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Inhibition of boar sperm hyaluronidase activity by tannic acid reduces polyspermy during in vitro fertilization of porcine oocytes

Published online by Cambridge University Press:  01 November 2006

Hideki Tatemoto*
Affiliation:
Department of Bioproduction, Faculty of Agriculture, University of the Ryukyus, Nishihara-cho, Okinawa 903-0213, Japan.
Isao Tokeshi
Affiliation:
Department of Bioproduction, Faculty of Agriculture, University of the Ryukyus, Nishihara-cho, Okinawa 903-0213, Japan.
Satoshi Nakamura
Affiliation:
Laboratory of Swine, Okinawa Prefectural Livestock Experiment Station, Nakijin-son, Okinawa 905-0426, Japan.
Norio Muto
Affiliation:
Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Shobara, Hiroshima 727-0023, Japan.
Tadashi Nakada
Affiliation:
Department of Bioproduction, Faculty of Agriculture, University of the Ryukyus, Nishihara-cho, Okinawa 903-0213, Japan.
*
All correspondence to: H. Tatemoto, Department of Bioproduction, Faculty of Agriculture, University of the Ryukyus, Nishihara-cho, Okinawa 903-0213, Japan. Fax: +81 98 895 8757. e-mail: [email protected]

Summary

The present study was conducted to examine the effects of three polyphenols (tannic acid, apigenin and quercetin) on hyaluronidase activity and in vitro fertilization (IVF) parameters. Among them, tannic acid showed by far the strongest potency for blocking hyaluronidase activity extracted from preincubated boar sperm, causing a dose-dependent inhibition over the range of 2–10 μg/ml. When cumulus-intact and cumulus-free oocytes were inseminated in IVF medium containing tannic acid, the penetration and the polyspermy rates were significantly decreased in the presence of 10 μg/ml tannic acid compared with those in the absence of tannic acid, and the addition of 5 μg/ml tannic acid significantly reduced the polyspermy rate (p < 0.05) compared with that of the control while maintaining the high penetration rate. However, apigenin and quercetin had no effect on the rate of polyspermy. Interestingly, the incidence of polyspermy was significantly reduced in oocytes inseminated with sperm pretreated with 5 μg/ml tannic acid (p < 0.05), although the pretreatment of oocytes had no effect against the polyspermy after insemination with untreated sperm. Treatment with tannic acid caused neither a protective proteolytic modification of the zona pellucida matrix before fertilization, nor a reduction of the proteolytic activity of acrosomal contents or the number of zona-bound spermatozoa. These data suggest that an appropriate concentration of tannic acid prevents polyspermy through the inhibition of sperm hyaluronidase activity during IVF of porcine oocytes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

