Non-coding RNA regulation in reproduction: Their potential use as biomarkers

Larriba, 2016, Role of non-coding RNAs in the transgenerational epigenetic transmission of the effects of reprotoxicants, Int. J. Mol. Sci., 17, 452, 10.3390/ijms17040452 Ha, 2014, Regulation of microRNA biogenesis, Nat. Rev. Mol. Cell Biol., 15, 509, 10.1038/nrm3838 Alarcón, 2015, N6-methyladenosine marks primary microRNAs for processing, Nature, 519, 482, 10.1038/nature14281 Miyoshi, 2010, Many ways to generate microRNA-like small RNAs: non-canonical pathways for microRNA production, Mol. Genet. Genom., 284, 95, 10.1007/s00438-010-0556-1 Peterson, 2014, Common features of microRNA target prediction tools, Front. Genet., 5, 23, 10.3389/fgene.2014.00023 Zhang, 2018, A novel class of microRNA-recognition elements that function only within open reading frames, Nat. Struct. Mol. Biol., 10.1038/s41594-018-0136-3 Russell, 2018, Transposons and the PIWI pathway: genome defense in gametes and embryos, Reproduction, 156, R111, 10.1530/REP-18-0218 Iwasaki, 2015, PIWI-interacting RNA: its biogenesis and functions, Annu. Rev. Biochem., 84, 405, 10.1146/annurev-biochem-060614-034258 Quinn, 2016, Unique features of long non-coding RNA biogenesis and function, Nat. Rev. Genet., 17, 47, 10.1038/nrg.2015.10 Luk, 2014, Long noncoding RNAs in spermatogenesis: insights from recent high-throughput transcriptome studies, Reproduction, 147, R131, 10.1530/REP-13-0594 Kung, 2013, Long noncoding RNAs: past, present, and future, Genetics, 193, 651, 10.1534/genetics.112.146704 Kotaja, 2007, The chromatoid body: a germ-cell-specific RNA-processing centre, Nat. Rev. Mol. Cell Biol., 8, 85, 10.1038/nrm2081 Ohinata, 2009, A signaling principle for the specification of the germ cell lineage in mice, Cell, 137, 571, 10.1016/j.cell.2009.03.014 Tang, 2016, Specification and epigenetic programming of the human germ line, Nat. Rev. Genet., 17, 585, 10.1038/nrg.2016.88 Lawson, 1999, Bmp4 is required for the generation of primordial germ cells in the mouse embryo, Genes Dev., 13, 424, 10.1101/gad.13.4.424 Ying, 2000, Requirement of Bmp8b for the generation of primordial germ cells in the mouse, Mol. Endocrinol., 14, 1053, 10.1210/mend.14.7.0479 Bhin, 2015, PGC-enriched miRNAs control germ cell development, Mol. Cell., 38, 895, 10.14348/molcells.2015.0146 Medeiros, 2011, Mir-290-295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects, Proc. Natl. Acad. Sci. Unit. States Am., 108, 14163, 10.1073/pnas.1111241108 Takada, 2009, Potential role of miR-29b in modulation of Dnmt3a and Dnmt3b expression in primordial germ cells of female mouse embryos, RNA, 15, 1507, 10.1261/rna.1418309 Zhang, 2017, MiR-202-5p is a novel germ plasm-specific microRNA in zebrafish, Sci. Rep., 7, 7055, 10.1038/s41598-017-07675-x Staton, 2011, miRNA regulation of Sdf1 chemokine signaling provides genetic robustness to germ cell migration, Nat. Genet., 43, 204, 10.1038/ng.758 Hong, 2016, Dnd is a critical specifier of primordial germ cells in the medaka fish, Stem Cell Reports, 6, 411, 10.1016/j.stemcr.2016.01.002 Weick, 2014, piRNAs: from biogenesis to function, Development, 141, 3458, 10.1242/dev.094037 Ku, 2014, PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression, Natl. Sci. Rev., 1, 205, 10.1093/nsr/nwu014 von Meyenn, 2016, Comparative principles of DNA methylation reprogramming during human and mouse in vitro primordial germ cell specification, Dev. Cell, 39, 104, 10.1016/j.devcel.2016.09.015 Houwing, 2007, A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish, Cell, 129, 69, 10.1016/j.cell.2007.03.026 Taylor, 2015, Long non-coding RNA regulation of reproduction and development, Mol. Reprod. Dev., 82, 932, 10.1002/mrd.22581 Zhang, 2016, LncRNA, a new component of expanding RNA-protein regulatory network important for animal sperm development, Semin. Cell Dev. Biol., 59, 110, 