Skip to main content Accessibility help
×
Home

Effect of mouse cumulus cells on the in vitro maturation and developmental potential of bovine denuded germinal vesicle oocytes

  • Xue-Ming Zhao (a1), Jing-Jing Ren (a1), Wei-Hua Du (a1), Hai-Sheng Hao (a1), Yan Liu (a1), Tong Qin (a1), Dong Wang (a1) and Hua-Bin Zhu (a2)...

Summary

We investigated the effect mouse cumulus cells (mCCs) on the in vitro maturation (IVM) and developmental potential of bovine denuded germinal vesicle oocytes (DOs). Cumulus–oocyte complexes (COCs), DOs and DOs cocultured with either mCCs (DOs + mCCs) or bovine cumulus cells (bCCs; DOs + bCCs) were subjected to IVM. The meiosis II (MII) rates of DOs, glutathione (GSH) contents, zona pellucida (ZP) hardening and parthenogenetic blastocyst rates of MII oocytes were determined. The relative expression levels of bone morphogenetic protein 15 (BMP-15) and growth differentiation factor 9 (GDF-9) in MII oocytes were measured using quantitative real-time polymerase chain reaction (PCR). mCCs significantly increased the MII rate of DOs from 53.5 ± 3.58% to 69.67 ± 4.72% (p < 0.05) but had no effect on the GSH content (2.17 ± 0.31 pmol/oocyte with mCCs, 2.14 ± 0.53 pmol/oocyte without mCCs). For the DOs + mCCs group, the BMP-15 and GDF-9 expression levels were significantly higher and the ZP dissolution time was significantly lower (162.49 ± 12.51 s) than that of the DOs group (213.95 ± 18.87 s; p < 0.05). The blastocyst rate of the DOs + mCCs group (32.56 ± 4.94%) was similar to that of the DOs group (31.75 ± 3.65%) but was significantly lower than that of the COCs group (43.52 ± 5.37%; p < 0.05). In conclusion, mCCs increased the MII rate of DOs and expression of certain genes in MII oocytes, and decreased the ZP hardening of MII oocytes, but could not improve their GSH content or developmental potential.

Copyright

Corresponding author

All correspondence to: Hua-Bin Zhu. Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS); No. 2 Yuanmingyuan Western Road, Haidian District, Beijing 100193, P.R. China. Tel: +86 10 62815892. Fax: +86 10 62895971. e-mail: huabinzhu@yahoo.com.cn.

