Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T07:59:49.889Z Has data issue: false hasContentIssue false
  • English
  • Français

Glutamine and hypotaurine improves intracellular oxidative status and in vitro development of porcine preimplantation embryos

Published online by Cambridge University Press:  01 November 2007

C. Suzuki ,
K. Yoshioka ,
M. Sakatani  and
M. Takahashi
C. Suzuki*
Affiliation:
Research Team for Production Diseases, National Institute of Animal Health, Kannondai 3–1–5, Tsukuba, Ibaraki 305–0856, Japan.
K. Yoshioka
Affiliation:
Research Team for Production Diseases, National Institute of Animal Health, Kannondai 3–1–5, Tsukuba, Ibaraki 305–0856, Japan.
M. Sakatani
Affiliation:
Research Team for Effects of Climate Change on Agriculture, National Agricultural Research Center for Kyushu Okinawa Region, 2421 Suya, Koshi, Kumamoto 861–1192, Japan.
M. Takahashi
Affiliation:
Research Team for Effects of Climate Change on Agriculture, National Agricultural Research Center for Kyushu Okinawa Region, 2421 Suya, Koshi, Kumamoto 861–1192, Japan.
*
All correspondence to: C. Suzuki, Research Team for Production Diseases, National Institute of Animal Health, Kannondai 3–1–5, Tsukuba, Ibaraki 305–0856, Japan. Tel: +81 29 838 7784. Fax: +81 29 838 7880. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

We previously developed an in vitro-production system for porcine embryos and reported that the addition of glutamine (Gln) and hypotaurine (HT) during in vitro culture improved embryo development. This study examined the effects of Gln and HT on in vitro development, intracellular oxidative status and DNA damage of porcine preimplantation embryos. Porcine zygotes produced by in vitro maturation (IVM) and in vitro fertilization (IVF) were cultured until day 2 (day 0 = day of IVF) in porcine zygote medium (PZM) including 2 mM Gln and 5 mM HT, namely PZM-5. On day 2, the cleaved embryos were selected and cultured for 24 h in PZM-5 to which one of the following substances was added: (1) none (control); (2) Gln; (3) HT; or (4) Gln + HT. After 24 h of culture in each medium, the embryos were then returned to PZM-5 and cultured until day 5. Day-5 blastocyst yield was significantly higher in the Gln and Gln + HT groups (p < 0.05) than in the control and HT groups. In addition, Gln + HT significantly increased the total number of cells in blastocysts (p < 0.05) compared with the control. Although the number of cells and the intracellular GSH levels in day-3 cleaved embryos did not differ among treatments, addition of Gln, HT or Gln + HT significantly (p < 0.05) reduced the intracellular H2O2 content and the extent of DNA damage compared with the control. These results indicate that the presence of Gln and HT in PZM-5 from day 2 to day 3 promotes the development of porcine embryos by improvement of intracellular oxidative status.

Keywords

Comet assayIn vitro culturePorcine embryosReactive oxygen species
Type
Research Article
Information
Zygote , Volume 15 , Issue 4 , November 2007 , pp. 317 - 324
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abeydeera, L.R., Wang, W.H., Cantley, T.C., Prather, R.S. & Day, B.N. (1999). Glutathione content and embryo development after in vitro fertilisation of pig oocytes matured in the presence of a thiol compound and various concentrations of cysteine. Zygote 7, 203–10.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
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
Anderson, J.E., Matteri, R.L., Abeydeera, L.R., Day, B.N. & Prather, R.S. (1999). Cyclin B1 transcript quantification over the maternal to zygotic transition in both in vivo- and in vitro-derived 4-cell porcine embryos. Biol. Reprod. 61, 1460–7.CrossRefGoogle Scholar
Babu, R., Eaton, S., Drake, D.P., Spitz, L. & Pierro, A. (2001). Glutamine and glutathione counteract the inhibitory effects of mediators of sepsis in neonatal hepatocytes. J. Pediatr. Surg. 36, 282–6.CrossRefGoogle ScholarPubMed
Bos, J.L., Fearon, E.R., Hamilton, S.R., Verlaan de, V.M., van Boom, J.H., Van Der Eb, A.J. & Vogelstein, B. (1987). Prevalence of Ras gene mutations in human colorectal cancers. Nature 327, 293–7.CrossRefGoogle ScholarPubMed
Boza, J.J., Moennoz, D., Bournot, C.E., Blum, S., Zbinden, I., Finot, P.A. & Ballevre, O. (2000). Role of glutamine on the de novo purine nucleotide synthesis in Caco-2 cells. Eur. J. Nutr. 39, 38–46.CrossRefGoogle Scholar
Burcham, P.C. (1998). Genotoxic lipid peroxidation products: their DNA damaging properties and role in formation of endogenous DNA adducts. Mutagenesis 13, 287–305.CrossRefGoogle ScholarPubMed
Calvin, H.I., Grosshans, K. & Blake, E.J. (1986). Estimation and manipulation of glutathione levels in prepuberal mouse ovaries and ova: relevance to sperm nucleus transformation in the fertilized egg. Gamete Res. 14, 265–75.CrossRefGoogle Scholar
Dumoulin, J.C.M., Evers, J.L.H., Bras, M., Pieters, M.H.E.C. & Geraedts, J.P.M. (1992). Positive effect of taurine on preimplantation development of mouse embryos in vitro. J. Reprod. Fertil. 94, 373–80.CrossRefGoogle ScholarPubMed
Evans, M.E., Jones, D.P. & Ziegler, T.R. (2003). Glutamine prevents cytokine-induced apoptosis in human colonic epithelial cells. J. Nutr. 133, 3065–71.CrossRefGoogle ScholarPubMed
Fox, R.E., Hopkins, I.B., Cabacungan, E.T. & Tildon, J.T. (1996). The role of glutamine and other alternate substrates as energy sources in the fetal rat lung type II cell. Pediatr. Res. 40, 135–41.CrossRefGoogle ScholarPubMed
Funahashi, H., Cantley, T.C., Stumpf, T.T., Terlouw, S.L. & Day, B.N. (1994). Use of low salt culture medium for in vitro maturation of porcine oocytes is associated with elevated oocyte glutathione levels and enhanced male pronuclear formation after in vitro fertilization. Biol. Reprod. 51, 633–9.CrossRefGoogle ScholarPubMed
Guérin, P., El Mouatassim, S. & Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–89 (review).CrossRefGoogle ScholarPubMed
Guyader-Joly, C., Guérin, P., Renard, J.P., Guillaud, J., Ponchon, S. & Ménézo, Y. (1998). Precursors of taurine in female genital tracts: effects on developmental capacity of bovine embryo produced in vitro. Amino Acids 15, 27–42.CrossRefGoogle ScholarPubMed
Halliwell, B. & Aruoma, O.I. (1991). DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Letts 281, 9–19 (review).CrossRefGoogle ScholarPubMed
Houghton, F.D., Hawkhead, J.A., Humpherson, P.G., Hogg, J.E., Balen, A.H., Rutherford, A.J. & Leese, H.J. (2002). Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum. Reprod. 17, 999–1005.CrossRefGoogle ScholarPubMed
Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J.L., Schroter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L.E. & Tscopp, J. (1997). Inhibition of death receptor signals by cellular FLIP. Nature 388, 190–5.CrossRefGoogle ScholarPubMed
Johnson, M.H. & Nasr Esfahani, M.H. (1994). Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Bioessays 16, 31–8 (review).CrossRefGoogle ScholarPubMed
Kitagawa, Y., Suzuki, k., Yoneda, A. & Watanabe, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS) and DNA fragmentation in porcine embryos. Theriogenology 62, 1186–97.CrossRefGoogle ScholarPubMed
Kosower, N.S. & Kosower, E.M. (1978). The glutathione status of cells. Int. Rev. Cytol. 54, 109–60.CrossRefGoogle ScholarPubMed
Manser, R.C., Leese, H.J. & Houghton, F.D. (2004). Effect of inhibiting nitric oxide production on mouse preimplantation embryo development and metabolism. Biol. Reprod. 71, 528–33.CrossRefGoogle ScholarPubMed
Marnett, L.J. (2000). Oxyradicals and DNA damage. Carcinogenesis 21, 361–70.CrossRefGoogle ScholarPubMed
Matés, J.M., Pérez-Gòmez, C., Núñez de Castro, I., Asenjo, M. & Márquez, J. (2002). Glutamine and its relationship with intracellular redox status, oxidative stress and cell proliferation/death. Int. J. Biochem. Cell. Biol. 34, 439–58.CrossRefGoogle ScholarPubMed
Mello-Filho, A.C. & Meneghini, R. (1984). In vivo formation of single-strand breaks in DNA by hydrogen peroxide is mediated by the Haber-Weiss reaction. Biochim. Biophys. Acta. 781, 56–63.CrossRefGoogle ScholarPubMed
Messina, S.A. & Dawson, R. (2000). Attenuation of oxidative damage to DNA by taurine and taurine analogues. Adv. Exp. Med. Biol. 483, 355–67.CrossRefGoogle Scholar
Miller, J.G.O. & Schultz, G.A. (1987). Amino acids content of preimplantation rabbit embryos and fluids of the reproductive tract. Biol. Reprod. 36, 125–9.CrossRefGoogle ScholarPubMed
Murphy, C. & Newsholme, P. (1997). Glutamine as a possible precursor of l-arginine and thus nitric oxide synthesis in murine macrophages. Biochem. Soc. Trans. 25, 404S.CrossRefGoogle ScholarPubMed
Nasr-Esfahani, M.H., Aitken, J.R. & 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.CrossRefGoogle ScholarPubMed
Petters, R.M., Johnson, B.H., Reed, M.L. & Archibong, A.E. (1990). Glucose, glutamine and inorganic phosphate in early development of the pig embryo in vitro. J. Reprod. Fertil. 89, 269–75.CrossRefGoogle ScholarPubMed
Reed, M.L., Illera, M.J. & Petters, R.M. (1992). In vitro culture of pig embryos. Theriogenology 37, 95–109.CrossRefGoogle Scholar
Sakatani, M., Kobayashi, S. & Takahashi, M. (2004). Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Mol. Reprod. Dev. 67, 77–82.CrossRefGoogle ScholarPubMed
Schoenbeck, R.A., Peters, M.S., Rickords, L.F., Stumpf, T.T. & Prather, R.S. (1992). Characterization of deoxyribonucleic acid synthesis and the transition from maternal to embryonic control in the 4-cell porcine embryo. Biol. Reprod. 47, 1118–25.CrossRefGoogle ScholarPubMed
Slater, T.F. (1984). Free-radical mechanisms in tissue injury. Biochem. J. 222, 1–15.CrossRefGoogle ScholarPubMed
Spiteller, G. (2001). Peroxidation of linoleic acid and its relation to aging and age dependent diseases. Mech. Ageing. Dev. 122, 617–57.CrossRefGoogle ScholarPubMed
Suzuki, C. & Yoshioka, K. (2006). Effects of amino acid supplements and replacement of polyvinyl alcohol with bovine serum albumin in porcine zygote medium. Reprod. Fertil. Dev. 18, 789–95.CrossRefGoogle ScholarPubMed
Takahashi, M., Keicho, K., Takahashi, H., Ogawa, H., Schultz, R.M. & Okano, A. (2000). Effect of oxidative stress on development and DNA damage in in-vitro cultured bovine embryos by comet assay. Theriogenology 54, 137–45.CrossRefGoogle ScholarPubMed
Tománek, M., Kopecny, V. & Kanka, J. (1989). Genome reactivation in developing early pig embryos: an ultrastructural and autoradiographic analysis. Anat. Embryol. 180, 309–16.CrossRefGoogle ScholarPubMed
Yang, H.W., Hwang, K.J., Kwon, H.C., Kim, H.S., Choi, K.W. & Oh, K.S. (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum. Reprod. 13, 998–1002.CrossRefGoogle ScholarPubMed
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M.K. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.CrossRefGoogle Scholar
Yoshioka, K., Suzuki, C., Itoh, S., Kikuchi, K., Iwamura, S. & Rodriguez Martinez, H. (2003). Production of piglets derived from in vitro-produced blastocysts fertilized and cultured in chemically defined media: Effects of theophylline, adenosine and cysteine during in vitro fertilization. Biol. Reprod. 69, 2092–9.CrossRefGoogle ScholarPubMed