Skip to main content
SpringerLink
Log in

Essential functions of microRNAs in animal reproductive organs

  • Reviews
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

The development of the reproductive organs and the gametogenesis in animals are complex and multistage processes that require the precise and efficient regulation. In this review, we summarized the recent findings about the essential functions of microRNAs (miRNAs) in the regulation of gene expression during the differentiation of germ cells in spermatogenesis and oogenesis. Most likely, main and common functions of the conserved and highly expressed miRNAs in the male and female reproductive organs of mammals are the control of differentiation and proliferation of cells. Also we discussed a possible involvement of germline-expressed miRNAs in the formation of reproductive barriers and speciation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bartel D.P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116, 281–297.

    Article  CAS  PubMed  Google Scholar 

  2. Kim V.N. 2005. MicroRNA biogenesis: Coordinated cropping and dicing. Nature Rev. Mol. Cell Biol. 6, 376–385.

    Article  CAS  Google Scholar 

  3. Altuvia Y., Landgraf P., Lithwick G., Elefant N., Pfeffer S., Aravin A., Brownstein M.J., Tuschl T., Margalit H. 2005. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res. 33, 2697–2706.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Merchan F., Boualem A., Crespi M., Frugier F. 2009. Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol. 10, R136.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  5. Ryazansky S.S., Gvozdev V.A., Berezikov E. 2011. Evidence for post-transcriptional regulation of clustered microRNAs in Drosophila. BMC Genomics. 12, 371.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Okamura K. 2012. Diversity of animal small RNA pathways and their biological utility. Wiley Interdiscip. Rev. RNA. 3, 351–368.

    Article  CAS  PubMed  Google Scholar 

  7. Bartel D.P. 2009. MicroRNAs: Target recognition and regulatory functions. Cell. 136, 215–233.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Filipowicz W., Bhattacharyya S.N., Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nature Rev. Genet. 9, 102–114.

    Article  CAS  PubMed  Google Scholar 

  9. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 466, 835–840.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Hendrickson D.G., Hogan D.J., McCullough H.L., Myers J.W., Herschlag D., Ferrell J.E., Brown P.O. 2009. Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol. 7, e1000238.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  11. Zeng Y. 2006. Principles of micro-RNA production and maturation. Oncogene. 25, 6156–6162.

    Article  CAS  PubMed  Google Scholar 

  12. Lewis B.P., Shih I.H., Jones-Rhoades M.W., Bartel D.P., Burge C.B. 2003. Prediction of mammalian microRNA targets. Cell. 115, 787–798.

    Article  CAS  PubMed  Google Scholar 

  13. Friedman R.C., Farh K.K.-H., Burge C.B., Bartel D.P. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92–105.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Cheng L.-C., Pastrana E., Tavazoie M., Doetsch F. 2009. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nature Neurosci. 12, 399–408.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Esau C., Davis S., Murray S.F., Yu X.X., Pandey S.K., Pear M., Watts L., Booten S.L., Graham M., McKay R., Subramaniam A., Propp S., Lollo B.A., Freier S., Bennett C.F., Bhanot S., Monia B.P. 2006. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 3, 87–98.

    Article  CAS  PubMed  Google Scholar 

  16. Yekta S., Shih I.-H., Bartel D.P. 2004. MicroRNAdirected cleavage of HOXB8 mRNA. Science. 304, 594–596.

    Article  CAS  PubMed  Google Scholar 

  17. Ryazansky S.S., Gvozdev V.A. 2008. Small RNAs and cancerogenesis. Biochemistry (Moscow). 73, 514–527.

    Article  CAS  Google Scholar 

  18. Calin G.A., Croce C.M. 2006. MicroRNA signatures in human cancers. Nature Rev. Cancer. 6, 857–866.

    Article  CAS  Google Scholar 

  19. Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., Mills A.A., Elledge S.J., Anderson K.V., Hannon G.J. 2003. Dicer is essential for mouse development. Nature Genet. 35, 215–217.

    Article  CAS  PubMed  Google Scholar 

  20. Wienholds E., Koudijs M.J., van Eeden F.J., Cuppen E., Plasterk R.H. 2003. The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nature Genet. 35, 217–218.

