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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Involvement of E-cadherin in early in vitro development of adult and juvenile sheep embryos

Silvia Modina A D , Giovanni G. Leoni B , Valentina Lodde A , Salvatore Naitana C , Silvia Pirani A , Sara Succu C , Fiammetta Berlinguer C and Alberto Maria Luciano A
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, University of Milan, Milan 20122, Italy.

B Department of Physiological, Biochemical and Cellular Sciences, University of Sassari, Sassari 07100, Italy.

C Department of Animal Biology, University of Sassari, Sassari 07100, Italy.

D Corresponding author. Email: silvia.modina@unimi.it

Reproduction, Fertility and Development 22(2) 468-477 https://doi.org/10.1071/RD09125
Submitted: 22 May 2009  Accepted: 1 September 2009   Published: 4 January 2010

Abstract

The oocyte-to-embryo transition in mammals depends on maternal proteins and transcripts, which accumulate during oocyte differentiation. The aim of the present study was to examine the role of the junctional proteins β-catenin and E-cadherin during preimplantation in vitro embryo development in sheep, comparing the competence of adult and prepubertal oocytes. We analysed the concentration of β-catenin and E-cadherin in immature and in vitro-matured oocytes. There was a significant increase in E-cadherin concentration after 24 h of in vitro maturation and this was lower in prepubertal oocytes than in adult ones. We therefore studied the expression and distribution of E-cadherin during the major transition from maternal to embryonic genome. E-cadherin distribution and localisation in sheep was age- and developmental-stage dependent and was related to developmental kinetics. In fact, in adults, the majority of embryos showed the proper distribution of E-cadherin just beneath the membrane surfaces of all blastomeres and the percentage of embryos with this distribution increased with the increase in cell number during development. On the contrary, and regardless of their developmental stage, the majority of prepubertal embryos showed an uneven distribution of the protein, often associated with the occurrence of cellular fragmentation. In conclusion, our results suggest that E-cadherin plays a pivotal role during preimplantation embryo growth in sheep and may be one of the possible cytoplasmic factors involved in the reduced developmental competence of prepubertal female gametes.

Additional keywords: oocytes, preimplantation embryo development, prepubertal sheep.


Acknowledgements

The authors thank Dr U. Fascio of the CIMA-Interdepartmental Center of Advanced Microscopy, University of Milan, for his work in confocal image analysis and Mrs. Laura Baraldi Scesi for her excellent technical support in morphological investigation and embryo manipulation. Work supported by PRIN 2005 MIUR and FIRST 2007 UMIL.


References

Alikani, M. (2005). Epithelial cadherin distribution in abnormal human pre-implantation embryos. Hum. Reprod. 20, 3369–3375.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology 55, 1303–1322.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Barcroft, L. C. , Hay-Schmidt, A. , Caveney, A. , Gilfoyle, E. , Overstrom, E. W. , Hyttel, P. , and Watson, A. J. (1998). Trophectoderm differentiation in the bovine embryo: characterization of a polarized epithelium. J. Reprod. Fertil. 114, 327–339.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Bettegowda, A. , and Smith, G. W. (2007). Mechanisms of maternal mRNA regulation: implications for mammalian early embryonic development. Front. Biosci. 12, 3713–3726.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Bettegowda, A. , Lee, K. B. , and Smith, G. W. (2008). Cytoplasmic and nuclear determinants of the maternal-to-embryonic transition. Reprod. Fertil. Dev. 20, 45–53.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Biensen, N. J. , Wilson, M. E. , and Ford, S. P. (1998). The impact of either a Meishan or Yorkshire uterus on Meishan or Yorkshire fetal and placental development to Days 70, 90, and 110 of gestation. J. Anim. Sci. 76, 2169–2176.
PubMed |

Bloor, D. J. , Metcalfe, A. D. , Rutherford, A. , Brison, D. R. , and Kimber, S. J. (2002). Expression of cell adhesion molecules during human preimplantation embryo development. Mol. Hum. Reprod. 8, 237–245.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Cognié, Y. , Poulin, N. , Locatelli, Y. , and Mermillod, P. (2004). State-of-the-art production, conservation and transfer of in vitro-produced embryos in small ruminants. Reprod. Fertil. Dev. 16, 437–445.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Damiani, P. , Fissore, R. A. , Cibelli, J. B. , Long, C. R. , Balise, J. J. , Robl, J. M. , and Duby, R. T. (1996). Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev. 45, 521–534.
Crossref | GoogleScholarGoogle Scholar | PubMed |

