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Co-culture embedded in cumulus clumps promotes maturation of denuded oocytes and reconstructs gap junctions between oocytes and cumulus cells

Published online by Cambridge University Press:  31 October 2012

Guixue Feng ,
Deshun Shi ,
Shufang Yang  and
Xiaoli Wang
Guixue Feng
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 53005, P.R. China. Reproductive Medical Center, Maternal and Child Health Hospital of Guangxi Zhuang Autonomous Region, Nanning 530003, P.R. China.
Deshun Shi*
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 53005, P.R. China. Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 53005, P.R. China.
Shufang Yang
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 53005, P.R. China.
Xiaoli Wang
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 53005, P.R. China.
*
All correspondence to: Deshun Shi. Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 53005, P.R. China. Fax: +86 771 3239202. e-mail: [email protected]
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Summary

The present study was undertaken to establish an effective method for in vitro maturation (IVM) of denuded oocytes (DOs) by simulating the ovarian three-dimensional status in vivo using buffalo ovarian tissues or cumulus cells, so as to provide a model for investigating the mechanisms of oocyte maturation. Buffalo cumulus–oocyte complexes from ovaries taken at slaughter were denuded by pipetting, and then allocated randomly into four groups for IVM by direct culture in maturation medium (M1, control group), co-culture with a monolayer of cumulus cells (M2), embedded in cumulus cell clumps (M3) and ovarian tissue (M4) for 24 h. The nuclear maturation of DOs was assessed by the extrusion of the first polar body and the cytoplasmic maturation was evaluated by subsequently developmental capacity after parthenogenetic activation. More DOs matured to MII (56.89%) and developed to blastocysts (25.75%) when they were matured in vitro with M3 in comparison with DOs matured in vitro with M1 (45.14 and 15.97%) and M4 (40.48 and 13.49%). Further detection of gap junctions by injecting Lucifer yellow directly into cytoplasm of matured DOs with adherent cumulus cells and scanning with confocal microscope showed that Lucifer yellow were found in nine out of 11 the adherent cumulus cells in M3, indicating that the gap junctions between oocytes and cumulus cells was reconstructed in vitro. These results indicate that co-culture of DOs embedded in cumulus cell clumps can improve their nuclear and cytoplasmic maturation of DOs, possibly through the reconstruction of gap junctions in vitro.

Keywords

Cumulus cellsDenuded oocyteGap junctionIn vitro maturation
Type
Research Article
Information
Zygote , Volume 21 , Issue 3 , August 2013 , pp. 231 - 237
Copyright
Copyright © Cambridge University Press 2012 