10.1016/j.semcdb.2016.06.013 Magnúsdóttir, 2014, How to make a primordial germ cell, Development, 141, 245, 10.1242/dev.098269 Yadav, 2014, Small RNAs in spermatogenesis, Mol. Cell. Endocrinol., 382, 498, 10.1016/j.mce.2013.04.015 Rinn, 2012, Genome regulation by long noncoding RNAs, Annu. Rev. Biochem., 81, 145, 10.1146/annurev-biochem-051410-092902 Yu, 2014, miR-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2, J. Cell. Biochem., 115, 232, 10.1002/jcb.24655 McIver, 2012, A unique combination of male germ cell miRNAs coordinates gonocyte differentiation, PLoS One, 7, e35553, 10.1371/journal.pone.0035553 Niu, 2011, MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells, Proc. Natl. Acad. Sci. Unit. States Am., 108, 12740, 10.1073/pnas.1109987108 Tong, 2011, Expression of Mirlet7 family microRNAs in response to retinoic acid-induced spermatogonial differentiation in mice, Biol. Reprod., 85, 189, 10.1095/biolreprod.110.089458 Huszar, 2013, MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in Mice1, Biol. Reprod., 88, 15, 10.1095/biolreprod.112.103747 He, 2013, MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1, Stem Cell., 31, 2205, 10.1002/stem.1474 Cui, 2016, MicroRNA-224 regulates self-renewal of mouse spermatogonial stem cells via targeting DMRT1, J. Cell Mol. Med., 20, 1503, 10.1111/jcmm.12838 Chen, 2016, MicroRNA-202 maintains spermatogonial stem cells by inhibiting cell cycle regulators and RNA binding proteins, Nucleic Acids Res., 45, gkw1287, 10.1093/nar/gkw1287 Chen, 2017, The roles of microRNAs in regulation of mammalian spermatogenesis, J. Anim. Sci. Biotechnol., 8, 35, 10.1186/s40104-017-0166-4 Luk, 2014, Long noncoding RNAs in spermatogenesis: insights from recent high-throughput transcriptome studies, Reproduction, 147, R131, 10.1530/REP-13-0594 Hu, 2017, LncRNA AK015322 promotes proliferation of spermatogonial stem cell C18-4 by acting as a decoy for microRNA-19b-3p, Vitro Anim. Cell Dev. Biol., 53, 277, 10.1007/s11626-016-0102-5 Liang, 2012, MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1, PLoS One, 7 Bouhallier, 2010, Role of miR-34c microRNA in the late steps of spermatogenesis, RNA, 16, 720, 10.1261/rna.1963810 Liu, 2012, Sperm-borne microRNA-34c is required for the first cleavage division in mouse, Proc. Natl. Acad. Sci. U.S.A., 109, 490, 10.1073/pnas.1110368109 Bao, 2012, MicroRNA-449 and MicroRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway, J. Biol. Chem., 287, 21686, 10.1074/jbc.M111.328054 Yu, 2005, MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA Cleavage1, Biol. Reprod., 73, 427, 10.1095/biolreprod.105.040998 Jia, 2015, Identification of MicroRNAs in zebrafish spermatozoa, Zebrafish, 12, 387, 10.1089/zeb.2015.1115 Anguera, 2011, Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain, PLoS Genet., 7, e1002248, 10.1371/journal.pgen.1002248 Nolasco, 2012, The expression of tubulin cofactor A (TBCA) is regulated by a noncoding antisense Tbca RNA during testis maturation, PLoS One, 7, e42536, 10.1371/journal.pone.0042536 Lü, 2015, Downregulation of miR-320a/383-sponge-like long non-coding RNA NLC1-C (narcolepsy candidate-region 1 genes) is associated with male infertility and promotes testicular embryonal carcinoma cell proliferation, Cell Death Dis., 6, 10.1038/cddis.2015.267 Knight, 2001, Potential local regulatory functions of inhibins, activins and follistatin in the ovary, Reproduction, 121, 503, 10.1530/rep.0.1210503 Tu, 2014, miR-34a targets the inhibin beta B gene, promoting granulosa cell apoptosis in the porcine ovary, Genet. Mol. Res., 13, 2504, 10.4238/2014.January.14.6 Ginther, 1996, Selection of the dominant follicle in cattle, Biol. Reprod., 55, 1187, 10.1095/biolreprod55.6.1187 Yada, 1999, Role of ovarian theca and granulosa cell interaction in hormone productionand cell growth during the bovine follicular maturation process, Biol. Reprod., 