059-8.

miRNAs in Follicular and Oviductal Fluids Support Global DNA Demethylation in Early-Stage Embryos.

Aoki S, Inoue Y, Hamazaki M, Hara S, Noguchi T, Shirasuna K Int J Mol Sci. 2024; 25(11).

PMID: 38892059 PMC: 11172648. DOI: 10.3390/ijms25115872.

microRNAs associated with the quality of follicular fluids affect oocyte and early embryonic development.

Aoki S, Inoue Y, Hara S, Itou J, Shirasuna K, Iwata H Reprod Med Biol. 2024; 23(1):e12559.

PMID: 38239486 PMC: 10795439. DOI: 10.1002/rmb2.12559.

References

Sirard M, Richard F, Blondin P, Robert C . Contribution of the oocyte to embryo quality. Theriogenology. 2005; 65(1):126-36. DOI: 10.1016/j.theriogenology.2005.09.020. View

Ikeda S, Sugimoto M, Kume S . Lipofection of siRNA into bovine 8-16-cell stage embryos using zona removal and the well-of-the-well culture system. J Reprod Dev. 2018; 64(2):199-202. PMC: 5902909. DOI: 10.1262/jrd.2017-137. View

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. DOI: 10.1530/REP-22-0036. View

DellAquila M, Cho Y, Minoia P, TRAINA V, Lacalandra G, Maritato F . Effects of follicular fluid supplementation of in-vitro maturation medium on the fertilization and development of equine oocytes after in-vitro fertilization or intracytoplasmic sperm injection. Hum Reprod. 1998; 12(12):2766-72. DOI: 10.1093/humrep/12.12.2766. View

Kaneda M, Tang F, OCarroll D, Lao K, Surani M . Essential role for Argonaute2 protein in mouse oogenesis. Epigenetics Chromatin. 2009; 2(1):9. PMC: 2736168. DOI: 10.1186/1756-8935-2-9. View

Lee M, Lee R, Lin M, Hwu Y . Cleavage speed and implantation potential of early-cleavage embryos in IVF or ICSI cycles. J Assist Reprod Genet. 2012; 29(8):745-50. PMC: 3430780. DOI: 10.1007/s10815-012-9777-z. View

Feng R, Sang Q, Zhu Y, Fu W, Liu M, Xu Y . MiRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro. Sci Rep. 2015; 5:8689. PMC: 4346788. DOI: 10.1038/srep08689. View

Somfai T, Inaba Y, Watanabe S, Geshi M, Nagai T . Follicular fluid supplementation during in vitro maturation promotes sperm penetration in bovine oocytes by enhancing cumulus expansion and increasing mitochondrial activity in oocytes. Reprod Fertil Dev. 2012; 24(5):743-52. DOI: 10.1071/RD11251. View

Rodrigues T, Tuna K, Alli A, Tribulo P, Hansen P, Koh J . Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock. Reprod Fertil Dev. 2019; 31(5):888-897. DOI: 10.1071/RD18450. View

10.

Ogawa K, Itami N, Ueda M, Kansaku K, Shirasuna K, Kuwayama T . Non-esterified fatty acid-associated ability of follicular fluid to support porcine oocyte maturation and development. Reprod Med Biol. 2018; 17(2):155-163. PMC: 5902458. DOI: 10.1002/rmb2.12084. View

11.

Kim K, Mitsumizo N, Fujita K, Utsumi K . The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos. Theriogenology. 1996; 45(4):787-99. DOI: 10.1016/0093-691x(96)00008-8. View

12.

Neira J, Tainturier D, Pena M, Martal J . Effect of the association of IGF-I, IGF-II, bFGF, TGF-beta1, GM-CSF, and LIF on the development of bovine embryos produced in vitro. Theriogenology. 2009; 73(5):595-604. DOI: 10.1016/j.theriogenology.2009.10.015. View

13.

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(10):2569-2579. PMC: 7550524. DOI: 10.1007/s10815-020-01909-0. View

14.

Romero-Arredondo A, Seidel Jr G . Effects of follicular fluid during in vitro maturation of bovine oocytes on in vitro fertilization and early embryonic development. Biol Reprod. 1996; 55(5):1012-6. DOI: 10.1095/biolreprod55.5.1012. View

15.

Asaadi A, Azari Dolatabad N, Atashi H, Raes A, Van Damme P, Hoelker M . Extracellular Vesicles from Follicular and Ampullary Fluid Isolated by Density Gradient Ultracentrifugation Improve Bovine Embryo Development and Quality. Int J Mol Sci. 2021; 22(2). PMC: 7826877. DOI: 10.3390/ijms22020578. View

16.

Mahe C, Lavigne R, Com E, Pineau C, Locatelli Y, Zlotkowska A . Spatiotemporal profiling of the bovine oviduct fluid proteome around the time of ovulation. Sci Rep. 2022; 12(1):4135. PMC: 8907256. DOI: 10.1038/s41598-022-07929-3. View

17.

Ali A, Coenen K, Bousquet D, Sirard M . Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes. Theriogenology. 2004; 62(9):1596-606. DOI: 10.1016/j.theriogenology.2004.03.011. View

18.

Gabrys J, Kij-Mitka B, Sawicki S, Kochan J, Nowak A, Lojko J . Extracellular vesicles from follicular fluid may improve the nuclear maturation rate of in vitro matured mare oocytes. Theriogenology. 2022; 188:116-124. DOI: 10.1016/j.theriogenology.2022.05.022. View

19.

Hansen C, Srikandakumar A, Downey B . Presence of follicular fluid in the porcine oviduct and its contribution to the acrosome reaction. Mol Reprod Dev. 1991; 30(2):148-53. DOI: 10.1002/mrd.1080300211. View

20.

Sorensen A, Wissing M, Englund A, Dalgaard L . MicroRNA Species in Follicular Fluid Associating With Polycystic Ovary Syndrome and Related Intermediary Phenotypes. J Clin Endocrinol Metab. 2016; 101(4):1579-89. PMC: 4880172. DOI: 10.1210/jc.2015-3588. View