Login Register Cart 0
Generic placeholder image

Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

MicroRNA: A Potential Diagnosis for Male Infertility

Author(s): Sedighe Forouhari, Elahe Mahmoudi, Esmat Safdarian, Zahra Beygi and Seyed Mohammad Gheibihayat*

Volume 21, Issue 10, 2021

Published on: 09 December, 2020

Page: [1226 - 1236] Pages: 11

DOI: 10.2174/1389557520999201209213319

Price: $65

Abstract

Male infertility is one of the major global health problems, in particular, in more than half of the affected men. Genetic factors are important for identifying men with idiopathic infertility along with semen analysis. Valid and useful information can be obtained through non-invasive molecular research. Among these, small single-stranded non-coding RNA molecules of microRNAs (abbreviated miRNAs) are non-invasive biomarkers with a diagnostic value by regulating the post-transcriptional gene silence through repression and prevention of the translation process. The association between various types of male infertility and miRNA regulation changes has been evaluated to understand the biological function of miRNA and gene targets. Accordingly, further study of the function of miRNAs associated with reproductive disorders could lead researchers to further understand the molecular mechanisms of male infertility in order to find effective biomarkers and therapeutic strategies. Therefore, the present review article aimed at scrutinizing those researches investigating the altered miRNA expression in testicles, epididymis, and spermatozoa.

Keywords: Infertility, MicroRNA, miRNA, spermatozoa, testis.

« Previous Next »
Graphical Abstract

[1]
Sharpe, R.M. Sperm counts and fertility in men: A rocky road ahead. Science & Society Series on Sex and Science. EMBO Rep., 2012, 13(5), 398-403.
[http://dx.doi.org/10.1038/embor.2012.50] [PMID: 22491033]
[2]
Coutton, C. Male infertility: Genetics, mechanism, and therapies. BioMed Res. Int., 2016.
[http://dx.doi.org/10.1155/2016/7372362]
[3]
Sedighe Forouhari, L.D.; Farzaneh, F.; Bahia, N; Firoozeh, N. Sexual function in fertile and infertile women with polycystic ovary syndrome.Int. J. Pharmaceut. Res., 2019, 8-12.,
[4]
Poongothai, J.; Gopenath, T.S.; Manonayaki, S. Genetics of human male infertility. Singapore Med. J., 2009, 50(4), 336-347.
[PMID: 19421675]
[5]
Korhonen, H.M. DICER regulates the formation and maintenance of cell-cell junctions in the mouse seminiferous epithelium. Biol. Reprod., 2015, 93(6), 1-13.
[6]
Barad, O.; Meiri, E.; Avniel, A.; Aharonov, R.; Barzilai, A.; Bentwich, I.; Einav, U.; Gilad, S.; Hurban, P.; Karov, Y.; Lobenhofer, E.K.; Sharon, E.; Shiboleth, Y.M.; Shtutman, M.; Bentwich, Z.; Einat, P. MicroRNA expression detected by oligonucleotide microarrays: System establishment and expression profiling in human tissues. Genome Res., 2004, 14(12), 2486-2494.
[http://dx.doi.org/10.1101/gr.2845604] [PMID: 15574827]
[7]
Liang, Y.; Ridzon, D.; Wong, L.; Chen, C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics, 2007, 8(1), 166.
[http://dx.doi.org/10.1186/1471-2164-8-166] [PMID: 17565689]
[8]
Salas-Huetos, A.; James, E.R.; Aston, K.I.; Carrell, D.T.; Jenkins, T.G.; Yeste, M. The role of miRNAs in male human reproduction: A systematic review. Andrology, 2020, 8(1), 7-26.
[http://dx.doi.org/10.1111/andr.12714] [PMID: 31578810]
[9]
He, Z.; Kokkinaki, M.; Pant, D.; Gallicano, G.I.; Dym, M. Small RNA molecules in the regulation of spermatogenesis. Reproduction, 2009, 137(6), 901-911.
[http://dx.doi.org/10.1530/REP-08-0494] [PMID: 19318589]
[10]
Shukla, G.C.; Singh, J.; Barik, S. MicroRNAs: Processing, maturation, target recognition and regulatory functions. Mol. Cell. Pharmacol., 2011, 3(3), 83-92.
[PMID: 22468167]
[11]
Ambros, V. The functions of animal microRNAs. Nature, 2004, 431(7006), 350-355.
[http://dx.doi.org/10.1038/nature02871] [PMID: 15372042]
[12]
Kozomara, A.; Birgaoanu, M.; Griffiths-Jones, S. miRBase: From microRNA sequences to function. Nucleic Acids Res., 2019, 47(D1), D155-D162.
[http://dx.doi.org/10.1093/nar/gky1141] [PMID: 30423142]
[13]
Pan, Q.; Chegini, N. MicroRNA signature and regulatory functions in the endometrium during normal and disease states. Seminars in reproductive medicine; Thieme Medical Publishers, 2008.