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References

Abeydeera, L.R. & Day, B.N. (1997). Fertilization and subsequent development in vitro of pig oocytes insemi-nated in a modified Tris-buffered medium with frozen-thawed ejaculated spermatozoa. Biol. Reprod. 57, 729–34.CrossRefGoogle Scholar
Asano, A. & Niwa, K. (2004). Activation and penetration in vitro of pig oocytes treated with calcium ionophore. J. Reprod. Dev. 50, 7785.CrossRefGoogle ScholarPubMed
Baba, D., Kashiwabara, S., Honda, A., Yamagata, K., Wu, Q., Ikawa, M., Okabe, M. & Baba, T. (2002). Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J. Biol. Chem. 277, 30310–14.CrossRefGoogle ScholarPubMed
Brad, A.M., Bormann, C.L., Swain, J.E., Durkin, R.E., Johnson, A.E., Clifford, A.L. & Krisher, R.L. (2003). Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol. Reprod. Dev. 64, 492–8.CrossRefGoogle ScholarPubMed
Cherr, G.N., Meyers, S.A., Yudun, A.I., VandeVoort, C.A., Myles, D.G., Primakoff, P. & Overstreet, J.W. (1996). The PH-20 protein in cynomolgus macaque sperma-tozoa: identification of two different forms exhibiting hyaluronidase activity. Dev. Biol. 175, 142–53.CrossRefGoogle ScholarPubMed
Cherr, G.N., Yudin, A.I., Li, M.-W., Vines, C.A. & Overstreet, J.W. (1999). Hyaluronic acid and the cumulus extracellular matrix induce increases in intracellular calcium in macaque sperm via the plasma membrane protein PH-20. Zygote 7, 211–22.CrossRefGoogle ScholarPubMed
Cherr, G.N., Yudin, A.I. & Overstreet, J.W. (2001). The dual functions of GPI-anchored PH-20: hyaluronidase and intracellular signaling. Matrix Biol. 20, 515–25.CrossRefGoogle ScholarPubMed
Fléchon, J.E., Degrouard, J., Kopečný, V., Pivko, J., Pavlok, A. & Motlik, J. (2003). The extracellular matrix of porcine mature oocytes: origin, composition and presumptive roles. Reprod. Biol. Endocrinol. 1, 124–36.CrossRefGoogle ScholarPubMed
Gmachl, M., Sagan, S., Ketter, S. & Kreil, G. (1993). The human sperm protein PH-20 has hyaluronidase activity. FEBS Lett. 336, 545–8.CrossRefGoogle ScholarPubMed
Gordo, A.C., Roodrigues, P., Kurokawa, M., Jellerette, T., Exley, G.E., Warner, C. & Fissore, R. (2002). Intracellular calcium oscillations signal apoptosis rather than activa-tion in in vitro aged mouse eggs. Biol. Reprod. 66, 1828–37.CrossRefGoogle Scholar
Honda, A., Siruntawineti, J. & Baba, T. (2002). Role of acrosomal matrix proteases in sperm–zona pellucida interactions. Hum. Reprod. Update 8, 405–12.CrossRefGoogle ScholarPubMed
Hunnicutt, G.R., Primakoff, P. & Myles, D.G. (1996). Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. Biol. Reprod. 55, 80–6.CrossRefGoogle Scholar
Kano, K., Miyano, T. & Kato, S. (1994). Effect of oviductal epithelial cells on fertilization of pig oocytes in vitro. Theriogenology 42, 1061–8.CrossRefGoogle ScholarPubMed
Kim, N.-H., Funahashi, H., Abeydeera, L.R., Moon, S.J., Prather, R.S. & Day, B.N. (1996). Effects of oviductal fluid on sperm penetration and cortical granule exocytosis during fertilization of pig oocytes in vitro. J. Reprod. Fertil. 107, 7986.CrossRefGoogle ScholarPubMed
Kline, D. & Kline, J. (1992). Repetitive calcium transient and the role of calcium in exocytosis and cell cycle activation in the mouse. Dev. Biol. 149, 80–9.CrossRefGoogle ScholarPubMed
Kouba, A.J., Abeydeera, L.R., Alvarez, I.M., Day, B.N. & Buhi, W.C. (2000). Effects of the porcine oviduct-specific glycoprotein on fertilization, polyspermy, and embryonic development in vitro. Biol. Reprod. 63, 242–50.CrossRefGoogle ScholarPubMed
Kuppusamy, U.R., Khoo, H.E. & Das, N.P. (1990). Structure–activity studies of flavonoids as inhibitors of hyaluronidase. Biochem. Pharmacol. 40, 397401.CrossRefGoogle ScholarPubMed
Li, M.-W., Cherr, G.N., Yudin, A.I. & Overstreet, J.W. (1997 a). Biochemical characterization of the PH-20 protein on the plasma membrane and inner acrosomal membrane of cynomolgus macaque spermatozoa. Mol. Reprod. Dev. 48, 356–66.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Li, M.-W., Yudin, A.I., VandeVoort, C.A., Sabeur, K., Primakoff, P. & Overstreet, J.W. (1997 b). Inhibition of monkey sperm hyaluronidase activity and heterologous cumu-lus penetration by flavonoids. Biol. Reprod. 56, 1383–9.CrossRefGoogle ScholarPubMed
Li, M.-W., Yudin, A.I., Robertson, K.R., Cherr, G.N. & Overstreet, J.W. (2002). Importance of glycosylation and disulfide bonds in hyaluronidase activity of macaque sperm surface PH-20. J. Androl. 23, 211–19.CrossRefGoogle ScholarPubMed
Lin, Y., Mahan, K., Lathrop, W.F., Myles, D.G. & Primakoff, P. (1994). A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg. J. Cell Biol. 125, 1157–63.CrossRefGoogle ScholarPubMed
Maeda, T., Tatemoto, H., Terada, T. & Tsutsumi, Y. (1990). A convenient method for evaluation of frozen-thawed damage to acrosomes of fowl spermatozoa using a gelatin substrate slide. Jpn. Poult. Sci. 27, 6671.CrossRefGoogle Scholar
Marchal, R., Caillaud, M., Martoriati, A., Gerard, N., Mermillod, P. & Goudet, G. (2003). Effect of growth hormone (GH) on in vitro nuclear and cytoplasmic oocyte maturation, cumulus expansion, hyaluronan syntheses, and connexins 32 and 43 expression, and GH receptor messenger RNA expression in equine and porcine species. Biol. Reprod. 69, 1013–22.CrossRefGoogle Scholar
