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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Expression of microRNA in male reproductive tissues and their role in male fertility

S. L. Pratt A B and S. M. Calcatera A
+ Author Affiliations
- Author Affiliations

A Department of Animal and Veterinary Sciences, Clemson University, Clemson, SC 29634-0311, USA.

B Corresponding author. Email: scottp@clemson.edu

Reproduction, Fertility and Development 29(1) 24-31 https://doi.org/10.1071/RD16293
Published: 2 December 2016

Abstract

MicroRNA (miRNA) are small non-coding RNA, approximately 22 nucleotides in length, that regulate gene expression through their ability to bind to mRNA. The role of miRNA in cellular and tissue development is well documented and their importance in male reproductive tissue development is actively being evaluated. They are present in spermatogonia, Sertoli and Leydig cells within the testis and are present in mature spermatozoa, indicating roles in normal testicular development, function and spermatogenesis. Their presence in spermatozoa has led to postulations about the roles of male miRNA during early embryonic development after fertilisation, including chromatin restructuring and possible epigenetic effects on embryo development. MiRNAs are also present in body fluids, such as blood serum, milk, ovarian follicular fluid and seminal fluid. Circulating miRNAs are stable, and aberrant expression of cellular or extracellular miRNA has been associated with multiple pathophysiological conditions, the most studied being numerous forms of cancer. Considering that miRNAs are present in spermatozoa and in seminal fluid, their stability and the relatively non-invasive procedures required to obtain these samples make miRNAs excellent candidates for use as biomarkers of male reproduction and fertility. Biomarkers, such as miRNAs, identifying fertile males would be of financial interest to the animal production industry.

Additional keywords: microarray, seminal fluid, sequencing, spermatogenesis, spermatozoa, testis.


References

Al-Dossary, A. A., Bathala, P., Caplan, J. L., and Martin-DeLeon, P. A. (2015). Oviductosome–sperm membrane interaction in cargo delivery: detection of fusion and underlying molecular players using three-dimensional super-resolution structured illumination microscopy (SR-SIM). J. Biol. Chem. 290, 17 710–17 723.
Oviductosome–sperm membrane interaction in cargo delivery: detection of fusion and underlying molecular players using three-dimensional super-resolution structured illumination microscopy (SR-SIM).Crossref | GoogleScholarGoogle Scholar |

Amanai, M., Brahmajosyula, M., and Perry, A. C. (2006). A restricted role for sperm-borne microRNAs in mammalian fertilization. Biol. Reprod. 75, 877–884.
A restricted role for sperm-borne microRNAs in mammalian fertilization.Crossref | GoogleScholarGoogle Scholar |

Balzer, E., and Moss, E. G. (2007). Localization of the developmental timing regulator Lin28 to mRNP complexes, P-bodies and stress granules. RNA Biol. 4, 16–25.
Localization of the developmental timing regulator Lin28 to mRNP complexes, P-bodies and stress granules.Crossref | GoogleScholarGoogle Scholar |

Bao, J., Li, D., Wang, L., Wu, J., Hu, Y., Wang, Z., Chen, Y., Cao, X., Jiang, C., Yan, W., and 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, 21 686–21 698.
MicroRNA-449 and microRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway.Crossref | GoogleScholarGoogle Scholar |

Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.
MicroRNAs: target recognition and regulatory functions.Crossref | GoogleScholarGoogle Scholar |

Belleannée, C., Legare, C., Calvo, E., Thimon, V., and Sullivan, R. (2013). microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum. Reprod. 28, 1455–1467.
microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy.Crossref | GoogleScholarGoogle Scholar |

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., and Hannon, G. J. (2003). Dicer is essential for mouse development. Nat. Genet. 35, 215–217.
Dicer is essential for mouse development.Crossref | GoogleScholarGoogle Scholar |

Björk, J. K., Sandqvist, A., Elsing, A. N., Kotaja, N., and Sistonen, L. (2010). miR-18, a member of Oncomir-1, targets heat shock transcription factor 2 in spermatogenesis. Development 137, 3177–3184.
miR-18, a member of Oncomir-1, targets heat shock transcription factor 2 in spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