References

Hide All
Abeydeera, L.R., Wang, W.H., Cantley, T.C., Rieke, A. & Day, B.N. (1998). Co-culture with follicular shell pieces can enhance the developmental competence of pig oocytes after in vitro fertilization: relevance to intracellular glutathione. Biol. Reprod. 158, 213–8.
Amano, T., Mori, T., Matsumoto, K., Iritani, A. & Watanabe, T. (2005). Role of cumulus cells during maturation of porcine oocytes in the rise in intracellular Ca2+ induced by inositol 1,4,5-trisphosphate. Theriogenology 64, 261–74.
Anderiesz, C. & Trounson, A.O. (1995). The effect of testosterone on the maturation and developmental capacity of murine oocytes in vitro . Hum. Reprod. 10, 2377–81.
Bongso, A., Ng, S.C., Fong, C.Y., Anandakumar, C., Marshall, B., Edirisinghe, R. & Ratnam, S. (1992). Improved pregnancy rate after transfer of embryos grown in human fallopian tubal cell coculture. Fertil. Steril. 58, 569–74.
Carabatsos, M.J., Sellitto, C., Goodenough, D.A. & Albertini, D.F. (2000). Oocyte–granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev. Biol. 226, 167–79.
Chin, A.H. & Chye, N.S. (2004). Investigations of oocyte in vitro maturation within a mouse model. Zygote 12, 118.
de Matos, D.G., Furnus, C.C. & Moses, D.F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–5.
El-Raey, M., Geshi, M., Somfai, T., Kaneda, M., Hirako, M., Abdel-Ghaffar, A.E., Sosa, G.A., El-Roos, M.E. & Nagai, T. (2011). Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol. Reprod. Dev. 78, 250–62.
Frasor, J., Sherbahn, R., Soltes, B., Molo, M.W., Binor, Z., Radwanska, E. & Rawlins, R.G. (1996). Optimizing tubal epithelial cell growth promotes mouse embryo hatching in coculture. J. Assist. Reprod. Genet. 13, 423–30.
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.
Ge, L., Han, D., Lan, G.C., Zhou, P., Liu, Y., Zhang, X., Sui, H.S. & Tan, J.H. (2008a). Factors affecting the in vitro action of cumulus cells on the maturing mouse oocytes. Mol. Reprod. Dev. 75, 136–42.
Ge, L., Sui, H.S., Lan, G.C., Liu, N., Wang, J.Z. & Tan, J.H. (2008b).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.
Geshi, M., Takenouchi, N., Yamauchi, N. & Nagai, T. (2000). Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells. Biol. Reprod. 63, 1730–4.
Gilchrist, R.B., Lane, M. & Thompson, J.G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–77.
Goldberg, J.M., Khalifa, E.A., Friedman, C.I. & Kim, M.H. (1991). Improvement of in vitro fertilization and early embryo development in mice by coculture with human fallopian tube epithelium. Am. J. Obstet. Gynecol. 165, 1802–5.
Goovaerts, I.G., Leroy, J.L., Rizos, D., Bermejo-Alvarez, P., Gutierrez-Adan, A., Jorssen, E.P. & Bols, P.E. (2011). Single in vitro bovine embryo production: coculture with autologous cumulus cells, developmental competence, embryo quality and gene expression profiles. Theriogenology 76, 12931303.
Hussein, T.S., Thompson, J.G. & Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.
Joo, B.S., Kim, M.K., Na, Y.J., Moon, H.S., Lee, K.S. & Kim, H.D. (2001). The mechanism of action of coculture on embryo development in the mouse model: direct embryo-to-cell contact and the removal of deleterious components. Fertil. Steril. 75, 193–9.
Lee, H.J., Quaas, A.M., Wright, D.L., Toth, T.L. & Teixeira, J.M. (2011). In vitro maturation (IVM) of murine and human germinal vesicle (GV)-stage oocytes by coculture with immortalized human fallopian tube epithelial cells. Fertil. Steril. 95, 1344–8.
Luberda, Z. (2005).The role of glutathione in mammalian gametes. Reprod. Biol. 5, 517.
Luciano, A.M., Lodde, V., Beretta, M.S., Colleoni, S., Lauria, A. & Modina, S. (2005). Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus–oocyte complexes: role of cumulus cells, cyclic adenosine 3’,5’-monophosphate, and glutathione. Mol. Reprod. Dev. 71, 389–97.
Machaty, Z., Funahashi, H., Day, B.N. & Prather, R.S. (1997). Developmental changes in the intracellular Ca2+ release mechanisms in porcine oocytes. Biol. Reprod. 56, 921–30.
Maedomari, N., Kikuchi, K., Ozawa, M., Noguchi, J., Kaneko, H., Ohnuma, K., Nakai, M., Shino, M., Nagai, T. & Kashiwazaki, N. (2007). Cytoplasmic glutathione regulated by cumulus cells during porcine oocyte maturation affects fertilization and embryonic development in vitro . Theriogenology 67, 983–93.
Matson, P.L., Graefling, J., Junk, S.M., Yovich, J.L. & Edirisinghe, W.R. (1997). Cryopreservation of oocytes and embryos: use of a mouse model to investigate effects upon zona hardness and formulate treatment strategies in an in-vitro fertilization programme. Hum. Reprod. 12, 1550–3.
Miao, Y.L., Liu, X.Y., Qiao, T.W., Miao, D.Q., Luo, M.J. & Tan, J.H. (2005). Cumulus cells accelerate aging of mouse oocytes. Biol. Reprod. 73, 1025–31.
Parikh, F.R., Nadkarni, S.G., Naik, N.J., Naik, D.J. & Uttamchandani, SA. (2006). Cumulus coculture and cumulus-aided embryo transfer increases pregnancy rates in patients undergoing in vitro fertilization. Fertil. Steril. 86, 839–47.
Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C (T) method. Nat. Protoc. 3, 1101–18.
Simón, C., Mercader, A., Garcia-Velasco, J., Nikas, G., Moreno, C., Remohí, J. & Pellicer, A. (1999). Coculture of human embryos with autologous human endometrial epithelial cells in patients with implantation failure. J. Clin. Endocrinol. Metab. 84, 2638–46.
Spandorfer, S.D., Pascal, P., Parks, J., Clark, R., Veeck, L., Davis, O.K. & Rosenwaks, Z. (2004). Autologous endometrial coculture in patients with IVF failure: outcome of the first 1,030 cases. J. Reprod. Med. 49, 463–7.
Vanderhyden, B.C. & Armstrong, D.T. (1989). Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol. Reprod. 40, 720–8.
Xu, J.S., Chan, S.T., Lee, W.W., Lee, K.F. & Yeung, W.S. (2004). Differential growth, cell proliferation, and apoptosis of mouse embryo in various culture media and in coculture. Mol. Reprod. Dev. 68, 7280.
Yeo, C.X., Gilchrist, R.B., Thompson, J.G. & Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 6773.
Zhang, L., Jiang, S., Wozniak, P.J., Yang, X. & Godke, R.A. (1995). Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro . Mol. Reprod. Dev. 40, 338–44.
Zuelke, K.A., Jeffay, SC., Zucker, RM. & Perreault, SD. (2003). Glutathione (GSH) concentrations vary with the cell cycle in maturing hamster oocytes, zygotes, and pre-implantation stage embryos. Mol. Reprod. Dev. 64, 106–12.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed