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http://dx.doi.org/10.5713/ajas.19.0707

MicroRNAs regulate granulosa cells apoptosis and follicular development - A review  

Gong, Zhuandi (Hospital, Northwest Minzu University)
Yang, Juan (College of Life Science and Engineering, Northwest Minzu University)
Bai, Shengju (Hospital, Northwest Minzu University)
Wei, Suocheng (College of Life Science and Engineering, Northwest Minzu University)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.33, no.11, 2020 , pp. 1714-1724 More about this Journal
Abstract
Objective: MicroRNAs (miRNAs) are the most abundant small RNAs. Approximately 2,000 annotated miRNAs genes have been found to be differentially expressed in ovarian follicles during the follicular development (FD). Many miRNAs exert their regulatory effects on the apoptosis of follicular granulosa cells (FGCs) and FD. However, accurate roles and mechanism of miRNAs regulating apoptosis of FGCs remain undetermined. Methods: In this review, we summarized the regulatory role of each miRNA or miRNA cluster on FGCs apoptosis and FD on the bases of 41 academic articles retrieved from PubMed and web of science and other databases. Results: Total of 30 miRNAs and 4 miRNAs clusters in 41 articles were reviewed and summarized in the present article. Twenty nine documents indicated explicitly that 24 miRNAs and miRNAs clusters in 29 articles promoted or induced FGCs apoptosis through their distinctive target genes. The remaining 10 miRNAs and miRNAs of 12 articles inhibited FGCs apoptosis. MiRNAs exerted modulation actions by at least 77 signal pathways during FGCs apoptosis and FD. Conclusion: We concluded that miRNAs or miRNAs clusters could modulate the apoptosis of GCs (including follicular GCs, mural GCs and cumulus cells) by targeting their specific genes. A great majority of miRNAs show a promoting role on apoptosis of FGCs in mammals. But the accurate mechanism of miRNAs and miRNA clusters has not been well understood. It is necessary to ascertain clearly the role and mechanism of each miRNA or miRNA cluster in the future. Understanding precise functions and mechanisms of miRNAs in FGCs apoptosis and FD will be beneficial in developing new diagnostic and treatment strategies for treating infertility and ovarian diseases in humans and animals.
Keywords
microRNAs; Apoptosis; Granulosa Cells; Cumulus Cells; Follicular Development;
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1 Shi L, Liu S, Zhao W, Shi J. miR-483-5p and miR-486-5p are down-regulated in cumulus cells of metaphase II oocytes from women with polycystic ovary syndrome. Reprod Biomed Online 2015;31:565-72. https://doi.org/10.1016/j.rbmo.2015.06.023   DOI
2 Liu J, Yao W, Yao Y, et al. MiR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene. FEBS Lett 2014;588:4497-503. https://doi.org/10.1016/j.febslet.2014. 10.021   DOI
3 Liu J, Tu F, Yao W, et al. Conserved miR-26b enhances ovarian granulosa cell apoptosis through HAS2-HA-CD44-Caspase-3 pathway by targeting HAS2. Sci Rep 2016;6:21197. https://doi.org/10.1038/srep21197   DOI
4 Li Y, Ganta S, Cheng C, Craig R, Ganta RR, Freeman LC. FSH stimulates ovarian cancer cell growth by action on growth factor variant receptor. Mol Cell Endocrinol 2007;267:26-37. https://doi.org/10.1016/j.mce.2006.11.010   DOI
5 Bhartiya D, James K. Very small embryonic-like stem cells (VSELs) in adult mouse uterine perimetrium and myometrium. J Ovarian Res 2017;10:29. https://doi.org/10.1186/s13048-017-0324-5   DOI
