The Importance of Small Non-Coding RNAs in Human Reproduction: A Review Article

References

• McCallie B, Schoolcraft WB, Katz-Jaffe MG. Aberration of blastocyst microRNA expression is associated with human infertility. Fertil Steril. 2010;93(7):2374–2382. doi:10.1016/j.fertnstert.2009.01.069
   Web of Science ®Google Scholar
• Anfossi S, Fu X, Nagvekar R, Calin GA. MicroRNAs, regulatory messengers inside and outside cancer cells. Adv Exp Med Biol. 2018;1056:87–108.
   PubMed Web of Science ®Google Scholar
• Galagali H, Kim JK. miRISC composition determines target fates in time and space. Dev Cell. 2018;47(2):142–143. doi:10.1016/j.devcel.2018.10.009
   Web of Science ®Google Scholar
• Mineno J, Okamoto S, Ando T, et al. The expression profile of microRNAs in mouse embryos. Nucleic Acids Res. 2006;34(6):1765–1771. doi:10.1093/nar/gkl096
   Web of Science ®Google Scholar
• Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006;11(4):441–450. doi:10.1016/j.devcel.2006.09.009
   PubMed Web of Science ®Google Scholar
• Perez-Cremades D, Mompeon A, Vidal-Gomez X, Hermenegildo C, Novella S. Role of miRNA in the regulatory mechanisms of estrogens in cardiovascular ageing. Oxid Med Cell Longev. 2018;2018:6082387. doi:10.1155/2018/6082387
   PubMed Web of Science ®Google Scholar
• Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci U S A. 2008;105(5):1608–1613. doi:10.1073/pnas.0707594105
   PubMed Web of Science ®Google Scholar
• Zhang X, Xiao S, Rameau RD, et al. Nucleolin phosphorylation regulates PARN deadenylase activity during cellular stress response. RNA Biol. 2018;15(2):251–260. doi:10.1080/15476286.2017.1408764
   PubMed Web of Science ®Google Scholar
• Bastet L, Turcotte P, Wade JT, Lafontaine DA. Maestro of regulation: riboswitches orchestrate gene expression at the levels of translation, transcription and mRNA decay. RNA Biol. 2018;15(6):679–682. doi:10.1080/15476286.2018.1451721
   PubMed Web of Science ®Google Scholar
• Tang F, Kaneda M, O’Carroll D, et al. Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007;21(6):644–648. doi:10.1101/gad.418707
   PubMed Web of Science ®Google Scholar
• Park K, Kim KB. miRTar Hunter: a prediction system for identifying human microRNA target sites. Mol Cells. 2013;35(3):195–201. doi:10.1007/s10059-013-2165-4
   Web of Science ®Google Scholar
• Schwarzenbacher D, Balic M, Pichler M. The role of microRNAs in breast cancer stem cells. Int J Mol Sci. 2013;14(7):14712–14723. doi:10.3390/ijms140714712
   PubMed Web of Science ®Google Scholar
• Ha T-Y. MicroRNAs in human diseases: from cancer to cardiovascular disease. Immune Netw. 2011;11(3):135–154. doi:10.4110/in.2011.11.3.135
   PubMedGoogle Scholar
• Khan F, Momtaz S, Abdollahi M. The relationship between mercury exposure and epigenetic alterations regarding human health, risk assessment and diagnostic strategies. J Trace Elem Med Biol. 2019;52:37–47. doi:10.1016/j.jtemb.2018.11.006
   PubMed Web of Science ®Google Scholar
