Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-22T08:13:05.412Z Has data issue: false hasContentIssue false
  • English
  • Français

Microtubule assembly and in vitro development of bovine oocytes with increased intracellular glutathione level prior to vitrification and in vitro fertilization

Published online by Cambridge University Press:  26 April 2013

H. Hara ,
I. Yamane ,
I. Noto ,
N. Kagawa ,
M. Kuwayama ,
M. Hirabayashi  and
S. Hochi
H. Hara
Affiliation:
Interdisciplinary Graduate School of Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan.
I. Yamane
Affiliation:
Graduate School of Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan.
I. Noto
Affiliation:
Graduate School of Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan.
N. Kagawa
Affiliation:
Kato Ladies Clinic, Shinjuku, Tokyo 160–0023, Japan.
M. Kuwayama
Affiliation:
Repro-Support Medical Research Centre, Shinjuku, Tokyo 160–0022, Japan.
M. Hirabayashi
Affiliation:
National Institute for Physiological Sciences, Okazaki, Aichi 444–8787, Japan. The Graduate University for Advanced Studies, Okazaki, Aichi 444–8787, Japan.
S. Hochi*
Affiliation:
Interdisciplinary Graduate School of Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan. Graduate School of Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan. Faculty of Textile Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan.
*
All correspondence to: S. Hochi. Interdisciplinary Graduate School of Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan. Tel: +81 268 215350. Fax: +81 268 215830. e-mail: shochi@shinshu-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

Although vitrification is a useful technique for preservation of bovine oocytes, the yield of blastocysts derived from the vitrified oocytes is still low. We have recently reported a new type of cryoinjury, multiple aster formation, by which pronuclear migration and development of vitrified–warmed and in vitro-fertilized bovine oocytes are impaired. The aim of the present study was to investigate the effect of glutathione (GSH) content of vitrified bovine oocytes on multiple aster formation and subsequent in vitro development. Treatment of bovine cumulus–oocyte complexes with β-mercaptoethanol (βME) and l-cysteine (Cys) during in vitro maturation resulted in 2.5-fold higher GSH content not only in fresh control but also in vitrified–warmed oocytes. The percentage of normally fertilized zygotes exhibiting sperm aster(s) was >95% in all four groups (with or without βME/Cys × fresh control or vitrified). The frequency of multiple aster formation in vitrified oocytes (three-fold higher than that in fresh control oocytes) was not affected by the increased level of intracellular GSH with βME/Cys. Consequently, the migration and development of pronuclei as well as the yield of blastocysts from vitrified–warmed oocytes (17 versus 41%) were not improved. In addition, there was no effect of increased GSH level on the yield of blastocysts in fresh control groups.

Keywords

Bovine oocytesIntracellular glutathioneβ-MercaptoethanolMultiple astersVitrification
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 476 - 482
Copyright
Copyright © Cambridge University Press 2013 

