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Spontaneous generation of reactive oxygen species and effect on motility and fertilizability of sea urchin spermatozoa

Published online by Cambridge University Press:  31 October 2012

Makoto Kazama ,
Taizo Sato  and
Akiya Hino
Makoto Kazama*
Affiliation:
Department of Biological Sciences, Faculty of Science, Kanagawa University, 2946 Tsuchiya, Hiratsuka City, Kanagawa, 259-1293, Japan.
Taizo Sato
Affiliation:
Department of Biological Sciences, Faculty of Science, Kanagawa University, 2946 Tsuchiya, Hiratsuka City, Kanagawa, 259-1293, Japan.
Akiya Hino
Affiliation:
Department of Biological Sciences, Faculty of Science, Kanagawa University, 2946 Tsuchiya, Hiratsuka City, Kanagawa, 259-1293, Japan.
*
All correspondence to: Makoto Kazama. Department of Biological Sciences, Faculty of Science, Kanagawa University, 2946 Tsuchiya, Hiratsuka City, Kanagawa, 259-1293, Japan. Tel: +81 463 59 4111. Fax: +81 463 58 9684. e-mail: ft101653@kanagawa-u.ac.jp
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Summary

We investigated the generation of reactive oxygen species (ROS) by spermatozoa in two species of sea urchin. ROS generation was accompanied by the initiation of motility and respiration and influenced the motility and fertilizability of spermatozoa. The sea urchin performs external fertilization in aerobic seawater. Sperm motility was initiated after spawning through Na+/H+ exchange. ROS generation was dependent on the respiration and sperm concentration and its generation was first observed at initiation of motility, via activation of respiration through ATP/ADP transport. The ROS generation rate increased at higher dilution ratios of spermatozoa, in a manner that was synchronous with the respiratory rate. This phenomenon resembled the previously defined ‘sperm dilution effect’ on respiration. The loss of motility and fertilizability was induced not only by treatment with hydrogen peroxide but also by sperm dilution. Storage of spermatozoa with a higher dilution ratio also accelerated the decrease in fertilizability. Thus, optimum sea urchin fertilizability is maintained by storage of undiluted spermatozoa on ice, in order to minimize oxidative stress and to maximize longevity.

Keywords

Dilution effectReactive oxygen speciesRespirationSea urchinSperm
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 246 - 258
Copyright
Copyright © Cambridge University Press 2012 