61, 1480, 10.1095/biolreprod61.6.1480 Aerts, 2010, Ovarian follicular dynamics: a review with emphasis on the bovine species. Part I: folliculogenesis and pre-antral follicle development, Reprod. Domest. Anim., 45, 171, 10.1111/j.1439-0531.2008.01302.x Buccione, 1990, Interactions between somatic cells and germ cells throughout mammalian oogenesis, Biol. Reprod., 43, 543, 10.1095/biolreprod43.4.543 Canty, 2006, Alterations in follicular IGFBP mRNA expression and follicular fluid IGFBP concentrations during the first follicle wave in beef heifers, Anim. Reprod. Sci., 93, 199, 10.1016/j.anireprosci.2005.06.033 Evans, 2004, Identification of genes involved in apoptosis and dominant follicle development during follicular waves in cattle, Biol. Reprod., 70, 1475, 10.1095/biolreprod.103.025114 Fayad, 2004, Gene expression profiling of differentially expressed genes in granulosa cells of bovine dominant follicles using suppression subtractive Hybridization1, Biol. Reprod., 70, 523, 10.1095/biolreprod.103.021709 Liang, 2007, Characterization of microRNA expression profiles in normal human tissues, BMC Genomics, 8, 166, 10.1186/1471-2164-8-166 Ro, 2007, Cloning and expression profiling of small RNAs expressed in the mouse ovary, RNA, 13, 2366, 10.1261/rna.754207 Li, 2011, Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing, Int. J. Biol. Sci., 7, 1045, 10.7150/ijbs.7.1045 Ling, 2014, Identification and characterization of microRNAs in the ovaries of multiple and uniparous goats (Capra hircus) during follicular phase, BMC Genomics, 15, 339, 10.1186/1471-2164-15-339 Hossain, 2009, Identification and characterization of miRNAs expressed in the bovine ovary, BMC Genomics, 10, 443, 10.1186/1471-2164-10-443 Hong, 2008, Dicer1 is essential for female fertility and normal development of the female reproductive system, Endocrinology, 149, 6207, 10.1210/en.2008-0294 Nagaraja, 2008, Deletion of Dicer in somatic cells of the female reproductive tract causes sterility, Mol. Endocrinol., 22, 2336, 10.1210/me.2008-0142 Gonzalez, 2009, Dicer is required for female reproductive tract development and fertility in the mouse, Mol. Reprod. Dev., 76, 678, 10.1002/mrd.21010 Gebremedhn, 2015, MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle, PLoS One, 10, e0125912, 10.1371/journal.pone.0125912 Bao, 1998, Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review, J. Anim. Sci., 76, 1903, 10.2527/1998.7671903x Vitt, 2000, Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat Follicles1, Biol. Reprod., 62, 370, 10.1095/biolreprod62.2.370 Hayashi, 2010, Differential genome-wide gene expression profiling of bovine largest and second-largest follicles: identification of genes associated with growth of dominant follicles, Reprod. Biol. Endocrinol., 8, 11, 10.1186/1477-7827-8-11 Donadeu, 2012, Involvement of miRNAs in ovarian follicular and luteal development, J. Endocrinol., 215, 323, 10.1530/JOE-12-0252 Yan, 2012, MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB, FEBS Lett., 586, 3263, 10.1016/j.febslet.2012.06.048 Dai, 2013, MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2, FEBS Lett., 587, 2474, 10.1016/j.febslet.2013.06.023 Zhang, 2013, MicroRNA-181a suppresses mouse granulosa cell proliferation by targeting activin receptor IIA, PLoS One, 8, e59667, 10.1371/journal.pone.0059667 Carletti, 2010, MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells, Biol. Reprod., 83, 286, 10.1095/biolreprod.109.081448 Lin, 2012, miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary, PLoS One, 7, e38640, 10.1371/journal.pone.0038640 Yang, 2012, Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis, Reproduction, 144, 235, 10.1530/REP-11-0371 Kitahara, 2013, Role of microRNA-136-3p on the expression of luteinizing hormone-human chorionic gonadotropin receptor mRNA in rat ovaries, Biol. Reprod., 89, 114, 10.1095/biolreprod.113.109207 