Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-20T08:12:57.477Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of vitrification of immature bovine oocytes to the subsequent in vitro development and gene expression

Published online by Cambridge University Press:  26 November 2014

Marwa S. Faheem ,
E. Baron ,
I. Carvalhais ,
A. Chaveiro ,
K. Pavani  and
F. Moreira da Silva
Marwa S. Faheem
Affiliation:
Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9701–851 Angra do Heroísmo, Portugal. Animal Production Department, Faculty of Agriculture, Cairo University, 12613 Giza, Egypt.
E. Baron
Affiliation:
Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9701–851 Angra do Heroísmo, Portugal.
I. Carvalhais
Affiliation:
Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9701–851 Angra do Heroísmo, Portugal.
A. Chaveiro
Affiliation:
Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9701–851 Angra do Heroísmo, Portugal.
K. Pavani
Affiliation:
Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9701–851 Angra do Heroísmo, Portugal.
F. Moreira da Silva*
Affiliation:
Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9700–042 Angra do Heroísmo, Portugal.
*
All correspondence to: Fernando Moreira da Silva. Animal Reproduction, Department of Agrarian Sciences, University of the Azores, CITA-A, 9700–042 Angra do Heroísmo, Portugal. Tel: +351 295 402420. Fax: +351 295 402421. e-mail: jsilva@uac.pt
Get access Rights & Permissions [Opens in a new window]

Summary

Immature bovine oocytes were vitrified using the cryotop method and their post-warming survivability and capability to undergo in vitro maturation, fertilization and subsequent embryonic development were evaluated. In addition throughout the embryonic 2-cell, 4-cell, morula and blastocyst stages, the expression of four developmentally important genes (Cx43, CDH1, DNMT1 and HSPA14) was analysed using the real-time polymerase chain reaction (PCR). Immature oocytes (n = 550) were randomly assigned to non-vitrified (fresh) or cryotop vitrification groups using ethylene glycol (EG) with 1,2 propanediol (PROH) or dimethylsulphoxide (DMSO). After warming, oocytes survivability, embryo cleavage and embryonic developmental rates were not statistically different between the two cryoprotectants groups. However, the DMSO group had a lower (P < 0.05) oocyte maturation rate compared with the fresh and PROH groups. For morula and blastocyst rates, the DMSO group achieved a lower (P < 0.05) morula rate compared with the fresh group, while at the blastocyst stage, there were no differences between fresh and both cryoprotectants groups. For molecular analysis, at the 4-cell stage, most studied genes showed an inconsistent pattern of expression either from the PROH or DMSO groups. Noteworthily, these differences were limited at the morula and blastocyst stages. In conclusion, the cryotop method is sufficient for vitrification of immature bovine oocytes, both for embryonic developmental competence and at the molecular level. Moreover, PROH showed some advantage over DMSO as a cryoprotectant.

Keywords

CryopreservationCryoprotectantsCryotopIn vitro fertilizationReal-time quantitative PCR
Type
Research Article
Information
Zygote , Volume 23 , Issue 6 , December 2015 , pp. 933 - 942
Copyright
Copyright © Cambridge University Press 2014 