de Vries, W. N. , Evsikov, A. V. , Haac, B. E. , Fancher, K. S. , Holbrook, A. E. , Kemler, R. , Solter, D. , and Knowles, B. B. (2004). Maternal β-catenin and E-cadherin in mouse development. Development 131, 4435–4445.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Fleming, T. P. , Sheth, B. , and Fesenko, I. (2001). Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front. Biosci. 6, d1000–d1007.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gandolfi, F. , Milanesi, E. , Pocar, P. , Luciano, A. M. , Brevini, T. A. , Acocella, F. , Lauria, A. , and Armstrong, D. T. (1998). Comparative analysis of calf and cow oocytes during in vitro maturation. Mol. Reprod. Dev. 49, 168–175.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Huelsken, J. , Vogel, R. , Brinkmann, V. , Erdmann, B. , Birchmeier, C. , and Birchmeier, W. (2000). Requirement for beta-catenin in anterior–posterior axis formation in mice. J. Cell Biol. 148, 567–578.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kochhar, H. P. , Wu, B. , Morris, L. H. , Buckrell, B. C. , Pollard, J. W. , Basrur, P. K. , and King, W. A. (2002). Maturation status, protein synthesis and developmental competence of oocytes derived from lambs and ewes. Reprod. Domest. Anim. 37, 19–25.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Larue, L. , Ohsugi, M. , Hirchenhain, J. , and Kemler, R. (1994). E-cadherin null-mutant embryos fail to form a trophectoderm epithelium. Proc. Natl. Acad. Sci. USA 91, 8263–8267.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ledda, S. , Loi, P. , Bogliolo, L. , Moor, R. M. , and Fulka, J. (1996). The effect of 6-dimethylaminopurine (6-DMAP) on DNA synthesis in activated mammalian oocytes. Zygote 4, 7–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ledda, S. , Bogliolo, L. , Calvia, P. , Leoni, G. , and Naitana, S. (1997). Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes. J. Reprod. Fertil. 109, 73–78.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ledda, S. , Bogliolo, L. , Leoni, G. , and Naitana, S. (1999a). Follicular size affects the meiotic competence of in vitro-matured prepubertal and adult oocytes in sheep. Reprod. Nutr. Dev. 39, 503–508.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ledda, S. , Bogliolo, L. , Leoni, G. , and Naitana, S. (1999b). Production and lambing rate of blastocysts derived from in vitro-matured oocytes after gonadotropin treatment of prepubertal ewes. J. Anim. Sci. 77, 2234–2239.
PubMed |

Leoni, G. G. , Succu, S. , Berlinguer, F. , Rosati, I. , Bebbere, D. , Bogliolo, L. , Ledda, S. , and Naitana, S. (2006). Delay in the in vitro kinetic development of prepubertal ovine embryos. Anim. Reprod. Sci. 92, 373–383.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Leoni, G. G. , Bebbere, D. , Succu, S. , Berlinguer, F. , Mossa, F. , Galioto, M. , Bogliolo, L. , Ledda, S. , and Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–257.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lonergan, P. , and Fair, T. (2008). In vitro-produced bovine embryos: dealing with the warts. Theriogenology 69, 17–22.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Memili, E. , and First, N. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Modina, S. , Beretta, M. , Lodde, V. , Lauria, A. , and Luciano, A. M. (2004). Cytoplasmic changes and developmental competence of bovine oocytes cryopreserved without cumulus cells. Eur. J. Histochem. 48, 337–346.
PubMed |

Modina, S. , Abbate, F. , Germana, G. P. , Lauria, A. , and Luciano, A. M. (2007a). Beta-catenin localization and timing of early development of bovine embryos obtained from oocytes matured in the presence of follicle stimulating hormone. Anim. Reprod. Sci. 100, 264–279.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Modina, S. , Borromeo, V. , Luciano, A. M. , Lodde, V. , Franciosi, F. , and Secchi, C. (2007b). Relationship between growth hormone concentrations in bovine oocytes and follicular fluid and oocyte developmental competence. Eur. J. Histochem. 51, 173–180.
PubMed |

Moor, R. M. (1988). Regulation of the meiotic cycle in oocytes of domestic mammals. Ann. N. Y. Acad. Sci. 541, 248–258.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Moor, R. M. , and Crosby, I. M. (1986). Protein requirements for germinal vesicle breakdown in ovine oocytes. J. Embryol. Exp. Morphol. 94, 207–220.
PubMed |

Morton, K. M. (2008). Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes. Reprod. Domest. Anim. 43(Suppl 2), 137–143.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nganvongpanit, K. , Muller, H. , Rings, F. , Gilles, M. , Jennen, D. , Holker, M. , Tholen, E. , Schellander, K. , and Tesfaye, D. (2006). Targeted suppression of E-cadherin gene expression in bovine preimplantation embryo by RNA interference technology using double-stranded RNA. Mol. Reprod. Dev. 73, 153–163.
Crossref | GoogleScholarGoogle Scholar | PubMed |