    Article  CAS  PubMed  Google Scholar 

  21. Huang C.C., Yao H.H. 2010. Inactivation of Dicer1 in Steroidogenic factor 1-positive cells reveals tissue-specific requirement for Dicer1 in adrenal, testis, and ovary. BMC Dev. Biol. 10, 66.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  22. Lei L., Jin S., Gonzalez G., Behringer R.R., Woodruff T.K. 2010. The regulatory role of Dicer in folliculogenesis in mice. Mol. Cell Endocrinol. 315, 63–73.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Papaioannou M.D., Pitetti J.L., Ro S., Park C., Aubry F., Schaad O., Vejnar C.E., Kühne F., Descombes P., Zdobnov E.M., McManus M.T., Guillou F., Harfe B.D., Yan W., Jégou B., Nef S. 2009. Sertoli cell Dicer is essential for spermatogenesis in mice. Dev. Biol. 326, 250–259.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Papaioannou M.D., Lagarrigue M., Vejnar C.E., Rolland A.D., Kühne F., Aubry F., Schaad O., Fort A., Descombes P., Neerman-Arbez M., Guillou F., Zdobnov E.M., Pineau C., Nef S. 2011. Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice. Mol. Cell. Proteomics. 10, M900587MCP200.

    Article  PubMed  CAS  Google Scholar 

  25. Bannister S.C., Tizard M.L., Doran T.J., Sinclair A.H., Smith C.A. 2009. Sexually dimorphic microRNA expression during chicken embryonic gonadal development. Biol. Reprod. 81, 165–176.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Cutting A.D., Bannister S.C., Doran T.J., Sinclair A.H., Tizard M.V, Smith C.A. 2012. The potential role of microRNAs in regulating gonadal sex differentiation in the chicken embryo. Chromosome Res. 20, 201–213.

    Article  CAS  PubMed  Google Scholar 

  27. Huang P., Gong Y., Peng X., Li S., Yang Y., Feng Y. 2010. Cloning, identification, and expression analysis at the stage of gonadal sex differentiation of chicken miR-363 and 363*. Acta Biochim. 42, 522–529.

    CAS  Google Scholar 

  28. Torley K.J., da Silveira J.C., Smith P., Anthony R.V., Veeramachaneni D.N., Winger Q.A., Bouma G.J. 2011. Expression of miRNAs in ovine fetal gonads: Potential role in gonadal differentiation. Reprod. Biol. Endocrinol. 9, 2.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Tripurani S.K., Xiao C., Salem M., Yao J. 2010. Cloning and analysis of fetal ovary microRNAs in cattle. Anim. Reprod. Sci. 120, 16–22.

    Article  CAS  PubMed  Google Scholar 

  30. Ro S., Park C., Young D., Sanders K.M., Yan W. 2007. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res. 35, 5944–5953.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Wainwright E.N., Jorgensen J.S., Kim Y., Truong V., Bagheri-Fam S., Davidson T., Svingen T., Fernandez-Valverde S.L., McClelland K.S., Taft R.J., Harley V.R., Koopman P., Wilhelm D. 2013. SOX9 regulates microRNA miR-202-5p/3p expression during mouse testis differentiation. Biol. Reprod. 89, 34.

    Article  PubMed  CAS  Google Scholar 

  32. Bizuayehu T.T., Babiak J., Norberg B., Fernandes J.M., Johansen S.D., Babiak I. 2012. Sex-biased miRNA expression in Atlantic halibut (Hippoglossus hippoglossus) brain and gonads. Sex Dev. 6, 257–266.

    Article  CAS  PubMed  Google Scholar 

  33. Li M., Liu Y., Wang T., Guan J., Luo Z., Chen H., Wang X., Chen L., Ma J., Mu Z., Jiang A.A., Zhu L., Lang Q., Zhou X., Wang J., Zeng W., Li N., Li K., Gao X., Li X. 2011. Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing. Int. J. Biol. Sci. 7, 1045–1055.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Luo L., Ye L., Liu G., Shao G., Zheng R., Ren Z., Zuo B., Xu D., Lei M., Jiang S., Deng C., Xiong Y., Li F. 2010. Microarray-based approach identifies differentially expressed microRNAs in porcine sexually immature and mature testes. PLoS ONE. 5, e11744.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  35. Michalak P., Malone J.H. 2008. Testis-derived microRNA profiles of African clawed frogs (Xenopus) and their sterile hybrids. Genomics. 91, 158–164.

