Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T07:54:53.389Z Has data issue: false hasContentIssue false
  • English
  • Français

The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress

Published online by Cambridge University Press:  18 May 2011

Hisashi Nabenishi ,
Hiroshi Ohta ,
Toshihumi Nishimoto ,
Tetsuo Morita ,
Koji Ashizawa  and
Yasuhiro Tsuzuki
Hisashi Nabenishi
Affiliation:
Domestic Animal Biotechnology Department, Miyazaki Livestock Research Institute, Takaharu-Cho, Nishi-Morokata-Gun, Miyazaki 889–4411, Japan. Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
Hiroshi Ohta
Affiliation:
Domestic Animal Biotechnology Department, Miyazaki Livestock Research Institute, Takaharu-Cho, Nishi-Morokata-Gun, Miyazaki 889–4411, Japan.
Toshihumi Nishimoto
Affiliation:
Domestic Animal Biotechnology Department, Miyazaki Livestock Research Institute, Takaharu-Cho, Nishi-Morokata-Gun, Miyazaki 889–4411, Japan.
Tetsuo Morita
Affiliation:
Animal Nutrition Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
Koji Ashizawa
Affiliation:
Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
Yasuhiro Tsuzuki*
Affiliation:
Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
*
All correspondence to: Yasuhiro Tsuzuki. Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan. Tel: +81 985 58 7195. Fax: +81 985 58 7195. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In the present study, we investigated the effects of various concentrations of cysteine (0.0, 0.6, 1.2 and 1.8 mM) added to the maturation medium on nuclear maturation and subsequent embryonic development of bovine oocytes exposed to heat stress (HS: set at 39.5 °C for 5 h, 40.0 °C for 5 h, 40.5 °C for 6 h, and 40.0 °C for 4 h versus 38.5 °C for 20 h as the control group). This regime mimicked the circadian rhythm of the vaginal temperature of lactating dairy cows during the summer season in southwestern Japan. Moreover, we also evaluated the oocyte's reactive oxygen species (ROS) and glutathione (GSH) levels and the apoptosis levels of the oocytes and cumulus cells in the presence or absence of 1.2 mM cysteine. As a result, HS in the without-cysteine group significantly suppressed (p < 0.05) both the nuclear maturation rate up to the metaphase (M)II stage and the blastocyst formation rate compared with that of the control group. In addition, this group showed significantly higher (p < 0.05) ROS levels and significantly lower (p < 0.05) GSH levels than those of the control group. Moreover, the level of TdT-mediated dUTP nick end labelling (TUNEL)-positive cumulus cells in the HS without-cysteine group was significantly higher (p < 0.05) than that of the control group. However, the addition of 1.2 mM cysteine to the maturation medium restored not only the nuclear maturation, blastocyst formation rates and GSH contents, but also increased the ROS and TUNEL-positive levels of the cumulus cells, but not oocytes, to that of the control group. These results indicate that the addition of 1.2 mM cysteine during in vitro maturation (IVM) may alleviate the influence of heat stress for oocyte developmental competence by increasing GSH content and inhibiting the production of oocyte ROS followed by apoptosis of cumulus cells.

Keywords

ApoptosisBovine oocytesCysteineGlutathioneHeat stressROS
Type
Research Article
Information
Zygote , Volume 20 , Issue 3 , August 2012 , pp. 249 - 259
Copyright
Copyright © Cambridge University Press 2011