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. (1998). Presence of β-mercaptoethanol can increase the glutathione content of pig oocytes matured in vitro and the rate of blastocyst development after in vitro fertilization. Theriogenology 50, 747–56.Google Scholar
Balasubramanian, S. & Rho, G.J. (2007). Effect of cysteamine supplementation of in vitro matured bovine oocytes on chilling sensitivity and development of embryos. Anim. Reprod. Sci. 98, 282–92.Google Scholar
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.Google Scholar
Chian, R.C., Kuwayama, M., Tan, L., Tan, J., Kato, O. & Nagai, T. (2004). High survival rate of bovine oocytes matured in vitro following vitrification. J. Reprod. Dev. 50, 685–96.Google Scholar
Choe, C., Shin, Y.W., Kim, E.J., Sho, S.R., Kim, H.J., Choi, S.H., Han, M.H., Han, J., Son, D.S. & Kang, D. (2010). Synergistic effects of glutathione and β-mercaptoethanol treatment during in vitro maturation of porcine oocytes on early embryonic development in a culture system supplemented with L-cysteine. J. Reprod. Dev. 56, 575–82.Google Scholar
de Matos, D.G., Furnus, C.C., Moses, D.F. & Baldassarre, H. (1995). Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol. Reprod. Dev. 42, 432–6.Google Scholar
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.Google Scholar
de Matos, D.G., Herrera, C., Cortvrindt, R., Smitz, J., Van Soom, A., Nogueira, D. & Pasqualini, R.S. (2002). Cysteamine supplementation during in vitro maturation and embryo culture: a useful tool for increasing the efficiency of bovine in vitro embryo production. Mol. Reprod. Dev. 62, 203–9.Google Scholar
Fuku, E., Kojima, T., Shioya, Y., Marcus, G.J. & Downey, B.R. (1992). In vitro fertilization and development of frozen–thawed bovine oocytes. Cryobiology 29, 485–92.Google Scholar
Furnus, C.C. & de Matos, D.G. (1999). The availability of cysteine in culture medium appears to be the limiting factor for glutathione synthesis in mammalian oocytes. Theriogenology 51, 373.Google Scholar
Ge, L., Sui, H.S., Lan, G.C., Liu, N., Wang, J.Z. & Tan, J.H. (2008). Coculture with cumulus cells improves maturation of mouse oocytes denuded of the cumulus oophorus: observations of nuclear and cytoplasmic events. Fertil. Steril. 90, 2376–88.Google Scholar
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010). Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil. Steril. 93, 2602–7.Google Scholar
Hara, H., Abdalla, H., Morita, H., Kuwayama, M., Hirabayashi, M. & Hochi, S. (2011). Procedure for bovine ICSI, not sperm freeze-drying, impairs the function of the microtubule-organizing center. J. Reprod. Dev. 57, 428–32.Google Scholar
Hara, H., Hwang, I.S., Kagawa, N., Kuwayama, M., Hirabayashi, M. & Hochi, S. (2012). High incidence of multiple aster formation in vitrified–warmed bovine oocytes after in vitro fertilization. Theriogenology 77, 908–15.Google Scholar
Holm, P., Booth, P.J., Schmidt, M.H., Greve, T. & Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.Google Scholar
Ishii, T., Bannai, S. & Sugita, Y. (1981). Mechanism of growth stimulation of L1210 cells by 2-mercaptoethanol in vitro. Role of the mixed disulfide of 2-mercaptoethanol and cysteine. J. Biol. Chem. 256, 12387–92.Google Scholar
Kim, M.K., Hossein, M.S., Oh, H.J., Fibrianto, H.Y., Jang, G., Kim, H.J., Hong, S.G., Park, J.E., Kang, S.K. & Lee, B.C. (2007). Glutathione content of in vivo and in vitro matured canine oocytes collected from different reproductive stages. J. Vet. Med. Sci. 69, 627–32.Google Scholar
Larman, M.G., Sheehan, C.B. & Gardner, D.K. (2006). Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction 131, 53–61.Google Scholar
Leibo, S.P. (1981). Preservation of ova and embryos by freezing. In: New Technologies in Animal Breeding (eds B.G. Brackett, G.E. Seidel Jr & S.M. Seidel). New York: Academic Press, pp 127–39.Google Scholar
Meister, A. (1983). Selective modification of glutathione metabolism. Science 220, 472–7.Google Scholar
Mizushima, S. & Fukui, Y. (2001). Fertilizability and developmental capacity of bovine oocytes cultured individually in a chemically defined maturation medium. Theriogenology 55, 1431–45.CrossRefGoogle Scholar
Ohmori, H. & Yamamoto, I. (1983). Mechanism of augmentation of the antibody response in vitro by 2-mercaptoethanol in murine lymphocytes. II. A major role of the mixed disulfide between 2-mercaptoethanl and cysteine. Cell. Immunol. 79, 173–85.Google Scholar
Perreault, S.D., Barbee, R.R. & Slott, V.L. (1988). Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev. Biol. 125, 181–6.CrossRefGoogle ScholarPubMed
Rodríguez-González, E., López-Bejar, M., Mertens, M.J. & Paramio, M.T. (2003). Effects on in vitro embryo development and intracellular glutathione content of the presence of thiol compounds during maturation of prepubertal goat oocytes. Mol. Reprod. Dev. 65, 446–53.Google Scholar
Schatten, G. (1994). The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev. Biol. 165, 299–335.Google Scholar
Shi, W.Q., Zhu, S.E., Zhang, D., Wang, W.H., Tang, G.L., Hou, Y.P. & Tian, S.J. (2006). Improved development by Taxol pretreatment after vitrification of in vitro matured porcine oocytes. Reproduction 131, 795–804.Google Scholar
Shimizu, H., Nagamori, I., Yabuta, N. & Nojima, H. (2009). GAK, a regulator of clathrin-mediated membrane traffic, also controls centrosome integrity and chromosome congression. J. Cell. Sci. 122, 3145–52.CrossRefGoogle Scholar
Somfai, T., Ozawa, M., Noguchi, J., Kaneko, H., Kuriani Karja, N.W., Farhudin, M., Dinnyés, A., Nagai, T. & Kikuchi, K. (2007). Developmental competence of in vitro-fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle stage. Cryobiology 55, 115–26.Google Scholar
Sutovsky, P. & Schatten, G. (1997). Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol. Reprod. 56, 1503–12.Google Scholar
Takahashi, M., Nagai, T., Hamano, S., Kuwayama, M., Okamura, N. & Okano, A. (1993). Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol. Reprod. 49, 228–32.Google Scholar
Yoshida, M., Ishigaki, K., Nagai, T., Chikyu, M. & Pursel, V.G. (1993). Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol. Reprod. 49, 89–94.Google Scholar