• Minogue AL, Tackett MR, Atabakhsh E, Tejada G, Arur S. Functional genomic analysis identifies miRNA repertoire regulating C. elegans oocyte development. Nat Commun. 2018;9(1):5318. doi:10.1038/s41467-018-07791-w
   Web of Science ®Google Scholar
• Real FM, Sekido R, Lupianez DG, Lovell-Badge R, Jimenez R, Burgos M. A microRNA (mmu-miR-124) prevents Sox9 expression in developing mouse ovarian cells. Biol Reprod. 2013;89(4):78. doi:10.1095/biolreprod.113.110957
   Web of Science ®Google Scholar
• Lakshmipathy U, Love B, Goff LA, et al. MicroRNA expression pattern of undifferentiated and differentiated human embryonic stem cells. Stem Cells Dev. 2007;16(6):1003–1016. doi:10.1089/scd.2007.0026
   Web of Science ®Google Scholar
• Yang Q, Lin J, Liu M, et al. Highly sensitive sequencing reveals dynamic modifications and activities of small RNAs in mouse oocytes and early embryos. Sci Adv. 2016;2(6):e1501482. doi:10.1126/sciadv.1501482
   Web of Science ®Google Scholar
• Tatsuguchi M, Seok HY, Callis TE, et al. Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol. 2007;42(6):1137–1141. doi:10.1016/j.yjmcc.2007.04.004
   Web of Science ®Google Scholar
• Yang Y, Bai W, Zhang L, et al. Determination of microRNAs in mouse preimplantation embryos by microarray. Dev Dyn. 2008;237(9):2315–2327. doi:10.1002/dvdy.21666
   Web of Science ®Google Scholar
• Singh SK, Pal Bhadra M, Girschick HJ, Bhadra U. MicroRNAs–micro in size but macro in function. FEBS J. 2008;275(20):4929–4944. doi:10.1111/j.1742-4658.2008.06624.x
   PubMed Web of Science ®Google Scholar
• Carletti M, Christenson L. MicroRNA in the ovary and female reproductive tract. J Anim Sci. 2009;87(14_suppl):E29–E38. doi:10.2527/jas.2008-1331
   Web of Science ®Google Scholar
• Krawczynski K, Bauersachs S, Reliszko ZP, Graf A, Kaczmarek MM. Expression of microRNAs and isomiRs in the porcine endometrium: implications for gene regulation at the maternal-conceptus interface. BMC Genomics. 2015;16:906. doi:10.1186/s12864-015-2172-2
   Web of Science ®Google Scholar
• Chakrabarty A, Tranguch S, Daikoku T, Jensen K, Furneaux H, Dey SK. MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc Natl Acad Sci U S A. 2007;104(38):15144–15149. doi:10.1073/pnas.0705917104
   PubMed Web of Science ®Google Scholar
• Johnson M, Everitt B. Adult ovarian function. In: Essential Reproduction. Vol. 5. 2000.
   Google Scholar
• Bhin J, Jeong HS, Kim JS, et al. PGC-Enriched miRNAs Control Germ Cell Development. Mol Cells. 2015;38(10):895–903.
   PubMed Web of Science ®Google Scholar
• Takada S, Berezikov E, Choi YL, Yamashita Y, Mano H. Potential role of miR-29b in modulation of Dnmt3a and Dnmt3b expression in primordial germ cells of female mouse embryos. RNA. 2009;15(8):1507–1514. doi:10.1261/rna.1418309
   PubMed Web of Science ®Google Scholar
• Rengaraj D, Lee BR, Lee SI, Seo HW, Han JY. Expression patterns and miRNA regulation of DNA methyltransferases in chicken primordial germ cells. PLoS One. 2011;6(5):e19524. doi:10.1371/journal.pone.0019524