    Article  CAS  PubMed  Google Scholar 

  36. Mishima T., Takizawa T., Luo S.S., Ishibashi O., Kawahigashi Y., Mizuguchi Y., Ishikawa T., Mori M., Kanda T., Goto T., Takizawa T. 2008. MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction. 136, 811–822.

    Article  CAS  PubMed  Google Scholar 

  37. Ro S., Park C., Sanders K.M., McCarrey J.R., Yan W. 2007. Cloning and expression profiling of testis-expressed microRNAs. Dev. Biol. 311, 592–602.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Bannister S.C., Smith C.A., Roeszler K.N., Doran T.J., Sinclair A.H., Tizard M.L. 2011. Manipulation of estrogen synthesis alters MIR202* expression in embryonic chicken gonads. Biol. Reprod. 85, 22–30.

    Article  CAS  PubMed  Google Scholar 

  39. Rakoczy J., Fernandez-Valverde S.L., Glazov E.A., Wainwright E.N., Sato T., Takada S., Combes A.N., Korbie D.J., Miller D., Grimmond S.M., Little M.H., Asahara H., Mattick J.S., Taft R.J., Wilhelm D. 2013. MicroRNAs-140-5p/140-3p modulate Leydig cell numbers in the developing mouse testis. Biol. Reprod. 88, 143.

    Article  PubMed  Google Scholar 

  40. Tripurani S.K., Wee G., Lee K.-B., Smith G.W., Wang L., Jianboyao 2013. MicroRNA-212 Post-transcriptionally regulates oocyte-specific basic-helix-loop-helix transcription factor, Factor In the Germline Alpha (FIGLA), during bovine early embryogenesis. PLoS ONE. 8, e76114.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Kotaja N., Sassone-Corsi P. 2007. The chromatoid body: a germ-cell-specific RNA-processing centre. Nature Rev. Mol. Cell Biol. 8, 85–90.

    Article  CAS  Google Scholar 

  42. Kotaja N., Bhattacharyya S.N., Jaskiewicz L., Kimmins S., Parvinen M., Filipowicz W., Sassone-Corsi P. 2006. The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc. Natl. Acad. Sci. U. S. A. 103, 2647–2652.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Krawetz S.A., Kruger A., Lalancette C., Tagett R., Anton E., Draghici S., Diamond M.P. 2011. A survey of small RNAs in human sperm. Hum. Reprod. 26, 3401–3412.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Linsen S.E., de W.E., de B.E., Cuppen E. 2010. Small RNA expression and strain specificity in the rat. BMC Genomics. 11, 249.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  45. Marcon E., Babak T., Chua G., Hughes T., Moens P.B. 2008. miRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Res. 16, 243–260.

    Article  CAS  PubMed  Google Scholar 

  46. McIver S.C., Stanger S.J., Santarelli D.M., Roman S.D., Nixon B., McLaughlin E.A. 2012. A unique combination of male germ cell miRNAs coordinates gonocyte differentiation. PLoS One. 7, e35553.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Niu Z., Goodyear S.M., Rao S., Wu X., Tobias J.W., Avarbock M.R., Brinster R.L. 2011. MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc. Natl. Acad. Sci. U. S. A. 108, 12740–12745.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Yan N., Lu Y., Sun H., Tao D., Zhang S., Liu W., Ma Y. 2007. A microarray for microRNA profiling in mouse testis tissues. Reproduction. 134, 73–79.

    Article  CAS  PubMed  Google Scholar 

  49. Yu Z., Raabe T., Hecht N.B. 2005. MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol. Reprod. 73, 427–433.

    Article  CAS  PubMed  Google Scholar 

  50. Hayashi K., Chuva de Sousa Lopes S.M., Kaneda M., Tang F., Hajkova P., Lao K., O’Carroll D., Das P.P., Tarakhovsky A., Miska E.A., Surani M.A. 2008. MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS ONE. 3, e1738.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  51. Korhonen H.M., Meikar O., Yadav R.P., Papaioannou M.D., Romero Y., Da Ros M., Herrera P.L., Toppari J., Nef S., Kotaja N. 2011. Dicer is required for haploid male germ cell differentiation in mice. PLoS ONE. 6, e24821.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Maatouk D.M., Loveland K.L., McManus M.T., Moore K., Harfe B.D. 2008. Dicer1 is required for differentiation of the mouse male germline. Biol. Reprod. 79, 696–703.