Braun, R. E. (1998). Post-transcriptional control of gene expression during spermatogenesis. Semin. Cell Dev. Biol. 9, 483–489.
Post-transcriptional control of gene expression during spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

Chevillet, J. R., Kang, Q., Ruf, I. K., Briggs, H. A., Vojtech, L. N., Hughes, S. M., Cheng, H. H., Arroyo, J. D., Meredith, E. K., Gallichotte, E. N., Pogosova-Agadjanyan, E. L., Morrissey, C., Stirewalt, D. L., Hladik, F., Yu, E. Y., Higano, C. S., and Tewari, M. (2014). Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc. Natl Acad. Sci. USA 111, 14 888–14 893.
Quantitative and stoichiometric analysis of the microRNA content of exosomes.Crossref | GoogleScholarGoogle Scholar |

Chieffi, P., Battista, S., Barchi, M., Di Agostino, S., Pierantoni, G. M., Fedele, M., Chiariotti, L., Tramontano, D., and Fusco, A. (2002). HMGA1 and HMGA2 protein expression in mouse spermatogenesis. Oncogene 21, 3644–3650.
HMGA1 and HMGA2 protein expression in mouse spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

Chim, S. S., Shing, T. K., Hung, E. C., Leung, T. Y., Lau, T. K., Chiu, R. W., and Lo, Y. M. (2008). Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem. 54, 482–490.
Detection and characterization of placental microRNAs in maternal plasma.Crossref | GoogleScholarGoogle Scholar |

Curry, E., Ellis, S. E., and Pratt, S. L. (2009). Detection of porcine sperm microRNAs using a heterologous microRNA microarray and reverse transcriptase polymerase chain reaction. Mol. Reprod. Dev. 76, 218–219.
Detection of porcine sperm microRNAs using a heterologous microRNA microarray and reverse transcriptase polymerase chain reaction.Crossref | GoogleScholarGoogle Scholar |

Curry, E., Safranski, T. J., and Pratt, S. L. (2011). Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76, 1532–1539.
Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility.Crossref | GoogleScholarGoogle Scholar |

Dai, L., Tsai-Morris, C. H., Sato, H., Villar, J., Kang, J. H., Zhang, J., and Dufau, M. L. (2011). Testis-specific miRNA-469 up-regulated in gonadotropin-regulated testicular RNA helicase (GRTH/DDX25)-null mice silences transition protein 2 and protamine 2 messages at sites within coding region: implications of its role in germ cell development. J. Biol. Chem. 286, 44 306–44 318.
Testis-specific miRNA-469 up-regulated in gonadotropin-regulated testicular RNA helicase (GRTH/DDX25)-null mice silences transition protein 2 and protamine 2 messages at sites within coding region: implications of its role in germ cell development.Crossref | GoogleScholarGoogle Scholar |

Das, P. J., Paria, N., Gustafson-Seabury, A., Vishnoi, M., Chaki, S. P., Love, C. C., Varner, D. D., Chowdhary, B. P., and Raudsepp, T. (2010). Total RNA isolation from stallion sperm and testis biopsies. Theriogenology 74, 1099–1106.e2.
Total RNA isolation from stallion sperm and testis biopsies.Crossref | GoogleScholarGoogle Scholar |

Eickhoff, R., Jennemann, G., Hoffbauer, G., Schuring, M. P., Kaltner, H., Sinowatz, F., Gabius, H. J., and Seitz, J. (2006). Immunohistochemical detection of macrophage migration inhibitory factor in fetal and adult bovine epididymis: release by the apocrine secretion mode? Cells Tissues Organs 182, 22–31.
Immunohistochemical detection of macrophage migration inhibitory factor in fetal and adult bovine epididymis: release by the apocrine secretion mode?Crossref | GoogleScholarGoogle Scholar |

Faller, M., and Guo, F. (2008). MicroRNA biogenesis: there’s more than one way to skin a cat. Biochim. Biophys. Acta 1779, 663–667.
MicroRNA biogenesis: there’s more than one way to skin a cat.Crossref | GoogleScholarGoogle Scholar |