[http://dx.doi.org/10.1055/s-0028-1096128]
[14]
Pan, Q.; Luo, X.; Chegini, N. Differential expression of microRNAs in myometrium and leiomyomas and regulation by ovarian steroids. J. Cell. Mol. Med., 2008, 12(1), 227-240.
[http://dx.doi.org/10.1111/j.1582-4934.2007.00207.x] [PMID: 18182067]
[15]
Rupaimoole, R.; Slack, F.J. MicroRNA therapeutics: Towards a new era for the management of cancer and other diseases. Nat. Rev. Drug Discov., 2017, 16(3), 203-222.
[http://dx.doi.org/10.1038/nrd.2016.246] [PMID: 28209991]
[16]
Yang, J.; Medvedev, S.; Reddi, P.P.; Schultz, R.M.; Hecht, N.B. The DNA/RNA-binding protein MSY2 marks specific transcripts for cytoplasmic storage in mouse male germ cells. Proc. Natl. Acad. Sci. USA, 2005, 102(5), 1513-1518.
[http://dx.doi.org/10.1073/pnas.0404685102] [PMID: 15665108]
[17]
Li, J.; Liu, Y.; Dong, D.; Zhang, Z. Evolution of an X-linked primate-specific micro RNA cluster. Mol. Biol. Evol., 2010, 27(3), 671-683.
[http://dx.doi.org/10.1093/molbev/msp284] [PMID: 19933172]
[18]
Rajender, S.; Meador, C.; Agarwal, A. Small RNA in spermatogenesis and male infertility. Front. Biosci. (Schol. Ed.), 2012, 4, 1266-1274.
[PMID: 22652870]
[19]
Lee, R.C.; Feinbaum, R.L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. cell, 1993, 75(5), 843-854.,
[20]
Wightman, B.; Ha, I.; Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell, 1993, 75(5), 855-862.
[http://dx.doi.org/10.1016/0092-8674(93)90530-4] [PMID: 8252622]
[21]
Cai, X.; Hagedorn, C.H.; Cullen, B.R. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA, 2004, 10(12), 1957-1966.
[http://dx.doi.org/10.1261/rna.7135204] [PMID: 15525708]
[22]
Kim, V.N.; Han, J.; Siomi, M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol., 2009, 10(2), 126-139.
[http://dx.doi.org/10.1038/nrm2632] [PMID: 19165215]
[23]
Saini, H.K.; Griffiths-Jones, S.; Enright, A.J. Genomic analysis of human microRNA transcripts. Proc. Natl. Acad. Sci. USA, 2007, 104(45), 17719-17724.
[http://dx.doi.org/10.1073/pnas.0703890104] [PMID: 17965236]
[24]
Lee, Y.; Jeon, K.; Lee, J.T.; Kim, S.; Kim, V.N. MicroRNA maturation: Stepwise processing and subcellular localization. EMBO J., 2002, 21(17), 4663-4670.
[http://dx.doi.org/10.1093/emboj/cdf476] [PMID: 12198168]
[25]
Lee, Y.; Ahn, C.; Han, J.; Choi, H.; Kim, J.; Yim, J.; Lee, J.; Provost, P.; Rådmark, O.; Kim, S.; Kim, V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature, 2003, 425(6956), 415-419.
[http://dx.doi.org/10.1038/nature01957] [PMID: 14508493]
[26]
Han, J.; Lee, Y.; Yeom, K.H.; Kim, Y.K.; Jin, H.; Kim, V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev., 2004, 18(24), 3016-3027.
[http://dx.doi.org/10.1101/gad.1262504] [PMID: 15574589]
[27]
Zeng, Y.; Cullen, B.R. Sequence requirements for micro RNA processing and function in human cells. RNA, 2003, 9(1), 112-123.
[http://dx.doi.org/10.1261/rna.2780503] [PMID: 12554881]
[28]
Berezikov, E.; Chung, W.J.; Willis, J.; Cuppen, E.; Lai, E.C. Mammalian mirtron genes. Mol. Cell, 2007, 28(2), 328-336.
[http://dx.doi.org/10.1016/j.molcel.2007.09.028] [PMID: 17964270]
[29]
Lund, E. Nuclear export of microRNA precursors.Science, 2004, 303, 5654, 95.,
[http://dx.doi.org/10.1126/science.1090599]
[30]
Chendrimada, T.P.; Gregory, R.I.; Kumaraswamy, E.; Norman, J.; Cooch, N.; Nishikura, K.; Shiekhattar, R. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature, 2005, 436(7051), 740-744.
[http://dx.doi.org/10.1038/nature03868] [PMID: 15973356]
[31]
Schwarz, D.S.; Hutvágner, G.; Du, T.; Xu, Z.; Aronin, N.; Zamore, P.D. Asymmetry in the assembly of the RNAi enzyme complex. Cell, 2003, 115(2), 199-208.
[http://dx.doi.org/10.1016/S0092-8674(03)00759-1] [PMID: 14567917]
[32]
Aravin, A.A.; Lagos-Quintana, M.; Yalcin, A.; Zavolan, M.; Marks, D.; Snyder, B.; Gaasterland, T.; Meyer, J.; Tuschl, T. The small RNA profile during Drosophila melanogaster development. Dev. Cell, 2003, 5(2), 337-350.