    Article  CAS  PubMed  Google Scholar 

  53. Romero Y., Meikar O., Papaioannou M.D., Conne B., Grey C., Weier M., Pralong F., De Massy B., Kaessmann H., Vassalli J.D., Kotaja N., Nef S. 2011. Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS ONE. 6, e25241.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Wu Q., Song R., Ortogero N., Zheng H., Evanoff R., Small C.L., Griswold M.D., Namekawa S.H., Royo H., Turner J.M., Yan W. 2012. The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J. Biol. Chem. 287, 25173–25190.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Song R., Ro S., Michaels J.D., Park C., McCarrey J.R., Yan W. 2009. Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nature Genet. 41, 488–493.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Vibranovski M.D., Zhang Y.E., Kemkemer C., Lopes H.F., Karr T.L., Long M. 2012. Re-analysis of the larval testis data on meiotic sex chromosome inactivation revealed evidence for tissue-specific gene expression related to the Drosophila X chromosome. BMC Biol. 10, 49.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Toledano H., D’Alterio C., Czech B., Levine E., Jones D.L. 2012. The let-7-Imp axis regulates ageing of the Drosophila testis stem-cell niche. Nature. 485, 605–610.

    Article  CAS  PubMed  Google Scholar 

  58. Pek J.W., Lim A.K., Kai T. 2009. Drosophila Maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev. Cell. 17, 417–424.

    Article  CAS  PubMed  Google Scholar 

  59. Sienski G., Dönertas D., Brennecke J. 2012. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 151, 964–980.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Eun S.H., Stoiber P.M., Wright H.J., McMurdie K.E., Choi C.H., Gan Q., Lim C., Chen X. 2013. MicroRNAs downregulate Bag of marbles to ensure proper terminal differentiation in the Drosophila male germline. Development. 140, 23–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Tong M.H., Mitchell D.A., McGowan S.D., Evanoff R., Griswold M.D. 2012. Two miRNA clusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of spermatogonial differentiation in mice. Biol. Reprod. 86, 72.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  62. Viswanathan S.R., Daley G.Q., Gregory R.I. 2008. Selective blockade of microRNA processing by Lin28. Science. 320, 97–100.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Dews M., Fox J.L., Hultine S., Sundaram P., Wang W., Liu Y.Y., Furth E., Enders G.H., El-Deiry W., Schelter J.M., Cleary M.A., Thomas-Tikhonenko A. 2010. The myc-miR-17∼92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors. Cancer Res. 70, 8233–8246.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Petrocca F., Vecchione A., Croce C.M. 2008. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res. 68, 8191–8194.

    Article  CAS  PubMed  Google Scholar 

  65. Tong M.H., Mitchell D., Evanoff R., Griswold M.D. 2011. Expression of Mirlet7 family microRNAs in response to retinoic acid-induced spermatogonial differentiation in mice. Biol. Reprod. 85, 189–197.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Melton C., Blelloch R. 2010. MicroRNA regulation of embryonic stem cell self-renewal and differentiation. Adv. Exp. Med. Biol. 695, 105–117.

    Article  CAS  PubMed  Google Scholar 

  67. Concepcion C.P., Bonetti C., Ventura A. 2012. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J. 18, 262–267.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Huszar J.M., Payne C.J. 2013. MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice. Biol. Reprod. 88, 15.

    Article  PubMed  CAS  Google Scholar 

  69. Liu D., Li L., Fu H., Li S., Li J. 2012. Inactivation of Dicer1 has a severe cumulative impact on the formation of mature germ cells in mouse testes. Biochem. Biophys. Res. Commun. 422, 114–120.

    Article  CAS  PubMed  Google Scholar 

  70. Bao J., Li D., Wang L., Wu J., Hu Y., Wang Z., Chen Y., Cao X., Jiang C., Yan W., Xu C. 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, 21686–21698.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Novotny G.W., Sonne S.B., Nielsen J.E., Jonstrup S.P., Hansen M.A., Skakkebaek N.E., Rajpert-De Meyts E., Kjems J., Leffers H. 2007. Translational repression of E2F1 mRNA in carcinoma in situ and normal testis correlates with expression of the miR-17-92 cluster. Cell Death Differ. 14, 879–882.