Friedman, R. C., Farh, K. K., Burge, C. B., and Bartel, D. P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92–105.
Most mammalian mRNAs are conserved targets of microRNAs.Crossref | GoogleScholarGoogle Scholar |

Gilbert, I., Bissonnette, N., Boissonneault, G., Vallee, M., and Robert, C. (2007). A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction 133, 1073–1086.
A molecular analysis of the population of mRNA in bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Govindaraju, A., Uzun, A., Robertson, L., Atli, M. O., Kaya, A., Topper, E., Crate, E. A., Padbury, J., Perkins, A., and Memili, E. (2012). Dynamics of microRNAs in bull spermatozoa. Reprod. Biol. Endocrinol. 10, 82.
Dynamics of microRNAs in bull spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Griffiths-Jones, S. (2004). The microRNA registry. Nucleic Acids Res. 32, D109–D111.
The microRNA registry.Crossref | GoogleScholarGoogle Scholar |

Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A., and Enright, A. J. (2006). miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140–D144.
miRBase: microRNA sequences, targets and gene nomenclature.Crossref | GoogleScholarGoogle Scholar |

Hagan, J. P., Piskounova, E., and Gregory, R. I. (2009). Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 16, 1021–1025.
Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar |

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., and Surani, M. A. (2008). MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3, e1738.
MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

He, Z., Jiang, J., Kokkinaki, M., Tang, L., Zeng, W., Gallicano, I., Dobrinski, I., and Dym, M. (2013). MiRNA-20 and miRNA-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem Cells 31, 2205–2217.
MiRNA-20 and miRNA-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1.Crossref | GoogleScholarGoogle Scholar |

Heo, I., Joo, C., Cho, J., Ha, M., Han, J., and Kim, V. N. (2008). Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol. Cell 32, 276–284.
Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA.Crossref | GoogleScholarGoogle Scholar |

Hu, L., Wu, C., Guo, C., Li, H., and Xiong, C. (2014). Identification of microRNAs predominately derived from testis and epididymis in human seminal plasma. Clin. Biochem. 47, 967–972.
Identification of microRNAs predominately derived from testis and epididymis in human seminal plasma.Crossref | GoogleScholarGoogle Scholar |

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., and Marsh, C. B. (2008). Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3, e3694.
Detection of microRNA expression in human peripheral blood microvesicles.Crossref | GoogleScholarGoogle Scholar |

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

Jodar, M., Kalko, S., Castillo, J., Ballesca, J. L., and Oliva, R. (2012). Differential RNAs in the sperm cells of asthenozoospermic patients. Hum. Reprod. 27, 1431–1438.
Differential RNAs in the sperm cells of asthenozoospermic patients.Crossref | GoogleScholarGoogle Scholar |

Kawamata, T., and Tomari, Y. (2010). Making RISC. Trends Biochem. Sci. 35, 368–376.
Making RISC.Crossref | GoogleScholarGoogle Scholar |

Kawano, M., Kawaji, H., Grandjean, V., Kiani, J., and Rassoulzadegan, M. (2012). Novel small noncoding RNAs in mouse spermatozoa, zygotes and early embryos. PLoS One 7, e44542.
Novel small noncoding RNAs in mouse spermatozoa, zygotes and early embryos.Crossref | GoogleScholarGoogle Scholar |

Kimmins, S., and Sassone-Corsi, P. (2005). Chromatin remodelling and epigenetic features of germ cells. Nature 434, 583–589.
Chromatin remodelling and epigenetic features of germ cells.Crossref | GoogleScholarGoogle Scholar |

Kimmins, S., Kotaja, N., Davidson, I., and Sassone-Corsi, P. (2004). Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 128, 5–12.
Testis-specific transcription mechanisms promoting male germ-cell differentiation.Crossref | GoogleScholarGoogle Scholar |

Klein, U., Lia, M., Crespo, M., Siegel, R., Shen, Q., Mo, T., Ambesi-Impiombato, A., Califano, A., Migliazza, A., Bhagat, G., and Dalla-Favera, R. (2010). The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17, 28–40.