   Web of Science ®Google Scholar
• Mei J, Yue H-M, Li Z, et al. C1q-like factor, a target of miR-430, regulates primordial germ cell development in early embryos of Carassius auratus. Int J Biol Sci. 2014;10(1):15–24. doi:10.7150/ijbs.7490
   Web of Science ®Google Scholar
• Takeda Y, Mishima Y, Fujiwara T, Sakamoto H, Inoue K. DAZL relieves miRNA-mediated repression of germline mRNAs by controlling poly (A) tail length in zebrafish. PLoS One. 2009;4(10):e7513. doi:10.1371/journal.pone.0007513
   Web of Science ®Google Scholar
• Virant-Klun I, Ståhlberg A, Kubista M, Skutella T. MicroRNAs: from female fertility, germ cells, and stem cells to cancer in humans. Stem Cells Int. 2016a;2016:3984937. doi:10.1155/2016/3984937
   Web of Science ®Google Scholar
• Donadeu FX, Schauer S, Sontakke S. Involvement of miRNAs in ovarian follicular and luteal development. J Endocrinol. 2012;215(3):323–334. doi:10.1530/JOE-12-0252
   Web of Science ®Google Scholar
• Lei L, Jin S, Gonzalez G, Behringer RR, Woodruff TK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol. 2010;315(1–2):63–73. doi:10.1016/j.mce.2009.09.021
   Web of Science ®Google Scholar
• Telfer EE, Zelinski MB. Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil Steril. 2013;99(6):1523–1533. doi:10.1016/j.fertnstert.2013.03.043
   PubMed Web of Science ®Google Scholar
• Nothnick WB. The role of micro-RNAs in the female reproductive tract. Reproduction. 2012;143(5):559–576. doi:10.1530/REP-11-0240
   PubMed Web of Science ®Google Scholar
• Robert C. Microarray analysis of gene expression during early development: a cautionary overview. Reproduction. 2010;140(6):787–801. doi:10.1530/REP-10-0191
   Web of Science ®Google Scholar
• Xu Y-W, Wang B, Ding C-H, Li T, Gu F, Zhou C. Differentially expressed micoRNAs in human oocytes. J Assist Reprod Genet. 2011;28(6):559–566. doi:10.1007/s10815-011-9590-0
   Web of Science ®Google Scholar
• Assou S, Al-Edani T, Haouzi D, et al. MicroRNAs: new candidates for the regulation of the human cumulus–oocyte complex. Hum Reprod. 2013;28(11):3038–3049. doi:10.1093/humrep/det321
   Web of Science ®Google Scholar
• Imbar T, Eisenberg I. Regulatory role of microRNAs in ovarian function. Fertil Steril. 2014;101(6):1524–1530. doi:10.1016/j.fertnstert.2014.04.024
   PubMed Web of Science ®Google Scholar
• Ecklund LC, Usadi RS. Endocrine and reproductive effects of polycystic ovarian syndrome. Obstet Gynecol Clin North Am. 2015;42(1):55–65. doi:10.1016/j.ogc.2014.09.003
   Web of Science ®Google Scholar
• Sørensen AE, Wissing ML, Salö S, Englund ALM, Dalgaard LT. MicroRNAs related to polycystic ovary syndrome (PCOS). Genes (Basel). 2014a;5(3):684–708. doi:10.3390/genes5030684
   PubMed Web of Science ®Google Scholar
• Ilie IR, Georgescu CE. Polycystic ovary syndrome-epigenetic mechanisms and aberrant MicroRNA. Adv Clin Chem. 2015;71:25–45.
   PubMed Web of Science ®Google Scholar
• Kropp J, Salih SM, Khatib H. Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front Genet. 2014;5:91.