6 Tesfaye D, Gebremedhn S, Salilew-Wondim D, et al. MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development. Reproduction 2018;155:R121-35. https://doi.org/10.1530/REP-17-0428   DOI
7 Grosshans H, Johnson T, Reinert KL, Gerstein M, Slack FJ. The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev Cell 2005;8:321-30. https://doi.org/10.1016/j. devcel.2004.12.019   DOI
8 Tesfaye D, Worku D, Rings F, et al. Identification and expression profiling of microRNAs during bovine oocyte maturation using heterologous approach. Mol Reprod Dev 2009;76:665-77. https://doi.org/10.1002/mrd.21005   DOI
9 Sinha PB, Tesfaye D, Rings F, et al. MicroRNA-130b is involved in bovine granulosa and cumulus cells function, oocyte maturation and blastocyst formation. J Ovarian Res 2017;10:37. https://doi.org/10.1186/s13048-017-0336-1   DOI
10 Lei L, Jin SY, Gonzalez G, Behringer RR, Woodruff TK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol 2010;315:63-73. https://doi.org/10.1016/j.mce.2009.09.021   DOI
11 Worku T, Rehman ZU, Talpur HS, et al. MicroRNAs: New insight in modulating follicular atresia: a review. Int J Mol Sci 2017;18:333. https://doi.org/10.3390/ijms18020333   DOI
12 Jiao J, Shi B, Wang T, et al. Characterization of long non-coding RNA and messenger RNA profiles in follicular fluid from mature and immature ovarian follicles of healthy women and women with polycystic ovary syndrome. Hum Reprod 2018;33:1735-48. https://doi.org/10.1093/humrep/dey255   DOI
13 Wei J, Zhang L, Li J, et al. Microrna-205 promotes cell invasion by repressing tcf21 in human ovarian cancer. J Ovarian Res 2017;10:33-8. https://doi.org/10.1186/s13048-017-0328-1   DOI
14 Xiong F, Hu L, Zhang Y, Xiao X, Xiao J. miR-22 inhibits mouse ovarian granulosa cell apoptosis by targeting SIRT1. Biol Open 2016;5:367-71. https://doi.org/10.1242/bio.016907   DOI
15 Eisenberg I, Nahmias N, Novoselsky Persky M, et al. Elevated circulating micro-ribonucleic acid (miRNA)-200b and miRNA-429 levels in anovulatory women. Fertil Ssteril 2017;107:269-75. https://doi.org/10.1016/j.fertnstert.2016.10.003   DOI
16 Rios C, Warren D, Olson B, Abbott AL. Functional analysis of microRNA pathway genes in the somatic gonad and germ cells during ovulation in C. elegans. Dev Biol 2017;426:115-25. https://doi.org/10.1016/j.ydbio.2017.04.007   DOI
17 Tu F, Pan ZX, Yao Y, et al. miR-34a targets the inhibin beta B gene, promoting granulosa cell apoptosis in the porcine ovary. Genet Mol Res GMR. 2014;13:2504-12. https://doi.org/10.4238/2014.January.14.6   DOI
18 Atwood CS, Vadakkadath Meethal S. The spatiotemporal hormonal orchestration of human folliculogenesis, early embryogenesis and blastocyst implantation. Mol Cell Endocrinol 2016;430:33-48. https://doi.org/10.1016/j.mce.2016.03.039   DOI
19 Liu J, Li X, Yao Y, Li Q, Pan Z, Li Q. miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis. Biochim Biophys Acta Gene Regul Mech 2018;1861:246-57. https://doi.org/10.1016/j.bbagrm. 2018.01.009   DOI
20 Ikeda S, Imai H, Yamada M. Apoptosis in cumulus cells during in vitro maturation of bovine cumulus-enclosed oocytes. Reproduction 2003;125:369-76.   DOI
21 Andrei D, Nagy RA, van Montfoort A, et al. Differential miRNA expression profiles in cumulus and mural granulosa cells from human pre-ovulatory follicles. MicroRNA (Shariqah, United Arab Emirates). 2019;8:61-7. https://doi.org/10.2174/2211536607666180912152618