Kloosterman, W. P., and Plasterk, R. H. (2006). The diverse functions of microRNAs in animal development and disease. Dev. Cell 11, 441–450.
The diverse functions of microRNAs in animal development and disease.Crossref | GoogleScholarGoogle Scholar |

Kornfeld, J. W., Baitzel, C., Konner, A. C., Nicholls, H. T., Vogt, M. C., Herrmanns, K., Scheja, L., Haumaitre, C., Wolf, A. M., Knippschild, U., Seibler, J., Cereghini, S., Heeren, J., Stoffel, M., and Bruning, J. C. (2013). Obesity-induced overexpression of miR-802 impairs glucose metabolism through silencing of Hnf1b. Nature 494, 111–115.
Obesity-induced overexpression of miR-802 impairs glucose metabolism through silencing of Hnf1b.Crossref | GoogleScholarGoogle Scholar |

Krawetz, S. A., Kruger, A., Lalancette, C., Tagett, R., Anton, E., Draghici, S., and Diamond, M. P. (2011). A survey of small RNAs in human sperm. Hum. Reprod. 26, 3401–3412.
A survey of small RNAs in human sperm.Crossref | GoogleScholarGoogle Scholar |

Lalancette, C., Miller, D., Li, Y., and Krawetz, S. A. (2008). Paternal contributions: new functional insights for spermatozoal RNA. J. Cell. Biochem. 104, 1570–1579.
Paternal contributions: new functional insights for spermatozoal RNA.Crossref | GoogleScholarGoogle Scholar |

Lee, Y. S., and Dutta, A. (2007). The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21, 1025–1030.
The tumor suppressor microRNA let-7 represses the HMGA2 oncogene.Crossref | GoogleScholarGoogle Scholar |

Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H., and Kim, V. N. (2004). MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051–4060.
MicroRNA genes are transcribed by RNA polymerase II.Crossref | GoogleScholarGoogle Scholar |

Liu, J., Carmell, M. A., Rivas, F. V., Marsden, C. G., Thomson, J. M., Song, J. J., Hammond, S. M., Joshua-Tor, L., and Hannon, G. J. (2004). Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437–1441.
Argonaute2 is the catalytic engine of mammalian RNAi.Crossref | GoogleScholarGoogle Scholar |

Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A., Downing, J. R., Jacks, T., Horvitz, H. R., and Golub, T. R. (2005). MicroRNA expression profiles classify human cancers. Nature 435, 834–838.
MicroRNA expression profiles classify human cancers.Crossref | GoogleScholarGoogle Scholar |

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

Luo, Z., Liu, Y., Chen, L., Ellis, M., Li, M., Wang, J., Zhang, Y., Fu, P., Wang, K., Li, X., and Wang, L. (2015). microRNA profiling in three main stages during porcine spermatogenesis. J. Assist. Reprod. Genet. 32, 451–460.
microRNA profiling in three main stages during porcine spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

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

McIver, S. C., Roman, S. D., Nixon, B., and McLaughlin, E. A. (2012). miRNA and mammalian male germ cells. Hum. Reprod. Update 18, 44–59.
miRNA and mammalian male germ cells.Crossref | GoogleScholarGoogle Scholar |

Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G., and Tuschl, T. (2004). Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185–197.
Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs.Crossref | GoogleScholarGoogle Scholar |

Miller, D., Tang, P. Z., Skinner, C., and Lilford, R. (1994). Differential RNA fingerprinting as a tool in the analysis of spermatozoal gene expression. Hum. Reprod. 9, 864–869.

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., and Tewari, M. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl Acad. Sci. USA 105, 10 513–10 518.
Circulating microRNAs as stable blood-based markers for cancer detection.Crossref | GoogleScholarGoogle Scholar |

Montjean, D., De La Grange, P., Gentien, D., Rapinat, A., Belloc, S., Cohen-Bacrie, P., Menezo, Y., and Benkhalifa, M. (2012). Sperm transcriptome profiling in oligozoospermia. J. Assist. Reprod. Genet. 29, 3–10.
Sperm transcriptome profiling in oligozoospermia.Crossref | GoogleScholarGoogle Scholar |