    Article  CAS  PubMed  Google Scholar 

  72. O’Donnell K.A., Wentzel E.A., Zeller K.I., Dang C. V, Mendell J.T. 2005. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 435, 839–843.

    Article  PubMed  CAS  Google Scholar 

  73. Liang X., Zhou D., Wei C., Luo H., Liu J., Fu R., Cui S. 2012. MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1. PLoS ONE. 7, e33861.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Bouhallier F., Allioli N., Lavial F., Chalmel F., Perrard M.H., Durand P., Samarut J., Pain B., Rouault J.P. 2010. Role of miR-34c microRNA in the late steps of spermatogenesis. RNA. 16, 720–731.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Idler R.K., Yan W. 2012. Control of messenger RNA fate by RNA-binding proteins: An emphasis on mammalian spermatogenesis. J. Androl. 33, 309–337.

    Article  CAS  PubMed  Google Scholar 

  76. Kleene K.C. 2003. Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenet. Res. 103, 217–224.

    Article  CAS  Google Scholar 

  77. Vibranovski M.D., Chalopin D.S., Lopes H.F., Long M., Karr T.L. 2010. Direct evidence for postmeiotic transcription during Drosophila melanogaster spermatogenesis. Genetics. 186, 431–433.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Vibranovski M.D., Lopes H.F., Karr T.L., Long M. 2009. Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet. 5, e1000731.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  79. Joti P., Ghosh-Roy A., Ray K. 2011. Dynein light chain 1 functions in somatic cyst cells regulate spermatogonial divisions in Drosophila. Sci. Rep. 1, 173.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  80. Mermall V., Bonafe N., Jones L., Sellers J.R., Cooley L., Mooseker M.S. 2005. Drosophila myosin V is required for larval development and spermatid individualization. Dev. Biol. 286, 238–255.

    Article  CAS  PubMed  Google Scholar 

  81. Nicholls P.K., Harrison C.A., Walton K.L., McLachlan R.I., O’Donnell L., Stanton P.G. 2011. Hormonal regulation of sertoli cell micro-RNAs at spermiation. Endocrinology. 152, 1670–1683.

    Article  CAS  PubMed  Google Scholar 

  82. Ahn H.W., Morin R.D., Zhao H., Harris R.A., Coarfa C., Chen Z.J., Milosavljevic A., Marra M.A., Rajkovic A. 2010. MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing. Mol. Hum. Reprod. 16, 463–471.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Huang J., Ju Z., Li Q., Hou Q., Wang C., Li J., Li R., Wang L., Sun T., Hang S., Gao Y., Hou M., Zhong J. 2011. Solexa sequencing of novel and differentially expressed microRNAs in testicular and ovarian tissues in Holstein cattle. Int. J. Biol. Sci. 7, 1016–1026.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. Zhang Q., Sun H., Jiang Y., Ding L., Wu S., Fang T., Yan G., Hu Y. 2013. MicroRNA-181a suppresses mouse granulosa cell proliferation by targeting activin receptor IIA. PLoS ONE. 8, e59667.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Lin F., Li R., Pan Z.X., Zhou B., Yu de B., Wang X.G., Ma X.S., Han J., Shen M., Liu H.L. 2012. miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary. PLoS ONE. 7, e38640.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  86. Carletti M.Z., Fiedler S.D., Christenson L.K. 2010. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol. Reprod. 83, 286–295.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  87. Otsuka M., Zheng M., Hayashi M., Lee J.-D., Yoshino O., Lin S., Han J. 2008. Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. J. Clin. Invest. 118, 1944–1954.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  88. Dai A., Sun H., Fang T., Zhang Q., Wu S., Jiang Y., Ding L., Yan G., Hu Y. 2013. MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2. FEBS Lett. 587, 2474–2482.

    Article  CAS  PubMed  Google Scholar 

  89. Yao G., Yin M., Lian J., Tian H., Liu L., Li X., Sun F. 2010. MicroRNA-224 is involved in transforming growth factor-beta-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Mol. Endocrinol. 24, 540–551.

