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Regulation and disruption of hamster sperm hyperactivation by progesterone, 17β-estradiol and diethylstilbestrol

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Reproductive Medicine and Biology

Abstract

Purpose

Hyperactivation of hamster sperm is dose-dependently enhanced by progesterone (P) and 17β-estradiol (E). In the first part of the present study, enhancement of hyperactivation in response to the concentrations of P and E was examined in detail and in the second part, it was examined whether enhancement of hyperactivation by P and E was disrupted by diethylstilbestrol (DES).

Methods

Hamster spermatozoa were hyperactivated by incubation in modified Tyrode’s albumin lactate pyruvate medium with P, E and/or DES. After spermatozoa were recorded using a video-microscope, observations were quantified by manually counting the numbers of total, motile and hyperactivated spermatozoa.

Results

Hyperactivation was enhanced in response to the concentrations of P and E. When spermatozoa were exposed to DES with E, moreover, DES significantly and strongly suppressed P-enhanced hyperactivation by accelerating the effect of E, but DES itself only weakly suppressed P-enhanced hyperactivation.

Conclusions

Enhancement of hyperactivation was regulated by the concentrations of P and E, suggesting that in vivo hamster spermatozoa are hyperactivated through “monitoring” these concentrations in the oviduct. DES in combination with E suppressed P-enhanced hyperactivation, suggesting that DES significantly disrupts hyperactivation by acting as an accelerator of the effect of E.

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References

  1. Yanagimachi R. Mammalian fertilization. In: Knobil E, Neill JD, editors. The physiology of reproduction. Vol. 1, 2nd ed. New York: Raven Press; 1994. p. 189–317.

  2. Schillo KK. Reproductive physiology of mammals: from farm to field and beyond. New York: Delmar; 2009.

    Google Scholar 

  3. Langlais J, Roberts KD. A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res. 1985;12:183–224.

    Article  CAS  Google Scholar 

  4. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, et al. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development. 1995;121:1139–50.

    CAS  PubMed  Google Scholar 

  5. Visconti PE, Kopf GS. Regulation of protein phosphorylation during sperm capacitation. Biol Reprod. 1998;59:1–6.

    Article  CAS  PubMed  Google Scholar 

  6. Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, et al. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod. 1999;61:76–84.

    Article  CAS  PubMed  Google Scholar 

  7. Fujinoki M, Ohtake H, Okuno M. Tyrosine phosphorylation and dephosphorylation associated with motility of hamster spermatozoa. Biomed Res. 2001;22:147–55.

    CAS  Google Scholar 

  8. Fujinoki M, Kawamura T, Toda T, Ohtake H, Ishimoda-Takagi T, Shimizu N, et al. Identification of 36-kDa flagellar phosphoproteins associated with hamster sperm motility. J Biochem. 2003;133:361–9.

    Article  CAS  PubMed  Google Scholar 

  9. Fujinoki M, Kawamura T, Toda T, Ohtake H, Ishimoda-Takagi T, Shimizu N, et al. Identification of 36 kDa phosphoprotein in fibrous sheath of hamster spermatozoa. Comp Biochem Physiol B Biochem Mol Biol. 2004;137:509–20.

    Article  PubMed  Google Scholar 

  10. Fujinoki M, Ishimoda-Takagi T, Ohtake H. Serine/threonine phosphorylation associated with hamster sperm hyperactivation. Reprod Med Biol. 2004;3:223–30.

    Article  CAS  Google Scholar 

  11. Fujinoki M, Suzuki T, Takayama T, Shibahara H, Ohtake H. Profiling of proteins phosphorylated or dephosphorylated during hyperactivation via activation on hamster spermatozoa. Reprod Med Biol. 2006;5:123–35.

    CAS  Google Scholar 

  12. Visconti PE, Galantino-Homer H, Moore GD, Bailey JL, Ning X, Fornes M, et al. The molecular basis of sperm capacitation. J Androl. 1998;19:242–8.

    CAS  PubMed  Google Scholar 

  13. Ho HC, Suarez SS. An inositol 1,4,5-trisphoshate receptor-gated intracellular Ca2+ store is involved in regulating sperm hyperactivated motility. Biol Reprod. 2001;65:1606–16.

    Article  CAS  PubMed  Google Scholar 

  14. Breitbart H. Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol Cell Endocrinol. 2002;187:139–44.

    Article  CAS  PubMed  Google Scholar 

  15. Ho HC, Granish KA, Suarez SS. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev Biol. 2002;250:208–17.

    Article  CAS  PubMed  Google Scholar 

  16. Marín-Briggiler CI, Jha KN, Chertihin O, Buffone MG, Herr JC, Vazquez-Levin MH, et al. Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation. J Cell Sci. 2005;118:2013–22.

    Article  PubMed  Google Scholar 

  17. Noguchi T, Fujinoki M, Kitazawa M, Inaba N. Regulation of hyperactivation of hamster spermatozoa by progesterone. Reprod Med Biol. 2008;7:63–74.