[http://dx.doi.org/10.1016/S1534-5807(03)00228-4] [PMID: 12919683]
[33]
Lagos-Quintana, M.; Rauhut, R.; Yalcin, A.; Meyer, J.; Lendeckel, W.; Tuschl, T. Identification of tissue-specific microRNAs from mouse. Curr. Biol., 2002, 12(9), 735-739.
[http://dx.doi.org/10.1016/S0960-9822(02)00809-6] [PMID: 12007417]
[34]
Lim, L.P.; Lau, N.C.; Weinstein, E.G.; Abdelhakim, A.; Yekta, S.; Rhoades, M.W.; Burge, C.B.; Bartel, D.P. The microRNAs of Caenorhabditis elegans. Genes Dev., 2003, 17(8), 991-1008.
[http://dx.doi.org/10.1101/gad.1074403] [PMID: 12672692]
[35]
Ro, S.; Park, C.; Young, D.; Sanders, K.M.; Yan, W. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res., 2007, 35(17), 5944-5953.
[http://dx.doi.org/10.1093/nar/gkm641] [PMID: 17726050]
[36]
Yekta, S.; Shih, I.H.; Bartel, D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science, 2004, 304(5670), 594-596.
[http://dx.doi.org/10.1126/science.1097434] [PMID: 15105502]
[37]
Rehwinkel, J.; Behm-Ansmant, I.; Gatfield, D.; Izaurralde, E. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA, 2005, 11(11), 1640-1647.
[http://dx.doi.org/10.1261/rna.2191905] [PMID: 16177138]
[38]
Liu, J.; Rivas, F.V.; Wohlschlegel, J.; Yates, J.R., III; Parker, R.; Hannon, G.J. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol., 2005, 7(12), 1261-1266.
[http://dx.doi.org/10.1038/ncb1333] [PMID: 16284623]
[39]
Wan, G.; Mathur, R.; Hu, X.; Zhang, X.; Lu, X. miRNA response to DNA damage. Trends Biochem. Sci., 2011, 36(9), 478-484.
[http://dx.doi.org/10.1016/j.tibs.2011.06.002] [PMID: 21741842]
[40]
Salmena, L.; Poliseno, L.; Tay, Y.; Kats, L.; Pandolfi, P.P. A ceRNA hypothesis: The Rosetta Stone of a hidden RNA language? Cell, 2011, 146(3), 353-358.
[http://dx.doi.org/10.1016/j.cell.2011.07.014] [PMID: 21802130]
[41]
Seitz, H. Redefining microRNA targets. Curr. Biol., 2009, 19(10), 870-873.
[http://dx.doi.org/10.1016/j.cub.2009.03.059] [PMID: 19375315]
[42]
Bartel, D.P.; Chen, C-Z. Micromanagers of gene expression: The potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet., 2004, 5(5), 396-400.
[http://dx.doi.org/10.1038/nrg1328] [PMID: 15143321]
[43]
Arvey, A.; Larsson, E.; Sander, C.; Leslie, C.S.; Marks, D.S. Target mRNA abundance dilutes microRNA and siRNA activity. Mol. Syst. Biol., 2010, 6(1), 363.
[http://dx.doi.org/10.1038/msb.2010.24] [PMID: 20404830]
[44]
Lee, D.Y.A. 3′-untranslated region (3′ UTR) induces organ adhesion by regulating miR-199a* functions. PLoS One, 2009, 4(2)
[http://dx.doi.org/10.1371/journal.pone.0004527]
[45]
Poliseno, L.; Salmena, L.; Zhang, J.; Carver, B.; Haveman, W.J.; Pandolfi, P.P. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature, 2010, 465(7301), 1033-1038.
[http://dx.doi.org/10.1038/nature09144] [PMID: 20577206]
[46]
Franco-Zorrilla, J.M.; Valli, A.; Todesco, M.; Mateos, I.; Puga, M.I.; Rubio-Somoza, I.; Leyva, A.; Weigel, D.; García, J.A.; Paz-Ares, J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet., 2007, 39(8), 1033-1037.
[http://dx.doi.org/10.1038/ng2079] [PMID: 17643101]
[47]
Cazalla, D.; Yario, T.; Steitz, J.A. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science, 2010, 328(5985), 1563-1566.
[http://dx.doi.org/10.1126/science.1187197] [PMID: 20558719]
[48]
Wilusz, C.J.; Wormington, M.; Peltz, S.W. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol., 2001, 2(4), 237-246.
[http://dx.doi.org/10.1038/35067025] [PMID: 11283721]
[49]
Carroll, A.P.; Tran, N.; Tooney, P.A.; Cairns, M.J. Alternative mRNA fates identified in microRNA-associated transcriptome analysis. BMC Genom, 2012, 13(1), 561.