Yin, 2012, Transactivation of microRNA-383 by steroidogenic factor-1 promotes estradiol release from mouse ovarian granulosa cells by targeting RBMS1, Mol. Endocrinol., 26, 1129, 10.1210/me.2011-1341 Xu, 2011, Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase, Endocrinology, 152, 3941, 10.1210/en.2011-1147 Yao, 2010, MicroRNA-224 is involved in transforming growth factor-β-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4, Mol. Endocrinol., 24, 540, 10.1210/me.2009-0432 Dai, 2013, MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2, FEBS Lett., 587, 2474, 10.1016/j.febslet.2013.06.023 Yao, 2014, MicroRNA-224 is involved in the regulation of mouse cumulus expansion by targeting Ptx3, Mol. Cell. Endocrinol., 382, 244, 10.1016/j.mce.2013.10.014 Zhang, 2017, MicroRNA mediating networks in granulosa cells associated with ovarian follicular development, BioMed Res. Int., 2017, 4585213 Grossman, 2016, A role of MicroRNAs in cell differentiation during gonad development, 309, 10.1007/978-3-319-31973-5_12 Ahn, 2010, MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing, Mol. Hum. Reprod., 16, 463, 10.1093/molehr/gaq017 Mishima, 2008, MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary, Reproduction, 136, 811, 10.1530/REP-08-0349 Di, 2014, Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season, BMC Genomics, 15, 899, 10.1186/1471-2164-15-899 Tripurani, 2010, Cloning and analysis of fetal ovary microRNAs in cattle, Anim. Reprod. Sci., 120, 16, 10.1016/j.anireprosci.2010.03.001 Huang, 2011, Solexa sequencing of novel and differentially expressed microRNAs in testicular and ovarian tissues in Holstein cattle, Int. J. Biol. Sci., 7, 1016, 10.7150/ijbs.7.1016 Miles, 2012, MicroRNA expression profile in bovine cumulus-oocyte complexes: possible role of let-7 and miR-106a in the development of bovine oocytes, Anim. Reprod. Sci., 130, 16, 10.1016/j.anireprosci.2011.12.021 Giraldez, 2006, Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs, Science, 312, 75, 10.1126/science.1122689 Bouchareb, 2017, Genome-wide identification of novel ovarian-predominant miRNAs: new insights from the medaka (Oryzias latipes), Sci. Rep., 7, 40241, 10.1038/srep40241 Juanchich, 2013, Identification of differentially expressed miRNAs and their potential targets during fish ovarian development, Biol. Reprod., 88, 128, 10.1095/biolreprod.112.105361 Bannister, 2011, Manipulation of estrogen synthesis alters MIR202* expression in embryonic chicken gonads, Biol. Reprod., 85, 22, 10.1095/biolreprod.110.088476 Armisen, 2009, Abundant and dynamically expressed miRNAs, piRNAs, and other small RNAs in the vertebrate Xenopus tropicalis, Genome Res., 19, 1766, 10.1101/gr.093054.109 Zhao, 2010, A pilot study of circulating miRNAs as potential biomarkers of early stage breast cancer, PLoS One, 5, e13735, 10.1371/journal.pone.0013735 Lian, 2009, Altered microRNA expression in patients with non-obstructive azoospermia, Reprod. Biol. Endocrinol., 7, 13, 10.1186/1477-7827-7-13 Tang, 2018, Altered miRNA profile in testis of post-cryptorchidopexy patients with non-obstructive azoospermia, Reprod. Biol. Endocrinol., 16, 78, 10.1186/s12958-018-0393-3 Wang, 2011, Altered profile of seminal plasma MicroRNAs in the molecular diagnosis of male infertility, Clin. Chem., 57, 1722, 10.1373/clinchem.2011.169714 Abu-Halima, 2013, Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments, Fertil. Steril., 99, 1249, 10.1016/j.fertnstert.2012.11.054 Dabaja, 2015, Possible germ cell-Sertoli cell interactions are critical for establishing appropriate expression levels for the Sertoli cell-specific MicroRNA, miR-202-5p, in human testis, Basic Clin. Androl., 25, 2, 10.1186/s12610-015-0018-z Zhao, 2015, miR-424/322 is downregulated in the semen of patients with severe DNA damage and may regulate sperm DNA damage, Reprod. Fertil. Dev., 28, 1598, 10.1071/RD15052 Hanson, 2009, Identification of forensically relevant body fluids using a panel of differentially expressed microRNAs, Anal. Biochem., 387, 303, 10.1016/j.ab.2009.01.037 Li, 2004, RNA profiling of cell-free saliva using microarray technology, J. Dent. Res., 83, 199, 10.1177/154405910408300303 Sørensen, 2014, MicroRNAs related to polycystic ovary syndrome (PCOS), Genes, 5, 684, 10.3390/genes5030684 Zhang, 2016, [Seminal plasma miR-122-3p and miR-141-5p stability and its diagnosis value for idiopathic asthenospermia], Zhonghua Yi Xue Yi Chuan Xue Za Zhi, 33, 320 Abu-Halima, 2016, Altered micro-ribonucleic acid expression profiles of extracellular microvesicles in the seminal plasma of patients with oligoasthenozoospermia, Fertil. Steril., 106, 1061, 10.1016/j.fertnstert.2016.06.030 Wu, 2012, Seminal plasma microRNAs: potential biomarkers for spermatogenesis status, MHR Basic Sci. Reprod. Med., 18, 489, 10.1093/molehr/gas022 Chen, 2018, Expression profile of microRNAs in expressed prostatic secretion of healthy men and patients with IIIA chronic prostatitis/chronic pelvic pain syndrome, Oncotarget, 9, 12186, 10.18632/oncotarget.24069 Guo, 2018, Five microRNAs in serum as potential biomarkers for prostate cancer risk assessment and therapeutic intervention, Int. Urol. Nephrol., 10.1007/s11255-018-2009-4 Zhang, 2018, MicroRNA-141 inhibits the proliferation of penile cavernous smooth muscle cells associated with down-regulation of the rhoa/rho kinase signaling pathway, Cell. Physiol. Biochem., 48, 348, 10.1159/000491741 Hong, 2016, Systematic characterization of seminal plasma piRNAs as molecular biomarkers for male infertility, Sci. Rep., 6, 24229, 10.1038/srep24229 Zhang, 2015, Low long non-coding RNA HOTAIR expression is associated with down-regulation of Nrf2 in the spermatozoa of patients with asthenozoospermia or oligoasthenozoospermia, Int. J. Clin. Exp. Pathol., 8, 14198 Long, 2014, Characterization of serum microRNAs profile of PCOS and identification of novel non-invasive biomarkers, Cell. Physiol. Biochem., 33, 1304, 10.1159/000358698 Sahin, 2018, microRNA Let-7b: a Novel treatment for endometriosis, J. Cell Mol. Med., 10.1111/jcmm.13807 La Ferlita, 2018, Non-coding RNAs in endometrial physiopathology, Int. J. Mol. Sci., 19, 2120, 10.3390/ijms19072120 Panoutsopoulou, 2018, miRNA and long non-coding RNA: molecular function and clinical value in breast and ovarian cancers, Expert Rev. Mol. Diagn., 10.1080/14737159.2018.1538794 Diez-Fraile, 2014, Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization, Hum. Fertil., 17, 90, 10.3109/14647273.2014.897006 Yan, 2014, Potential roles of noncoding RNAs in environmental epigenetic transgenerational inheritance, Mol. Cell. Endocrinol., 398, 24, 10.1016/j.mce.2014.09.008 Fullston, 2013, Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content, FASEB J., 27, 4226, 10.1096/fj.12-224048 Gapp, 2014, Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice1, Nat. Neurosci., 17, 667, 10.1038/nn.3695 Rodgers, 2013, Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation, J. Neurosci., 33, 10.1523/JNEUROSCI.0914-13.2013 Short, 2016, Elevated paternal glucocorticoid exposure alters the small noncoding RNA profile in sperm and modifies anxiety and depressive phenotypes in the offspring, Transl. Psychiatry, 6, e837, 10.1038/tp.2016.109 Short, 2017, Exercise alters mouse sperm small noncoding RNAs and induces a transgenerational modification of male offspring conditioned fear and anxiety, Transl. Psychiatry, 7, e1114, 10.1038/tp.2017.82 Skinner, 2016, Epigenetic transgenerational inheritance, Nat. Rev. Endocrinol., 12, 68, 10.1038/nrendo.2015.206 Metzler-Guillemain, 2015, Sperm mRNAs and microRNAs as candidate markers for the impact of toxicants on human spermatogenesis: an application to tobacco smoking, Syst. Biol. Reprod. Med., 61, 139, 10.3109/19396368.2015.1022835