O’Brien, J. K. , Dwarte, D. , Ryan, J. P. , Maxwell, W. M. , and Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fertil. Dev. 8, 1029–1037.
Crossref | GoogleScholarGoogle Scholar | PubMed |

O’Brien, J. K. , Catt, S. L. , Ireland, K. A. , Maxwell, W. M. , and Evans, G. (1997). In vitro and in vivo developmental capacity of oocytes from prepubertal and adult sheep. Theriogenology 47, 1433–1443.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ohsugi, M. , Larue, L. , Schwarz, H. , and Kemler, R. (1997). Cell-junctional and cytoskeletal organization in mouse blastocysts lacking E-cadherin. Dev. Biol. 185, 261–271.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ohsugi, M. , Butz, S. , and Kemler, R. (1999). Beta-catenin is a major tyrosine-phosphorylated protein during mouse oocyte maturation and preimplantation development. Dev. Dyn. 216, 168–176.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Peluso, J. J. (2006). N-cadherin mediated cell contact inhibits germinal vesicle breakdown in mouse oocytes maintained in vitro. Reproduction 131, 429–437.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Poehland, R. , Tomek, W. , Becker, F. , Kurth, J. , Kanitz, W. , and Bhojwani, S. (2008). Qualitative and quantitative differences of cytoskeleton proteins in embryos produced in vitro, in vivo and by somatic nuclear transfer. Mol. Reprod. Dev. 75, 1109–1119.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pokutta, S. , and Weis, W. I. (2007). Structure and mechanism of cadherins and catenins in cell–cell contacts. Annu. Rev. Cell Dev. Biol. 23, 237–261.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Presicce, G. A. , Jiang, S. , Simkin, M. , Zhang, L. , Looney, C. R. , Godke, R. A. , and Yang, X. (1997). Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves. Biol. Reprod. 56, 386–392.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ptak, G. , Loi, P. , Dattena, M. , Tischner, M. , and Cappai, P. (1999). Offspring from one-month-old lambs: studies on the developmental capability of prepubertal oocytes. Biol. Reprod. 61, 1568–1574.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Reima, I. , Lehtonen, E. , Virtanen, I. , and Flechon, J. E. (1993). The cytoskeleton and associated proteins during cleavage, compaction and blastocyst differentiation in the pig. Differentiation 54, 35–45.
PubMed |

Revel, F. , Mermillod, P. , Peynot, N. , Renard, J. P. , and Heyman, Y. (1995). Low developmental capacity of in vitro-matured and fertilized oocytes from calves compared with that of cows. J. Reprod. Fertil. 103, 115–120.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sirard, M. A. , Florman, H. M. , Leibfried-Rutledge, M. L. , Barnes, F. L. , Sims, M. L. , and First, N. L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Steeves, T. E. , and Gardner, D. K. (1999). Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows. Mol. Reprod. Dev. 54, 92–101.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Telford, N. A. , Watson, A. J. , and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Thélie, A. , Papillier, P. , Pennetier, S. , Perreau, C. , Traverso, J. M. , Uzbekova, S. , Mermillod, P. , Joly, C. , Humblot, P. , and Dalbiès-Tran, R. (2007). Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 7, 125.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vestweber, D. , Gossler, A. , Boller, K. , and Kemler, R. (1987). Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev. Biol. 124, 451–456.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vigneron, C. , Perreau, C. , Dalbies-Tran, R. , Joly, C. , Humblot, P. , Uzbekova, S. , and Mermillod, P. (2004). Protein synthesis and mRNA storage in cattle oocytes maintained under meiotic block by roscovitine inhibition of MPF activity. Mol. Reprod. Dev. 69, 457–465.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Watson, A. J. , and Barcroft, L. C. (2001). Regulation of blastocyst formation. Front. Biosci. 6, d708–d730.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Watson, A. J. , Natale, D. R. , and Barcroft, L. C. (2004). Molecular regulation of blastocyst formation. Anim. Reprod. Sci. 82–83, 583–592.
Crossref | GoogleScholarGoogle Scholar |

Wells, D. , Bermudez, M. G. , Steuerwald, N. , Malter, H. E. , Thornhill, A. R. , and Cohen, J. (2005). Association of abnormal morphology and altered gene expression in human preimplantation embryos. Fertil. Steril. 84, 343–355.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wrenzycki, C. , Herrmann, D. , Lucas-Hahn, A. , Gebert, C. , Korsawe, K. , Lemme, E. , Carnwath, J. W. , and Niemann, H. (2005). Epigenetic reprogramming throughout preimplantation development and consequences for assisted reproductive technologies. Birth Defects Res. C Embryo Today 75, 1–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ziv, S. , Rufas, O. , and Shalgi, R. (2002). Cadherins expression during gamete maturation and fertilization in the rat. Mol. Reprod. Dev. 62, 547–556.
Crossref | GoogleScholarGoogle Scholar | PubMed |