[http://dx.doi.org/10.1186/1471-2164-13-561] [PMID: 23083446]
[50]
Vasudevan, S.; Tong, Y.; Steitz, J.A. Switching from repression to activation: MicroRNAs can up-regulate translation. Science, 2007, 318(5858), 1931-1934.
[http://dx.doi.org/10.1126/science.1149460] [PMID: 18048652]
[51]
Wilusz, J.E.; Sharp, P.A. Molecular biology. A circuitous route to noncoding RNA. Science, 2013, 340(6131), 440-441.
[http://dx.doi.org/10.1126/science.1238522] [PMID: 23620042]
[52]
Hansen, T.B.; Wiklund, E.D.; Bramsen, J.B.; Villadsen, S.B.; Statham, A.L.; Clark, S.J.; Kjems, J. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J., 2011, 30(21), 4414-4422.
[http://dx.doi.org/10.1038/emboj.2011.359] [PMID: 21964070]
[53]
Tulay, P.; Sengupta, S.B. MicroRNA expression and its association with DNA repair in preimplantation embryos. J. Reprod. Dev., 2016, 62(3), 225-234.
[http://dx.doi.org/10.1262/jrd.2015-167] [PMID: 26853522]
[54]
Sempere, L.F.; Freemantle, S.; Pitha-Rowe, I.; Moss, E.; Dmitrovsky, E.; Ambros, V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol., 2004, 5(3), R13.
[http://dx.doi.org/10.1186/gb-2004-5-3-r13] [PMID: 15003116]
[55]
Calin, G.A.; Liu, C.G.; Sevignani, C.; Ferracin, M.; Felli, N.; Dumitru, C.D.; Shimizu, M.; Cimmino, A.; Zupo, S.; Dono, M.; Dell’Aquila, M.L.; Alder, H.; Rassenti, L.; Kipps, T.J.; Bullrich, F.; Negrini, M.; Croce, C.M. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc. Natl. Acad. Sci. USA, 2004, 101(32), 11755-11760.
[http://dx.doi.org/10.1073/pnas.0404432101] [PMID: 15284443]
[56]
Liu, C-G.; Calin, G.A.; Meloon, B.; Gamliel, N.; Sevignani, C.; Ferracin, M.; Dumitru, C.D.; Shimizu, M.; Zupo, S.; Dono, M.; Alder, H.; Bullrich, F.; Negrini, M.; Croce, C.M. An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proc. Natl. Acad. Sci. USA, 2004, 101(26), 9740-9744.
[http://dx.doi.org/10.1073/pnas.0403293101] [PMID: 15210942]
[57]
Schmittgen, T.D.; Jiang, J.; Liu, Q.; Yang, L. A high-throughput method to monitor the expression of microRNA precursors. Nucleic Acids Res., 2004, 32(4), e43-e43.
[http://dx.doi.org/10.1093/nar/gnh040] [PMID: 14985473]
[58]
Babak, T.; Zhang, W.; Morris, Q.; Blencowe, B.J.; Hughes, T.R. Probing microRNAs with microarrays: Tissue specificity and functional inference. RNA, 2004, 10(11), 1813-1819.
[http://dx.doi.org/10.1261/rna.7119904] [PMID: 15496526]
[59]
Miska, E.A.; Alvarez-Saavedra, E.; Townsend, M.; Yoshii, A.; Sestan, N.; Rakic, P.; Constantine-Paton, M.; Horvitz, H.R. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol., 2004, 5(9), R68.
[http://dx.doi.org/10.1186/gb-2004-5-9-r68] [PMID: 15345052]
[60]
Sun, Y.; Koo, S.; White, N.; Peralta, E.; Esau, C.; Dean, N.M.; Perera, R.J. Development of a micro-array to detect human and mouse microRNAs and characterization of expression in human organs. Nucleic Acids Res., 2004, 32(22), e188-e188.
[http://dx.doi.org/10.1093/nar/gnh186] [PMID: 15616155]
[61]
Forouhari, S. Effect of some hormones related to polycystic ovary syndrome on health-related quality of life. Majallah-i Zanan, Mamai va Nazai-i Iran, 2016, 18(186), 17-27.
[62]
Johnson, S.M.; Lin, S-Y.; Slack, F.J. The time of appearance of the C. elegans let-7 microRNA is transcriptionally controlled utilizing a temporal regulatory element in its promoter. Dev. Biol., 2003, 259(2), 364-379.
[http://dx.doi.org/10.1016/S0012-1606(03)00202-1] [PMID: 12871707]
[63]
Ghosh, S. Micro RNA-biogenesis, mechanism of action and applications- A review. Int. J. Res. Biotechnol. Biochem., 2011, 1(1), 11-36.
[64]
Chen, X.; Ba, Y.; Ma, L.; Cai, X.; Yin, Y.; Wang, K.; Guo, J.; Zhang, Y.; Chen, J.; Guo, X.; Li, Q.; Li, X.; Wang, W.; Zhang, Y.; Wang, J.; Jiang, X.; Xiang, Y.; Xu, C.; Zheng, P.; Zhang, J.; Li, R.; Zhang, H.; Shang, X.; Gong, T.; Ning, G.; Wang, J.; Zen, K.; Zhang, J.; Zhang, C.Y. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res., 2008, 18(10), 997-1006.