22 Chang HM, Qiao J, Leung PC. Oocyte-somatic cell interactions in the human ovary-novel role of bone morphogenetic proteins and growth differentiation factors. Hum Reprod Update 2016;23:1-18. https://doi.org/10.1093/humupd/dmw039   DOI
23 Suh YS, Bhat S, Hong SH, et al. Genome-wide microRNA screening reveals that the evolutionary conserved miR-9a regulates body growth by targeting sNPFR1/NPYR. 2015;6: 7693. https://doi.org/10.1038/ncomms8693   DOI
24 Zhang B, Chen L, Feng G, et al. MicroRNA mediating networks in granulosa cells associated with ovarian follicular development. BioMed Res Int 2017;2017:4585213. https://doi.org/10.1155/2017/4585213
25 Orom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 2008;30:460-71. https://doi.org/10.1016/j.molcel.2008.05.001   DOI
26 Yan G, Zhang L, Fang T, et al. MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB. FEBS Lett 2012;586:3263-70. https://doi.org/10.1016/j.febslet.2012.06.048   DOI
27 Donadeu FX, Mohammed BT, Ioannidis J. A miRNA target network putatively involved in follicular atresia. Domest Anim Endocrinol 2017;58:76-83. https://doi.org/10.1016/j.domani end.2016.08.002   DOI
28 Yang X, Zhou Y, Peng S, et al. Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis. Reproduction 2012;144:235-44. https://doi.org/10.1530/REP-11-0371   DOI
29 Nie M, Yu S, Peng S, Fang Y, Wang H, Yang X. miR-23a and miR-27a promote human granulosa cell apoptosis by targeting SMAD5. Biol Reprod 2015;93:98. https://doi.org/10.1095/biolreprod.115.130690   DOI
30 Huang X, Liu C, Hao C, et al. Identification of altered microRNAs and mRNAs in the cumulus cells of PCOS patients: miRNA-509-3p promotes oestradiol secretion by targeting MAP3K8. Reproduction 2016;151:643-55. https://doi.org/10.1530/REP-16-0071   DOI
31 O'Doherty AM, O'Brien YM, Browne JA, Wingfield M, O'Shea LC. Expression of granulosa cell microRNAs, AVEN and ATRX are associated with human blastocyst development. Mol Reprod Dev 2018;85:836-48. https://doi.org/10.1002/mrd.22990   DOI
32 Lee J, Park H, Eom J, Kang SG. MicroRNA-mediated regulation of the development and functions of follicular helper T cells. Immune Netw 2018;18:e7. https://doi.org/10.4110/in.2018.18.e7   DOI
33 Wigglesworth K, Lee KB, Emori C, Sugiura K, Eppig JJ. Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod 2015;92:23. https://doi.org/10.1095/biolreprod.114.121756   DOI
34 Zhou J, Lei B, Li H, et al. MicroRNA-144 is regulated by CP2 and decreases COX-2 expression and PGE2 production in mouse ovarian granulosa cells. Cell Death Disease 2017;8:e2597. https://doi.org/10.1038/cddis.2017.24   DOI
35 Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-33. https://doi.org/10.1016/j.cell.2009.01.002   DOI
36 Li D, Xu D, Xu Y, et al. MicroRNA-141-3p targets DAPK1 and inhibits apoptosis in rat ovarian granulosa cells. Cell Biochem Funct 2017;35:197-201. https://doi.org/10.1002/cbf.3248   DOI
37 Liu J, Du X, Zhou J, Pan Z, Liu H, Li Q. MicroRNA-26b functions as a proapoptotic factor in porcine follicular Granulosa cells by targeting Sma-and Mad-related protein 4. Biol Reprod 2014;91:146. https://doi.org/10.1095/biolreprod.114.122788   DOI
38 Yao YL, Niu JQ, Sizhu SL, et al. microRNA-125b regulates apoptosis by targeting bone morphogenetic protein receptor 1B in yak granulosa cells. DNA Cell Biol 2018;37:878-87. http://doi.org/10.1089/dna.2018.4354   DOI
39 Lockhart J, Canfield J, Mong EF, VanWye J, Totary-Jain H. Nucleotide modification alters microRNA-dependent silencing of microRNA switches. Mol Ther Nucleic Acids 2019;14:339-50. https://doi.org/10.1016/j.omtn.2018.12.007   DOI