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

Niu, Z., Goodyear, S. M., Rao, S., Wu, X., Tobias, J. W., Avarbock, M. R., and Brinster, R. L. (2011). MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc. Natl Acad. Sci. USA 108, 12 740–12 745.
MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells.Crossref | GoogleScholarGoogle Scholar |

Okamura, K., Hagen, J. W., Duan, H., Tyler, D. M., and Lai, E. C. (2007). The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89–100.
The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila.Crossref | GoogleScholarGoogle Scholar |

Ostermeier, G. C., Goodrich, R. J., Diamond, M. P., Dix, D. J., and Krawetz, S. A. (2005). Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil. Steril. 83, 1687–1694.
Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility.Crossref | GoogleScholarGoogle Scholar |

Panneerdoss, S., Chang, Y. F., Buddavarapu, K. C., Chen, H. I., Shetty, G., Wang, H., Chen, Y., Kumar, T. R., and Rao, M. K. (2012). Androgen-responsive microRNAs in mouse Sertoli cells. PLoS One 7, e41146.
Androgen-responsive microRNAs in mouse Sertoli cells.Crossref | GoogleScholarGoogle Scholar |

Park, S. M., Shell, S., Radjabi, A. R., Schickel, R., Feig, C., Boyerinas, B., Dinulescu, D. M., Lengyel, E., and Peter, M. E. (2007). Let-7 prevents early cancer progression by suppressing expression of the embryonic gene HMGA2. Cell Cycle 6, 2585–2590.
Let-7 prevents early cancer progression by suppressing expression of the embryonic gene HMGA2.Crossref | GoogleScholarGoogle Scholar |

Park, J. E., Heo, I., Tian, Y., Simanshu, D. K., Chang, H., Jee, D., Patel, D. J., and Kim, V. N. (2011). Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature 475, 201–205.
Dicer recognizes the 5′ end of RNA for efficient and accurate processing.Crossref | GoogleScholarGoogle Scholar |

Platts, A. E., Dix, D. J., Chemes, H. E., Thompson, K. E., Goodrich, R., Rockett, J. C., Rawe, V. Y., Quintana, S., Diamond, M. P., Strader, L. F., and Krawetz, S. A. (2007). Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum. Mol. Genet. 16, 763–773.
Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs.Crossref | GoogleScholarGoogle Scholar |

Reeves, R., and Beckerbauer, L. (2001). HMGI/Y proteins: flexible regulators of transcription and chromatin structure. Biochim. Biophys. Acta 1519, 13–29.
HMGI/Y proteins: flexible regulators of transcription and chromatin structure.Crossref | GoogleScholarGoogle Scholar |

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

Ronquist, G. K., Larsson, A., Ronquist, G., Isaksson, A., Hreinsson, J., Carlsson, L., and Stavreus-Evers, A. (2011). Prostasomal DNA characterization and transfer into human sperm. Mol. Reprod. Dev. 78, 467–476.
Prostasomal DNA characterization and transfer into human sperm.Crossref | GoogleScholarGoogle Scholar |

Ruby, J. G., Jan, C. H., and Bartel, D. P. (2007). Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83–86.
Intronic microRNA precursors that bypass Drosha processing.Crossref | GoogleScholarGoogle Scholar |

Salas-Huetos, A., Blanco, J., Vidal, F., Mercader, J. M., Garrido, N., and Anton, E. (2014). New insights into the expression profile and function of micro-ribonucleic acid in human spermatozoa. Fertil. Steril. 102, 213–222.e4.
New insights into the expression profile and function of micro-ribonucleic acid in human spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58–63.
Widespread changes in protein synthesis induced by microRNAs.Crossref | GoogleScholarGoogle Scholar |

Skog, J., Wurdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Sena-Esteves, M., Curry, W. T., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470–1476.
Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers.Crossref | GoogleScholarGoogle Scholar |

Sohel, M. M., Hoelker, M., Noferesti, S. S., Salilew-Wondim, D., Tholen, E., Looft, C., Rings, F., Uddin, M. J., Spencer, T. E., Schellander, K., and Tesfaye, D. (2013). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One 8, e78505.
Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |

Stowe, H. M., Curry, E., Calcatera, S. M., Krisher, R. L., Paczkowski, M., and Pratt, S. L. (2012). Cloning and expression of porcine Dicer and the impact of developmental stage and culture conditions on microRNA expression in porcine embryos. Gene 501, 198–205.
Cloning and expression of porcine Dicer and the impact of developmental stage and culture conditions on microRNA expression in porcine embryos.Crossref | GoogleScholarGoogle Scholar |

Stowe, H. M., Miller, M., Burns, M. G., Calcatera, S. M., Andrae, J. G., Aiken, G. E., Schrick, F. N., Cushing, T., Bridges, W. C., and Pratt, S. L. (2013). Effects of fescue toxicosis on bull growth, semen characteristics, and breeding soundness evaluation. J. Anim. Sci. 91, 3686–3692.
Effects of fescue toxicosis on bull growth, semen characteristics, and breeding soundness evaluation.Crossref | GoogleScholarGoogle Scholar |

Stowe, H. M., Calcatera, S. M., Dimmick, M. A., Andrae, J. G., Duckett, S. K., and Pratt, S. L. (2014). The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression. PLoS One 9, e113163.
The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression.Crossref | GoogleScholarGoogle Scholar |

Suh, N., and Blelloch, R. (2011). Small RNAs in early mammalian development: from gametes to gastrulation. Development 138, 1653–1661.
Small RNAs in early mammalian development: from gametes to gastrulation.Crossref | GoogleScholarGoogle Scholar |

Sullivan, R., and Saez, F. (2013). Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction 146, R21–R35.
Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology.Crossref | GoogleScholarGoogle Scholar |

Tessari, M. A., Gostissa, M., Altamura, S., Sgarra, R., Rustighi, A., Salvagno, C., Caretti, G., Imbriano, C., Mantovani, R., Del Sal, G., Giancotti, V., and Manfioletti, G. (2003). Transcriptional activation of the cyclin A gene by the architectural transcription factor HMGA2. Mol. Cell. Biol. 23, 9104–9116.
Transcriptional activation of the cyclin A gene by the architectural transcription factor HMGA2.Crossref | GoogleScholarGoogle Scholar |

Thornton, J. E., and Gregory, R. I. (2012). How does Lin28 let-7 control development and disease? Trends Cell Biol. 22, 474–482.
How does Lin28 let-7 control development and disease?Crossref | GoogleScholarGoogle Scholar |

Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., and Lotvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659.
Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.Crossref | GoogleScholarGoogle Scholar |

van Rooij, E., and Olson, E. N. (2012). MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat. Rev. Drug Discov. 11, 860–872.
MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles.Crossref | GoogleScholarGoogle Scholar |

Vijayaraghavan, S., Mohan, J., Gray, H., Khatra, B., and Carr, D. W. (2000). A role for phosphorylation of glycogen synthase kinase-3alpha in bovine sperm motility regulation. Biol. Reprod. 62, 1647–1654.
A role for phosphorylation of glycogen synthase kinase-3alpha in bovine sperm motility regulation.Crossref | GoogleScholarGoogle Scholar |

Viswanathan, S. R., and Daley, G. Q. (2010). Lin28: a microRNA regulator with a macro role. Cell 140, 445–449.
Lin28: a microRNA regulator with a macro role.Crossref | GoogleScholarGoogle Scholar |

Viswanathan, S. R., Powers, J. T., Einhorn, W., Hoshida, Y., Ng, T. L., Toffanin, S., O’Sullivan, M., Lu, J., Phillips, L. A., Lockhart, V. L., Shah, S. P., Tanwar, P. S., Mermel, C. H., Beroukhim, R., Azam, M., Teixeira, J., Meyerson, M., Hughes, T. P., Llovet, J. M., Radich, J., Mullighan, C. G., Golub, T. R., Sorensen, P. H., and Daley, G. Q. (2009). Lin28 promotes transformation and is associated with advanced human malignancies. Nat. Genet. 41, 843–848.
Lin28 promotes transformation and is associated with advanced human malignancies.Crossref | GoogleScholarGoogle Scholar |