[http://dx.doi.org/10.1038/cr.2008.282] [PMID: 18766170]
[65]
Arroyo, J.D.; Chevillet, J.R.; Kroh, E.M.; Ruf, I.K.; Pritchard, C.C.; Gibson, D.F.; Mitchell, P.S.; Bennett, C.F.; Pogosova-Agadjanyan, E.L.; Stirewalt, D.L.; Tait, J.F.; Tewari, M. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA, 2011, 108(12), 5003-5008.
[http://dx.doi.org/10.1073/pnas.1019055108] [PMID: 21383194]
[66]
Cogswell, J.P.; Ward, J.; Taylor, I.A.; Waters, M.; Shi, Y.; Cannon, B.; Kelnar, K.; Kemppainen, J.; Brown, D.; Chen, C.; Prinjha, R.K.; Richardson, J.C.; Saunders, A.M.; Roses, A.D.; Richards, C.A. Identification of miRNA changes in Alzheimer’s disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis., 2008, 14(1), 27-41.
[http://dx.doi.org/10.3233/JAD-2008-14103] [PMID: 18525125]
[67]
Gallo, A.; Tandon, M.; Alevizos, I.; Illei, G.G. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One, 2012, 7(3)e30679
[http://dx.doi.org/10.1371/journal.pone.0030679] [PMID: 22427800]
[68]
Zhou, Q.; Li, M.; Wang, X.; Li, Q.; Wang, T.; Zhu, Q.; Zhou, X.; Wang, X.; Gao, X.; Li, X. Immune-related microRNAs are abundant in breast milk exosomes. Int. J. Biol. Sci., 2012, 8(1), 118-123.
[http://dx.doi.org/10.7150/ijbs.8.118] [PMID: 22211110]
[69]
Weber, J.A.; Baxter, D.H.; Zhang, S.; Huang, D.Y.; Huang, K.H.; Lee, M.J.; Galas, D.J.; Wang, K. The microRNA spectrum in 12 body fluids. Clin. Chem., 2010, 56(11), 1733-1741.
[http://dx.doi.org/10.1373/clinchem.2010.147405] [PMID: 20847327]
[70]
da Silveira, J.C. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: A possible new form of cell communication within the ovarian follicle. Biol. Reprod., 2012, 86(3), 1-10.
[http://dx.doi.org/10.1095/biolreprod.111.093252]
[71]
Mitchell, P.S.; Parkin, R.K.; Kroh, E.M.; Fritz, B.R.; Wyman, S.K.; Pogosova-Agadjanyan, E.L.; Peterson, A.; Noteboom, J.; O’Briant, K.C.; Allen, A.; Lin, D.W.; Urban, N.; Drescher, C.W.; Knudsen, B.S.; Stirewalt, D.L.; Gentleman, R.; Vessella, R.L.; Nelson, P.S.; Martin, D.B.; Tewari, M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. USA, 2008, 105(30), 10513-10518.
[http://dx.doi.org/10.1073/pnas.0804549105] [PMID: 18663219]
[72]
Iftikhar, H.; Carney, G.E. Evidence and potential in vivo functions for biofluid miRNAs: From expression profiling to functional testing: Potential roles of extracellular miRNAs as indicators of physiological change and as agents of intercellular information exchange. BioEssays, 2016, 38(4), 367-378.
[http://dx.doi.org/10.1002/bies.201500130] [PMID: 26934338]
[73]
Turchinovich, A.; Weiz, L.; Langheinz, A.; Burwinkel, B. Characterization of extracellular circulating microRNA. Nucleic Acids Res., 2011, 39(16), 7223-7233.
[http://dx.doi.org/10.1093/nar/gkr254] [PMID: 21609964]
[74]
Vickers, K.C.; Palmisano, B.T.; Shoucri, B.M.; Shamburek, R.D.; Remaley, A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol., 2011, 13(4), 423-433.
[http://dx.doi.org/10.1038/ncb2210] [PMID: 21423178]
[75]
Tabet, F.; Vickers, K.C.; Cuesta Torres, L.F.; Wiese, C.B.; Shoucri, B.M.; Lambert, G.; Catherinet, C.; Prado-Lourenco, L.; Levin, M.G.; Thacker, S.; Sethupathy, P.; Barter, P.J.; Remaley, A.T.; Rye, K.A. HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nat. Commun., 2014, 5(1), 3292.
[http://dx.doi.org/10.1038/ncomms4292] [PMID: 24576947]
[76]
Turchinovich, A.; Weiz, L.; Burwinkel, B. Extracellular miRNAs: The mystery of their origin and function. Trends Biochem. Sci., 2012, 37(11), 460-465.
[http://dx.doi.org/10.1016/j.tibs.2012.08.003] [PMID: 22944280]
[77]
Wang, K.; Zhang, S.; Weber, J.; Baxter, D.; Galas, D.J. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res., 2010, 38(20), 7248-7259.
