Ovarian follicular development is a controlled series of events culminating with an ovulatory or atretic follicle. MicroRNAs (miRNAs) are small noncoding RNAs involved in translational regulation of genes in different developmental processes. Deletion of Dicer in mice ovaries demonstrated the importance of miRNAs in reproduction, which led to infertility. The miRNAs were thought to act only within host cells; however, these molecules are also present in cell-secreted vesicles. These vesicles are present in body fluids such as milk, serum, and ovarian follicular fluid. Vesicles are secreted in extracellular fluids and travel from donor to target cells, mediating transfer of bioactive material. Herein we discuss the role of hormonal-regulated miRNAs within different ovarian follicular cells as well as cell-secreted vesicles participation in mammalian ovarian follicular fluid. Furthermore, we discuss the possibility of miRNAs transference mediated by cell-secreted vesicles present in ovarian follicular fluid, increasing the versatility of miRNA functions during antral follicle development.
KimVNNamJW. Genomics of microRNA. Trends Genet. 2014;22
(3):165–173.
2.
AltuviaYLandgrafPLithwickGClustering and conservation patterns of human microRNAs. Nucleic Acids Res. 2005;33
(8):2697–2706.
3.
ValadiHEkströmKBossiosASjöstrandMLeeJJLötvallJO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9
(6):654–659.
4.
FortuneJE. Ovarian follicular growth and development in mammals. 1994;50
(2):225–232.
5.
GintherOJBegMADonadeuFXBergfeltDR. Mechanism of follicle deviation in monovular farm species. Anim Reprod Sci. 2014;78
(3-4):239–257.
6.
GintherOJBegMAGastalMOGastalEL. Follicle dynamics and selection in mares. Anim Reprod Sci. 2004;1:45–63.
7.
LesseyBA. Fine tuning of endometrial function by estrogen and progesterone through microRNAs. Biol Reprod. 2010;82
(4):653–655.
8.
FriedmanRCFarhKKBurgeCBBartelDP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19
(1):92–105.
9.
FabianMRSonenbergNFilipowiczW. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem. 2010;79:351–379.
10.
AmbrosV. The functions of animal microRNAs. Nature. 2004;431
(7006):350–355.
11.
BartelDP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136
(2):215–233.
12.
FaziFNerviC. MicroRNA: basic mechanisms and transcriptional regulatory networks for cell fate determination. Cardiovasc Res. 2008;79
(4):553–561.
13.
LeiLJinSGonzalezGBehringerRRWoodruffTK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol. 2010;315
(1-2):63–73.
14.
NagarajaAKAndreu-VieyraCFrancoHLDeletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol Endocrinol. 2008;22
(10):2336–2352.
15.
MurchisonEPSteinPXuanZCritical roles for Dicer in the female germline. Genes Dev. 2007;21
(6):682–693.
16.
YuanSOrtogeroNWuQZhengHYanW. Murine follicular development requires oocyte DICER, but not DROSHA. Biol Reprod. 2014;91
(2):39.
17.
SuhNBaehnerLMoltzahnFMicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol. 2010;20:271–277.
18.
Salilew-WondimDAhmadIGebremedhnSThe expression pattern of micrornas in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle. PLoS One. 2014;9
(9):e106795.
19.
SontakkeSDMohammedBTMcNeillyASDonadeuFX. Characterization of microRNAs differentially expressed during bovine follicle development. Reproduction. 2014;148
(3):271–283.
20.
SenAPrizantHLightAAndrogens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proc Natl Acad Sci USA. 2014;111
(8):3008–3013.
21.
YaoNYangBQLiuYFollicle-stimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells. Endocrine. 2010;38
(2):158–166.
22.
XuSLinher-MelvilleKYangBBWuDLiJ. Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology. 2011;152
(10):3941–3951.
23.
FiedlerSDCarlettiMZHongXChristensonLK. Hormonal regulation of MicroRNA expression in periovulatory mouse mural granulosa cells. Biol Reprod. 2008;79
(6):1030–1037.
