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Treatment of aromatase (CYP19A1) inhibitor reduces fertility in porcine sperm

Published online by Cambridge University Press:  26 January 2015

Jong-Nam Oh
Affiliation:
Department of Agricultural Biotechnology, Animal Biotechnology Major, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea.
Jae Yeon Hwang
Affiliation:
Department of Agricultural Biotechnology, Animal Biotechnology Major, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea.
Kwang-Hwan Choi
Affiliation:
Department of Agricultural Biotechnology, Animal Biotechnology Major, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea.
Chang-Kyu Lee*
Affiliation:
Department of Agricultural Biotechnology, Animal Biotechnology Major, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921Korea. Designed Animal and Transplantation Research Institute (DATRI), Institute of Green Bio Science and Technology, Seoul National University, Kangwon-do 232-916, Korea.
*
All correspondence to: Chang-Kyu Lee. Department of Agricultural Biotechnology, Animal Biotechnology Major, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921Korea. Tel: +82 2 880 4805. Fax: +82 2 873 4805. e-mail: [email protected]

Summary

To ascertain whether aromatase (CYP19A1) expression is linked to sperm fertility of pigs, the present study determined the expression of the CYP19A1 gene in porcine sperm and its relationship with fertilization in vitro. First, to investigate its role in fertility, the presence of CYP19A1 of mRNA and protein expression in porcine sperm were confirmed by real-time (RT) or quantitative polymerase chain reaction (q-PCR) and by western blots. The expression levels were determined quantitatively using two sperm groups recovered by a Percoll gradient, which revealed that the sperm group with a low density had a higher penetration rate than that of the high-density group (P < 0.05). However, the expression level of CYP19A1 was not significantly different between the two groups. Secondly, to examine the effect of aromatase activity on fertilization, fresh semen was treated with a steroidal inhibitor, exemestane (50 μM for 0.5 h), followed by the dose- and time-dependent viability test. Our results clearly showed that an exemestane treatment effect (P < 0.05) was found for both the sperm-penetration rate and the oocyte cleavage rate. These results indicated that CYP19A1 could be involved in sperm fertility and its expression in sperm plays an important role in fertilization.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

Abeydeera, L.R. & Day, B.N. (1997). Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified Tris-buffered medium with frozen–thawed ejaculated spermatozoa. Biol. Reprod. 57, 729–34.CrossRefGoogle Scholar
Aitken, R.J. & West, K.M. (1990). Analysis of the relationship between reactive oxygen species production and leucocyte infiltration in fractions of human semen separated on Percoll gradients. Int. J. Androl. 13, 433–51.Google Scholar
Akhtar, M., Calder, M.R., Corina, D.L. & Wright, J.N. (1982). Mechanistic studies on C-19 demethylation in oestrogen biosynthesis. Biochem. J. 201, 569–80.CrossRefGoogle ScholarPubMed
Aoki, V.W., Liu, L. & Carrell, D.T. (2005). Identification and evaluation of a novel sperm protamine abnormality in a population of infertile males. Hum. Reprod. 20, 1298–306.Google Scholar
Aquila, S., Sisci, D., Gentile, M., Carpino, A., Middea, E., Catalano, S., Rago, V. & Ando, S. (2003). Towards a physiological role for cytochrome P450 aromatase in ejaculated human sperm. Hum. Reprod. 18, 1650–9.CrossRefGoogle ScholarPubMed
Behringer, R.R., Eakin, G.S. & Renfree, M.B. (2006). Mammalian diversity: gametes, embryos and reproduction. Reprod. Fertil. Dev. 18, 99107.Google Scholar
Bilinska, B., Schmalz-Fraczek, B., Kotula, M. & Carreau, S. (2001). Photoperiod-dependent capability of androgen aromatization and the role of estrogens in the bank vole testis visualized by means of immunohistochemistry. Mol. Cell. Endocrinol. 178, 189–98.Google Scholar
Bissonnette, N., Levesque-Sergerie, J.P., Thibault, C. & Boissonneault, G. (2009). Spermatozoal transcriptome profiling for bull sperm motility: a potential tool to evaluate semen quality. Reproduction 138, 6580.Google Scholar
Boerke, A., Dieleman, S.J. & Gadella, B.M. (2007). A possible role for sperm RNA in early embryo development. Theriogenology 68 (Suppl 1), S147–55.CrossRefGoogle ScholarPubMed
Bujan, L., Mieusset, R., Audran, F., Lumbroso, S. & Sultan, C. (1993). Increased oestradiol level in seminal plasma in infertile men. Hum. Reprod. 8, 74–7.Google Scholar
Carani, C., Qin, K., Simoni, M., Faustini-Fustini, M., Serpente, S., Boyd, J., Korach, K.S. & Simpson, E.R. (1997). Effect of testosterone and estradiol in a man with aromatase deficiency. New Engl. J. Med. 337, 91–5.CrossRefGoogle Scholar
Carreau, S., Delalande, C., Silandre, D., Bourguiba, S. & Lambard, S. (2006). Aromatase and estrogen receptors in male reproduction. Mol. Cell. Endocrinol. 246, 65–8.Google Scholar
Carreau, S., Delalande, C. & Galeraud-Denis, I. (2009). Mammalian sperm quality and aromatase expression. Microsc. Res. Tech. 72, 552–7.CrossRefGoogle ScholarPubMed
D’Occhio, M.J., Hengstberger, K.J. & Johnston, S.D. (2007). Biology of sperm chromatin structure and relationship to male fertility and embryonic survival. Anim Reprod. Sci. 101, 117.Google Scholar
Feugang, J.M., Rodriguez-Osorio, N., Kaya, A., Wang, H., Page, G., Ostermeier, G.C., Topper, E.K. & Memili, E. (2010). Transcriptome analysis of bull spermatozoa: implications for male fertility. Reprod. Biomed. Online 21, 312–24.Google Scholar
Hong, Y. & Chen, S. (2006). Aromatase inhibitors: structural features and biochemical characterization. Ann. New York Acad. Sci. 1089, 237–51.Google Scholar
Hwang, J.Y., Mulligan, B.P., Kim, H.M., Yang, B.C. & Lee, C.K. (2013). Quantitative analysis of sperm mRNA in the pig: relationship with early embryo development and capacitation. Reprod. Fertil. Dev. 25, 807–17.CrossRefGoogle ScholarPubMed
Janulis, L., Bahr, J.M., Hess, R.A., Janssen, S., Osawa, Y. & Bunick, D. (1998). Rat testicular germ cells and epididymal sperm contain active P450 aromatase. J. Androl. 19, 6571.Google Scholar
Jodar, M., Selvaraju, S., Sendler, E., Diamond, M.P., Krawetz, S.A. & the Reproductive Medicine Network (2013). The presence, role and clinical use of spermatozoal RNAs. Hum. Reprod. Update 19, 604–24.Google Scholar
Johnson, L.A., Weitze, K.F., Fiser, P. & Maxwell, W.M. (2000). Storage of boar semen. Anim. Reprod. Sci. 62, 143–72.Google Scholar
Kashiwabara, S., Arai, Y., Kodaira, K. & Baba, T. (1990). Acrosin biosynthesis in meiotic and postmeiotic spermatogenic cells. Biochem. Biophys. Res. Commun. 173, 240–5.CrossRefGoogle ScholarPubMed
Kleene, K.C., Distel, R.J. & Hecht, N.B. (1984). Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev. Biol. 105, 71–9.CrossRefGoogle ScholarPubMed
Kumar, G., Patel, D. & Naz, R.K. (1993). c-MYC mRNA is present in human sperm cells. Cell. Mol. Biol. Res. 39, 111–7.Google Scholar
Kwon, W.S., Park, Y.J., El Mohamed, S.A. & Pang, M.G. (2013). Voltage-dependent anion channels are a key factor of male fertility. Fertil. Steril. 99, 354–61.Google Scholar
Lambard, S., Silandre, D., Delalande, C., Denis-Galeraud, I., Bourguiba, S. & Carreau, S. (2005). Aromatase in testis: expression and role in male reproduction. J. Steroid Biochem. Mol. Biol. 95, 63–9.Google Scholar
Liao, T.T., Xiang, Z., Zhu, W.B. & Fan, L.Q. (2009). Proteome analysis of round-headed and normal spermatozoa by 2-D fluorescence difference gel electrophoresis and mass spectrometry. Asian J. Androl. 11, 683–93.Google Scholar
Luboshitzky, R., Kaplan-Zverling, M., Shen-Orr, Z., Nave, R. & Herer, P. (2002). Seminal plasma androgen/oestrogen balance in infertile men. Int. J. Androl. 25, 345–51.Google Scholar
Mengual, L., Ballesca, J.L., Ascaso, C. & Oliva, R. (2003). Marked differences in protamine content and P1/P2 ratios in sperm cells from Percoll fractions between patients and controls. J. Androl. 24, 438–47.Google Scholar
Miller, W.R., Bartlett, J., Brodie, A.M., Brueggemeier, R.W., di Salle, E., Lonning, P.E., Llombart, A., Maass, N., Maudelonde, T., Sasano, H. & Goss, P.E. (2008). Aromatase inhibitors: are there differences between steroidal and nonsteroidal aromatase inhibitors and do they matter? The Oncologist 13, 829–37.CrossRefGoogle ScholarPubMed
Nolan, M.A., Babcock, D.F., Wennemuth, G., Brown, W., Burton, K.A. & McKnight, G.S. (2004). Sperm-specific protein kinase A catalytic subunit Ca2 orchestrates cAMP signaling for male fertility. Proc. Natl Acad. Sci. USA 101, 13483–8.Google Scholar
Park, C.H., Lee, S.G., Choi, D.H. & Lee, C.K. (2009). A modified swim-up method reduces polyspermy during in vitro fertilization of porcine oocytes. Anim. Reprod. Sci. 115, 169–81.Google Scholar
Park, C.H., Jeong, Y.H., Jeong, Y.I., Lee, S.Y., Jeong, Y.W., Shin, T., Kim, N.H., Jeung, E.B., Hyun, S.H., Lee, C.K., Lee, E. & Hwang, W.S. (2012a). X-linked gene transcription patterns in female and male in vivo, in vitro and cloned porcine individual blastocysts. PLoS One 7, e51398.Google Scholar
Park, Y.J., Kwon, W.S., Oh, S.A. & Pang, M.G. (2012b). Fertility-related proteomic profiling bull spermatozoa separated by Percoll. J. Prot. Res. 11, 4162–8.CrossRefGoogle ScholarPubMed
Parrish, J.J., Krogenaes, A. & Susko-Parrish, J.L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–69.Google Scholar
Petrunkina, A.M., Waberski, D., Gunzel-Apel, A.R. & Topfer-Petersen, E. (2007). Determinants of sperm quality and fertility in domestic species. Reproduction 134, 317.Google Scholar
Primakoff, P., Hyatt, H. & Tredick-Kline, J. (1987). Identification and purification of a sperm surface protein with a potential role in sperm–egg membrane fusion. J. Cell Biol. 104, 141–9.CrossRefGoogle ScholarPubMed
Rago, V., Aquila, S., Panza, R. & Carpino, A. (2007). Cytochrome P450arom, androgen and estrogen receptors in pig sperm. Reprod. Biol. Endocrinol. 5, 23.Google Scholar
Robertson, K.M., Simpson, E.R., Lacham-Kaplan, O. & Jones, M.E. (2001). Characterization of the fertility of male aromatase knockout mice. J. Androl. 22, 825–30.Google Scholar
Rodriguez-Martinez, H. (2007). State of the art in farm animal sperm evaluation. Reprod. Fertil. Dev. 19, 91101.Google Scholar
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swann, K. & Lai, F.A. (2002). PLC zeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.CrossRefGoogle ScholarPubMed
Simpson, E.R., Zhao, Y., Agarwal, V.R., Michael, M.D., Bulun, S.E., Hinshelwood, M.M., Graham-Lorence, S., Sun, T., Fisher, C.R., Qin, K. & Mendelson, C.R. (1997). Aromatase expression in health and disease. Recent Prog. Horm. Res. 52, 185213; discussion 213–4.Google Scholar
Suzuki, K. & Nagai, T. (2003). In vitro fertility and motility characteristics of frozen thawed boar epididymal spermatozoa separated by Percoll. Theriogenology 60, 14811494.Google Scholar
Swanson, W.J. & Vacquier, V.D. (2002). The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3, 137–44.Google Scholar
Tiwari, A., Singh, D., Kumar, O.S. & Sharma, M.K. (2008). Expression of cytochrome P450 aromatase transcripts in buffalo (Bubalus bubalis)-ejaculated spermatozoa and its relationship with sperm motility. Dom. Anim. Endocrinol. 34, 238–49.Google Scholar
Torgerson, D.G., Kulathinal, R.J. & Singh, R.S. (2002). Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes. Mol. Biol. Evol. 19, 1973–80.Google Scholar
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