Altered microRNAs expression levels of sperm and seminal plasma in patients with infertile ejaculates compared with normozoospermic males

References

• Abu-Halima, M., Hammadeh, M., Schmitt, J., Leidinger, P., Keller, A., Meese, E., & Backes, C. (2013). Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertility and Sterility, 99, 1249–1255. doi: 10.1016/j.fertnstert.2012.11.054.
   PubMed Web of Science ®Google Scholar
• Abu-Halima, M., Hammadeh, M., Backes, C., Fischer, U., Leidinger, P., Lubbad, A.M., … Meese, E. (2014). Panel of five microRNAs as potential biomarkers for the diagnosis and assessment of male infertility. Fertility and Sterility, 102, 989–997. doi: 10.1016/j.fertnstert.2014.07.001.
   PubMed Web of Science ®Google Scholar
• Agarwal, A., & Allamaneni, S.S. (2005). Sperm DNA damage assessment: A test whose time has come. Fertility and Sterility, 84, 850–853. doi: 10.1016/j.fertnstert.2005.03.080.
   PubMed Web of Science ®Google Scholar
• Ambros, V. (2004). The functions of animal microRNAs. Nature, 431, 350–355. doi: 10.1038/nature02871.
   PubMed Web of Science ®Google Scholar
• Aqeilan, R.I., Calin, G.A., & Croce, C.M. (2010). miR-15a and miR-16-1 in cancer: Discovery, function and future perspectives. Cell Death and Differentiation, 17, 215–220. doi: 10.1038/cdd.2009.69.
   PubMed Web of Science ®Google Scholar
• Bao, J., Li, D., Wang, L., Wu, J., Hu, Y., Wang, Z., … Xu, C. (2012). MicroRNA-449 and microRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. Journal of Biological Chemistry, 287, 21686–21698. doi: 10.1074/jbc.M111.328054.
   PubMed Web of Science ®Google Scholar
• Barad, O., Meiri, E., Avniel, A., Aharonov, R., Barzilai, A., Bentwich, I., … Einat, P. (2004). MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Research, 14, 2486–2494. doi: 10.1101/gr.2845604.
   PubMed Web of Science ®Google Scholar
• Barceló, M., Mata, A., Bassas, L., & Larriba, S. (2018). Exosomal microRNAs in seminal plasma are markers of the origin of azoospermia and can predict the presence of sperm in testicular tissue. Human Reproduction, 33, 1087–1098. doi: 10.1093/humrep/dey072.
   PubMed Web of Science ®Google Scholar
• Bartel, D.P. (2009). MicroRNAs: Target recognition and regulatory functions. Cell, 136, 215–233. doi: 10.1016/j.cell.2009.01.002.
   PubMed Web of Science ®Google Scholar
• Bouhallier, F., Allioli, N., Lavial, F., Chalmel, F., Perrard, M.-H., Durand, P., … Rouault, J.-P. (2010). Role of miR-34c microRNA in the late steps of spermatogenesis. RNA, 16, 720–731. doi: 10.1261/rna.1963810.
   PubMed Web of Science ®Google Scholar
• Calin, G.A., Dumitru, C.D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., … Croce, C.M. (2002). Frequent deletions and downregulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proceedings of the National Academy of Sciences USA, 99, 15524–15529. doi: 10.1073/pnas.242606799.
   PubMed Web of Science ®Google Scholar
• Carleton, M., Cleary, M.A., & Linsley, P.S. (2007). MicroRNAs and cell cycle regulation. Cell Cycle, 6, 2127–2132. doi: 10.4161/cc.6.17.4641.
   PubMed Web of Science ®Google Scholar
• Castellano, L., & Stebbing, J. (2013). Deep sequencing of small RNAs identifies canonical and non-canonical miRNA and endogenous siRNAs in mammalian somatic tissues. Nucleic Acids Research, 41, 3339–3351. doi: 10.1093/nar/gks1474.
