Low physiological levels of prostaglandins E2 and F2α improve human sperm functions
Mariana Rios A , Daniela V. Carreño A , Carolina Oses A , Nelson Barrera A , Bredford Kerr B and Manuel Villalón A CA Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Alameda 340, 8331150, Santiago, Chile.
B Centro de Estudios Científicos, Valdivia, Chile.
C Corresponding author. Email: mvillalon@bio.puc.cl
Reproduction, Fertility and Development 28(4) 434-439 https://doi.org/10.1071/RD14035
Submitted: 12 February 2014 Accepted: 23 June 2014 Published: 13 August 2014
Abstract
Prostaglandins (PGs) have been reported to be present in the seminal fluid and cervical mucus, affecting different stages of sperm maturation from spermatogenesis to the acrosome reaction. This study assessed the effects of low physiological PGE2 and PGF2α concentrations on human sperm motility and on the ability of the spermatozoa to bind to the zona pellucida (ZP). Human spermatozoa were isolated from seminal samples with normal concentration and motility parameters and incubated with 1 μM PGE2, 1 μM PGF2α or control solution to determine sperm motility and the ability to bind to human ZP. The effects of both PGs on intracellular calcium levels were determined. Incubation for 2 or 18 h with PGE2 or PGF2α resulted in a significant (P < 0.05) increase in the percentage of spermatozoa with progressive motility. In contrast with PGF2α, PGE2 alone induced an increase in sperm intracellular calcium levels; however, the percentage of sperm bound to the human ZP was doubled for both PGs. These results indicate that incubation of human spermatozoa with low physiological levels of PGE2 or PGF2α increases sperm functions and could improve conditions for assisted reproduction protocols.
Additional keywords: assisted reproduction technologies, human spermatozoa.
References
Aitken, R. J., and Kelly, R. W. (1985). Analysis of the direct effects of prostaglandins on human sperm function. J. Reprod. Fertil. 73, 139–146.| Analysis of the direct effects of prostaglandins on human sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht1Khurg%3D&md5=ec7ebf800f60c7f8750fb44ec455d5f7CAS | 3855460PubMed |
Aitken, R. J., Irvine, S., and Kelly, R. W. (1986). Significance of intracellular calcium and cyclic adenosine 3′,5′-monophosphate in the mechanisms by which prostaglandins influence human sperm function. J. Reprod. Fertil. 77, 451–462.
| Significance of intracellular calcium and cyclic adenosine 3′,5′-monophosphate in the mechanisms by which prostaglandins influence human sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltVyktrg%3D&md5=23af57af89c5c202037a5b2b725f8d1eCAS | 3016256PubMed |
Akhondi, M. A., Chapple, C., and Moore, H. D. (1997). Prolonged survival of human spermatozoa when co-incubated with epididymal cell cultures. Hum. Reprod. 12, 514–522.
| Prolonged survival of human spermatozoa when co-incubated with epididymal cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3nslSlsg%3D%3D&md5=e880ece5113ca553cddf76290848cb34CAS | 9130753PubMed |
Alasmari, W., Barratt, C. L., Publicover, S. J., Whalley, K. M., Foster, E., Kay, V., Martins da Silva, S., and Oxenham, S. K. (2013). The clinical significance of calcium-signalling pathways mediating human sperm hyperactivation. Hum. Reprod. 28, 866–876.
| The clinical significance of calcium-signalling pathways mediating human sperm hyperactivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFKmsbY%3D&md5=64ccf98644bea756fd8ff561e16dee38CAS | 23406974PubMed |
Barrera, N. P., Morales, B., and Villalon, M. (2007). ATP and adenosine trigger the interaction of plasma membrane IP3 receptors with protein kinase A in oviductal ciliated cells. Biochem. Biophys. Res. Commun. 364, 815–821.
| ATP and adenosine trigger the interaction of plasma membrane IP3 receptors with protein kinase A in oviductal ciliated cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaltrrL&md5=52daa5bbebca6dd01963a0ad8a307631CAS | 18163243PubMed |
Bendvold, E., Svanborg, K., Eneroth, P., Gottlieb, C., and Byqdeman, M. (1984). The natural variations in prostaglandin concentration in human seminal fluid and its relation to sperm quality. Fertil. Steril. 41, 743–747.
| 1:CAS:528:DyaL2cXktVWlsLo%3D&md5=32cd29261c9adf5494001f2dce07af19CAS | 6546921PubMed |
Brokaw, C. J. (1987). Regulation of sperm flagellar motility by calcium and cAMP-dependant phosphorylation. J. Cell. Biochem. 35, 175–184.
| Regulation of sperm flagellar motility by calcium and cAMP-dependant phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjsl2n&md5=61dd8b1b742942cf310a933c3dd6cb24CAS | 2826504PubMed |
Burkman, L. J., Coddington, C. C., Franken, D. R., Kruger, T. F., Rosenwaks, Z., and Hodgen, G. D. (1988). The hemizona assay (HZA): development of a diagnostic test for the binding of human spermatozoa to the human hemizona pellucida to predict fertilization potential. Fertil. Steril. 49, 688–697.
| 1:STN:280:DyaL1c7mslahuw%3D%3D&md5=3ed7f5bf1bd3ffb0d27ff30ad3acce81CAS | 3350165PubMed |
Collins, D., Hogan, A. M., Skelly, M. M., Baird, A. W., and Winter, D. C. (2009). Cyclic AMP-mediated chloride secretion is induced by prostaglandin F2α in human isolated colon. Br. J. Pharmacol. 158, 1771–1776.
| Cyclic AMP-mediated chloride secretion is induced by prostaglandin F2α in human isolated colon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Whtr%2FE&md5=7ecc8f88817d5a4d4f2a25ab23c8aff5CAS | 19889058PubMed |
Cross, N. L., Morales, P., Overstreet, J. W., and Hanson, F. W. (1988). Induction of acrosome reactions by the human zona pellucida. Biol. Reprod. 38, 235–244.
| Induction of acrosome reactions by the human zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3gvFKntw%3D%3D&md5=ffcffb2d1c969a31b524228c73c2aea7CAS | 3365471PubMed |
Darszon, A., Nishigaki, T., Beltran, C., and Treviño, C. L. (2011). Calcium channels in the development, maturation and function of spermatozoa. Physiol. Rev. 91, 1305–1355.
| Calcium channels in the development, maturation and function of spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOjsbrK&md5=a0a46fd9dc43b7f1a64f39b66a14a679CAS | 22013213PubMed |
Fujino, H., Srinivasan, D., Pierce, K. L., and Regan, J. W. (2000). Differential regulation of prostaglandin receptor isoforms by protein kinase C. Mol. Pharmacol. 57, 353–358.
| 1:CAS:528:DC%2BD3cXhtVakt7o%3D&md5=28087afacc0e43be784583148983a49bCAS | 10648645PubMed |
Gerozissis, K., Jouannet, P., Soufir, J. C., and Dray, F. (1982). Origin of prostaglandins in human semen. J. Reprod. Fertil. 65, 401–404.
| Origin of prostaglandins in human semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XkvVKjtLc%3D&md5=b79797decf9714fb6897554b4086becaCAS | 6896529PubMed |
Gottlieb, C., Svanborg, K., Eneroth, P., and Byqdeman, M. (1988). Effect of prostaglandins on human function in vitro and seminal adenosine triphosphate content. Fertil. Steril. 49, 322–327.
| 1:CAS:528:DyaL1cXhsVCjtLw%3D&md5=736806451f3c46508566ab59d057ddacCAS | 3338588PubMed |
Hayashi, S., Noda, Y., and Mori, T. (1988). Analysis of the role of prostaglandins in the fertilization process. Eur. J. Obstet. Gynecol. Reprod. Biol. 29, 287–297.
| Analysis of the role of prostaglandins in the fertilization process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtVygtLY%3D&md5=81e73f0c9781d2a87b568700aa61b3c0CAS | 3229543PubMed |
Herrero, M. B., Viggiano, J. M., Boquet, M., and Gimeno, M. A. (1997). Prostaglandins modulation of mouse and human sperm capacitation. Prostaglandins Leukot. Essent. Fatty Acids 57, 279–284.
| Prostaglandins modulation of mouse and human sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntFSntbw%3D&md5=473864586f84130a5e2a2f48ffa865a6CAS | 9384517PubMed |
Joyce, C. L., Nuzzo, N. A., Wilson, L., and Zaneveld, L. J. (1987). Evidence for a role of cyclooxygenase (prostaglandin synthetase) and prostaglandins in the sperm acrosome reaction and fertilization. J. Androl. 8, 74–82.
| 1:CAS:528:DyaL2sXhvV2kt7s%3D&md5=ba8608cfd079949950afb348f17e8b30CAS | 3108222PubMed |
Kervancioglu, M. E., Saridogan, E., Atasu, T., Camlibel, T., Demircan, A., Sarikamis, B., and Djahanbakhch, O. (1997). Human Fallopian tube epithelial cell co-culture increases fertilization rates in male factor infertility but not in tubal or unexplained infertility. Hum. Reprod. 12, 1253–1258.
| Human Fallopian tube epithelial cell co-culture increases fertilization rates in male factor infertility but not in tubal or unexplained infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szmsFSrtQ%3D%3D&md5=ad856769f38f7939eda9b5c22755d716CAS | 9222012PubMed |
Killian, G. J. (2004). Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim. Reprod. Sci. 82–83, 141–153.
| Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development.Crossref | GoogleScholarGoogle Scholar | 15271449PubMed |
Kodithuwakku, S. P., Miyamoto, A., and Wijayagunawardane, M. P. (2007). Spermatozoa stimulate prostaglandin synthesis and secretion in bovine oviduct epithelial cells. Reproduction 133, 1087–1094.
| Spermatozoa stimulate prostaglandin synthesis and secretion in bovine oviduct epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGnu7Y%3D&md5=f73fe24ee35aeabe71f7a1f6be30c97dCAS | 17636163PubMed |
Lippes (1979) Analysis of human oviductal fluid for low molecular weight compounds. In ‘The Biology of the Fluid in the Female Genital Tract’. (Eds F. K. Beller and G. F. B. Schumacher.) pp. 373–387. (Elsevier: North Holland.)
Lishko, P. V., Botchkina, I. L., and Kirichok, Y. (2011). Progesterone activates the principal Ca2+ channel of human sperm. Nature 471, 387–391.
| Progesterone activates the principal Ca2+ channel of human sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVKru7o%3D&md5=0903acede00f597cbc0a81cc4724583bCAS | 21412339PubMed |
Meizel, S., and Turner, K. O. (1984). The effects of products and inhibitors of arachidonic acid metabolism on the hamster sperm acrosome reaction. J. Exp. Zool. 231, 283–288.
| The effects of products and inhibitors of arachidonic acid metabolism on the hamster sperm acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1ersb0%3D&md5=47f96ad1b46aa840be6f8592dfc8c896CAS | 6434693PubMed |
Menegazzo, M., Zuccarello, D., Luca, G., Ferlin, A., Calvitti, M., Mancuso, F., Calafiore, R., and Foresta, C. (2011). Improvements in human sperm quality by long-term in vitro co-culture with isolated porcine Sertoli cells. Hum. Reprod. 26, 2598–2605.
| Improvements in human sperm quality by long-term in vitro co-culture with isolated porcine Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 21771775PubMed |
Morales, P., Cross, N. L., Overstreet, J. W., and Hanson, F. W. (1989). Acrosome intact and acrosime reacted human sperm can initiate binding to the zona pellucida. Dev. Biol. 133, 385–392.
| Acrosome intact and acrosime reacted human sperm can initiate binding to the zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M3ns1Kqsg%3D%3D&md5=a1be04ff0ab73cbb5df5dd1d390be958CAS | 2731635PubMed |
Morales, P., Vantman, D., Barros, C., and Vigil, P. (1991). Human spermatozoa selected by Percoll gradient or swim-up are equally capable of binding to the human zona pellucida and undergoing the acrosome reaction. Hum. Reprod. 6, 401–404.
| 1:STN:280:DyaK38%2FmsVOlsw%3D%3D&md5=d65b8a232d2334f9cf191df944301280CAS | 1659585PubMed |
Morales, P., Kerr, B., Oliva, C., Pizarro, E., and Kong, M. (1999). Gonadotropin-releasing hormone antagonists inhibit sperm binding to the human zona pellucida. Hum. Reprod. 14, 2069–2074.
| Gonadotropin-releasing hormone antagonists inhibit sperm binding to the human zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvVahtrw%3D&md5=473ba003132052b62bac191a35a6652eCAS | 10438428PubMed |
Morales, P., Pizarro, E., Kong, M., Kerr, B., Ceric, F., and Vigil, P. (2000). Gonadotropin-releasing hormone-stimulated sperm binding to the human zona is mediated by a calcium influx. Biol. Reprod. 63, 635–642.