40 Mohr AM, Mott JL. Overview of microRNA biology. Semin Liver Dis 2015;35:3-11. https://doi.org/10.1055/s-0034-1397344   DOI
41 Shin C, Nam JW, Farh KK, Chiang HR, Shkumatava A, Bartel DP. Expanding the microRNA targeting code: functional sites with centered pairing. Mol Cell 2010;38:789-802. https://doi.org/10.1016/j.molcel.2010.06.005   DOI
42 Carletti MZ, Fiedler SD, Christenson LK. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol Reprod 2010;83:286-95. https://doi.org/10.1095/biolreprod.109.081448   DOI
43 Cao C, Ding Y, Kong X, et al. Reproductive role of miRNA in the hypothalamic-pituitary axis. Mol Cell Neurosci 2018;88:130-7. https://doi.org/10.1016/j.mcn.2018.01.008   DOI
44 Sun XF, Li YP, Pan B. Molecular regulation of miR-378 on the development of mouse follicle and the maturation of oocyte in vivo. Cell Cycle (Georgetown, Tex). 2018;17:2230-42. https://doi.org/10.1080/15384101.2018.1520557   DOI
45 Naji M, Aleyasin A, Nekoonam S, Arefian E, Mahdian R. Differential Expression of miR-93 and miR-21 in granulosa cells and follicular fluid of polycystic ovary syndrome associating with different phenotypes. Sci Rep 2017;7:14671. https://doi.org/10.1038/s41598-017-13250-1   DOI
46 Han X, Xue R, Yuan HJ, et al. MicroRNA-21 plays a pivotal role in the oocyte-secreted factor-induced suppression of cumulus cell apoptosis. Biol Reprod 2017;96:1167-80. https://doi.org/10.1093/biolre/iox044   DOI
47 Fu X, He Y, Wang X, et al. Overexpression of miR-21 in stem cells improves ovarian structure and function in rats with chemotherapy-induced ovarian damage by targeting PDCD4 and PTEN to inhibit granulosa cell apoptosis. Stem Cell Res Therapy 2017;8:187. https://doi.org/10.1186/s13287-017- 0641-z   DOI
48 Tscherner A, Brown AC, Stalker L, et al. STAT3 signaling stimulates miR-21 expression in bovine cumulus cells during in vitro oocyte maturation. Sci Rep 2018;8:11527. https://doi.org/10.1038/s41598-018-29874-w   DOI
49 Li X, Jin Y, Mu Z, Chen W, Jiang S. MicroRNA146a5p enhances cisplatininduced apoptosis in ovarian cancer cells by targeting multiple antiapoptotic genes. Int J Oncol 2017;51:327-35. https://doi.org/10.3892/ijo.2017.4023   DOI
50 Chen X, Xie M, Liu D, Shi K. Downregulation of microRNA- 146a inhibits ovarian granulosa cell apoptosis by simultaneously targeting interleukin-1 receptor-associated kinase and tumor necrosis factor receptor-associated factor 6. Mol Med Rep 2015;12:5155-62. https://doi.org/10.3892/mmr.2015. 4036   DOI
51 Du X, Li Q, Pan Z, Li Q. Androgen receptor and miRNA-126* axis controls follicle-stimulating hormone receptor expression in porcine ovarian granulosa cells. Reproduction 2016;152:161-9. https://doi.org/10.1530/REP-15-0517   DOI
52 Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011;39(Suppl 1):D152-7. https://doi.org/10.1093/nar/gkq1027   DOI
53 Weixi X, Lin LY, Lili X, et al. Circulatory microRNA 23a and microRNA 23b and polycystic ovary syndrome (PCOS): the effects of body mass index and sex hormones in an Eastern Han Chinese population. J Ovarian Res 2017;10:10. https://doi.org/10.1186/s13048-016-0298-8   DOI
54 Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001;294:858-62. https://doi.org/10.1126/science.1065062   DOI
55 Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004;23:4051-60. https://doi.org/10.1038/sj.emboj.7600385   DOI