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

Borges, E.N., Silva, R.C., Futino, D.O., Rocha-Junior, C.M., Amorim, C.A., Bao, S.N. & Lucci, C.M. (2009). Cryopreservation of swine ovarian tissue: effect of different cryoprotectants on the structural preservation of preantral follicle oocytes. Cryobiology 59, 195–200.CrossRefGoogle ScholarPubMed
Cetin, Y. & Bastan, A. (2006). Cryopreservation of immature bovine oocytes by vitrification in straws. Anim. Reprod. Sci. 92, 29–36.CrossRefGoogle ScholarPubMed
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
Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E. & Reik, W. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc. Natl. Acad. Sci. USA 98, 13734–8.CrossRefGoogle ScholarPubMed
Dutta, D.J., Dev, H. & Raj, H. (2013). In vitro blastocyst development of post-thaw vitrified bovine oocytes, Vet. World 6 (10): 730–3.CrossRefGoogle Scholar
Ebrahimi, B., Valojerdi, M.R., Eftekhari-Yazdi, P. & Baharvand, H. (2010). In vitro maturation, apoptotic gene expression and incidence of numerical chromosomal abnormalities following cryotop vitrification of sheep cumulus–oocyte complexes. J. Assist. Reprod. Genet. 27, 239–46.CrossRefGoogle ScholarPubMed
Faheem, M.S., Carvalhais, I., Chaveiro, A. & Moreira da Silva, F. (2011). In vitro oocyte fertilization and subsequent embryonic development after cryopreservation of bovine ovarian tissue, using an effective approach for oocyte collection. Anim. Reprod. Sci. 125, 49–55.CrossRefGoogle ScholarPubMed
Fleming, T.P., Sheth, B. & Fesenko, I. (2001). Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front. Biosci. 6, D1000–7.CrossRefGoogle ScholarPubMed
Golding, M.C. & Westhusin, M.E. (2003). Analysis of DNA (cytosine 5) methyltransferase mRNA sequence and expression in bovine preimplantation embryos, fetal and adult tissues. Gene Expr. Patterns 3, 551–8.Google Scholar
Goodall, H. & Johnson, M.H. (1984). The nature of intercellular coupling within the preimplantation mouse embryo. J. Embryol. Exp. Morphol. 79, 53–76.Google ScholarPubMed
Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A. & Peelman, L.J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5:27. doi:10.1186/1471-213X-5-27.Google Scholar
Gurtovenko, A.A. & Anwar, J. (2007). Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J. Phys. Chem. B. 111, 10453–60.Google Scholar
Habibi, A., Farrokhi, N., Moreira da Silva, F., Bettencourt, B.F., Bruges-Armas, J., Amidi, F. & Hosseini, A. (2010). The effects of vitrification on gene expression in mature mouse oocytes by nested quantitative PCR. J. Assist. Reprod. Genet. 27, 599–604.CrossRefGoogle ScholarPubMed
Hajarian, H., Wahid, H., Rosnina, Y., Daliri, M., Dashtizad, M., Mirzapour, T., Yimer, N., Bukar, M.M., Iswadi, M.I. & Abas Mazni, O. (2011). Cryotop device enhances vitrification outcome of immature bovine oocytes. J. Anim. Vet. Advan. 10, 2541–5.Google Scholar
Houghton, F.D. (2005). Role of gap junctions during early embryo development. Reproduction 129, 129–35.Google Scholar
Hyafil, F., Morello, D., Babinet, C. & Jacob, F. (1980). A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell 21, 927–34.CrossRefGoogle ScholarPubMed
Johnson, M.H. & Pickering, S.J. (1987). The effect of dimethylsulfoxide on the microtubular system of the mouse oocyte. Development 100, 313–24.CrossRefGoogle ScholarPubMed
Khatir, H., Anouassi, A. & Tibary, A. (2004). Production of dromedary (Camelus dromedarius) embryos by IVM and IVF and co-culture with oviductal or granulosa cells. Theriogenology 62, 1175–85.CrossRefGoogle ScholarPubMed
Kuwayama, M. (2007). Highly efficient vitrification for cryopreservation of human oocytes and embryos: the cryotop method. Theriogenology 67, 73–80.CrossRefGoogle ScholarPubMed
Levy, R. (2001). Genetic regulation of preimplantation embryo survival. Int. Rev. Cytol. 210, 1–37.Google Scholar
Liebermann, J. & Tucker, M.J. (2002). Effect of carrier system on the yield of human oocytes and embryos as assessed by survival and developmental potential after vitrification. Reproduction 124, 483–9.CrossRefGoogle ScholarPubMed