   PubMed Web of Science ®Google Scholar
• Rosenbluth EM, Shelton DN, Wells LM, Sparks AE, Van Voorhis BJ. Human embryos secrete microRNAs into culture media—a potential biomarker for implantation. Fertil Steril. 2014;101(5):1493–1500. doi:10.1016/j.fertnstert.2014.01.058
   PubMed Web of Science ®Google Scholar
• Simon A, Laufer N. Assessment and treatment of repeated implantation failure (RIF). J Assist Reprod Genet. 2012;29(11):1227–1239. doi:10.1007/s10815-012-9861-4
   PubMed Web of Science ®Google Scholar
• Revel A, Achache H, Stevens J, Smith Y, Reich R. MicroRNAs are associated with human embryo implantation defects. Hum Reprod. 2011;26(10):2830–2840. doi:10.1093/humrep/der255
   PubMed Web of Science ®Google Scholar
• Hawkins SM, Creighton CJ, Han DY, et al. Functional microRNA involved in endometriosis. Mol Endocrinol. 2011;25(5):821–832. doi:10.1210/me.2010-0371
   PubMedGoogle Scholar
• Aznaurova YB, Zhumataev MB, Roberts TK, Aliper AM, Zhavoronkov AA. Molecular aspects of development and regulation of endometriosis. Reprod Biol Endocrinol. 2014;12:50. doi:10.1186/1477-7827-12-50
   PubMed Web of Science ®Google Scholar
• Merrill RM, Layman AB, Oderda G, Asche C. Risk estimates of hysterectomy and selected conditions commonly treated with hysterectomy. Ann Epidemiol. 2008;18(3):253–260. doi:10.1016/j.annepidem.2007.10.011
   Web of Science ®Google Scholar
• Verkauf B. Incidence, symptoms, and signs of endometriosis in fertile and infertile women. J Fla Med Assoc. 1987;74(9):671.
   Google Scholar
• Ohlsson Teague EMC, Print CG, Hull ML. The role of microRNAs in endometriosis and associated reproductive conditions. Hum Reprod Update. 2009;16(2):142–165. doi:10.1093/humupd/dmp034
   Web of Science ®Google Scholar
• Pan Q, Luo X, Toloubeydokhti T, Chegini N. The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression. Mol Hum Reprod. 2007;13(11):797–806. doi:10.1093/molehr/gam063
   Web of Science ®Google Scholar
• Harchegani AB, Shafaghatian H, Tahmasbpour E, Shahriary A. Regulatory functions of MicroRNAs in male reproductive health: a new approach to understanding male infertility. Reprod Sci. 2018. doi:10.1177/1933719118765972
   Google Scholar
• Rajender S, Meador C, Agarwal A. Small RNA in spermatogenesis and male infertility. Front Biosci (Schol Ed). 2012;4:1266–1274. doi:10.2741/s330
   Google Scholar
• Hever A, Roth RB, Hevezi P, et al. Human endometriosis is associated with plasma cells and overexpression of B lymphocyte stimulator. Proc Natl Acad Sci. 2007;104(30):12451–12456. doi:10.1073/pnas.0703451104
   PubMed Web of Science ®Google Scholar
• Eyster KM, Klinkova O, Kennedy V, Hansen KA. Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium. Fertil Steril. 2007;88(6):1505–1533. doi:10.1016/j.fertnstert.2007.01.056
   PubMed Web of Science ®Google Scholar
• Litwin M, Szczepańska‑Buda A, Piotrowska A, Dzięgiel P, Witkiewicz W. The meaning of PIWI proteins in cancer development. Oncol Lett. 2017;13(5):3354–3362. doi:10.3892/ol.2017.5932
   PubMed Web of Science ®Google Scholar
• Gong J, Zhang Q, Wang Q, et al. Identification and verification of potential piRNAs from domesticated yak testis. Reproduction. 2018;155(2):115–125. doi:10.1530/REP-17-0592
   Web of Science ®Google Scholar
• Juliano C, Wang J, Lin H. Uniting germline and stem cells: the function of piwi proteins and the piRNA pathway in diverse organisms. Annu Rev Genet. 2011;45:447–469. doi:10.1146/annurev-genet-110410-132541
   PubMed Web of Science ®Google Scholar
• Tan Y, Liu L, Liao M, et al. Emerging roles for PIWI proteins in cancer. Acta Biochim Biophys Sin. 2015;47(5):315–324. doi:10.1093/abbs/gmv018
   Google Scholar
• Thomson T, Lin H. The biogenesis and function PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol. 2009;25:355. doi:10.1146/annurev.cellbio.24.110707.175327
   PubMed Web of Science ®Google Scholar
• Klattenhoff C, Theurkauf W. Biogenesis and germline functions of piRNAs. Development. 2008;135(1):3–9. doi:10.1242/dev.006486
   PubMed Web of Science ®Google Scholar
• Clark JP, Lau NC. Piwi proteins and piRNAs step onto the systems biology stage. In: Systems Biology of RNA Binding Proteins. Springer; 2014:159–197.
