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Hypotaurine and taurine in gamete and embryo environments: de novo synthesis via the cysteine sulfinic acid pathway in oviduct cells

Published online by Cambridge University Press:  26 September 2008

Pierre Guérin  and
Yves Ménézo
Pierre Guérin*
Affiliation:
Ecole Vétérinaire Lyon, Marcy l'Etoile, and INSA Biologie 406, Villeurbanne, France.
Yves Ménézo
Affiliation:
Ecole Vétérinaire Lyon, Marcy l'Etoile, and INSA Biologie 406, Villeurbanne, France.
*
P. Guérin, Ecole Vétérinaire Lyon, BP 83, F-69280 Marcy L'Etoile cedex, France.
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Summary

Taurine and hypotaurine seem to be important compounds for sperm survival and capacitation, the fertilisation process and embryo development, and are present in both sperm and genital secretions. Hypotaurine has protective effects against peroxidative damage. We have established a simple method for hypotaurine quantification in sperm and genital secretions. The mean concentration of hypotaurine is significantly higher in bovine than in human spermatozoa and in seminal plasma. We observed that both molecules are secreted by cow, sow, goat and rabbit oviduct epithelial cell monolayers. In rabbit the release is ascorbic acid dependent. Goat oviduct epithelial cells are able to use the transsulfuration pathway to form hypotaurine and taurine from methionine. We were able to identify cysteine sulfinate decarboxylase (EC 4.1.1.29) activity in cow and goat tubal monolayers. Our results demonstrate that hypotaurine and taurine are secreted by oviduct epithelium, and synthesised by tubal cells via the cysteine sulfinic acid pathway. The data obtained emphasise the importance of hypotaurine and taurine for gamete maturation, fertilisation and early embryonic development.

Keywords

Cysteine sulfinate decarboxylaseGenital secretionsHypotaurineOviduct cellsSpermatozoa
Type
Article
Information
Zygote , Volume 3 , Issue 4 , November 1995 , pp. 333 - 343
Copyright
Copyright © Cambridge University Press 1995