Vojtech, L., Woo, S., Hughes, S., Levy, C., Ballweber, L., Sauteraud, R. P., Strobl, J., Westerberg, K., Gottardo, R., Tewari, M., and Hladik, F. (2014). Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 42, 7290–7304.
Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions.Crossref | GoogleScholarGoogle Scholar |

Wang, L., and Xu, C. (2015). Role of microRNAs in mammalian spermatogenesis and testicular germ cell tumors. Reproduction 149, R127–R137.
Role of microRNAs in mammalian spermatogenesis and testicular germ cell tumors.Crossref | GoogleScholarGoogle Scholar |

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., and Zhang, C. (2011). Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clin. Chem. 57, 1722–1731.
Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility.Crossref | GoogleScholarGoogle Scholar |

Weber, J. A., Baxter, D. H., Zhang, S., Huang, D. Y., Huang, K. H., Lee, M. J., Galas, D. J., and Wang, K. (2010). The microRNA spectrum in 12 body fluids. Clin. Chem. 56, 1733–1741.
The microRNA spectrum in 12 body fluids.Crossref | GoogleScholarGoogle Scholar |

West, J. A., Viswanathan, S. R., Yabuuchi, A., Cunniff, K., Takeuchi, A., Park, I. H., Sero, J. E., Zhu, H., Perez-Atayde, A., Frazier, A. L., Surani, M. A., and Daley, G. Q. (2009). A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460, 909–913.

Wu, W., Qin, Y., Li, Z., Dong, J., Dai, J., Lu, C., Guo, X., Zhao, Y., Zhu, Y., Zhang, W., Hang, B., Sha, J., Shen, H., Xia, Y., Hu, Z., and 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. Hum. Reprod. 28, 1827–1836.
Genome-wide microRNA expression profiling in idiopathic non-obstructive azoospermia: significant up-regulation of miR-141, miR-429 and miR-7-1-3p.Crossref | GoogleScholarGoogle Scholar |

Yan, N., Lu, Y., Sun, H., Tao, D., Zhang, S., Liu, W., and Ma, Y. (2007). A microarray for microRNA profiling in mouse testis tissues. Reproduction 134, 73–79.
A microarray for microRNA profiling in mouse testis tissues.Crossref | GoogleScholarGoogle Scholar |

Yan, W., Morozumi, K., Zhang, J., Ro, S., Park, C., and Yanagimachi, R. (2008). Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and microRNAs in the sperm nuclei. Biol. Reprod. 78, 896–902.
Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and microRNAs in the sperm nuclei.Crossref | GoogleScholarGoogle Scholar |

Yan, N., Lu, Y., Sun, H., Qiu, W., Tao, D., Liu, Y., Chen, H., Yang, Y., Zhang, S., Li, X., and Ma, Y. (2009). Microarray profiling of microRNAs expressed in testis tissues of developing primates. J. Assist. Reprod. Genet. 26, 179–186.
Microarray profiling of microRNAs expressed in testis tissues of developing primates.Crossref | GoogleScholarGoogle Scholar |

Yang, Q. E., Racicot, K. E., Kaucher, A. V., Oatley, M. J., and Oatley, J. M. (2013). MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells. Development 140, 280–290.
MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells.Crossref | GoogleScholarGoogle Scholar |

Yi, R., Qin, Y., Macara, I. G., and Cullen, B. R. (2003). Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011–3016.
Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs.Crossref | GoogleScholarGoogle Scholar |

Yoda, M., Kawamata, T., Paroo, Z., Ye, X., Iwasaki, S., Liu, Q., and Tomari, Y. (2010). ATP-dependent human RISC assembly pathways. Nat. Struct. Mol. Biol. 17, 17–23.
ATP-dependent human RISC assembly pathways.Crossref | GoogleScholarGoogle Scholar |

Yu, Z., Raabe, T., and 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.
MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage.Crossref | GoogleScholarGoogle Scholar |

Zheng, K., Wu, X., Kaestner, K. H., and Wang, P. J. (2009). The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev. Biol. 9, 38.
The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse.Crossref | GoogleScholarGoogle Scholar |