| Gonadotropin-releasing hormone-stimulated sperm binding to the human zona is mediated by a calcium influx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltl2gurc%3D&md5=e48137e2275fc0e8351c31b95e34cdc7CAS | 10906075PubMed |
Overstreet, J. W., Yanagimachi, R., Katz, D. F., Hayashi, K., and Hanson, F. W. (1980). Penetration of human into the human zona pellucid and the zona-free hamster egg: a study of fertile donors and infertile patients. Fertil. Steril. 33, 534–542.
| 1:STN:280:DyaL3c7nvFaksQ%3D%3D&md5=eac3a5646134b8d09a64b58aa4cc05fbCAS | 7371883PubMed |
Ren, D., Navarro, B., Perez, G., Jackson, A. C., Hsu, S., Shi, Q., Tilly, J. L., and Clapham, D. E. (2001). A sperm ion channel required for sperm motility and male fertility. Nature 413, 603–609.
| A sperm ion channel required for sperm motility and male fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslehurk%3D&md5=e430686eccf4ca17d828b8250085b74aCAS | 11595941PubMed |
Rodriguez, P. C., Satorre, M. M., and Beconi, M. T. (2012). Effect of two intracellular calcium modulators on sperm motility and heparin-induced capacitation in cryopreserved bovine spermatozoa. Anim. Reprod. Sci. 131, 135–142.
| Effect of two intracellular calcium modulators on sperm motility and heparin-induced capacitation in cryopreserved bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVynsb4%3D&md5=1a90692e7b4d8e0631b94ea8767d207eCAS | 22516227PubMed |
Schaefer, M., Hofmann, T., Schultz, G., and Gudermann, T. (1998). A new prostaglandin E receptor mediates calcium influx and acrosome reaction in human spermatozoa. Proc. Natl Acad. Sci. USA 95, 3008–3013.
| A new prostaglandin E receptor mediates calcium influx and acrosome reaction in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitV2itrk%3D&md5=85963f49bebf68651bd971ee2df8e613CAS | 9501206PubMed |
Schlegel, W., Fischer, B., Beier, H. M., and Schneider, H. P. G. (1983). Effects on fertilization of rabbit of insemination with ejaculates treated with PG-dehydrogenase and antisense to PGE-2 and PGF2α. J. Reprod. Fertil. 68, 45–50.
| Effects on fertilization of rabbit of insemination with ejaculates treated with PG-dehydrogenase and antisense to PGE-2 and PGF2α.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktlelsLw%3D&md5=01eee3b7a1fd87772754304c95d65d5cCAS | 6573512PubMed |
Schuffner, A., Morshedi, M., Vaamonde, D., Duran, E. H., and Oehninger, S. (2002). Effect of different incubation conditions on phosphatidylserine externalization and motion parameters of purified fractions of highly motile human spermatozoa. J. Androl. 23, 194–201.
| 1:CAS:528:DC%2BD38XitVWqsLY%3D&md5=afdecfa9c3a16be6873158a369d7d63aCAS | 11868812PubMed |
Shalev, Y., Shemesh, M., Levinshal, T., Marcus, S., and Breitbart, H. (1994). Localization of cyclooxygenase and production of prostaglandins in bovine spermatozoa. J. Reprod. Fertil. 101, 405–413.
| Localization of cyclooxygenase and production of prostaglandins in bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmslarsLk%3D&md5=4634529fd55473c232e70aa8791a50efCAS | 7932376PubMed |
Shimizu, Y., Yorimitsu, A., Maruyama, Y., Kubota, T., Adso, T., and Bronson, R. A. (1998). Prostaglandins induce calcium influx in human spermatozoa. Mol. Hum. Reprod. 4, 555–561.
| Prostaglandins induce calcium influx in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktlaqsLg%3D&md5=7033de04b95e0df687bceed519adc532CAS | 9665338PubMed |
Wijayagunawardane, M. P., Miyamoto, A., Taquahashi, Y., Gabler, C., Acosta, T. J., Nishimura, M., Killian, G., and Sato, K. (2001). In vitro regulation of local secretion and contraction of the bovine oviduct: stimulation by luteinizing hormone, endothelin-1 and prostaglandins, and inhibition by oxytocin. J. Endocrinol. 168, 117–130.
| In vitro regulation of local secretion and contraction of the bovine oviduct: stimulation by luteinizing hormone, endothelin-1 and prostaglandins, and inhibition by oxytocin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVKjtg%3D%3D&md5=3d16b15ff5ed69d425808e9ec152c197CAS | 11139776PubMed |
World Health Organization (WHO). (2010) ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 5th edn. (WHO Press: Geneva.)