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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of ovary storage temperature and embryo vitrification on somatic cell nuclear transfer outcomes in goats

Mehdi Hajian A C , Farnoosh Jafarpour A , Sayed Morteza Aghamiri B , Shiva Rouhollahi Varnosfaderani A and Mohammad Hossein Nasr Esfahani https://orcid.org/0000-0003-1983-3435 A C
+ Author Affiliations
- Author Affiliations

A Department of Reproductive Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, Academic Center for Education, Culture and Research, Salman Street, Royan Street, 81593-58686, Isfahan, Iran.

B Department of Clinical Studies, School of Veterinary Medicine, Shahid Bahonar University of Kerman, 22th Bahman Street, 76169-14111, Kerman, Iran.

C Corresponding authors. Email: mh.nasr-esfahani@royaninstitute.org; Mehdihajian2002@gmail.com

Reproduction, Fertility and Development 32(4) 419-424 https://doi.org/10.1071/RD18529
Submitted: 8 October 2018  Accepted: 19 July 2019   Published: 10 December 2019

Abstract

Improving the genetic potential of farm animals is one of the primary aims in the field of assisted reproduction. In this regard, somatic cell nuclear transfer (SCNT) can be used to produce a large number of embryos from genetically elite animals. The aims of the present study were to assess the effects of: (1) ovary storage conditions on preimplantation development of recovered oocytes and the freezability of the derived blastocysts; and (2) vitrification of goat SCNT-derived blastocysts on postimplantation development. Goat oocytes were recovered from ovaries and stored under warm (25°C-27°C) or cold (11°C-12°C) conditions before being used to produce SCNT embryos. There were no differences in oocytes recovered from ovaries kept under cold versus warm storage conditions in terms of cleavage (mean (± s.d.) 95.68 ± 1.67% vs 95.91 ± 2.93% respectively) and blastocyst formation (10.69 ± 1.17% vs 10.94 ± 0.9% respectively) rates. The re-expansion rate of vitrified blastocysts was significantly lower for cold- than warm-stored ovaries (66.3 ± 8.7% vs 90 ± 11% respectively). To assess the effects of vitrification on postimplantation development, blastocysts from cold-stored ovaries only were transferred from fresh and vitrified–warmed groups. The pregnancy rate was comparable between the fresh and vitrified–warmed groups (41.65% and 45.45% respectively). In addition, established pregnancy in Day 28-38 and full-term pregnancy rates were similar between the two groups. In conclusion, this study shows similar in vitro preimplantation developmental potential of warm- and cold-stored ovaries. This study introduces the vitrification technique as an appropriate approach to preserve embryos produced by SCNT for transfer to recipient goats at a suitable time.

Additional keywords: blastocysts, somatic cell nuclear transfer-derived embryos.


References

Baguisi, A., Behboodi, E., Melican, D. T., Pollock, J. S., Destrempes, M. M., Cammuso, C., Williams, J. L., Nims, S. D., Porter, C. A., Midura, P., and Palacios, M. J. (1999). Production of goats by somatic cell nuclear transfer. Nat. Biotechnol. 17, 456–461.
Production of goats by somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 10331804PubMed |

Bedzhov, I., Graham, S. J., Leung, C. Y., and Zernicka-Goetz, M. (2014). Developmental plasticity, cell fate specification and morphogenesis in the early mouse embryo. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130538.
Developmental plasticity, cell fate specification and morphogenesis in the early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 25349447PubMed |

Choi, J. K., Yue, T., Huang, H., Zhao, G., Zhang, M., and He, X. (2015). The crucial role of zona pellucida in cryopreservation of oocytes by vitrification. Cryobiology 71, 350–355.
The crucial role of zona pellucida in cryopreservation of oocytes by vitrification.Crossref | GoogleScholarGoogle Scholar | 26297946PubMed |

Cohen, J., Simons, R. F., Edwards, R. G., Fehilly, C. B., and Fishel, S. B. (1985). Pregnancies following the frozen storage of expanding human blastocysts. J In Vitro Fert Embryo Transf. 2, 59–64.
Pregnancies following the frozen storage of expanding human blastocysts.Crossref | GoogleScholarGoogle Scholar | 4020239PubMed |

Du, Y., Zhang, Y., Li, J., Kragh, P. M., Kuwayama, M., Ieda, S., Zhang, X., Schmidt, M., Bøgh, I. B., Purup, S., and Pedersen, A. M. (2007). Simplified cryopreservation of porcine cloned blastocysts. Cryobiology 54, 181–187.
Simplified cryopreservation of porcine cloned blastocysts.Crossref | GoogleScholarGoogle Scholar | 17359960PubMed |

García-Álvarez, O., Maroto-Morales, A., Berlinguer, F., Fernández-Santos, M. R., Esteso, M. C., Mermillod, P., Ortiz, J. A., Ramon, M., Pérez-Guzmán, M. D., Garde, J. J., and Soler, A. J. (2011). Effect of storage temperature during transport of ovaries on in vitro embryo production in Iberian red deer (Cervus elaphus hispanicus). Theriogenology 75, 65–72.
Effect of storage temperature during transport of ovaries on in vitro embryo production in Iberian red deer (Cervus elaphus hispanicus).Crossref | GoogleScholarGoogle Scholar | 21040958PubMed |

George, A., Sharma, R., Singh, K. P., Panda, S. K., Singla, S. K., Palta, P., Manik, R., and Chauhan, M. S. (2011). Production of cloned and transgenic embryos using buffalo (Bubalus bubalis) embryonic stem cell-like cells isolated from in vitro fertilized and cloned blastocysts. Cell. Reprogram. 13, 263–272.
Production of cloned and transgenic embryos using buffalo (Bubalus bubalis) embryonic stem cell-like cells isolated from in vitro fertilized and cloned blastocysts.Crossref | GoogleScholarGoogle Scholar | 21548826PubMed |

Hosseini, S. M., Hajian, M., Moulavi, F., Asgari, V., Forouzanfar, M., and Nasr-Esfahani, M. H. (2013). Cloned sheep blastocysts derived from oocytes enucleated manually using a pulled Pasteur pipette. Cell. Reprogram. 15, 15–23.
Cloned sheep blastocysts derived from oocytes enucleated manually using a pulled Pasteur pipette.Crossref | GoogleScholarGoogle Scholar | 23379580PubMed |

Katayama, M., Ellersieck, M. R., and Roberts, R. M. (2010). Development of monozygotic twin mouse embryos from the time of blastomere separation at the two-cell stage to blastocyst. Biol. Reprod. 82, 1237–1247.
Development of monozygotic twin mouse embryos from the time of blastomere separation at the two-cell stage to blastocyst.Crossref | GoogleScholarGoogle Scholar | 20181620PubMed |

Kelly, J. M., Kleemann, D. O., Kuwayama, M., and Walker, S. K. (2004). 102 vitrification of in vitro-produced bovine and ovine embryos using the minimum volume cooling Cryotop method. Reprod. Fertil. Dev. 16, 172–173.
102 vitrification of in vitro-produced bovine and ovine embryos using the minimum volume cooling Cryotop method.Crossref | GoogleScholarGoogle Scholar |

Koo, D. B., Kang, Y. K., Choi, Y. H., Park, J. S., Kim, H. N., Oh, K. B., Son, D. S., Park, H., Lee, K. K., and Han, Y. M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol. Reprod. 67, 487–492.
Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts.Crossref | GoogleScholarGoogle Scholar | 12135886PubMed |

Kovačič, B., Taborin, M., and Vlaisavljević, V. (2018). Artificial blastocoel collapse of human blastocysts before vitrification and its effect on re-expansion after warming – a prospective observational study using time-lapse microscopy. Reprod. Biomed. Online 36, 121–129.
Artificial blastocoel collapse of human blastocysts before vitrification and its effect on re-expansion after warming – a prospective observational study using time-lapse microscopy.Crossref | GoogleScholarGoogle Scholar | 29212605PubMed |

Lan, G. C., Han, D., Wu, Y. G., Han, Z. B., Ma, S. F., Liu, X. Y., Chang, C. L., and Tan, J. H. (2005). Effects of duration, concentration, and timing of ionomycin and 6-dimethylaminopurine (6-DMAP) treatment on activation of goat oocytes. Mol. Reprod. Dev. 71, 380–388.
Effects of duration, concentration, and timing of ionomycin and 6-dimethylaminopurine (6-DMAP) treatment on activation of goat oocytes.Crossref | GoogleScholarGoogle Scholar | 15806561PubMed |

Nakano, K., Matsunari, H., Nakayama, N., Ogawa, B., Kurome, M., Takahashi, M., Matsumoto, M., Murakami, H., Kaji, Y., and Nagashima, H. (2011). Cloned porcine embryos can maintain developmental ability after cryopreservation at the morula stage. J. Reprod. Dev. 57, 312–316.
Cloned porcine embryos can maintain developmental ability after cryopreservation at the morula stage.Crossref | GoogleScholarGoogle Scholar | 21242653PubMed |

Nasr-Esfahani, M. H., Hosseini, S. M., Hajian, M., Forouzanfar, M., Ostadhosseini, S., Abedi, P., Khazaie, Y., Dormiani, K., Ghaedi, K., Forozanfar, M., and Gourabi, H. (2011). Development of an optimized zona-free method of somatic cell nuclear transfer in the goat. Cell. Reprogram. 13, 157–170.
Development of an optimized zona-free method of somatic cell nuclear transfer in the goat.Crossref | GoogleScholarGoogle Scholar | 21473692PubMed |

Panda, S. K., George, A., Saha, A. P., Sharma, R., Manik, R. S., Chauhan, M. S., Palta, P., and Singla, S. K. (2011). Effect of cytoplasmic volume on developmental competence of buffalo (Bubalus bubalis) embryos produced through hand-made cloning. Cell. Reprogram. 13, 257–262.
Effect of cytoplasmic volume on developmental competence of buffalo (Bubalus bubalis) embryos produced through hand-made cloning.Crossref | GoogleScholarGoogle Scholar | 21563942PubMed |

Park, C. H., Jeong, Y. H., Lee, D. K., Hwang, J. Y., Uh, K. J., Yeom, S. C., Ahn, C., and Lee, C. K. (2015). Availability of empty zona pellucida for generating embryonic chimeras. PLoS One 10, e0123178.
Availability of empty zona pellucida for generating embryonic chimeras.Crossref | GoogleScholarGoogle Scholar | 26383864PubMed |

Paterson, L., DeSousa, P., Ritchie, W., King, T., and Wilmut, I. (2003). Application of reproductive biotechnology in animals: implications and potentials: applications of reproductive cloning. Anim. Reprod. Sci. 79, 137–143.
Application of reproductive biotechnology in animals: implications and potentials: applications of reproductive cloning.Crossref | GoogleScholarGoogle Scholar | 14643101PubMed |

Pezhman, M., Hosseini, S. M., Ostadhosseini, S., Varnosfaderani, S. R., Sefid, F., and Nasr-Esfahani, M. H. (2017). Cathepsin B inhibitor improves developmental competency and cryo-tolerance of in vitro ovine embryos. BMC Dev. Biol. 17, 10.
Cathepsin B inhibitor improves developmental competency and cryo-tolerance of in vitro ovine embryos.Crossref | GoogleScholarGoogle Scholar | 28676034PubMed |

Preis, K. A., Carnevale, E. M., da Silva, M. C., di Brienza, V. C., Gomes, G. M., Maclellan, L. J., and Squires, E. L. (2004). In vitro maturation and transfer of equine oocytes after transport of ovaries at 12 or 22 C. Theriogenology 61, 1215–1223.
In vitro maturation and transfer of equine oocytes after transport of ovaries at 12 or 22 C.Crossref | GoogleScholarGoogle Scholar | 15036956PubMed |

Ribas, R., Oback, B., Ritchie, W., Chebotareva, T., Taylor, J., Mauricio, A. C., Sousa, M., and Wilmut, I. (2006). Modifications to improve the efficiency of zona-free mouse nuclear transfer. Cloning Stem Cells 8, 10–15.
Modifications to improve the efficiency of zona-free mouse nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 16571073PubMed |

Saha, A., Panda, S. K., Chauhan, M. S., Manik, R. S., Palta, P., and Singla, S. K. (2013). Birth of cloned calves from vitrified–warmed zona-free buffalo (Bubalus bubalis) embryos produced by hand-made cloning. Reprod. Fertil. Dev. 25, 860–865.
Birth of cloned calves from vitrified–warmed zona-free buffalo (Bubalus bubalis) embryos produced by hand-made cloning.Crossref | GoogleScholarGoogle Scholar | 22950886PubMed |

Selokar, N. L., George, A., Saha, A. P., Sharma, R., Muzaffer, M., Shah, R. A., Palta, P., Chauhan, M. S., Manik, R. S., and Singla, S. K. (2011). Production of interspecies handmade cloned embryos by nuclear transfer of cattle, goat and rat fibroblasts to buffalo (Bubalus bubalis) oocytes. Anim. Reprod. Sci. 123, 279–282.
Production of interspecies handmade cloned embryos by nuclear transfer of cattle, goat and rat fibroblasts to buffalo (Bubalus bubalis) oocytes.Crossref | GoogleScholarGoogle Scholar | 21288667PubMed |

Selokar, N. L., Shah, R. A., Saha, A. P., Muzaffar, M., Saini, M., Chauhan, M. S., Manik, R. S., Palta, P., and Singla, S. K. (2012). Effect of post-fusion holding time, orientation and position of somatic cell-cytoplasts during electrofusion on the development of handmade cloned embryos in buffalo (Bubalus bubalis). Theriogenology 78, 930–936.
Effect of post-fusion holding time, orientation and position of somatic cell-cytoplasts during electrofusion on the development of handmade cloned embryos in buffalo (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar | 22541327PubMed |

Shah, R. A., George, A., Singh, M. K., Kumar, D., Chauhan, M. S., Manik, R., Palta, P., and Singla, S. K. (2008). Hand-made cloned buffalo (Bubalus bubalis) embryos: comparison of different media and culture systems. Cloning Stem Cells 10, 435–442.
Hand-made cloned buffalo (Bubalus bubalis) embryos: comparison of different media and culture systems.Crossref | GoogleScholarGoogle Scholar | 18800862PubMed |

Shu, Y., Peng, W., and Zhang, J. (2010). Pregnancy and live birth following the transfer of vitrified–warmed blastocysts derived from zona- and corona-cell-free oocytes. Reprod. Biomed. Online 21, 527–532.
Pregnancy and live birth following the transfer of vitrified–warmed blastocysts derived from zona- and corona-cell-free oocytes.Crossref | GoogleScholarGoogle Scholar | 20800550PubMed |

Sirisha, K., Selokar, N. L., Saini, M., Palta, P., Manik, R. S., Chauhan, M. S., and Singla, S. K. (2013). Cryopreservation of zona-free cloned buffalo (Bubalus bubalis) embryos: slow freezing vs open-pulled straw vitrification. Reprod. Domest. Anim. 48, 538–544.
Cryopreservation of zona-free cloned buffalo (Bubalus bubalis) embryos: slow freezing vs open-pulled straw vitrification.Crossref | GoogleScholarGoogle Scholar | 23281817PubMed |

Periyasamy, V., and Sri Balaji, N. (2010). Use of assisted reproductive technologies for livestock development. Vet. World 3, 238–240.

Suzuki, H., Togashi, M., Adachi, J., and Toyoda, Y. (1995). Developmental ability of zona-free mouse embryos is influenced by cell association at the 4-cell stage. Biol. Reprod. 53, 78–83.
Developmental ability of zona-free mouse embryos is influenced by cell association at the 4-cell stage.Crossref | GoogleScholarGoogle Scholar | 7669859PubMed |

Taylor-Robinson, A. W., Walton, S., Swain, D. L., Walsh, K. B., and Vajta, G. (2014). The potential for modification in cloning and vitrification technology to enhance genetic progress in beef cattle in northern Australia. Anim. Reprod. Sci. 148, 91–96.
The potential for modification in cloning and vitrification technology to enhance genetic progress in beef cattle in northern Australia.Crossref | GoogleScholarGoogle Scholar | 24998156PubMed |

Vajta, G., Holm, P., Greve, T., and Callesen, H. (1996). Factors affecting survival rates of in vitro produced bovine embryos after vitrification and direct in-straw rehydration. Anim. Reprod. Sci. 45, 191–200.
Factors affecting survival rates of in vitro produced bovine embryos after vitrification and direct in-straw rehydration.Crossref | GoogleScholarGoogle Scholar | 9227922PubMed |

Vajta, G., Bartels, P., Joubert, J., de la Rey, M., Treadwell, R., and Callesen, H. (2004). Production of a healthy calf by somatic cell nuclear transfer without micromanipulators and carbon dioxide incubators using the handmade cloning (HMC) and the submarine incubation system (SIS). Theriogenology 62, 1465–1472.
Production of a healthy calf by somatic cell nuclear transfer without micromanipulators and carbon dioxide incubators using the handmade cloning (HMC) and the submarine incubation system (SIS).Crossref | GoogleScholarGoogle Scholar | 15451255PubMed |

Velásquez, A. E., Manríquez, J. R., Castro, F. O., and Rodríguez-Alvarez, L. (2013). Effect of zona pellucida removal on early development of in vitro produced bovine embryos. Arch. Med. Vet. 45, 7–15.
Effect of zona pellucida removal on early development of in vitro produced bovine embryos.Crossref | GoogleScholarGoogle Scholar |

Wang, Y. S., Zhao, X., Su, J. M., An, Z. X., Xiong, X. R., Wang, L. J., Liu, J., Quan, F. S., Hua, S., and Zhang, Y. (2011). Lowering storage temperature during ovary transport is beneficial to the developmental competence of bovine oocytes used for somatic cell nuclear transfer. Anim. Reprod. Sci. 124, 48–54.
Lowering storage temperature during ovary transport is beneficial to the developmental competence of bovine oocytes used for somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 21333472PubMed |

Yang, C. Y., Pang, C. Y., Yang, B. Z., Li, R. C., Lu, Y. Q., and Liang, X. W. (2012). Optimization of cryopreservation of buffalo (Bubalus bubalis) blastocysts produced by in vitro fertilization and somatic cell nuclear transfer. Theriogenology 78, 1437–1445.
Optimization of cryopreservation of buffalo (Bubalus bubalis) blastocysts produced by in vitro fertilization and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 22925650PubMed |

Zhang, S., Chen, X., Wang, F., An, X., Tang, B., Zhang, X., Sun, L., and Li, Z. (2016). Aberrant DNA methylation reprogramming in bovine SCNT preimplantation embryos. Sci. Rep. 6, 30345.
Aberrant DNA methylation reprogramming in bovine SCNT preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 27456302PubMed |