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

Al-Gubory, K.H., Fowler, P.A. & Garrel, C. (2010). The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int. J. Biochem. Cell Biol. 42, 1634–50.CrossRefGoogle ScholarPubMed
Arav, A., Zeron, Y., Leslie, S.B., Behboodi, E., Anderson, G.B. & Crowe, J.H. (1996). Phase transition temperature and chilling sensitivity of bovine oocytes. Cryobiology 33, 589–99.CrossRefGoogle ScholarPubMed
Balboula, A.Z., Yamanaka, K., Sakatani, M., Hegab, A.O., Zaabel, S.M. & Takahashi, M. (2010). Cathepsin B activity is related to the quality of bovine cumulus oocyte complexes and its inhibition can improve their developmental competence. Mol. Reprod. Dev. 77, 439–48.CrossRefGoogle Scholar
Chian, R.C., Niwa, K. & Nakahara, H. (1992). Effect of sperm penetration in vitro on completion of first meiosis by bovine oocytes arrested at various stages in culture. J. Reprod. Fertil. 96, 73–8.CrossRefGoogle ScholarPubMed
Chebel, R.C., Santos, J.E., Reynolds, J.P., Cerri, R.L., Juchem, S.O. & Overton, M. (2004). Factors affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows. Anim. Reprod. Sci. 84, 239–55.CrossRefGoogle ScholarPubMed
Circu, M.L. & Aw, T.Y. (2008). Glutathione and apoptosis. Free Radic. Res. 42, 689–706.CrossRefGoogle ScholarPubMed
Circu, M.L. & Aw, T.Y. (2010). Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 48, 749–62.CrossRefGoogle ScholarPubMed
Combelles, C.M., Gupta, S. & Agarwal, A. (2009). Could oxidative stress influence the in-vitro maturation of oocytes? Reprod. Biomed. Online 18, 864–80.CrossRefGoogle ScholarPubMed
Deleuze, S. & Goudet, G. (2010). Cysteamine supplementation of in vitro maturation media: a review. Reprod. Dom. Anim. 45, e476–82.CrossRefGoogle ScholarPubMed
de Matos, D.G., Furnus, C.C., Moses, D.F., Martinez, A.G. & Matkovic, M. (1996). Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Mol. Reprod. Dev. 45, 451–7.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Dominko, T. & First, N.L. (1997). Timing of meiotic progression in bovine oocytes and its effect on early embryo development. Mol. Reprod. Dev. 47, 456–67.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Ealy, A.D., Drost, M., Barros, C.M. & Hansen, P.J. (1992). Thermoprotection of preimplantation bovine embryos from heat shock by glutathione and taurine. Cell. Biol. Int Reprod. 16, 125–31.Google ScholarPubMed
Edwards, J.L. & Hansen, P.J. (1996). Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biol. Reprod. 55, 341–6.Google ScholarPubMed
Edwards, J.L. & Hansen, P.J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–45.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Edwards, J.L., Saxton, A.M., Lawrence, J.L., Payton, R.R. & Dunlap, J.R. (2005). Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J. Dairy Sci. 88, 4326–33.CrossRefGoogle ScholarPubMed
Franco, R. & Cidlowski, J.A. (2009). Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ. 16, 1303–14.CrossRefGoogle ScholarPubMed
Furnus, C.C., de Matos, D.G., Picco, S., García, P.P., Inda, A.M., Mattioli, G. & Errecalde, A.L. (2008). Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim. Reprod. Sci. 109, 88–99.CrossRefGoogle ScholarPubMed
Hansen, P.J. (2009). Effects of heat stress on mammalian reproduction. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 3341–50.CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Yamada, M. & Imai, H. (2000). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol. Reprod. Dev. 56, 520–6.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Kim, H.S., Jeong, Y.I., Lee, J.Y., Jeong, Y.W., Hossein, M.S., Hyun, H.S. & Hwang, W.S. (2010). Effects of recombinant relaxin on in vitro maturation of porcine oocytes. J. Vet. Med. Sci. 72, 333–7.CrossRefGoogle ScholarPubMed
Ju, J.C., Jiang, S., Tseng, J.K., Parks, J.E. & Yang, X. (2005). Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes. Theriogenology 64, 1677–89.CrossRefGoogle ScholarPubMed
Lawrence, J.L., Payton, R.R., Godkin, J.D., Saxton, A.M., Schrick, F.N. & Edwards, J.L. (2004). Retinol improves development of bovine oocytes compromised by heat stress during maturation. J. Dairy Sci. 87, 2449–54.CrossRefGoogle ScholarPubMed
Luberda, Z. (2005). The role of glutathione in mammalian gametes. Reprod. Biol. 5, 5–17.Google ScholarPubMed
Matsuzuka, T., Ozawa, M., Nakamura, A., Ushitani, A., Hirabayashi, M. & Kanai, Y. (2005a). Effects of heat stress on the redox status in the oviduct and early embryonic development in mice. J. Reprod. Dev. 51, 281–7.CrossRefGoogle ScholarPubMed
Matsuzuka, T., Sakamoto, N., Ozawa, M., Ushitani, A., Hirabayashi, M. & Kanai, Y. (2005b). Alleviation of maternal hyperthermia-induced early embryonic death by administration of melatonin to mice. J. Pineal Res. 39, 217–23.CrossRefGoogle ScholarPubMed
Meister, A. & Tate, S.S. (1976). Glutathione and related γ-glutamyl compounds: biosynthesis and utilization. Annu. Rev. Biochem. 45, 559–604.CrossRefGoogle ScholarPubMed