    Article  CAS  PubMed  Google Scholar 

  90. Xu S., Linher-Melville K., Yang B.B., Wu D., Li J. 2011. Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology. 152, 3941–3951.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  91. Yin M., Lü M., Yao G., Tian H., Lian J., Liu L., Liang M., Wang Y., Sun F. 2012. Transactivation of microRNA-383 by steroidogenic factor-1 promotes estradiol release from mouse ovarian granulosa cells by targeting RBMS1. Mol. Endocrinol. 26, 1129–1143.

    Article  CAS  PubMed  Google Scholar 

  92. Ma J., Flemr M., Stein P., Berninger P., Malik R., Zavolan M., Svoboda P., Schultz R.M. 2010. MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 20, 265–270.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  93. Suh N., Baehner L., Moltzahn F., Melton C., Shenoy A., Chen J., Blelloch R. 2010. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 20, 271–277.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. Chen L., Hu X., Dai Y., Li Q., Wang X., Li Q., Xue K., Li Y., Liang J., Wang Y., Liu X., Li N. 2012. MicroRNA-27a activity is not suppressed in porcine oocytes. Front. Biosci. (Elite Ed.). 4, 2679–2685.

    Article  Google Scholar 

  95. Cui X.S., Sun S.C., Kang Y.K., Kim N.H. 2013. Involvement of microRNA-335-5p in cytoskeleton dynamics in mouse oocytes. Reprod. Fertil. Dev. 25, 691–699.

    Article  CAS  PubMed  Google Scholar 

  96. Suh N., Blelloch R. 2011. Small RNAs in early mammalian development: From gametes to gastrulation. Development. 138, 1653–1661.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  97. Murchison E.P., Stein P., Xuan Z., Pan H., Zhang M.Q., Schultz R.M., Hannon G.J. 2007. Critical roles for Dicer in the female germline. Genes Dev. 21, 682–693.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  98. Flemr M., Malik R., Franke V., Nejepinska J., Sedlacek R., Vlahovicek K., Svoboda P. 2013. A retrotransposon-driven Dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell. 155, 807–816.

    Article  CAS  PubMed  Google Scholar 

  99. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., Hodges E., Anger M., Sachidanandam R., Schultz R.M., Hannon G.J. 2008. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature. 453, 534–538.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  100. Fiedler S.D., Carletti M.Z., Hong X., Christenson L.K. 2008. Hormonal regulation of microRNA expression in periovulatory mouse mural granulosa cells. Biol. Reprod. 79, 1030–1037.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  101. Sirotkin A. V, Ovcharenko D., Grossmann R., Lauková M., Mlyncek M. 2009. Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. J. Cell. Physiol. 219, 415–420.

    Article  CAS  PubMed  Google Scholar 

  102. Sirotkin A. V, Lauková M., Ovcharenko D., Brenaut P., Mlyncek M. 2010. Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. J. Cell. Physiol. 223, 49–56.

    CAS  PubMed  Google Scholar 

  103. Yao N., Lu C.L., Zhao J.J., Xia H.F., Sun D.G., Shi X.Q., Wang C., Li D., Cui Y., Ma X. 2009. A network of miRNAs expressed in the ovary are regulated by FSH. Front. Biosci. (Landmark Ed.). 14, 3239–3245.

    Article  CAS  Google Scholar 

  104. Velthut-Meikas A., Simm J., Tuuri T., Tapanainen J.S., Metsis M., Salumets A. 2013. Research resource: small RNA-seq of human granulosa cells reveals miR-NAs in FSHR and aromatase genes. Mol. Endocrinol. 27, 1128–1141.

    Article  CAS  PubMed  Google Scholar 

  105. Schauer S.N., Sontakke S.D., Watson E.D., Esteves C.L., Donadeu F.X. 2013. Involvement of miRNAs in equine follicle development. Reproduction. 146, 273–282.

    Article  CAS  PubMed  Google Scholar 

  106. Ma T., Jiang H., Gao Y., Zhao Y., Dai L., Xiong Q., Xu Y., Zhao Z., Zhang J. 2011. Microarray analysis of differentially expressed microRNAs in non-regressed and regressed bovine corpus luteum tissue; microRNA-378 may suppress luteal cell apoptosis by targeting the interferon gamma receptor 1 gene. J. Appl. Genet. 52, 481–486.

