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Oviductal high concentration of K+ suppresses hyperpolarization but does not prevent hyperactivation, acrosome reaction and in vitro fertilization in hamsters

Published online by Cambridge University Press:  05 October 2020

Gen L. Takei Open the ORCID record for Gen L. Takei [Opens in a new window]  and
Hiroe Kon
Gen L. Takei*
Affiliation:
Department of Regulatory Physiology, Dokkyo Medical University 880 Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, 321-0293Japan
Hiroe Kon
Affiliation:
Laboratory Animal Research Center, Dokkyo Medical University 880 Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, 321-0293Japan
*
Author for correspondence: Gen Leon Takei. Department of Pharmacology and Toxicology, Dokkyo Medical University 880 Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, 321–0293Japan. E-mail: [email protected]
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Summary

Mammalian sperm have to undergo capacitation to be fertilization competent. Capacitated sperm in vitro show hyperpolarization of the membrane potential. It has been reported that in mouse membrane hyperpolarization is necessary for the acrosome reaction. We recently found that the fluid of the hamster oviduct, where fertilization occurs, contained a high potassium (K+) concentration (~20 mEq/l). This high K+ concentration could depolarize the membrane potential and prevent the acrosome reaction/fertilization. Conversely, some beneficial effects on capacitation of high K+ concentration or a high K/Na ratio were also reported. In the present study, we investigated the effects of oviduct high K+ concentration on hamster sperm capacitation-associated events and fertilization. The present study confirmed that, in hamster sperm, membrane potential was hyperpolarized upon in vitro capacitation, indicating that capacitation-associated hyperpolarization is a universal phenomenon among mammalian species. An increase in KCl concentration in the medium to 20 mM significantly depolarized the membrane potential and suppressed hyperpolarization when in the presence of >101 mM NaCl. However, an increase in the KCl concentration to 20 mM did not significantly affect the percentage of motile sperm, hyperactivation or the acrosome reaction. No effect of 20 mM KCl on in vitro fertilization was observed. In addition, no correlative changes in hyperactivation and the acrosome reaction with K/Na ratio were observed. These results suggested that in hamsters the oviduct K+ concentration suppressed hyperpolarization but had no effect on capacitation and in vitro fertilization. Our results raised a question over the physiological significance of capacitation-associated hyperpolarization.

Keywords

Acrosome reactionFertilizationHyperpolarizationPotassium ionSperm capacitation
Type
Research Article
Information
Zygote , Volume 29 , Issue 1 , February 2021 , pp. 66 - 74
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

Present address: Department of Pharmacology and Toxicology, Dokkyo Medical University 880 Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, 321-0293 Japan.