   PubMed Web of Science ®Google Scholar
• Chen, C.Z., Li, L., Lodish, H.F., & Bartel, D.P. (2004). MicroRNAs modulate hematopoietic lineage differentiation. Science, 303, 83–86. doi: 10.1126/science.1091903.
   PubMed Web of Science ®Google Scholar
• Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., … Guegler, K.J. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research, 33, e179. doi: 10.1093/nar/gni178.
   PubMed Web of Science ®Google Scholar
• Cimmino, A., Calin, G.A., Fabbri, M., Iorio, M.V., Ferracin, M., Shimizu, M., … Croce, C.M. (2005). miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences USA, 102, 13944–13949. doi: 10.1073/pnas.0506654102.
   PubMed Web of Science ®Google Scholar
• Corney, D.C., Flesken-Nikitin, A., Godwin, A.K., Wang, W., & Nikitin, A.Y. (2007). MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Research, 67, 8433–8438. doi: 10.1158/0008-5472.CAN-07-1585.
   PubMed Web of Science ®Google Scholar
• Curry, E., Safranski, T.J., & Pratt, S.L. (2011). Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology, 76, 1532–1539. doi: 10.1016/j.theriogenology.2011.06.025.
   PubMed Web of Science ®Google Scholar
• Czimmerer, Z., Hulvely, J., Simandi, Z., Varallyay, E., Havelda, Z., Szabo, E., … Balint, B.L. (2013). A versatile method to design stem-loop primer-based quantitative PCR assays for detecting small regulatory RNA molecules. PLoS One, 8, e55168. doi: 10.1371/journal.pone.0055168.
   PubMed Web of Science ®Google Scholar
• Goodrich, R., Johnson, G., & Krawetz, S.A. (2007). The preparation of human spermatozoal RNA for clinical analysis. Archives of Andrology, 53, 161–167. doi: 10.1080/01485010701216526.
   PubMed Web of Science ®Google Scholar
• Hanlon, K., Rudin, C.E., & Harries, L.W. (2009). Investigating the targets of MIR-15a and MIR-16-1 in patients with chronic lymphocytic leukemia (CLL). PLoS One, 4, e7169. doi: 10.1371/journal.pone.0007169.
   PubMed Web of Science ®Google Scholar
• Hayashi, T., Kageyama, Y., Ishizaka, K., Xia, G., Kihara, K., & Oshima, H. (2001). Requirement of Notch 1 and its ligand jagged 2 expressions for spermatogenesis in rat and human testes. Journal of Andrology, 22, 999–1011. doi: 10.1002/j.1939-4640.2001.tb03441.x.
   PubMedGoogle Scholar
• Hayashi, K., Chuva de Sousa Lopes, S.M., Kaneda, M., Tang, F., Hajkova, P., Lao, K., … Surani, M.A. (2008). MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One, 3, e1738. doi: 10.1371/journal.pone.0001738.
   PubMed Web of Science ®Google Scholar
• He, X., He, L., & Hannon, G.J. (2007). The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Research, 67, 11099–110101. doi: 10.1158/0008-5472.CAN-07-2672.
   PubMed Web of Science ®Google Scholar
• Ji, Z., Lu, R., Mou, L., Duan, Y.-G., Zhang, Q., Wang, Y., … Cai, Z. (2014). Expressions of miR-15a and its target gene HSPA1B in the spermatozoa of patients with varicocele. Reproduction, 147, 693–701. doi: 10.1530/REP-13-0656.
   PubMed Web of Science ®Google Scholar
• Jungwirth, A., Giwercman, A., Tournaye, H., Diemer, T., Kopa, Z., Dohle, G., & Krausz, C. European Association of Urology Working Group on Male Infertility. (2012). European association of urology guidelines on male infertility: the 2012 update. European Urology, 62, 324–332. doi: 10.1016/j.eururo.2012.04.048.
   PubMed Web of Science ®Google Scholar
• Kasimanickam, V.R., Kasimanickam, R.K., & Dernell, W.S. (2014). Dysregulated microRNA clusters in response to retinoic acid and CYP26B1 inhibitor induced testicular function in dogs. PLoS One, 9, e99433. doi: 10.1371/journal.pone.0099433.
   PubMed Web of Science ®Google Scholar
• Klingmuller, D., & Haidl, G. (1997). Inhibin B in men with normal and disturbed spermatogenesis. Human Reproduction, 12, 2376–2378. doi: 10.1093/humrep/12.11.2376.
   PubMed Web of Science ®Google Scholar
• Konrad, L., Keilani, M.M., Laible, L., Nottelmann, U., & Hofmann, R. (2006). Effects of TGF-betas and a specific antagonist on apoptosis of immature rat male germ cells in vitro. Apoptosis, 11, 739–748. doi: 10.1007/s10495-006-5542-z.
   PubMed Web of Science ®Google Scholar
• Krausz, C. (2011). Male infertility: pathogenesis and clinical diagnosis. Best Practice and Research: Clinical Endocrinology and Metabolism, 25, 271–285. doi: 10.1016/j.beem.2010.08.006.
   PubMed Web of Science ®Google Scholar
• 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. Human Reproduction, 26, 3401–3412. doi: 10.1093/humrep/der329.
   PubMed Web of Science ®Google Scholar
• Lakshmipathy, U., Love, B., Goff, L.A., Jörnsten, R., Graichen, R., Hart, R.P., & Chesnut, J.D. (2007). MicroRNA expression pattern of undifferentiated and differentiated human embryonic stem cells. Stem Cells and Development, 16, 1003–1016. doi: 10.1089/scd.2007.0026.
   PubMed Web of Science ®Google Scholar
• Li, Q.J., Chau, J., Ebert, P.J., Sylvester, G., Min, H., Liu, G., … Chen, C.Z. (2007). miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell. 129, 147–161. doi: 10.1016/j.cell.2007.03.008.
   PubMed Web of Science ®Google Scholar
• Lian, J., Zhang, X., Tian, H., Liang, N., Wang, Y., Liang, C., … Sun, F. (2009). Altered microRNA expression in patients with non-obstructive azoospermia. Reproductive Biology and Endocrinology, 7, 13. doi: 10.1186/1477-7827-7-13.
   PubMed Web of Science ®Google Scholar
• 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. doi: 10.1371/journal.pone.0033861.
   PubMed Web of Science ®Google Scholar
• 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. Biology of Reproduction, 79, 696–703. doi: 10.1095/biolreprod.108.067827.
   PubMed Web of Science ®Google Scholar
• McCallie, B., Schoolcraft, W.B., & Katz-Jaffe, M.G. (2010). Aberration of blastocyst microRNA expression is associated with human infertility. Fertility and Sterility, 93, 2374–2382. doi: 10.1016/j.fertnstert.2009.01.069.
   PubMed Web of Science ®Google Scholar
• McIver, S.C., Roman, S.D., Nixon, B., & McLaughlin, E.A. (2012). miRNA and mammalian male germ cells. Human Reproduction Update, 18, 44–59. doi: 10.1093/humupd/dmr041.
   PubMed Web of Science ®Google Scholar
• Mostafa, T., Rashed, L.A., Nabil, N.I., Osman, I., Mostafa, R., & Farag, M. (2016). Seminal miRNA relationship with apoptotic markers and oxidative stress in infertile men with varicocele. Biomed Research International, 2016, 1. doi: 10.1155/2016/4302754.
   Web of Science ®Google Scholar
• Natali, A., & Turek, P.J. (2011). An assessment of new sperm tests for male infertility. Urology, 77, 1027–1034. doi: 10.1016/j.urology.2010.10.005.
   PubMed Web of Science ®Google Scholar
• Obholz, K.L., Akopyan, A., Waymire, K.G., & MacGregor, G.R. (2006). FNDC3A is required for adhesion between spermatids and Sertoli cells. Developmental Biology, 298, 498–513. doi: 10.1016/j.ydbio.2006.06.054.