[http://dx.doi.org/10.1093/nar/gkq601] [PMID: 20615901]
[78]
Etheridge, A.; Lee, I.; Hood, L.; Galas, D.; Wang, K. Extracellular microRNA: A new source of biomarkers. Mutat. Res., 2011, 717(1-2), 85-90.
[http://dx.doi.org/10.1016/j.mrfmmm.2011.03.004] [PMID: 21402084]
[79]
Pal, M.K.; Jaiswar, S.P.; Dwivedi, V.N.; Tripathi, A.K.; Dwivedi, A.; Sankhwar, P. MicroRNA: A new and promising potential biomarker for diagnosis and prognosis of ovarian cancer. Cancer Biol. Med., 2015, 12(4), 328-341.
[PMID: 26779370]
[80]
Vashisht, A.; Gahlay, G.K. Using miRNAs as diagnostic biomarkers for male infertility: Opportunities and challenges. Mol. Hum. Reprod., 2020, 26(4), 199-214.
[http://dx.doi.org/10.1093/molehr/gaaa016] [PMID: 32084276]
[81]
Turchinovich, A.; Burwinkel, B. Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol., 2012, 9(8), 1066-1075.
[http://dx.doi.org/10.4161/rna.21083] [PMID: 22858679]
[82]
Hunter, M.P.; Ismail, N.; Zhang, X.; Aguda, B.D.; Lee, E.J.; Yu, L.; Xiao, T.; Schafer, J.; Lee, M.L.; Schmittgen, T.D.; Nana-Sinkam, S.P.; Jarjoura, D.; Marsh, C.B. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One, 2008, 3(11)e3694
[http://dx.doi.org/10.1371/journal.pone.0003694] [PMID: 19002258]
[83]
Wagner, J.; Riwanto, M.; Besler, C.; Knau, A.; Fichtlscherer, S.; Röxe, T.; Zeiher, A.M.; Landmesser, U.; Dimmeler, S. Characterization of levels and cellular transfer of circulating lipoprotein-bound microRNAs. Arterioscler. Thromb. Vasc. Biol., 2013, 33(6), 1392-1400.
[http://dx.doi.org/10.1161/ATVBAHA.112.300741] [PMID: 23559634]
[84]
Sohel, M.H. Extracellular/circulating microRNAs: Release mechanisms, functions and challenges. Aciev. Life Sci., 2016, 10(2), 175-186.
[http://dx.doi.org/10.1016/j.als.2016.11.007]
[85]
Wang, C.; Yang, C.; Chen, X.; Yao, B.; Yang, C.; Zhu, C.; Li, L.; Wang, J.; Li, X.; Shao, Y.; Liu, Y.; Ji, J.; Zhang, J.; Zen, K.; Zhang, C.Y.; Zhang, C. Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clin. Chem., 2011, 57(12), 1722-1731.
[http://dx.doi.org/10.1373/clinchem.2011.169714] [PMID: 21933900]
[86]
Gilad, S.; Meiri, E.; Yogev, Y.; Benjamin, S.; Lebanony, D.; Yerushalmi, N.; Benjamin, H.; Kushnir, M.; Cholakh, H.; Melamed, N.; Bentwich, Z.; Hod, M.; Goren, Y.; Chajut, A. Serum microRNAs are promising novel biomarkers. PLoS One, 2008, 3(9)e3148
[http://dx.doi.org/10.1371/journal.pone.0003148] [PMID: 18773077]
[87]
Glinge, C.; Clauss, S.; Boddum, K.; Jabbari, R.; Jabbari, J.; Risgaard, B.; Tomsits, P.; Hildebrand, B.; Kääb, S.; Wakili, R.; Jespersen, T.; Tfelt-Hansen, J. Stability of circulating blood-based MicroRNAs–pre-analytic methodological considerations. PLoS One, 2017, 12(2)e0167969
[http://dx.doi.org/10.1371/journal.pone.0167969] [PMID: 28151938]
[88]
Jung, M.; Schaefer, A.; Steiner, I.; Kempkensteffen, C.; Stephan, C.; Erbersdobler, A.; Jung, K. Robust microRNA stability in degraded RNA preparations from human tissue and cell samples. Clin. Chem., 2010, 56(6), 998-1006.
[http://dx.doi.org/10.1373/clinchem.2009.141580] [PMID: 20378769]
[89]
Ge, Q.; Zhou, Y.; Lu, J.; Bai, Y.; Xie, X.; Lu, Z. miRNA in plasma exosome is stable under different storage conditions. Molecules, 2014, 19(2), 1568-1575.
[http://dx.doi.org/10.3390/molecules19021568] [PMID: 24473213]
[90]
He, Z.; Jiang, J.; Kokkinaki, M.; Tang, L.; Zeng, W.; Gallicano, I.; Dobrinski, I.; Dym, M. MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem Cells, 2013, 31(10), 2205-2217.