References

Austin, CR (1952). The capacitation of the mammalian sperm. Nature 170, 326.CrossRefGoogle ScholarPubMed
Bavister, BD (1989). A consistently successful procedure for in vitro fertilization of golden hamster spermatozoa. Gamete Res 23, 139–58.CrossRefGoogle Scholar
Bendahmanel, M, Zeng, H and Tulsiani, DRP (2002). Assessment of acrosomal status in rat spermatozoa: studies on carbohydrate and non-carbohydrate agonists. Arch Biochem Biophys 404, 38–47.CrossRefGoogle Scholar
Borland, RM, Hazra, S, Biggers, JD and Lechene, CP (1977). The elemental composition of the environments of the gametes and preimplantation embryo during the initiation of pregnancy. Biol Reprod 16, 147–57.CrossRefGoogle ScholarPubMed
Borland, RM, Biggers, JD, Lechene, CP and Taymor, ML (1980). Elemental composition of fluid in the human fallopian tube. J Reprod Fert 58, 479–82.CrossRefGoogle ScholarPubMed
Brenker, C, Zhou, Y, Müller, A, Echeverry, FA, Trötschel, C, Poetsch, A, Xia, XM, Bönigk, W, Lingle, CJ, Kaupp, UB and Strünker, T (2014). The Ca2+-activated K+ current of human sperm is mediated by Slo3. eLife 3, e01438.CrossRefGoogle ScholarPubMed
Brewis, IA, Morton, IE, Mohammad, SN, Browes, CE and Moor, HDM (2000). Measurement of intracellular calcium concentration and plasma membrane potential in human spermatozoa using flow cytometry. J Androl 21, 238–49.Google ScholarPubMed
Chávez, JC, de la Vega-Beltrán, JL, Escoffier, J, Visconti, PE, Treviño, CL, Darszon, A, Salkoff, L and Santi, CM (2013). Ion permeabilities in mouse sperm reveal an external trigger for SLO3-dependent hyperpolarization. PLoS ONE 8, e60578.CrossRefGoogle ScholarPubMed
de la Vega-Beltrán, JL, Sánchez-Cárdenas, C, Krapf, D, Hernández-González, EO, Wertheimer, E, Treviño, CL, Visconti, PE and Darszon, A (2012). Mouse sperm membrane potential hyperpolarization is necessary and sufficient to prepare sperm for the acrosome reaction. J Biol Chem 287, 44384–93.CrossRefGoogle ScholarPubMed
Escoffier, J, Krapf, D, Navarrete, F, Darszon, A and Visconti, PE (2011). Flow cytometry analysis reveals a decrease in intracellular sodium during sperm capacitation. J Cell Sci 125, 473–85.CrossRefGoogle Scholar
Escoffier, J, Navarette, F, Haddad, D, Santi, CM, Darszon, A and Visconti, PE (2015). Flow cytometry analysis reveals that only a subpopulation of mouse sperm undergoes hyperpolarization during capacitation. Biol Reprod 92, 1–11.CrossRefGoogle Scholar
Espinosa, F and Darszon, A (1995). Mouse sperm membrane potential: changes induced by Ca2+ . FEBS Lett 372, 119–25.CrossRefGoogle ScholarPubMed
Fujinoki, M, Takei, GL and Kon, H (2016). Non-genomic regulation and disruption of spermatozoal in vitro hyperactivation by oviductal hormones. J Physiol Sci 66, 207–12.CrossRefGoogle ScholarPubMed
Hernández-González, EO, Sosnik, J, Edwards, J, Acevedo, JJ, Mendoza-Lujambio, I, López-González, I, Demarco, I, Wertheimer, E, Darszon, A and Visconti, PE (2006). Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm. J Biol Chem 281, 5623–33.CrossRefGoogle ScholarPubMed
Hernández-González, EO, Treviño, CL, Castellano, LE, de la Vega-Beltrán, JL, Ocampo, AY, Wertheimer, E, Visconti, PE and Darszon, A (2007). Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation. J Biol Chem 282, 24397–406.CrossRefGoogle ScholarPubMed
Hino, T, Muro, Y, Tamura-Nakano, M, Okabe, M, Tateno, H and Yanagimachi, R (2016). The behavior and acrosomal status of mouse spermatozoa in vitro, and within the oviduct during fertilization after natural mating. Biol Reprod 95, 1–11.CrossRefGoogle ScholarPubMed
Hirohashi, N and Yanagimachi, R (2018). Sperm acrosome reaction: its site and role in fertilization. Biol Reprod 99, 127–33.CrossRefGoogle ScholarPubMed
Howard, E and De Feo, VJ (1959). Potassium and sodium content of uterine and seminal vesicle secretions. Am J Physiol 196, 65–8.CrossRefGoogle ScholarPubMed