   PubMed Web of Science ®Google Scholar
• Papaioannou, M.D., & Nef, S. (2010). microRNAs in the testis: Building up male fertility. Journal of Andrology, 31, 26–33. doi: 10.2164/jandrol.109.008128.
   PubMedGoogle Scholar
• Plasterk, R.H. (2006). Micro RNAs in animal development. Cell, 124, 877–881. doi: 10.1016/j.cell.2006.02.030.
   PubMed Web of Science ®Google Scholar
• Pons, S., Asano, T., Glasheen, E., Miralpeix, M., Zhang, Y., Fisher, T.L., … White, M.F. (1995). The structure and function of p55PIK reveal a new regulatory subunit for phosphatidylinositol 3-kinase. Molecular and Cellular Biology, 15, 4453–4465. doi: 10.1128/MCB.15.8.4453.
   PubMed Web of Science ®Google Scholar
• Ro, S., Park, C., Sanders, K.M., McCarrey, J.R., & Yan, W. (2007). Cloning and expression profiling of testis-expressed microRNAs. Developmental Biology, 311, 592–602. doi: 10.1016/j.ydbio.2007.09.009.
   PubMed Web of Science ®Google Scholar
• Sood, P., Krek, A., Zavolan, M., Macino, G., & Rajewsky, N. (2006). Cell-type-specific signatures of microRNAs on target mRNA expression. Proceedings of the National Academy of Sciences USA, 103, 2746–2751. doi: 10.1073/pnas.0511045103.
   PubMed Web of Science ®Google Scholar
• Tan, K.A., Turner, K.J., Saunders, P.T., Verhoeven, G., De Gendt, K., Atanassova, N., & Sharpe, R.M. (2005). Androgen regulation of stage-dependent cyclin D2 expression in Sertoli cells suggests a role in modulating androgen action on spermatogenesis. Biology of Reproduction, 72, 1151–1160. doi: 10.1095/biolreprod.104.037689.
   PubMed Web of Science ®Google Scholar
• Tan, J.Y., Habib, N.A., Chuah, Y.W., Yau, Y.H., Geifman-Shochat, S., & Chen, W.N. (2015). Identification of cellular targets of microRNA-181a in HepG2 cells: A new approach for functional analysis of microRNAs. PLoS One, 10, e0123167. doi: 10.1371/journal.pone.0123167.
   PubMed Web of Science ®Google Scholar
• Tandon, A., Tovey, J.C., Sharma, A., Gupta, R., & Mohan, R.R. (2010). Role of transforming growth factor Beta in corneal function, biology and pathology. Current Molecular Medicine, 10, 565–578. doi: 10.2174/1566524011009060565.
   PubMed Web of Science ®Google Scholar
• Tang, F., Kaneda, M., O'Carroll, D., Hajkova, P., Barton, S.C., Sun, Y.A., … Surani, M.A. (2007). Maternal microRNAs are essential for mouse zygotic development. Genes and Development, 21, 644–648. doi: 10.1101/gad.418707.
   PubMed Web of Science ®Google Scholar
• Tang, W., Liu, D.F., Kai, H., Zhao, L.M., Mao, J.M., Zhuang, X.J., … Hui, J. (2015). miRNA-mediated regulation of heat shock proteins in human ejaculated spermatozoa. Turkish Journal of Medical Sciences, 45, 1285–1291. doi: 10.3906/sag-1406-27.
   PubMed Web of Science ®Google Scholar
• 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. Biology of Reproduction, 85, 189–197. doi: 10.1095/biolreprod.110.089458.
   PubMed Web of Science ®Google Scholar
• Wang, C., Yang, C., Chen, X., Yao, B., Yang, C., Zhu, C., … Zhang, C. (2011). Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clinical Chemistry, 57, 1722–1731. doi: 10.1373/clinchem.2011.169714.