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References

Canipari, R. (2000). Oocyte–granulosa cell interactions. Hum. Reprod. Update 6, 279–89.CrossRefGoogle ScholarPubMed
Cha, K.Y. & Chian, R.C. (1998). Maturation in vitro of immature human oocytes for clinical use. Hum. Reprod. Update 4, 103–120CrossRefGoogle ScholarPubMed
Chang, H.C., Liu, H., Zhang, J., Grifo, J. & Krey, L.C. (2005). Developmental incompetency of denuded mouse oocytes undergoing maturation in vitro is ooplasmic in nature and is associated with aberrant Oct-4 expression. Hum. Reprod. 20, 1958–68.CrossRefGoogle ScholarPubMed
Chian, R.C., Niwa, K. & Sirard, M.A. (1994). Effects of cumulus cells on male pronuclear formation and subsequent early development of bovine oocytes in vitro. Theriogenology 41, 1499–508.CrossRefGoogle ScholarPubMed
Combelles, C.M., Cekleniak, N.A., Racowsky, C. & Albertini, D.F. (2002) Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum. Reprod. 17, 1006–16.CrossRefGoogle ScholarPubMed
Combelles, C.M., Fissore, R.A., Albertini, D.F. & Racowsky, C. (2005). In vitro maturation of human oocytes and cumulus cells using a co-culture three-dimensional collagen gel system. Hum. Reprod. 20, 1349–58.CrossRefGoogle ScholarPubMed
Conti, M. (2010) Signaling networks in somatic cells and oocytes activated during ovulation. annales d endocrinologie (Paris) 71, 189–90.CrossRefGoogle ScholarPubMed
Eppig, J.J., Pendola, F.L., Wigglesworth, K. & Pendola, J.K. (2005). Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol. Reprod. 73, 351–7.CrossRefGoogle ScholarPubMed
Fatehi, A.N., Roelen, B.A., Colenbrander, B., Schoevers, E.J., Gadella, B.M., Beverst, M.M. & van denHurk, R. (2005). Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development. Zygote 13, 177–85.CrossRefGoogle Scholar
Fatehi, A.N., Zeinstra, E.C., Kooij, R.V., Colenbrander, B. & Bevers, M.M. (2002). Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 57, 1347–55.CrossRefGoogle ScholarPubMed
Fitzharris, G. & Baltz, J.M. (2006). Granulosa cells regulate intracellular pH of the murine growing oocyte via gap junctions: development of independent homeostasis during oocyte growth. Development 133, 591–9.CrossRefGoogle ScholarPubMed
Ge, L., Sui, H.S., Lan, G.C., Liu, N., Wang, J.Z. & TanJ, H. 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.CrossRefGoogle ScholarPubMed
Hardy, K., Wright, C.S., Franks, S. & Winston, R.M. (2000). In vitro maturation of oocytes. Br. Med. Bull. 56, 588–602.CrossRefGoogle ScholarPubMed
Hashimoto, S., Saeki, K., Nagao, Y., Minami, N., Yamada, M. & Utsumi, K. (1998). Effects of cumulus cell density during in vitro maturation of the developmental competence of bovine oocytes. Theriogenology 49, 1451–63.CrossRefGoogle ScholarPubMed
Isobe, N. & Terada, T. (2001). Effect of the factor inhibiting germinal vesicle breakdown on the disruption of gap junctions and cumulus expansion of pig cumulus-oocyte complexes cultured in vitro. Reproduction 121, 249–57.CrossRefGoogle ScholarPubMed
Isobe, N., Maeda, T. & Terada, T. (1998). Involvement of meiotic resumption in the disruption of gap junctions between cumulus cells attached to pig oocytes. J. Reprod. Fertil 113, 167–72.CrossRefGoogle ScholarPubMed
Li, R., Norman, R.J., Armstrong, D.T. & Gilchrist, R.B. (2000). Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol. Reprod. 63, 839–45.CrossRefGoogle ScholarPubMed
Lu, F., Shi, D., Wei, J., Yang, S. & Wei, Y. (2005). Development of embryos reconstructed by interspecies nuclear transfer of adult fibroblasts between buffalo (Bubalus bubalis) and cattle (Bos indicus). Theriogenology 64, 1309–19.CrossRefGoogle ScholarPubMed
Ma, S., Lin, H., Miao, Y., Liu, X., Wang, B. & Dai, J. (2007). The effect of three-dimensional demineralized bone matrix on in vitro cumulus-free oocyte maturation. Biomaterials 28, 3198–207.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
Mermillod, P., Oussaid, B. & Cognie, Y. (1999). Aspects of follicular and oocyte maturation that affect the developmental potential of embryos. J. Reprod. Fertil. (Suppl.) 54, 449–60.Google ScholarPubMed
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
Norris, R.P., Ratzan, W.J., Freudzon, M., Mehlmann, L.M., Krall, J., Movsesian, M.A., Wang, H., Ke, H., Nikolaev, V.O. & Jaffe, L.A. (2009). Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136, 1869–78.CrossRefGoogle ScholarPubMed
Orisaka, M., Tajima, K., Tsang, B.K. & Kotsuji, F. (2009). Oocyte–granulosa–theca cell interactions during preantral follicular development. J. Ovarian. Res. 2, 9.CrossRefGoogle ScholarPubMed
Schroeder, A.C. & Eppig, J.J. (1984). The developmental capacity of mouse oocytes that matured spontaneously in vitro is normal. Dev. Biol 102, 493–97.CrossRefGoogle Scholar
Thomas, F.H. & Vanderhyden, B.C. (2006). Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod. Biol Endocrinol. 4, 19.CrossRefGoogle ScholarPubMed
Trounson, A., Anderiesz, C. & Jones, G. (2001). Maturation of human oocytes in vitro and their developmental competence. Reproduction 121, 51–75.CrossRefGoogle ScholarPubMed
Vaccari, S., Horner, K., Mehlmann, L.M. & Conti, M. (2008). Generation of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Dev. Biol. 316, 124–34.CrossRefGoogle ScholarPubMed
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
Vanhoutte, L., Nogueira, D. & De Sutter, P. (2009). Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence. Hum. Reprod. 24, 658–69.CrossRefGoogle Scholar
Wongsrikeao, P., Kaneshige, Y., Ooki, R., Taniguchi, M., Agung, B., Nii, M. & Otoi, T. (2005). Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod. Domest. Anim. 40, 166–70.CrossRefGoogle ScholarPubMed
Wongsrikeao, P., Otoi, T., Murakami, M., Karja, N.W., Budiyanto, A., Murakami, M., Nii, M. & Suzuki, T. (2004). Relationship between DNA fragmentation and nuclear status of in vitro-matured porcine oocytes: role of cumulus cells. Reprod. Fertil. Dev. 16, 773–80.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