Meister, A. (1983). Selective modification of glutathione metabolism. Science 220, 472–7.CrossRefGoogle ScholarPubMed
Morado, S.A., Cetica, P.D., Beconi, M.T. & Dalvit, G.C. (2009). Reactive oxygen species in bovine oocyte maturation in vitro. Reprod. Fertil. Dev. 21, 608–14.CrossRefGoogle ScholarPubMed
Nabenishi, H., Ohta, H., Nishimoto, T., Morita, T., Ashizawa, K. & Tsuzuki, Y. (2011). Effect of the temperature–humidity index on body temperature and conception rate of lactating dairy cows in southwestern Japan. J. Reprod. Dev. (in press).CrossRefGoogle Scholar
Niwa, K., Park, C.K. & Okuda, K. (1991). Penetration in vitro of bovine oocytes during maturation by frozen–thawed spermatozoa. J. Reprod. Fertil. 91, 329–36.CrossRefGoogle ScholarPubMed
Ozawa, M., Hirabayashi, M. & Kanai, Y. (2002). Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reproduction 124, 683–9.CrossRefGoogle ScholarPubMed
Rivera, R.M. & Hansen, P.J. (2001). Development of cultured embryos after exposure to high temperatures in the physiological range. Reproduction 121, 107–15.CrossRefGoogle ScholarPubMed
Roth, Z., Meidan, R., Braw-Tal, R. & Wolfenson, D. (2000). Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J. Reprod. Fertil. 120, 83–90.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2004a). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–1906.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2004b). Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol. Reprod. 71, 2072–8.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–44.CrossRefGoogle ScholarPubMed
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
Sakatani, M., Suda, I., Oki, T., Kobayashi, S., Kobayashi, S. & Takahashi, M. (2007). Effects of purple sweet potato anthocyanins on development and intracellular redox status of bovine preimplantation embryos exposed to heat shock. J. Reprod. Dev. 53, 605–14.CrossRefGoogle ScholarPubMed
Sakatani, M., Yamanaka, K., Kobayashi, S. & Takahashi, M. (2008). Heat shock-derived reactive oxygen species induce embryonic mortality in in vitro early stage bovine embryos. J. Reprod. Dev. 54, 496–501.CrossRefGoogle ScholarPubMed
Somfai, T., Kashiwazaki, N., Ozawa, M., Nakai, M., Maedomari, N., Noguchi, J., Kaneko, H., Nagai, T. & Kikuchi, K. (2008). Effect of centrifugation treatment before vitrification on the viability of porcine mature oocytes and zygotes produced in vitro. J. Reprod. Dev. 54, 149–55.CrossRefGoogle ScholarPubMed
Soto, P. & Smith, L.C. (2009). BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Mol. Reprod. Dev. 76, 637–46.CrossRefGoogle ScholarPubMed
Sugiyama, S., McGowan, M., Kafi, M., Phillips, N. & Young, M. (2003). Effects of increased ambient temperature on the development of in vitro derived bovine zygotes. Theriogenology 60, 1039–47.CrossRefGoogle ScholarPubMed
Sugiyama, S., McGowan, M., Phillips, N., Kafi, M. & Young, M. (2007). Effects of increased ambient temperature during IVM and/or IVF on the in vitro development of bovine zygotes. Reprod. Domest. Anim. 42, 271–4.CrossRefGoogle ScholarPubMed
Suzuki, Y., Watanabe, H. & Fukui, Y. (2010). Effects of seasonal changes on in vitro developmental competence of porcine oocytes. J. Reprod. Dev. 56, 396–9.CrossRefGoogle ScholarPubMed
Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M. & de Kruif, A. (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414–24.CrossRefGoogle ScholarPubMed
Tatemoto, H., Sakurai, N. & Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–10.CrossRefGoogle ScholarPubMed
Thompson, J.G., Lane, M. & Gilchrist, R.B. (2007). Metabolism of the bovine cumulus–oocyte complex and influence on subsequent developmental competence. Soc. Reprod. Fertil. Suppl. 64, 179–90.Google ScholarPubMed
Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A. & Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68S, S131–7.CrossRefGoogle Scholar
Viet-Linh, N., Dang-Nguyen, T.Q., Nguyen, B.X., Manabe, N. & Nagai, T. (2009). Effects of cysteine during in vitro maturation of porcine oocytes under low oxygen tension on their subsequent in vitro fertilization and development. J. Reprod. Dev. 55, 594–8.CrossRefGoogle ScholarPubMed
Yuan, Y.Q., Van Soom, A., Leroy, J.L.M.R., Dewulf, J., Van Zeveren, A., de Kruif, A. & Peelman, L.J. (2005). Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 63, 2147–63.CrossRefGoogle Scholar
Yuan, Y., Hao, Z.D., Liu, J., Wu, Y., Yang, L., Liu, G.S., Tian, J.H., Zhu, S.E. & Zeng, S.M. (2008). Heat shock at the germinal vesicle breakdown stage induces apoptosis in surrounding cumulus cells and reduces maturation rates of porcine oocytes in vitro. Theriogenology 70, 168–78.CrossRefGoogle ScholarPubMed
Zhandi, M., Towhidi, A., Nasr-Esfahani, M.H., Eftekhari-Yazdi, P. & Zare-Shahneh, A. (2009). Unexpected detrimental effect of insulin like growth factor-1 on bovine oocyte developmental competence under heat stress. J. Assist. Reprod. Genet. 26, 605–11.CrossRefGoogle ScholarPubMed