   Google Scholar
• Qiu L, Xu L, Chang G, et al. DNA methylation-mediated transcription factors regulate Piwil1 expression during chicken spermatogenesis. J Reprod Dev. 2016;62(4):367–372. doi:10.1262/jrd.2016-003
   Web of Science ®Google Scholar
• Bak CW, Yoon T-K, Choi Y. Functions of PIWI proteins in spermatogenesis. Clin Exp Reprod Med. 2011;38(2):61–67. doi:10.5653/cerm.2011.38.2.61
   PubMedGoogle Scholar
• Heyn H, Ferreira HJ, Bassas L, et al. Epigenetic disruption of the PIWI pathway in human spermatogenic disorders. PLoS One. 2012;7(10):e47892. doi:10.1371/journal.pone.0047892
   PubMed Web of Science ®Google Scholar
• Lim SL, Qu ZP, Kortschak RD, et al. Correction: HENMT1 and piRNA stability are required for adult male germ cell transposon repression and to define the spermatogenic program in the mouse. PLoS Genet. 2015;11(12):e1005782.
   Google Scholar
• Ma X, Wang S, Do T, et al. Piwi is required in multiple cell types to control germline stem cell lineage development in the Drosophila ovary. PLoS One. 2014;9(3):e90267. doi:10.1371/journal.pone.0090267
   PubMed Web of Science ®Google Scholar
• Assumpção CB, Calcagno DQ, Araújo TMT, et al. The role of piRNA and its potential clinical implications in cancer. Epigenomics. 2015;7(6):975–984. doi:10.2217/epi.15.37
   PubMed Web of Science ®Google Scholar
• Aravin AA, Sachidanandam R, Bourc’his D, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31(6):785–799. doi:10.1016/j.molcel.2008.09.003
   PubMed Web of Science ®Google Scholar
• Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007;316(5825):744–747. doi:10.1126/science.1142612
   PubMed Web of Science ®Google Scholar
• Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science. 2007;318(5851):761–764. doi:10.1126/science.1146484
   PubMed Web of Science ®Google Scholar
• Brennecke J, Aravin AA, Stark A, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–1103. doi:10.1016/j.cell.2007.01.043
   PubMed Web of Science ®Google Scholar
• Carmell MA, Girard A, van de Kant HJ, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell. 2007;12(4):503–514. doi:10.1016/j.devcel.2007.03.001
   PubMed Web of Science ®Google Scholar
• Williams Z, Morozov P, Mihailovic A, et al. Discovery and characterization of piRNAs in the human fetal ovary. Cell Rep. 2015;13(4):854–863. doi:10.1016/j.celrep.2015.09.030
   PubMed Web of Science ®Google Scholar
• Guo R, Yu Z, Guan J, et al. Stage‐specific and tissue‐specific expression characteristics of differentially expressed genes during mouse spermatogenesis. Mol Reprod Dev. 2004;67(3):264–272. doi:10.1002/(ISSN)1098-2795
   Web of Science ®Google Scholar
• Kuramochi-Miyagawa S, Kimura T, Ijiri TW, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 2004;131(4):839–849. doi:10.1242/dev.00973
   PubMed Web of Science ®Google Scholar
• Deng W, Lin H. Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell. 2002;2(6):819–830. doi:10.1016/S1534-5807(02)00165-X
   PubMed Web of Science ®Google Scholar
• Malki S, van der Heijden GW, O’Donnell KA, Martin SL, Bortvin A. A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev Cell. 2014;29(5):521–533. doi:10.1016/j.devcel.2014.04.027
   Web of Science ®Google Scholar