YinMWangXYaoGTransactivation of MicroRNA-320 by MicroRNA-383 regulates granulosa cell functions by targeting E2F1 and SF-1 proteins. J Biol Chem. 2014;289
(26):18239–18257.
26.
QinXQLivingstonDMKaelinWGAdamsPD. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc Natl Acad Sci. 1994;91
(23):10918–10922.
27.
JeyasuriaPIkedaYJaminSPCell-specific knockout of steroidogenic factor 1 reveals its essential roles in gonadal function. Mol Endocrinol. 2004;18
(7):1610–1619.
28.
NilssonEE. Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol Reprod. 2002;67
(3):1018–1024.
29.
NilssonEESkinnerMK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod. 2003;69
(4):1265–1272.
30.
NilssonEESkinnerMK. Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol Cell Endocrinol. 2004;214
(1-2):19–25.
31.
PangasSAMatzukMM. The TGF-β family in the reproductive tract. In: MiyazonaDRK, eds. The TGF-β Family. New York, NY: Cold Spring Harbor Laboratory Press; 2008:861–888.
YaoGYinMLianJMicroRNA-224 is involved in transforming growth factor-beta-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Mol Endocrinol. 2010;24
(3):540–551.
34.
YanGZhangLFangTMicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB. FEBS Lett. 2012;586:3263–3270.
35.
YangSWangSLuoAExpression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary. Biol Reprod. 2013;89
(5):126.
36.
MilesJRMcDaneldTGWiedmannRTMicroRNA expression profile in bovine cumulus–oocyte complexes: possible role of let-7 and miR-106a in the development of bovine oocytes. Anim Reprod Sci. 2012;130
(1-2):16–26.
37.
da SilveiraJCVeeramachaneniDNRWingerQACarnevaleEMBoumaGJ. 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.
38.
MacaulayADGilbertICaballeroJThe gametic synapse: RNA transfer to the bovine oocyte. Biol Reprod. 2014;91
(4):90.
39.
MaJFlemrMSteinPMicroRNA activity is suppressed in mouse oocytes. Curr Biol. 2010;20
(3):265–270.
40.
DaiASunHFangTMicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2. FEBS Lett. 2013;587
(15):2474–2482.
41.
XiaoGXiaCYangJMiR-133b regulates the expression of the Actin protein TAGLN2 during oocyte growth and maturation: a potential target for infertility therapy. PLoS One. 2014;9
(6):e100751.
42.
DonadeuFXSchauerSNSontakkeSD. Involvement of miRNAs in ovarian follicular and luteal development. J Endocrinol. 2012;215
(3):323–334.
43.
McBrideDCarréWSontakkeSDIdentification of miRNAs associated with the follicular–luteal transition in the ruminant ovary. Reproduction. 2012;144
(2):221–233.
44.
OtsukaMZhengMHayashiMImpaired microRNA causes corpus luteum insufficiency and infertility in mice. J Clin Invest. 2008;118
(5):1944–1954.
45.
GyörgyBSzabóTGPásztóiMMembrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68
(16):2667–2688.
46.
PanBTTengKWuCAdamMJohnstoneRM. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol. 1985;101
(3):942–948.
47.
ThéryCAmigorenaSRaposoGClaytonA. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006, Chapter 3: Unit 3.22.
Van NielGPorto-CarreiroISimoesSRaposoG. Exosomes: a common pathway for a specialized function. J Biochem. 2006;140
(1):13–21.
50.
SkogJWürdingerTvan RijnSGlioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10
(12):1470–1476.
51.
KalraHSimpsonRJJiHVesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012;10
(12):e1001450.
52.
SohelMMHHoelkerMNoferestiSSExosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One. 2013;8
(11):e78505.
53.
SantonocitoMVentoMGuglielminoMRMolecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil Steril. 2014;102
(6):1–12.
54.
da SilveiraJCCarnevaleEMWingerQABoumaGJ. Regulation of ACVR1 and ID2 by cell-secreted exosomes during follicle maturation in the mare. Reprod Biol Endocrinol. 2014;12:44.