56 Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008;9:102-14. https://doi.org/10.1038/nrg2290   DOI
57 Yates LA, Norbury CJ, Gilbert RJC. The long and short of microRNA. Cell 2013;153:516-9. https://doi.org/10.1016/j.cell.2013.04.003   DOI
58 Sirotkin AV, Laukova M, Ovcharenko D, Brenaut P, Mlyncek M. Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. J Cell Physiol 2010;223:49-56. https://doi.org/10.1002/jcp.21999   DOI
59 Luo M, Li L, Xiao C, Sun Y, Wang GL. Heat stress impairs mice granulosa cell function by diminishing steroids production and inducing apoptosis. Mol Cell Biochem 2016;412:81-90. https://doi.org/10.1007/s11010-015-2610-0   DOI
60 Aherne ST, Lao NT. Manipulating miRNA expression to uncover hidden functions. Methods Mol Biol (Clifton, NJ). 2017;1509:151-60. https://doi.org/10.1007/978-1-4939-6524- 3_14   DOI
61 Dai A, Sun H, Fang T, et al. MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2. FEBS Lett 2013;587:2474-82. https://doi.org/10.1016/j.febslet.2013.06.023   DOI
62 Kitahara Y, Nakamura K, Kogure K, Minegishi T. Role of microRNA-136-3p on the expression of luteinizing hormone-human chorionic gonadotropin receptor mRNA in rat ovaries. Biol Reprod 2013;89:114. https://doi.org/10.1095/biolreprod.113.109207   DOI
63 Yang S, Wang S, Luo A, et al. Expression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary. Biol Reprod 2013;89:126. https://doi.org/10.1095/biolreprod.113.107730   DOI
64 Donadeu FX, Schauer SN, Sontakke SD. Involvement of miRNAs in ovarian follicular and luteal development. J Endocrinol 2012;215:323-34. https://doi.org/10.1530/joe-12-0252   DOI
65 Xu S, Linher-Melville K, Yang BB, Wu D, Li J. Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology 2011;152:3941-51. https://doi.org/10.1210/en.2011-1147   DOI
66 Zhou J, Liu J, Pan Z, et al. The let-7g microRNA promotes follicular granulosa cell apoptosis by targeting transforming growth factor-beta type 1 receptor. Mol Cell Endocrinol 2015;409:103-12. https://doi.org/10.1016/j.mce.2015.03.012   DOI
67 Aherne ST, Lao NT. Manipulating miRNA expression to uncover hidden functions. In: Rani S, editor. MicroRNA profiling. Methods in Molecular Biology. New York, NY, USA: Humana Press; 2017. vol 1509 pp. 151-60. https://doi.org/10.1007/978-1-4939-6524-3_14
68 Zhou J, Yao W, Liu K, et al. MicroRNA let-7g regulates mouse granulosa cell autophagy by targeting insulin-like growth factor 1 receptor. Int J Biochem Cell Biol 2016;78:130-40. https://doi.org/10.1016/j.biocel.2016.07.008   DOI
69 Su JL, Chen PS, Johansson G, Kuo ML. Function and regulation of let-7 family microRNAs. MicroRNA 2012;1:34-9.   DOI
70 Cao R, Wu WJ, Zhou XL, Xiao P, Wang Y, Liu HL. Expression and preliminary functional profiling of the let-7 family during porcine ovary follicle atresia. Mol Cells 2015;38:304-11. https://doi.org/10.14348/molcells.2015.2122   DOI
71 Cao R, Wu W, Zhou X, et al. Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary. Int J Biochem Cell Biol 2015;68:148-57. https://doi.org/10.1016/j.biocel.2015.08.011   DOI
72 Gebremedhn S, Salilew-Wondim D, Ahmad I, et al. MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle. PloS one 2015;10:e0125912. https://doi.org/10.1371/journal.pone.0125912   DOI
73 Zhang J, Xu Y, Liu H, Pan Z. MicroRNAs in ovarian follicular atresia and granulosa cell apoptosis. Reprod Biol Endocrinol 2019;17:9. https://doi.org/10.1186/s12958-018-0450-y   DOI