McCauley, T.C., Buhi, W.C., Wu, G.M., Mao, J., Caamano, J.N., Didion, B.A. & Day, B.N. (2003). Oviduct-specific glycoprotein modulates sperm-zona binding and improves efficiency of porcine fertilization in vitro. Biol. Reprod. 69, 828–34.CrossRefGoogle ScholarPubMed
McRorie, R.A. & Williams, W.L. (1974). Biochemistry of mammalian fertilization. Annu. Rev. Biochem. 43, 777803.CrossRefGoogle ScholarPubMed
Meyers, S.A., Yudin, A.I., Cherr, G.N., VandeVoort, C.A., Myles, D.G., Primakoff, P. & Overstreet, J.W. (1997). Hyaluronidase activity of in vitro capacitated macaque sperm assessed by an in vitro cumulus penetration assay. Mol. Reprod. Dev. 46, 392400.3.0.CO;2-0>CrossRefGoogle Scholar
Meyers, S.A. (2001). Equine sperm–oocyte interaction: the role of sperm surface hyaluronidase. Anim. Reprod. Sci. 68, 291303.CrossRefGoogle ScholarPubMed
Miyazaki, S. (1990). Cell signaling at fertilization of hamster eggs. J. Reprod. Fertil. Suppl. 42, 163–75.Google ScholarPubMed
Miyazaki, S., Yuzaki, M., Nakada, K., Shirakawa, H., Nakanishi, S., Nakada, S. & Mikoshiba, K. (1992). Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-triphosphate receptor in fertilized hamster eggs. Science 257, 251–5.CrossRefGoogle Scholar
Nagai, T. & Moor, R.M. (1990). Effect of oviductal cells on the incidence of polyspermy in pig eggs fertilized in vitro. Mol. Reprod. Dev. 26, 377–82.CrossRefGoogle ScholarPubMed
Nagai, T., Niwa, K. & Iritani, A. (1984). Effect of sperm concentration at preincubation in chemically defined medium on fertilization in vitro of pig follicular oocytes. J. Reprod. Fertil. 70, 271–5.CrossRefGoogle Scholar
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 6173.Google ScholarPubMed
Phelps, B.M., Primakoff, P., Koppel, D.E., Low, M.G. & Myles, D.G. (1988). Restricted lateral diffusion of PH-20, a PI-anchored sperm membrane protein. Science 240, 1780–82.CrossRefGoogle ScholarPubMed
Primakoff, P. & Myles, D.G. (1983). A map of the guinea pig sperm surface constructed with monoclonal antibodies. Dev. Biol. 98, 417–28.CrossRefGoogle ScholarPubMed
Primakoff, P., Hyatt, H. & Myles, D.G. (1985). A role for the migrating sperm surface antigen PH-20 in guinea pig sperm binding to the egg zona pellucida. J. Cell Biol. 101, 2239–44.CrossRefGoogle Scholar
Ryan, T.A. (1960). Significance tests for multiple comparison of proportions, variances, and other statistics. Psychol. Bull. 57, 318–28.CrossRefGoogle ScholarPubMed
Tatemoto, H. & Terada, T. (1999 a). Analysis of zona pellucida modifications due to cortical granule exocytosis in single porcine oocytes, using enhance chemiluminescence. Theriogenology 52, 629–40.CrossRefGoogle ScholarPubMed
Tatemoto, T. & Terada, T. (1999 b). Time course analyses of cortical granule exocytosis and zona pellucida modifications after artificial activation in in vitro matured porcine oocytes. J. Mamm. Ova Res. 16, 110–17.CrossRefGoogle Scholar
Tatemoto, H., Ootaki, K., Shigeta, K. & Muto, N. (2001). Enhancement of developmental competence after in vitro fertilization of porcine oocytes by treatment with ascorbic acid 2-O-α-glucoside during in vitro maturation. Biol. Reprod. 65, 1800–6.CrossRefGoogle ScholarPubMed
Tatemoto, H., Muto, N., Sunagawa, I., Shinjo, A. & Nakada, T. (2004). Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol. Reprod. 71, 1150–7.CrossRefGoogle ScholarPubMed
Tatemoto, H., Muto, N., Yim, S.-D. & Nakada, T. (2005). Anti-hyaluronidase oligosaccharide derived from chondroitin sulfate A effectively reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 72, 127–34.CrossRefGoogle ScholarPubMed
Thaler, C.D. & Cardullo, R.A. (1995). Biochemical char-acterization of a glycosylphosphatidylinositol-linked hya-luronidase on mouse sperm. Biochemistry 34, 7788–95.CrossRefGoogle Scholar
Thundathil, J., Palomino, J., Barth, A., Mapletoft, R. & Barros, C. (2001). Fertilizing characteristics of bovine sperm with flattened or indented acrosomes. Anim. Reprod. Sci. 67, 231–43.CrossRefGoogle ScholarPubMed
Wang, W.H., Abeydeera, L.R., Okuda, K. & Niwa, K. (1994). Penetration of porcine oocytes during maturation in vitro by cryopreserved, ejaculated spermatozoa. Biol. Reprod. 50, 510–15.CrossRefGoogle ScholarPubMed
Wolf, D.P. & Hamada, M. (1977). Induction of zonal and oolemmal blocks to sperm penetration in mouse eggs with cortical granule exudates. Biol. Reprod. 17, 350–4.CrossRefGoogle Scholar
Wu, H., Smyth, J., Luzzi, V., Fukami, K., Takenawa, T., Black, S.L., Allbritton, N.L. & Fissore, R.A. (2001). Sperm factor induces intracellular free calcium oscillations by stimulating the phosphoinositide pathway. Biol. Reprod. 64, 1338–49.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction, 2nd edn (ed. Knobil, E. & Neill, J.D.), pp. 135–85. New York: Raven Press.Google Scholar
Yudin, A.I., Vandevoort, C.A., Li, M.-W, & Overstreet, J.W. (1999). PH-20 but not acrosin is involved in sperm penetration of the macaque zona pellucida. Mol. Reprod. Dev. 53, 350–62.3.0.CO;2-9>CrossRefGoogle Scholar