    Article  CAS  PubMed  Google Scholar 

  107. McBride D., Hogg C.O., Donadeu F.X., Sontakke S.D., Clinton M., Carre W., Law A. 2012. Identification of miRNAs associated with the follicular-luteal transition in the ruminant ovary. Reproduction. 144, 221–233.

    Article  CAS  PubMed  Google Scholar 

  108. Juanchich A., Le Cam A., Montfort J., Guiguen Y., Bobe J. 2013. Identification of differentially expressed miRNAs and their potential targets during fish ovarian development. Biol. Reprod. 88, 128.

    Article  PubMed  CAS  Google Scholar 

  109. Kang L., Cui X., Zhang Y., Yang C., Jiang Y. 2013. Identification of miRNAs associated with sexual maturity in chicken ovary by Illumina small RNA deep sequencing. BMC Genomics. 14, 352.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  110. Zhang X.-D., Zhang Y.-H., Ling Y.-H., Liu Y., Cao H.-G., Yin Z.-J., Ding J.-P., Zhang X.-R. 2013. Characterization and differential expression of microRNAs in the ovaries of pregnant and non-pregnant goats (Capra hircus). BMC Genomics. 14, 157.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  111. Donadeu F.X., Schauer S., Sontakke S. 2012. Involvement of miRNAs in ovarian follicular and luteal development. J. Endocrinol. 215, 323–334

    Article  CAS  PubMed  Google Scholar 

  112. Nakahara K., Kim K., Sciulli C., Dowd S.R., Minden J.S., Carthew R.W. 2005. Targets of microRNA regulation in the Drosophila oocyte proteome. Proc. Natl. Acad. Sci. U. S. A. 102, 12023–12028.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  113. Azzam G., Smibert P., Lai E.C., Liu J.L. 2012. Drosophila Argonaute 1 and its miRNA biogenesis partners are required for oocyte formation and germline cell division. Dev. Biol. 365, 384–394.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  114. Yang L., Chen D., Duan R., Xia L., Wang J., Qurashi A., Jin P. 2007. Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development. 134, 4265–4272.

    Article  CAS  PubMed  Google Scholar 

  115. Yu J.Y., Reynolds S.H., Hatfield S.D., Shcherbata H.R., Fischer K.A., Ward E.J., Long D., Ding Y., Ruohola-Baker H. 2009. Dicer-1-dependent Dacapo suppression acts downstream of Insulin receptor in regulating cell division of Drosophila germline stem cells. Development. 136, 1497–1507.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  116. Iovino N., Pane A., Gaul U. 2009. miR-184 has multiple roles in Drosophila female germline development. Dev. Cell. 17, 123–133.

    Article  CAS  PubMed  Google Scholar 

  117. Landgraf P., Rusu M., Sheridan R., Sewer A., Iovino N., Aravin A., Pfeffer S., Rice A., Kamphorst A.O., Landthaler M., Lin C., Socci N.D., Hermida L., Fulci V., Chiaretti S., Foá R., Schliwka J., Fuchs U., Novosel A., Müller R.U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., Trompeter H.I., Hornung V., Teng G., Hartmann G., Palkovits M., Di Lauro R., Wernet P., Macino G., Rogler C.E., Nagle J.W., Ju J., Papavasiliou F.N., Benzing T., Lichter P., Tam W., Brownstein M.J., Bosio A., Borkhardt A., Russo J.J., Sander C., Zavolan M., Tuschl T. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 129, 1401–1414.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  118. Hossain M.M., Ghanem N., Hoelker F., Phatsara C., Tholen E., Schellander K., Tesfaye D. 2009. Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genomics. 10, 443.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  119. Mondol V., Pasquinelli A.E. 2012. Let’s make it happen: The role of let-t microRNA in development. In: Current Topics in Developmental Biology, vol. 99, pp. 1–30.

    Article  CAS  PubMed  Google Scholar 

  120. Thornton J.E., Gregory R.I. 2012. How does Lin28 let-7 control development and disease? Trends Cell Biol. 22, 474–482.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  121. Barckmann B., Simonelig M. 2013. Control of maternal mRNA stability in germ cells and early embryos. Biochim. Biophys. Acta. 1829, 714–724.

    Article  CAS  PubMed  Google Scholar 

  122. Tripurani S.K., Lee K.-B., Wee G., Smith G.W., Yao J. 2011. MicroRNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis. BMC Dev. Biol. 11, 25.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  123. Lingenfelter B.M., Tripurani S.K., Tejomurtula J., Smith G.W., Yao J. 2011. Molecular cloning and expression of bovine nucleoplasmin 2 (NPM2): A maternal effect gene regulated by miR-181a. Reprod. Biol. Endocrinol. 9, 40.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  124. Giraldez A.J., Mishima Y., Rihel J., Grocock R.J., Van D.S., Inoue K., Enright A.J., Schier A.F. 2006. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science. 312, 75–79.

    Article  CAS  PubMed  Google Scholar 

  125. Bazzini A.A., Lee M.T., Giraldez A.J. 2012. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science. 336, 233–237.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  126. Lund E., Liu M., Hartley R.S., Sheets M.D., Dahlberg J.E. 2009. Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos. RNA. 15, 2351–2363.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  127. Bushati N., Stark A., Brennecke J., Cohen S.M. 2008. Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr. Biol. 18, 501–506.

    Article  CAS  PubMed  Google Scholar 

  128. Rouget C., Papin C., Boureux A., Meunier A.-C., Franco B., Robine N., Lai E.C., Pelisson A., Simonelig M. 2010. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature. 467, 1128–1132.

    Article  CAS  PubMed  Google Scholar 

  129. Ostermeier G.C., Miller D., Huntriss J.D., Diamond M.P., Krawetz S.A. 2004. Reproductive biology: Delivering spermatozoan RNA to the oocyte. Nature. 429, 154.

    Article  CAS  PubMed  Google Scholar 

  130. Rassoulzadegan M., Grandjean V., Gounon P., Vincent S., Gillot I., Cuzin F. 2006. RNA-mediated nonmendelian inheritance of an epigenetic change in the mouse. Nature. 441, 469–474.

    Article  CAS  PubMed  Google Scholar 

  131. Sendler E., Johnson G.D., Mao S., Goodrich R.J., Diamond M.P., Hauser R., Krawetz S.A. 2013. Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res. 41, 4104–4117.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  132. Clark N.L., Aagaard J.E., Swanson W.J. 2006. Evolution of reproductive proteins from animals and plants. Reproduction. 131, 11–22.

    Article  CAS  PubMed  Google Scholar 

  133. Dorus S., Busby S.A., Gerike U., Shabanowitz J., Hunt D.F., Karr T.L. 2006. Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nature Genet. 38, 1440–1445.

    Article  CAS  PubMed  Google Scholar 

  134. Guo X., Su B., Zhou Z., Sha J. 2009. Rapid evolution of mammalian X-linked testis microRNAs. BMC Genomics. 10, 97.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  135. Zhang R., Peng Y., Wang W., Su B. 2007. Rapid evolution of an X-linked microRNA cluster in primates. Genome Res. 17, 612–617.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  136. Intra J., Cenni F., Pavesi G., Pasini M., Perotti M.E. 2009. Interspecific analysis of the glycosidases of the sperm plasma membrane in Drosophila. Mol. Reprod. Dev. 76, 85–100.

    Article  CAS  PubMed  Google Scholar 

  137. Cattaneo F., Ogiso M., Hoshi M., Perotti M.E., Pasini M.E. 2002. Purification and characterization of the plasma membrane glycosidases of Drosophila melanogaster spermatozoa. Insect Biochem. 32, 929–941.

    Article  CAS  Google Scholar 

  138. Panhuis T.M., Clark N.L., Swanson W.J. 2006. Rapid evolution of reproductive proteins in abalone and Drosophila. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 361, 261–268.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, 123182, Russia

    S. S. Ryazansky, E. A. Mikhaleva & O. V. Olenkina

Authors
  1. S. S. Ryazansky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. A. Mikhaleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. V. Olenkina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. S. Ryazansky.

Additional information

Original Russian Text © S.S. Ryazansky, E.A. Mikhaleva, O.V. Olenkina, 2014, published in Molekulyarnaya Biologiya, 2014, Vol. 48, No. 3, pp. 371–385.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ryazansky, S.S., Mikhaleva, E.A. & Olenkina, O.V. Essential functions of microRNAs in animal reproductive organs. Mol Biol 48, 319–331 (2014). https://doi.org/10.1134/S0026893314030182

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893314030182

Keywords

Search

Navigation