Jin, M, Fujiwara, E, Kakiuchi, Y, Okabe, M, Satouh, Y, Baba, SA, Chiba, K and Hirohashi, N (2011). Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 108, 4892–6.CrossRefGoogle ScholarPubMed
Lopata, A, Patullo, MJ, Chang, A and James, B (1976). A method for collecting motile spermatozoa from human semen. Fertil Steril 27, 677–84.CrossRefGoogle ScholarPubMed
Maleszewski, M, Kline, D and Yanagimachi, R (1995). Activation of hamster zona-free oocytes by homologous and heterologous spermatozoa. J Reprod Fert 105, 99–107.CrossRefGoogle ScholarPubMed
Mannowetz, N, Naidoo, NM, Choo, SS, Smith, JF and Lishko, PV (2013). Slo1 is the principal potassium channel of human spermatozoa. eLife 2, e01009.CrossRefGoogle ScholarPubMed
Martínez-López, P, Santi, CM, Treviño, CL, Ocampo-Gutiérrez, AY, Acevedo, JJ, Alisio, A, Salkoff, LB and Darszon, A (2009). Mouse sperm K+ currents stimulated by pH and cAMP possibly coded by Slo3 channels. Biochem Biophys Res Commun 381, 204–9.CrossRefGoogle ScholarPubMed
McPartlin, LA, Visconti, PE and Bedford-Guaus, SJ (2011). Guanine-nucleotide exchange factors (RAPGEF3/RAPGEF4) induce sperm membrane depolarization and acrosomal exocytosis in capacitated stallion sperm. Biol Reprod 51, 179–88.CrossRefGoogle Scholar
Muro, Y, Hasuwa, H, Isotani, A, Miyata, H, Yamagata, K, Ikawa, M, Yanagimachi, R and Okabe, M (2016). Behavior of mouse spermatozoa in the female reproductive tract from soon after mating to the beginning of fertilization. Biol Reprod 94, 1–7.CrossRefGoogle ScholarPubMed
Navarro, B, Kirichok, Y and Clapham, DE (2007). KSper, a pH-sensitive K+ current that controls sperm membrane potential. Proc Natl Acad Sci USA 104, 7688–92.CrossRefGoogle ScholarPubMed
Roblero, LS and Riffo, MD (1986). High potassium concentration improves preimplantation development of mouse embryos in vitro . Fertil Steril 45, 412–6.CrossRefGoogle ScholarPubMed
Roblero, L, Biggers, JD and Lechene, CP (1976). Electron probe analysis of the elemental microenvironment of oviducal mouse embryos. J Reprod Fert 46, 431–4.CrossRefGoogle ScholarPubMed
Roblero, L, Guadarrama, A, Ortiz, ME, Fernández, E and Zegers-Hochschild, F (1988). High potassium concentration improves the rate of acrosome reaction in human spermatozoa. Fertil Steril 49, 676–9.CrossRefGoogle ScholarPubMed
Santi, CM, Martínez-López, P, de la Beltrán, JL, Butler, A, Alisio, A, Darszon, A and Salkoff, L (2010). The SLO3 sperm specific potassium channel plays a vital role in male fertility. FEBS Lett 584, 1041–6.CrossRefGoogle Scholar
Schreiber, M, Wei, A, Yuan, A, Gaut, J, Saito, M and Salkoff, L (1998). Slo3, a novel pH-sensitive K+ channel from mammalian spermatocytes. J Biol Chem 273, 3509–16.CrossRefGoogle ScholarPubMed
Takei, GL and Fujinoki, M (2016). Regulation of hamster sperm hyperactivation by extracellular Na+ . Reproduction 151, 589–603.CrossRefGoogle ScholarPubMed
Toyoda, Y and Chang, MC (1974). Capacitation of epididymal spermatozoa in a medium with high K/Na ratio and cyclic AMP for the fertilization of rat eggs in vitro . J Reprod Fert 36, 125–34.CrossRefGoogle Scholar
Visconti, PE, Bailey, JL, Moore, GD, Pan, D, Olds-Clarke, P and Kopf, GS (1995). Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121, 1129–37.Google ScholarPubMed
Yanagimachi, R (1994). Mammalian fertilization, In The Physiology of Reproduction, 2nd edn (eds Knobil, E. and Neil, J.), pp. 189–317. New York: Raven Press.Google Scholar
Zeng, Y, Clark, E and Florman, H (1995). Sperm membrane-potential-hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion. Dev Biol 171, 554–63.CrossRefGoogle ScholarPubMed
Zeng, XH, Yang, C, Kim, ST, Lingle, CJ and Xia, XM (2011). Deletion of the Slo3 gene abolishes alkalization-activated K+ current in mouse spermatozoa. Proc Natl Acad Sci USA 108, 5879–84.CrossRefGoogle ScholarPubMed