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References

Andreyev, A.Y., Kushnareva, Y.E. & Starkov, A.A. (2005). Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70, 200–14.Google Scholar
Atkinson, D.E. (1968). The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7, 4030–4.Google Scholar
Baker, M.A. & Aitken, R.J. (2005). Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod. Biol. Endocrinol. 3, 67.Google Scholar
Boldt, J., Schuel, H., Schuel, R., Dandekar, P.V. & Troll, W. (1981). Reaction of sperm with egg-derived hydrogen peroxide helps prevent polyspermy during fertilization in the sea urchin. Gamete Res. 4, 365–77.Google Scholar
Byrne, M., Soars, N., Selvakumaraswamy, P., Dworjanyn, S.A. & Davis, A.R. (2010). Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. Mar. Environ. Res. 69, 234–9.Google Scholar
Christen, R., Schackmann, R.W. & Shapiro, B.M. (1982). Elevation of the intracellular pH activates respiration and motility of sperm of the sea urchin, Strongylocentrotus purpuratus. J. Biol. Chem. 257, 14881–90.Google Scholar
Christen, R., Schackmann, R.W. & Shapiro, B.M. (1983). Metabolism of sea urchin sperm. Interrelationships between intracellular pH, ATPase activity and mitochondrial respiration. J. Biol. Chem. 258, 5392–9.CrossRefGoogle ScholarPubMed
Coburn, M., Schuel, H. & Troll, W. (1981). A hydrogen peroxide block to polyspermy in the sea urchin Arbacia punctulata. Dev. Biol. 84, 235–8.CrossRefGoogle ScholarPubMed
de Lamirande, E., Jiang, H., Zini, A., Kodama, H. & Gagnon, C. (1997). Reactive oxygen species and sperm physiology. Rev. Reprod. 2, 48–54.Google Scholar
Dorsten, F.A., Wyss, M., Wallimann, T. & Nicolay, K. (1997). Activation of sea-urchin sperm motility is accompanied by an increase in the creatine kinase exchange flux. Biochem. J. 325, 411–6.Google Scholar
Duan, Y., Gross, R.A. & Sheu, S.S. (2007). Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J. Physiol. 585, 741–58.Google Scholar
Foerder, C.A., Klebanoff, S.J. & Shapiro, B.M. (1978). Hydrogen peroxide production, chemiluminescence and the respiratory burst of fertilization: interrelated events in early sea urchin development. Proc. Natl. Acad. Sci. USA 75, 3183–7.Google Scholar
Gray, J. (1928). The effect of dilution on the activity of spermatozoa. J. Exp. Biol. 5, 337–44.Google Scholar
Hino, A., Fujiwara, A. & Yasumasu, I. (1980a). Inhibition of respiration in sea urchin spermatozoa with unfertilized eggs. I. Change in the respiratory rate of spermatozoa in the presence of fixed eggs. Dev. Growth Differ. 22, 421–8.CrossRefGoogle ScholarPubMed
Hino, A., Hiruma, T., Fujiwara, A. & Yasumasu, I. (1980b). Inhibition of respiration in sea urchin spermatozoa with unfertilized eggs. IV. State 4 respiration in spermatozoa of Hemicentrotus pulcherrimus after their interaction with fixed unfertilized eggs. Dev. Growth Differ. 22, 813–20.Google Scholar
Hiruma, T., Hino, A., Fujiwara, A. & Yasumasu, I. (1982). Inhibition of respiration in sea urchin spermatozoa with unfertilized eggs. V. Inhibition of electron transport in a span of mitochondrial respiratory chain between cytochrome b and c in sea urchin spermatozoa, induced by the interaction with glutaraldehyde fixed eggs. Dev. Growth Differ. 24, 17–24.Google Scholar
Kazama, M., Asami, K. & Hino, A. (2006). Fertilization induced changes in sea urchin sperm: mitochondrial deformation and phosphatidylserine exposure. Mol. Reprod. Dev. 73, 1303–11.Google Scholar
Kazama, M. & Hino, A. (2012). Sea urchin spermatozoa generate at least two reactive oxygen species; the type of reactive oxygen species changes under different conditions. Mol. Reprod. Dev. 79, 283–95.CrossRefGoogle ScholarPubMed
Kinukawa, M., Nomura, M. & Vacquier, V.D. (2007). A sea urchin sperm flagellar adenylate kinase with triplicated catalytic domains. J. Biol. Chem. 282, 2947–55.CrossRefGoogle ScholarPubMed
Kirkland, R.A. & Franklin, J.L. (2001). Evidence for redox regulation of cytochrome c release during programmed neuronal death: antioxidant effects of protein synthesis and caspase inhibition. J. Neurosci. 21, 1949–63.CrossRefGoogle ScholarPubMed
Koppers, A.J., De Iuliis, G.N., Finnie, J.M., McLaughlin, E.A. & Aitken, R.J. (2008). Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab. 93, 3199–207.Google Scholar
Liu, S.X., Athar, M., Lippai, I., Waldren, C. & Hei, T.K. (2001). Induction of oxyradicals by arsenic: implication for mechanism of genotoxicity. Proc. Natl. Acad. Sci. USA 98, 1643–8.Google Scholar
Liu, Y., Fiskum, G. & Schubert, D. (2002). Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780–7.Google Scholar
Mathai, J.C. & Sitaramam, V. (1994). Stretch sensitivity of transmembrane mobility of hydrogen peroxide through voids in the bilayer. Role of cardiolipin. J. Biol. Chem. 269, 17784–93.Google Scholar
Mita, M., Hino, A. & Yasumasu, I. (1984). Effect of temperature on interaction between eggs and spermatozoa of sea urchin. Biol. Bull. 166, 68–77.CrossRefGoogle Scholar
Mita, M. & Nakamura, M. (1998). Energy metabolism of sea urchin spermatozoa: an approach based on echinoid phylogeny. Zoolog. Sci. 15, 1–10.Google Scholar
Mohri, H. & Yasumasu, I. (1963). Studies on the respiration of sea-urchin spermatozoa. V. The effect of pCO2. J. Exp. Biol. 40, 573–86.Google Scholar
Myhre, O., Andersen, J.M., Aarnes, H. & Fonnum, F. (2003). Evaluation of the probes 2′,7′-dichlorofluorescin diacetate, luminol and lucigenin as indicators of reactive species formation. Biochem. Pharmacol. 65, 1575–82.Google Scholar
Nishioka, D. & Cross, N. (1978). The role of external sodium in sea urchin fertilization. In Cell Reproduction (eds Dirksen, E.R., Prescott, D. & Fox, C.F.), pp. 403–13. New York: Academic Press.CrossRefGoogle Scholar
Rothschild, L. (1948). The physiology of sea-urchin spermatozoa; senescence and the dilution effect. J. Exp. Biol. 25, 353–68.Google Scholar
Shapiro, B.M., Cook, S., Quest, A.F., Oberdorf, J. & Wothe, D. (1990). Molecular mechanisms of sea-urchin sperm activation before fertilization. J. Reprod. Fertil. 42, 3–8.Google Scholar
Tombes, R.M., Brokaw, C.J. & Shapiro, B.M. (1987). Creatine kinase-dependent energy transport in sea urchin spermatozoa. Flagellar wave attenuation and theoretical analysis of high energy phosphate diffusion. Biophys. J. 52, 75–86.Google Scholar
Tombes, R.M. & Shapiro, B.M. (1989). Energy transport and cell polarity: relationship of phosphagen kinase activity to sperm function. J. Exp. Zool. 251, 82–90.Google Scholar
Turner, T.T. & Giles, R.D. (1982). The effects of cyclic adenine nucleotides, phosphodiesterase inhibitors and cauda epididymidal fluid on the motility of rat epididymal spermatozoa. J. Androl. 3, 134–9.Google Scholar
Vacquier, V.D. (2011). Laboratory on sea urchin fertilization. Mol. Reprod. Dev. 78, 553–564.CrossRefGoogle ScholarPubMed
Vacquier, V.D. & N. Hirohashi, N. (2004). Sea urchin spermatozoa. Methods Cell Biol. 74, 523–44.Google Scholar
Wilson, D.F. & Epel, D. (1968). The cytochrome system of sea urchin sperm. Arch. Biochem. Biophys. 126, 83–90.Google Scholar