[http://dx.doi.org/10.1002/stem.1474] [PMID: 23836497]
[91]
Valadi, H.; Ekström, K.; Bossios, A.; Sjöstrand, M.; Lee, J.J.; Lötvall, J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 2007, 9(6), 654-659.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[92]
Stenvang, J.; Petri, A.; Lindow, M.; Obad, S.; Kauppinen, S. Inhibition of microRNA function by antimiR oligonucleotides. Silence, 2012, 3(1), 1.
[http://dx.doi.org/10.1186/1758-907X-3-1] [PMID: 22230293]
[93]
Chakraborty, C.; Sharma, A.R.; Sharma, G.; Doss, C.G.P.; Lee, S.S. Therapeutic miRNA and siRNA: Moving from bench to clinic as next generation medicine. Mol. Ther. Nucleic Acids, 2017, 8, 132-143.
[http://dx.doi.org/10.1016/j.omtn.2017.06.005] [PMID: 28918016]
[94]
Miller, A.D. Delivery of RNAi therapeutics: Work in progress. Expert Rev. Med. Devices, 2013, 10(6), 781-811.
[http://dx.doi.org/10.1586/17434440.2013.855471] [PMID: 24195461]
[95]
Hong, C.A.; Nam, Y.S. Functional nanostructures for effective delivery of small interfering RNA therapeutics. Theranostics, 2014, 4(12), 1211-1232.
[http://dx.doi.org/10.7150/thno.8491] [PMID: 25285170]
[96]
Gilleron, J.; Querbes, W.; Zeigerer, A.; Borodovsky, A.; Marsico, G.; Schubert, U.; Manygoats, K.; Seifert, S.; Andree, C.; Stöter, M.; Epstein-Barash, H.; Zhang, L.; Koteliansky, V.; Fitzgerald, K.; Fava, E.; Bickle, M.; Kalaidzidis, Y.; Akinc, A.; Maier, M.; Zerial, M. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat. Biotechnol., 2013, 31(7), 638-646.
[http://dx.doi.org/10.1038/nbt.2612] [PMID: 23792630]
[97]
Khazaie, Y.; Nasr Esfahani, M.H. MicroRNA and male infertility: A potential for diagnosis. Int. J. Fertil. Steril., 2014, 8(2), 113-118.
[PMID: 25083174]
[98]
Yang, Q.; Hua, J.; Wang, L.; Xu, B.; Zhang, H.; Ye, N.; Zhang, Z.; Yu, D.; Cooke, H.J.; Zhang, Y.; Shi, Q. MicroRNA and piRNA profiles in normal human testis detected by next generation sequencing. PLoS One, 2013, 8(6)e66809
[http://dx.doi.org/10.1371/journal.pone.0066809] [PMID: 23826142]
[99]
Lian, J.; Zhang, X.; Tian, H.; Liang, N.; Wang, Y.; Liang, C.; Li, X.; Sun, F. Altered microRNA expression in patients with non-obstructive azoospermia. Reprod. Biol. Endocrinol., 2009, 7(1), 13.
[http://dx.doi.org/10.1186/1477-7827-7-13] [PMID: 19210773]
[100]
Lian, J.; Tian, H.; Liu, L.; Zhang, X.S.; Li, W.Q.; Deng, Y.M.; Yao, G.D.; Yin, M.M.; Sun, F. Downregulation of microRNA-383 is associated with male infertility and promotes testicular embryonal carcinoma cell proliferation by targeting IRF1. Cell Death Dis., 2010, 1(11), e94-e94.
[http://dx.doi.org/10.1038/cddis.2010.70] [PMID: 21368870]
[101]
Tang, D.; Huang, Z.; He, X.; Wu, H.; Peng, D.; Zhang, L.; Zhang, X. Altered miRNA profile in testis of post-cryptorchidopexy patients with non-obstructive azoospermia. Reprod. Biol. Endocrinol., 2018, 16(1), 78.
[http://dx.doi.org/10.1186/s12958-018-0393-3] [PMID: 30103742]
[102]
Belleannée, C.; Calvo, E.; Thimon, V.; Cyr, D.G.; Légaré, C.; Garneau, L.; Sullivan, R. Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoS One, 2012, 7(4)e34996
[http://dx.doi.org/10.1371/journal.pone.0034996] [PMID: 22511979]
[103]
Zhang, J.; Liu, Q.; Zhang, W.; Li, J.; Li, Z.; Tang, Z.; Li, Y.; Han, C.; Hall, S.H.; Zhang, Y. Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides. Acta Biochim. Biophys. Sin. (Shanghai), 2010, 42(2), 145-153.
[http://dx.doi.org/10.1093/abbs/gmp116] [PMID: 20119626]
[104]
Belleannée, C.; Légaré, C.; Calvo, E.; Thimon, V.; Sullivan, R. microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum. Reprod., 2013, 28(6), 1455-1467.
[http://dx.doi.org/10.1093/humrep/det088] [PMID: 23539611]
[105]
Cui, L. Spermatozoa micro ribonucleic acid–34c level is correlated with intracytoplasmic sperm injection outcomes. Fertil. Steril., 2015, 104(2), 312-317.
[http://dx.doi.org/10.1016/j.fertnstert.2015.05.003]
[106]
Yazdanpanahi, Z.; Forouhari, S.; Parsanezhad, M. Prepregnancy body mass index and gestational weight gain and their association with some pregnancy outcomes, 2008.
[107]
Liu, T.; Cheng, W.; Gao, Y.; Wang, H.; Liu, Z. Microarray analysis of microRNA expression patterns in the semen of infertile men with semen abnormalities. Mol. Med. Rep., 2012, 6(3), 535-542.
[http://dx.doi.org/10.3892/mmr.2012.967] [PMID: 22735917]
[108]
Abu-Halima, M. Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil. Steril., 2013, 99(5), 1249-1255.
[http://dx.doi.org/10.1016/j.fertnstert.2012.11.054]
[109]
Zhou, J-H. The expression of cysteine-rich secretory protein 2 (CRISP2) and its specific regulator miR-27b in the spermatozoa of patients with asthenozoospermia. Biol. Reprod., 2015, 92(1), 1-9.
[110]
Zhou, J-H.; Zhou, Q.Z.; Yang, J.K.; Lyu, X.M.; Bian, J.; Guo, W.B.; Chen, Z.J.; Xia, M.; Xia, H.; Qi, T.; Li, X.; Liu, C.D. MicroRNA-27a-mediated repression of cysteine-rich secretory protein 2 translation in asthenoteratozoospermic patients. Asian J. Androl., 2017, 19(5), 591-595.
[http://dx.doi.org/10.4103/1008-682X.185001] [PMID: 27517483]
[111]
Ji, Z.; Lu, R.; Mou, L.; Duan, Y.G.; Zhang, Q.; Wang, Y.; Gui, Y.; Cai, Z. Expressions of miR-15a and its target gene HSPA1B in the spermatozoa of patients with varicocele. Reproduction, 2014, 147(5), 693-701.
[http://dx.doi.org/10.1530/REP-13-0656] [PMID: 24481955]
[112]
Li, H.; Huang, S.; Guo, C.; Guan, H.; Xiong, C. Cell-free seminal mRNA and microRNA exist in different forms. PLoS One, 2012, 7(4)e34566
[http://dx.doi.org/10.1371/journal.pone.0034566] [PMID: 22506029]
[113]
Vojtech, L.; Woo, S.; Hughes, S.; Levy, C.; Ballweber, L.; Sauteraud, R.P.; Strobl, J.; Westerberg, K.; Gottardo, R.; Tewari, M.; Hladik, F. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res., 2014, 42(11), 7290-7304.
[http://dx.doi.org/10.1093/nar/gku347] [PMID: 24838567]
[114]
Abu-Halima, M. Altered micro-ribonucleic acid expression profiles of extracellular microvesicles in the seminal plasma of patients with oligoasthenozoospermia. Fertil. Steril., 2016, 106(5), 1061-1069.
[http://dx.doi.org/10.1016/j.fertnstert.2016.06.030]
[115]
Hu, L.; Wu, C.; Guo, C.; Li, H.; Xiong, C. Identification of microRNAs predominately derived from testis and epididymis in human seminal plasma. Clin. Biochem., 2014, 47(10-11), 967-972.
[http://dx.doi.org/10.1016/j.clinbiochem.2013.11.009] [PMID: 24275253]
[116]
Zhao, K.; Chen, Y.; Yang, R.; Bai, Y.; Li, C.; Li, H.; Xiong, C. miR-424/322 is downregulated in the semen of patients with severe DNA damage and may regulate sperm DNA damage. Reprod. Fertil. Dev., 2015, 28(10), 1598-1607.
[http://dx.doi.org/10.1071/RD15052] [PMID: 25872494]
[117]
Chiu, Y-L.; Rana, T.M. siRNA function in RNAi: A chemical modification analysis. RNA, 2003, 9(9), 1034-1048.
[http://dx.doi.org/10.1261/rna.5103703] [PMID: 12923253]
[118]
Harborth, J.; Elbashir, S.M.; Vandenburgh, K.; Manninga, H.; Scaringe, S.A.; Weber, K.; Tuschl, T. Sequence, chemical, and structural variation of small interfering RNAs and short hairpin RNAs and the effect on mammalian gene silencing. Antisense Nucleic Acid Drug Dev., 2003, 13(2), 83-105.
[http://dx.doi.org/10.1089/108729003321629638] [PMID: 12804036]
[119]
Rupaimoole, R.; Han, H.D.; Lopez-Berestein, G.; Sood, A.K. MicroRNA therapeutics: Principles, expectations, and challenges. Chin. J. Cancer, 2011, 30(6), 368-370.
[http://dx.doi.org/10.5732/cjc.011.10186] [PMID: 21627858]
[120]
Sheng, R. Assembly of plasmid DNA with pyrene-amines cationic amphiphiles into nanoparticles and their visible lysosome localization. RSC Advances, 2015, 5(16), 12338-12345.
[http://dx.doi.org/10.1039/C4RA06879C]

Rights & Permissions Print Cite
Article Metrics
40
1
© 2024 Bentham Science Publishers | Privacy Policy