   PubMed Web of Science ®Google Scholar
• Wang, Y., Li, M., Zang, W., Ma, Y., Wang, N., Li, P., … Zhao, G. (2013). MiR429 upregulation induces apoptosis and suppresses invasion by targeting Bcl-2 and SP-1 in esophageal carcinoma. Cellular Oncology, 36, 385–394. doi: 10.1007/s13402-013-0144-6.
   PubMed Web of Science ®Google Scholar
• Wang, Z., Yao, H., Lin, S., Zhu, X., Shen, Z., Lu, G., … Kung, H-F. (2013). Transcriptional and epigenetic regulation of human microRNAs. Cancer Letters, 331, 1–10. doi: 10.1016/j.canlet.2012.12.006.
   PubMed Web of Science ®Google Scholar
• World Health Organization. (2010). WHO Laboratory Manual for the Examination and Processing of Human Semen (5th ed.). Geneva, CH: World Health Organization.
   Google Scholar
• Wu, W., Hu, Z., Qin, Y., Dong, J., Dai, J., Lu, C., … Wang, X. (2012). Seminal plasma microRNAs: Potential biomarkers for spermatogenesis status. MHR: Basic Science of Reproductive Medicine, 18, 489–497. doi: 10.1093/molehr/gas022.
   Google Scholar
• Wu, W., Qin, Y., Li, Z., Dong, J., Dai, J., Lu, C., … Wang, X. (2013). Genome-wide microRNA expression profiling in idiopathic non-obstructive azoospermia: Significant up-regulation of miR-141, miR-429 and miR-7-1-3p. Human Reproduction, 28, 1827–1836. doi: 10.1093/humrep/det099.
   PubMed Web of Science ®Google Scholar
• Yamamoto, C.I.N.D.Y.M., Hikim, A.M.I.Y.A.P.S.I.N.H.A., Lue, Y.A.N.H.E., Portugal, A.D.A.M.A.E., Guo, T.A.Y.L.O.R.B., Hsu, S.H.E.A.U.Y., … Swerdloff, R.O.N.A.L.D.S. (2001). Impairment of spermatogenesis in transgenic mice with selective overexpression of Bcl-2 in the somatic cells of the testis. Journal of Andrology, 22, 981–991. doi: 10.1002/j.1939-4640.2001.tb03439.x.
   PubMedGoogle Scholar
• 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. doi: 10.1530/REP-07-0056.
   PubMed Web of Science ®Google Scholar
• Yan, N., Lu, Y., Sun, H., Qiu, W., Tao, D., Liu, Y., … Ma, Y. (2009). Microarray profiling of microRNAs expressed in testis tissues of developing primates. Journal of Assisted Reproduction and Genetics, 26, 179–186. doi: 10.1007/s10815-009-9305-y.
   PubMed Web of Science ®Google Scholar
• 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. Biology of Reproduction, 73, 427–433. doi: 10.1095/biolreprod.105.040998.
   PubMed Web of Science ®Google Scholar
• Zhang, L., Huang, J., Yang, N., Greshock, J., Liang, S., Hasegawa, K., … Coukos, G. (2007). Integrative genomic analysis of phosphatidylinositol 3'-kinase family identifies PIK3R3 as a potential therapeutic target in epithelial ovarian cancer. Clinical Cancer Research, 13, 5314–5321. doi: 10.1158/1078-0432.CCR-06-2660.
   PubMed Web of Science ®Google Scholar
• Zhang, S., Chen, L., Jung, E.J., & Calin, G.A. (2010). Targeting microRNAs with small molecules: From dream to reality. Clinical Pharmacology and Therapeutics, 87, 754–758. doi: 10.1038/clpt.2010.46.
   PubMed Web of Science ®Google Scholar
• Zheng, S., Turner, T.T., & Lysiak, J.J. (2006). Caspase 2 activity contributes to the initial wave of germ cell apoptosis during the first round of spermatogenesis. Biology of Reproduction, 74, 1026–1033. doi: 10.1095/biolreprod.105.044610.
   PubMed Web of Science ®Google Scholar