Liebermann, J. & Tucker, M.J. (2006). Comparison of vitrification and conventional cryopreservation of day 5 and day 6 blastocysts during clinical application. Fertil. Steril. 86, 20–6.Google Scholar
Modina, S., Leoni, G.G., Lodde, V., Naitana, S., Pirani, S., Succu, S., Berlinguer, F. & Luciano, A.M. (2010). Involvement of E-cadherin in early in vitro development of adult and juvenile sheep embryos. Reprod. Fertil. Dev. 22, 468–77.Google Scholar
Morato, R., Izquierdo, D., Paramio, M.T. & Mogas, T. (2008). Cryotops versus open-pulled straws (OPS) as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development. Cryobiology 57, 137–41.CrossRefGoogle ScholarPubMed
Neuer, A., Spandorfer, S.D., Giraldo, P., Dieterle, S., Rosenwaks, Z. & Witkin, S.S. (2000). The role of heat shock proteins in reproduction. Hum. Reprod. Update 6, 149–59.Google Scholar
Ogawa, H., Oyamada, M., Mori, T., Mori, M. & Shimizu, H. (2000). Relationship of gap junction formation to phosphorylation of connexin43 in mouse preimplantation embryos. Mol. Reprod. Dev. 55, 393–8.Google Scholar
Pavani, K.C. (2012). Optimization of the messenger RNA (mRNA) extraction protocol from fresh and vitrified bovine oocytes for gene expression studies. MSc. thesis. University of Skövde. http://his.diva-portal.org/smash/record.jsf?pid=diva2:575417 Google Scholar
Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002). Relative Expression Software Tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 1–10.CrossRefGoogle Scholar
Riethmacher, D., Brinkmann, V. & Birchmeier, C. (1995). A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl. Acad. Sci. USA 92, 855–9.Google Scholar
Rozen, S. & Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–86.Google ScholarPubMed
Santos, R.R., Tharasanit, T., Van Haeften, T., Figueiredo, J.R., Silva, J.R. & Van den Hurk, R. (2007). Vitrification of goat preantral follicles enclosed in ovarian tissue by using conventional and solid-surface vitrification methods. Cell Tissue Res. 327, 167–76.Google Scholar
Sharma, G.T., Dubey, P.K. & Chandra, V. (2010). Morphological changes, DNA damage and developmental competence of in vitro matured, vitrified-thawed buffalo (Bubalus bubalis) oocytes: A comparative study of two cryoprotectants and two cryodevices. Cryobiology 60, 315–21.Google Scholar
Shi, L. & Wu, J. (2009). Epigenetic regulation in mammalian preimplantation embryo development. Reprod. Biol. Endocrinol. doi:10.1186/1477-7827-7-59.CrossRefGoogle ScholarPubMed
Stinshoff, H., Wilkening, S., Hanstedt, A., Bruning, K. & Wrenzycki, C. (2011). Cryopreservation affects the quality of in vitro produced bovine embryos at the molecular level. Theriogenology 76, 1433–41.Google Scholar
Succu, S., Bebbere, D., Bogliolo, L., Ariu, F., Fois, S., Leoni, G.G., Berlinguer, F., Naitana, S. & Ledda, S. (2008). Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance. Mol. Reprod. Dev. 75, 538–46.CrossRefGoogle ScholarPubMed
Telford, N.A., Watson, A.J. & 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.Google Scholar
Tesfaye, D., Lonergan, P., Hoelker, M., Rings, F., Nganvongpanit, K., Havlicek, V., Besenfelder, U., Jennen, D., Tholen, E. & Schellander, K. (2007). Suppression of connexin 43 and E-cadherin transcripts in in vitro derived bovine embryos following culture in vitro or in vivo in the homologous bovine oviduct. Mol. Reprod. Dev. 74, 978–88.CrossRefGoogle ScholarPubMed
Vajta, G. & Kuwayama, M. (2006). Improving cryopreservation system. Theriogenology 65, 236–44.Google Scholar
Varghese, A.C., Nagy, Z.P. & Agarwal, A. (2009). Current trends, biological foundations and future prospects of oocyte and embryo cryopreservation. Reprod. Biomed. Online 19, 126–40.CrossRefGoogle ScholarPubMed
Vestweber, D. & Kemler, R. (1984). Rabbit antiserum against a purified surface glycoprotein decompacts mouse preimplantation embryos and reacts with specific adult tissues. Exp. Cell. Res. 152, 169–78.Google Scholar
Yang, X.G., Wang, X.W., Zuo, E.W., Hao, C.L., Lu, S.S., Liu, H.B., Xu, H.Y., Lu, Y.Q. & Lu, K.H. (2012). cDNA cloning of porcine CDH1 and its expression profile in porcine early parthenotes. Anim. Sci. Pap. Rep. 30, 249–59.Google Scholar