    Article  CAS  Google Scholar 

  18. Fujinoki M. Melatonin-enhanced hyperactivation of hamster sperm. Reproduction. 2008;136:533–41.

    Article  CAS  PubMed  Google Scholar 

  19. Fujinoki M. Serotonin-enhanced hyperactivation of hamster sperm. Reproduction. 2011;142:255–66.

    Article  CAS  PubMed  Google Scholar 

  20. Sueldo CE, Alexander NJ, Oehninger S, Burkman LJ, Subias E, Acosta AA, et al. Effect of progesterone on human zona pellucida sperm binding and oocyte penetrating capacity. Fertil Steril. 1993;60:137–40.

    CAS  PubMed  Google Scholar 

  21. Baldi E, Luconi M, Bonaccorsi L, Forti G. Nongenomic effects of progesterone on spermatozoa: mechanisms of signal transduction and clinical implications. Front Biosci. 1998;3:D1051–9.

    CAS  PubMed  Google Scholar 

  22. Luconi M, Muratori M, Forti G, Baldi E. Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J Clin Endocrinol Metab. 1999;84:1670–8.

    Article  CAS  PubMed  Google Scholar 

  23. Baldi E, Luconi M, Muratori M, Forti G. A novel functional estrogen receptor on human sperm membrane interferes with progesterone effects. Mol Cell Endocrinol. 2000;161:31–5.

    Article  CAS  PubMed  Google Scholar 

  24. Lösel R, Wehling M. Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol. 2003;4:46–56.

    Article  PubMed  Google Scholar 

  25. Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E. Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids. 2004;69:553–9.

    Article  CAS  PubMed  Google Scholar 

  26. Baldi E, Luconi M, Muratori M, Marchiani S, Tamburrino L, Forti G. Nongenomic activation of spermatozoa by steroid hormones: facts and fictions. Mol Cell Endocrinol. 2009;308:39–46.

    Article  CAS  PubMed  Google Scholar 

  27. Fujinoki M. Non-genomic regulation of mammalian sperm hyperactivation. Reprod Med Biol. 2009;8:47–52.

    Article  CAS  Google Scholar 

  28. Fujinoki M. Suppression of progesterone enhanced hyperactivation in hamster spermatozoa by estrogen. Reproduction. 2010;140:453–64.

    Article  CAS  PubMed  Google Scholar 

  29. Armon L, Eisenbach M. Behavioral mechanism during human sperm chemotaxis: involvement of hyperactivation. PLoS One. 2011;6:e28359.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Libersky EA, Boatman DE. Effects of progesterone on in vitro sperm capacitation and egg penetration in the golden hamster. Biol Reprod. 1995;53:483–7.

    Article  CAS  PubMed  Google Scholar 

  31. Libersky EA, Boatman DE. Progesterone concentration in serum, follicular fluid, and oviductal fluid of the golden hamster during the periovulatory period. Biol Reprod. 1995;53:477–82.

    Article  CAS  PubMed  Google Scholar 

  32. Iguchi T, Watanabe H, Katsu Y, Mizutani T, Miyagawa S, Suzuki A, et al. Developmental toxicity of estrogenic chemicals on rodents and other species. Congenit Anom. 2002;42:94–105.

    Article  CAS  Google Scholar 

  33. Iguchi T, Watanabe H, Ohta Y, Blumberg B. Developmental effects: oestrogen-induced vaginal changes and organotin-induced adipogenesis. Int J Androl. 2008;31:263–8.

    Article  CAS  PubMed  Google Scholar 

  34. Fujinoki M, Ohtake H, Okuno M. Serine phosphorylation of flagellar proteins associated with the motility activation of hamster spermatozoa. Biomed Res. 2001;22:45–58.

    CAS  Google Scholar 

  35. Suarez SS, Ho HC. Hyperactivated motility in sperm. Reprod Domest Anim. 2003;38:119–24.

    Article  CAS  PubMed  Google Scholar 

  36. Mohri H, Inaba K, Ishijima S, Baba SA. Tubulin–dynein system in flagellar and ciliary movement. Proc Jpn Acad Ser B. 2012;88:397–415.

    Article  CAS  Google Scholar 

  37. Ho HC, Suarez SS. Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol Reprod. 2003;68:1590–6.

    Article  CAS  PubMed  Google Scholar 

  38. Fujinoki M. Progesterone-enhanced sperm hyperactivation through IP3-PKC and PKA signals. Reprod Med Biol. 2013;12:27–33.

    Article  CAS  Google Scholar 

  39. Alasmari W, Barratt CLR, Publicover SJ, Whalley M, Foster E, Kay V, et al. The clinical significance of calcium-signalling pathways mediating human sperm hyperactivation. Hum Reprod. 2013;28:866–76.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, School of Medicine, Dokkyo Medical University, Mibu, Tochigi, 321-0293, Japan

    Masakatsu Fujinoki

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  1. Masakatsu Fujinoki
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Correspondence to Masakatsu Fujinoki.

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Fujinoki, M. Regulation and disruption of hamster sperm hyperactivation by progesterone, 17β-estradiol and diethylstilbestrol. Reprod Med Biol 13, 143–152 (2014). https://doi.org/10.1007/s12522-013-0175-8

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  • DOI: https://doi.org/10.1007/s12522-013-0175-8

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