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References

Aitken, R.J. & Clarkson, J.S. (1987). Cellulat basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81, 459–69.Google Scholar
Aitken, R.J. & Fisher, H. (1994). Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. BioEssays 16, 259–67.CrossRefGoogle ScholarPubMed
Aitken, R.J., Clarkson, J.S. & Fishel, S. (1989). Generation of reactive oxygen species, lipid peroxidation and human sperm function. Biol. Reprod. 40, 183–97.CrossRefGoogle Scholar
Almarghini, K., Barbagli, B. & Tappaz, M. (1994). Production and characterization of a new specific antiserum against the taurine putative biosynthetic enzyme cysteine sulfinate decarboxylase. J. Neurochem. 62, 1604–14.Google Scholar
Alvarez, J.G. & Storey, B.T. (1982). Spontaneous lipid peroxidation in rabbit epididymal spermatozoa: its effect on sperm motility. Biol. Reprod. 27, 1102–8.Google Scholar
Alvarez, J.G. & Storey, B.T. (1983). Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol. Reprod. 29, 548–55.CrossRefGoogle ScholarPubMed
Alvarez, J.G. & Storey, B.T. (1984). Assessment of cell damage caused by spontaneous lipid peroxidation in rabbit spermatozoa. Biol. Reprod. 30, 323–31.Google Scholar
Alvarez, J.G., Touchstone, J.C., Blasco, L. & Storey, B.T. (1987). Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa: superoxide dismutase as major enzyme protectant against oxygen toxicity. J. Androl. 8, 338–48.CrossRefGoogle ScholarPubMed
Apud, J.A., Tappaz, M., Celotti, F., Negri-cesi, P., Masotto, C. & Ragnani, G. (1984). Biochemical and immunochemical studies on the GABAergic system in the rat fallopian tube and ovary. J. Neurochem. 43, 120–5.CrossRefGoogle ScholarPubMed
Aruoma, O.I., Halliwell, B., Hoey, M. & Butler, J. (1988). The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem. J. 256, 251–5.CrossRefGoogle ScholarPubMed
Barnett, D.K. & Bavister, B.D. (1992). Hypotaurine requirement for in vitro development of golden hamster one-cell embryos into morulae and blastocysts, and production of term offspring from in vitro-fertilized ova. Biol. Reprod. 47, 297–304.CrossRefGoogle ScholarPubMed
Boatman, D.E., Bavister, B.D. & Cruz, E. (1990). Addition of hypotaurine can reactivate immotile golden hamster spermatozoa. J. Androl. 11. 66–72.CrossRefGoogle ScholarPubMed
Boice, M.L., Geisert, R.D., Blair, R.M. & Verhage, H.G. (1990). Identification and characterization of bovine oviductal glycoproteins synthesized at estrus. Biol. Reprod. 43, 457–65.CrossRefGoogle ScholarPubMed
Bonnot, G. & Febvay, G. (1994). Fourier processing of liquid chromatograms using flow radioactivity detection. Anal. Biochem. 224. 354–63.CrossRefGoogle Scholar
Buhi, W.C., Alvarez, I.M., Sudhipong, V. & Dones-Smith, M.M. (1990). Identification and characterization of de novosynthesized porcine oviductal secretory proteins. Biol. Reprod. 43, 929–38.CrossRefGoogle ScholarPubMed
Clewe, T.H. & Mastroianni, L. Jr (1960). A method for continuous volumetric collection of oviduct secretion. J. Reprod. Fertil. 1, 146–50.CrossRefGoogle Scholar
David, A., Brackett, B.G., Garcia, C.R. & Mastroianni, L. (1969). Composition of rabbit oviduct fluid in ligated segments of the fallopian tube. J. Reprod. Fertil. 19, 285–9.Google Scholar
Downs, S.M. & Dow, M.P.D. (1991). Hypoxanthine maintained 2-cell block in mouse embryos: dependence on glucose and effect of hypoxanthine phosporibosyltransferase inhibitiors. Biol. Reprod. 44, 1025–39.CrossRefGoogle Scholar
Fellman, J.H. & Roth, E.S. (1985). The biological oxidation of hypotaurine to taurine: hypotaurine as an antioxidant. Prog. Clin. Biol. Res. 179, 71–82.Google ScholarPubMed
Futani, S., Ubuka, T. & Abe, T. (1994). High-performance liquid chromatographic determination of hypotaurine and taurine after conversion to 4-dimethylaminoazobenzene-4– -sulfonyl derivatives and its application to the urine of cysteine-administered rats. J. Chromatogr. B. 660, 164–9.Google Scholar
Gandolfi, F., Brevini, T.A.L., Richardson, L., Brown, C.R. & Moor, R.M. (1989). Chartacterization of proteins secreted by sheep oviduct epithelial cells and their function in empryonic development. Development 106, 303–12.CrossRefGoogle Scholar
Guérin, P., Gharib, A. & Ménézo, Y. (1991). Synthesis of S-adenosyl methionine and S-adenosyl homocysteine in human and bovine ejaculated spermatozoa. Mol. Androl. 3, 9–17.Google Scholar
Guérin, P., Guillaud, J. & Ménézo, Y. (1995a). Hypotaurine in spermatozoa and genital secretions and its production by oviduct epithelial cells in vitro. Hum. Reprod. 10. 866–72.Google Scholar
Guérin, P., Tappaz, M., Guillaud, J. & Ménézo, Y. (1995b). Mise en évidence de la cystéine sulfinate décarboxylase (EC 4.1.1.29) dans les cellules épithéliales tubaires devache et de chévre. C.R. Acad. Sci. Ser. III 318, 523–8.Google Scholar
Gwatkin, R.B.L. (1983). Effect of compounds structurally related to taurine and of taurine uptake inhibitors on the motility of hamster sperm in vitro. Gamete Res. 4, 347–50.Google Scholar
Hansen, C., Srikandakumar, A. & Downey, B.R. (1991). Presence of follicular fluid in the porcine oviduct and its contribution to the acrosome reaction. Mol. Reprod. Dev. 30, 148–53.Google Scholar
Henault, M.A. & Killian, G.J. (1993). Synthesis and secretion of lipids by bovine oviduct mucosal explants. J. Reprod. Fertil. 98, 431–8.CrossRefGoogle ScholarPubMed
Holmes, R.P., Goodman, H.O., Shihabi, Z.K.Jarow, J.P. (1992). The Taurine and hypotaurine content of human semen. J. Androl. 13, 289–92.CrossRefGoogle ScholarPubMed
Horst, C.J.G.van der, & Brand, A. (1969). Occurrence of hypotaurine and inositol in the reproductive tract of the ewe and its regulation by pregnenolone and progesterone. Nature 223, 67–8.CrossRefGoogle Scholar
Horst, C.J.G.van der, & Grooten, H.J.G. (1966). The occurrence of hypotaurine and other sulfur-containing amino acids in seminal plasma and spermatozoa of boar, bull and dog. Biochim. Biophys. Acta 117, 495–7.CrossRefGoogle ScholarPubMed
Huxtable, R.J. (1992). The physiological actions of taurine. Physiol. Rev. 72, 101–63.Google Scholar
Jones, R., Mann, T. & Sherins, R. (1979). Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxidases and protective action of seminal plasma. Fertil. Steril. 31, 531–7.Google Scholar
Kochakian, C.D. (1973). Hypotaurine: regulation of production in seminal vesicles and prostate of guinea-pig by testosterone. Nature 241, 202–3.CrossRefGoogle ScholarPubMed
Kroll, W.A. & Schneider, J.A. (1974). Decrease in free cystine content of cultured cystinotic fibroblasts by ascorbic acid. Science 86, 1040–2.CrossRefGoogle Scholar
Leese, H.J. (1988). The formation and function of oviduct fluid. J. Reprod. Fertil. 82, 843–56.CrossRefGoogle ScholarPubMed
Legay, F., Weise, V.K., Oertel, W.H. & Tappaz, M.L. (1987). Taurine biosynthesis in rat brain: a new specific and sensitive microassay of cysteine sulfinate decarboxylase (CSDI) activity through selective immunotrapping and its use for distribution studies. J. Neurochem. 48, 345–51.CrossRefGoogle Scholar
Legge, M. & Sellens, M.H. (1991). Free radical scavengers ameliorate the 2-cell block in mouse embryo culture. Hum. Reprod. 6, 867–71.CrossRefGoogle ScholarPubMed
Leibfried, M.L. & Bavister, B. (1981). The effect of taurine and hypotaurine on in vitro fertilization in the golden hamster. Gamete Res. 4, 57–63.CrossRefGoogle Scholar
Meizel, S., Lui, C.W., Working, P.K. & Mrsny, R.J. (1980). Taurine and hypotaurine: their effects on motility, capacitation and the acrosome reaction of hamster sperm in vitro and their presence in sperm and reproductive tract fluids of several mammals. Dev. Growth Differ. 22, 483–94.CrossRefGoogle ScholarPubMed
Ménézo, Y., Khatchadourian, C., Gharib, A., Hamidi, J., Greenland, T. & Sarda, N. (1989). Regulation of S-adenosyl methionine synthesis in the mouse embryo. Life Sci. 44, 1601–9.CrossRefGoogle ScholarPubMed
Mrsny, R.J. & Meizel, S. (1985). Inhibition of hamster Na+/K+-ATPase activity by taurine and hypotaurine. Life Sci. 36, 271–5.CrossRefGoogle ScholarPubMed
Nasr-Esfahani, M.H., Aitken, R.J. & Johnson, M.H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109, 501–7.Google Scholar
Noda, Y., Matsumoto, H., Umaoka, Y., Tatsumi, K., Kishi, J. & Mori, T. (1991). Involvement of superoxide radicals in the mouse 2-cell block. Mol. Reprod. Dev. 28, 356–60.CrossRefGoogle Scholar
Oertel, W.H., Schmechel, D.E., Weise, V.K., Ranson, D.H., Tappaz, M., Krutzsch, H.C. & Kopin, I.J. (1981). Comparison of cysteine sulphinic acid decarboxylase isoenzymes and glutamic acid decarboxylase in rat liver and brain. Neuroscience 6, 2701–14.CrossRefGoogle ScholarPubMed
Ouhibi, N., Ménézo, Y., Benet, G. & Nicollet, B. (1989). Culture of epithelial cells derived from the oviduct of different species. Hum. Reprod. 4, 229–35.Google Scholar
Pascu, T., Suteanu, M. & Lunca, H. (1970). Concentration de la vitamine C dans le liquide folliculaire normal pendant les différentes phases du cycle œstral et dans le liquide des kystes ovariens (folliculaires et lutéiniques), ainsi que dans le sang des mémes vaches. Rec. Med. Vet. 146, 1021–9.Google Scholar
Ricci, G., Dupré, S., Federici, G., Spoto, G., Matarese, R.M. & Cavallini, D. (1978). Oxidation of hypotaurine to taurine by ultraviolet irradiation. Physiol. Chem. Phys. 10, 435–41.Google ScholarPubMed
Sloan, M.H. & Johnson, A.D. (1974). The influence of a cannula in the rabbit oviduct. I. Oviduct fluid lipids and proteins. J. Reprod. Fertil. 37, 149–53.CrossRefGoogle ScholarPubMed
Stanke, D.F., De Young, D.W., Sikes, J.D. & Mather, E.C. (1973). Collection of bovine oviduct secretion. J. Reprod. Fertil. 32, 535–7.CrossRefGoogle Scholar
Tappaz, M., Almarghini, K., Legay, F. & Remy, A. (1992). Taurine biosynthesis enzyme cysteine sulfinate decarboxylase (CSD) from brain: the long and tricky trail to identification. Neurochem. Res. 17, 849–59.CrossRefGoogle Scholar
Timbrell, J.A., Seabra, V. & Waterfield, C.J. (1995). The in vivo and in vitro protective properties of taurine. Gen. Pharmacol. 26, 453–62.Google Scholar
Van Winkle, L.J., Patel, M., Wasserlauf, H.GDickinson, H.R. & Campione, A.L. (1994). Osmotic regulation of taurine transport via system β and novel processes in mouse preimplantation conceptuses. Biochim. Biophys. Acta 1191, 244–55.Google Scholar
Wegner, C.C. & Killian, G.J. (1991). in vitro and in vivo association of an oviduct estrus-associated protein with bovine zona pellucida. Mol. Reprod. Dev. 29, 77–84.Google Scholar