74 Shippy DC, Bearson BL, Cai G, Brunelle BW, Kich JD, Bearson SMD. Modulation of porcine microRNAs associated with apoptosis and NF-kappaB signaling pathways in response to Salmonella enterica serovar Typhimurium. Gene 2018;676:290-7. https://doi.org/10.1016/j.gene.2018.08.044   DOI
75 Gebremedhn S, Salilew-Wondim D, Hoelker M, et al. MicroRNA-183-96-182 cluster regulates bovine granulosa cell proliferation and cell cycle transition by coordinately targeting FOXO1. Biol Reprod 2016;94:127. https://doi.org/10.1095/biolreprod.115.137539
76 Herndon MK, Law NC, Donaubauer EM, Kyriss B, Hunzicker-Dunn M. Forkhead box O member FOXO1 regulates the majority of follicle-stimulating hormone responsive genes in ovarian granulosa cells. Mol Cell Endocrinol 2016;434:116-26.   DOI
77 Askandar Iqbal M, Arora S, Prakasam G, Calin GA, Syed MA. MicroRNA in lung cancer: role, mechanisms, pathways and therapeutic relevance. Mol Aspects Med 2019;70:3-20. https://doi.org/10.1016/j.mam.2018.07.003   DOI
78 Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 2008;133:217-22. https://doi.org/10.1016/j.cell.2008.04.001   DOI
79 Thomson DW, Dinger ME. Endogenous microRNA sponges: evidence and controversy. Nat Rev Genet 2016;17:272-83. https://doi.org/10.1038/nrg.2016.20   DOI
80 Silveira Zavalhia L, Weber Medeiros A, Oliveira Silva A, Vial Roehe A. Do FHIT gene alterations play a role in human solid tumors? 2018;14:e214-23. https://doi.org/10.1111/ajco.12868   DOI
81 Cha HJ, An SK, Kim TJ, Lee JH. Alteration of microRNA profiling in sphere-cultured ovarian carcinoma cells. Oncol Lett 2018;16:2016-22. https://doi.org/10.3892/ol.2018.8818   DOI
82 Richards JS. From follicular development and ovulation to ovarian cancers: an unexpected journey. Vitam Horm 2018;107:453-72. https://doi.org/10.1016/bs.vh.2018.01.019   DOI
83 Saliminejad K, Khorram Khorshid HR, Soleymani Fard S, Ghaffari SH. An overview of microRNAs: Biology, functions, therapeutics, and analysis methods. J Cell Physiol 2019;234:5451-65. https://doi.org/10.1002/jcp.27486   DOI
84 Inoue K, Hirose M, Inoue H, et al. The rodent-specific microRNA cluster within the Sfmbt2 gene is imprinted and essential for placental development. Cell Rep 2017;19:949-56. https://doi.org/10.1016/j.celrep.2017.04.018   DOI
85 Schauer SN, Sontakke SD, Watson ED, Esteves CL, Donadeu FX. Involvement of miRNAs in equine follicle development. Reproduction 2013;146:273-82. https://doi.org/10.1530/REP-13-0107   DOI
86 Battaglia R, Vento ME, Ragusa M, et al. MicroRNAs are stored in human MII oocyte and their expression profile changes in reproductive aging. Biol Reprod 2016;95:131. https://doi.org/10.1095/biolreprod.116.142711   DOI
87 Li X, Zhuang X, Xu T, et al. Expression analysis of microRNAs and mRNAs in ovarian granulosa cells after microcystin-LR exposure. Toxicon 2017;129:11-9. https://doi.org/10.1016/j. toxicon.2017.01.022   DOI
88 Wang J, Xu B, Tian GG, Sun T, Wu J. Ablation of the MiR-17-92 MicroRNA cluster in germ cells causes subfertility in female mice. Cell Physiol Biochem 2018;45:491-504. https://doi.org/10.1159/000487028   DOI
89 Andreas E, Hoelker M, Neuhoff C, et al. MicroRNA 17-92 cluster regulates proliferation and differentiation of bovine granulosa cells by targeting PTEN and BMPR2 genes. Cell Tissue Res 2016;366:219-30. https://doi.org/10.1007/s00441-016-2425-7   DOI
90 Li P, Sheng C, Huang L, et al. MiR-183/-96/-182 cluster is up-regulated in most breast cancers and increases cell proliferation and migration. Breast Cancer Res 2014;16:473. https://doi.org/10.1186/s13058-014-0473-z   DOI