Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-27T22:19:23.389Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  01 February 2013

Xue-Ming Zhao ,
Jing-Jing Ren ,
Wei-Hua Du ,
Hai-Sheng Hao ,
Yan Liu ,
Tong Qin ,
Dong Wang  and
Hua-Bin Zhu
Xue-Ming Zhao
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Jing-Jing Ren
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Wei-Hua Du
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Hai-Sheng Hao
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Yan Liu
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Tong Qin
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Dong Wang
Affiliation:
Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, P.R. China.
Hua-Bin Zhu*
Affiliation:
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.
*
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: [email protected].
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

BovineCo-cultureCumulus cellsMouseOocyte
Type
Research Article
Information
Zygote , Volume 22 , Issue 3 , August 2014 , pp. 348 - 355
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., 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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Chin, A.H. & Chye, N.S. (2004). Investigations of oocyte in vitro maturation within a mouse model. Zygote 12, 1–18.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.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
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 1293–1303.CrossRefGoogle ScholarPubMed
Hussein, T.S., Thompson, J.G. & Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Luberda, Z. (2005).The role of glutathione in mammalian gametes. Reprod. Biol. 5, 5–17.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C (T) method. Nat. Protoc. 3, 1101–18.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 72–80.CrossRefGoogle ScholarPubMed
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, 67–73.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed