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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Normal developmental competence to the blastocyst stage is preserved in rabbit ovarian tissue following cryopreservation and autografting to the mesometrium

Lan Chao A , Xiaohui Deng A D , Xiao Wang B , Qingzhao Fu A , Anran Xu A , Chunyan Hao C , Hongling Yu A and Xuan Yu A
+ Author Affiliations
- Author Affiliations

A Infertility Center, Qilu Hospital, Shandong University, Jinan 250012, China.

B Department of Surgery, Medical College, Shandong University, Jinan 250012, China.

C Department of Pathology, Qilu Hospital, Shandong University, Jinan 250012, China.

D Corresponding author. Email: qlsz@yahoo.cn

Reproduction, Fertility and Development 20(4) 466-473 https://doi.org/10.1071/RD07199
Submitted: 26 October 2007  Accepted: 6 February 2008   Published: 11 April 2008

Abstract

The aim of the present study was to evaluate mesometrial autotransplantation of frozen–thawed ovarian tissue in the adult rabbit and investigate the developmental competence of oocytes retrieved from grafts by in vitro maturation, fertilisation and blastocyst formation. Twenty-five rabbits were divided into control, fresh tissue transplantation and frozen–thawed tissue transplantation groups. Rabbits were stimulated with follicle-stimulating hormone (FSH) and oocytes were retrieved 3 months after transplantation. Oocytes matured in vivo or in vitro were then fertilised by conventional in vitro fertilisation (IVF) or intracytoplasmic sperm injection (ICSI), followed by observation and evaluation of fertilisation and blastocyst formation rates. No significant differences were found in the percentage of oocytes, maturation, fertilisation, cleavage and blastocyst formation among the three groups. Significantly higher fertilisation rates of in vitro-matured (IVM) oocytes were observed with ICSI compared with IVF in each group (81.1% v. 58.5%, 79.2% v. 59.6% and 80.4% v. 56.0% in the control, fresh tissue transplantation and frozen–thawed tissue transplantation groups, respectively). The blastocyst formation rate of IVM oocytes was significantly lower than that of in vivo-matured oocytes in each group (25.5% v. 65.7%, 22.4% v. 61.8% and 28.9% v. 63.0% in the control, fresh tissue transplantation and frozen–thawed tissue transplantation groups, respectively). In concusion, the mesometrium is a promising site for ovarian autografts in the rabbit. Oocytes retrieved from mesometrial grafts can develop to the blastocyst stage.

Additional keywords: autotransplantation, follicle development, in vitro fertilisation, oocyte maturation.


References

Al-Hasani, S. , Trotnow, S. , Sadtler, C. , and Hahn, J. (1986). In vitro fertilization and embryo transfer of pre-ovulatory rabbit oocytes. Eur. J. Obstet. Gynecol. Reprod. Biol. 21, 187–195.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Almodin, C. G. , Minguetti-Camara, V. C. , Meister, H. , Ferreira, J. O. , Franco, R. L. , Cavalcante, A. A. , Radaelli, M. R. , Bahls, A. S. , Moron, A. F. , and Murta, C. G. (2004). Recovery of fertility after grafting of cryopreserved germinative tissue in female rabbits following radiotherapy. Hum. Reprod. 19, 1287–1293.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Aubard, Y. , Piver, P. , Cognie, Y. , Fermeaux, V. , Poulin, N. , and Driancourt, M. A. (1999). Orthotopic and heterotopic autografts of frozen–thawed ovarian cortex in sheep. Hum. Reprod. 14, 2149–2154.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Baird, D. T. , Webb, R. , Campbell, B. K. , Harkness, L. M. , and Gosden, R. G. (1999). Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at –196°C. Endocrinology 140, 462–471.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Brackett, B. G. , and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Callejo, J. , Salvador, C. , Miralles, A. , Vilaseca, S. , Lailla, J. M. , and Balasch, J. (2001). Long-term ovarian function evaluation after autografting by implantation with fresh and frozen–thawed human ovarian tissue. J. Clin. Endocrinol. Metab. 86, 4489–4494.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Carneiro, G. , Lorenzo, P. , Pimentel, C. , Pegoraro, L. , Bertolini, M. , Ball, B. , Anderson, G. , and Liu, I. (2001). Influence of insulin-like growth factor-I and its interaction with gonadotropins, estradiol, and fetal calf serum on in vitro maturation and parthenogenic development in equine oocytes. Biol. Reprod. 65, 899–905.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Dell’Aquila, M. E. , Cho, Y. S. , Minoia, P. , Traina, V. , Fusco, S. , Lacalandra, G. M. , and Maritato, F. (1997). Intracytoplasmic sperm injection (ICSI) versus conventional IVF on abattoir-derived and in vitro-matured equine oocytes. Theriogenology 47, 1139–1156.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Demeestere, I. , Simon, P. , Buxant, F. , Robin, V. , Fernandez, S. A. , Centner, J. , Delbaere, A. , and Englert, Y. (2006). Ovarian function and spontaneous pregnancy after combined heterotopic and orthotopic cryopreserved ovarian tissue transplantation in a patient previously treated with bone marrow transplantation: case report. Hum. Reprod. 21, 2010–2014.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Demeestere, I. , Simon, P. , Emiliani, S. , Delbaere, A. , and Englert, Y. (2007). Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin’s disease. Oncologist 12, 1437–1442.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Deng, M. , and Yang, X. J. (2001). Full term development of rabbit oocytes fertilized by intracytoplasmic sperm injection. Mol. Reprod. Dev. 59, 38–43.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Deng, X. H. , Xu, A. R. , Chao, L. , Yu, H. L. , Zhen, J. H. , Hashimoto, S. , and Morimoto, Y. (2007). Effect of different sites for cryopreserved ovarian tissue implantation in rabbit. Hum. Reprod. 22, 662–668.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Donnez, J. , Dolmans, M. M. , Demylle, D. , Jadoul, P. , Pirard, C. , Squifflet, J. , Martinez-Madrid, B. , and Van Langendonckt, A. (2004). Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 364, 1405–1410.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Eppig, J. J. , and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesie and development to live young after growth, maturation and fertilization in vitro. Biol. Reprod. 41, 268–276.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Fukuda, A. , Roudebush, W. E. , and Thatcher, S. S. (1992). Influences of in vitro oocyte aging on microfertilization in the mouse with reference to zona hardening. J. Assist. Reprod. Genet. 9, 378–383.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gook, D. A. , Edgar, D. H. , Borg, J. , Archer, J. , Lutjen, P. J. , and McBain, J. C. (2003). Oocyte maturation, follicle rupture and luteinization in human cryopreserved ovarian tissue following xenografting. Hum. Reprod. 18, 1772–1781.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gosden, R. G. , Baird, D. T. , Wade, J. C. , and Webb, R. (1994). Restoration of fertility to oophorectomized sheep by ovarian autografts stored at –196°C. Hum. Reprod. 9, 597–603.
PubMed |

Gunasena, K. T. , Villines, P. M. , Critser, E. S. , and Ctitser, J. K. (1997). Live births after autologous transplant of cryopreserved mouse ovaries. Hum. Reprod. 12, 101–106.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hasegawa, A. , Mochida, N. , Ogasawara, T. , and Koyama, K. (2006). Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization. Fertil. Steril. 86((Suppl. 3)), 1182–1192.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hernandez-Fonseca, H. , Bosch, P. , Sirisathien, S. , Wininger, J. D. , Massey, J. B. , and Brackett, B. G. (2004). Effect of site of transplantation on follicular development of human ovarian tissue transplanted into intact or castrated immunodeficient mice. Fertil. Steril. 81((Suppl. 1)), 888–892.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kim, S. S. (2006). Fertility preservation in female cancer patients: current developments and future directions. Fertil. Steril. 85, 1–11.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kim, S. S. , Soules, M. R. , and Battaglia, D. E. (2002). Follicular development, ovulation, and corpus luteum formation in cryopreserved human ovarian tissue after xenotransplantation. Fertil. Steril. 78, 77–82.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kim, S. S. , Hwang, I. T. , and Lee, H. C. (2004). Heterotopic autotransplantation of cryobanked human ovarian tissue as a strategy to restore ovarian function. Fertil. Steril. 82, 930–932.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kiran, G. , Kiran, H. , Coban, Y. K. , Guven, A. M. , and Yuksel, M. (2004). Fresh autologous transplantation of ovarian cortical strip to the anterior abdominal wall at the pfannenstiel incision site. Fertil. Steril. 82, 954–956.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lechniak, D. , Warzych, E. , Pers-Kamczyc, E. , Sosnowski, J. , Antosik, P. , and Rubes, J. (2007). Gilts and sows produce similar rate of diploid oocytes in vitro whereas the incidence of aneuploidy differs significantly. Theriogenology 68, 755–762.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lee, R. K. , Ho, H. Y. , Yu, S. L. , and Lu, C. H. (2005). Blastocyst development after cryopreservation and subcutaneous transplantation of mouse ovarian tissue. J. Assist. Reprod. Genet. 22, 95–101.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Li, G. P. , Chen, D. Y. , Lian, L. , Sun, Q. Y. , Wang, K. M. , Liu, J. L. , Li, J. S. , and Han, Z. M. (2001). Viable rabbits derived from reconstructed oocytes by germinal vesicle transfer after intracytoplasmic sperm injection (ICSI). Mol. Reprod. Dev. 58, 180–185.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Liu, J. , Van der Elst, J. , Van den Broecke, R. , Dumortier, F. , and Dhont, M. (2000). Maturation of mouse primordial follicles by combination of grafting and in vitro culture. Biol. Reprod. 62, 1218–1223.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Liu, J. , Rybouchkin, A. , Van der Elst, J. , and Dhont, M. (2002a). Fertilization of mouse oocytes from in vitro-matured preantral follicles using classical in vitro fertilization or intracytoplasmic sperm injection. Biol. Reprod. 67, 575–579.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lorenzo, P. L. , Rebollar, P. G. , Illera, M. J. , Illera, J. C. , Illera, M. , and Alvarino, J. M. (1996). Stimulatory effect of insulin-like growth factor I and epidermal growth factor on the maturation of rabbit oocytes in vitro. J. Reprod. Fertil. 107, 109–117.
PubMed |

Mao, J. , Smith, M. F. , Rucker, E. B. , Wu, G. M. , McCauley, T. C. , Cantley, T. C. , Prather, R. S. , Didion, B. A. , and Day, B. N. (2004). Effect of epidermal growth factor and insulin-like growth factor I on porcine preantral follicular growth, antrum formation, and stimulation of granulosal cell proliferation and suppression of apoptosis in vitro. J. Anim. Sci. 82, 1967–1975.
PubMed |

Meirow, D. , Levron, J. , Eldar-Geva, T. , Hardan, I. , Fridman, E. , Yemini, Z. , and Dor, J. (2007). Monitoring the ovaries after autotransplantation of cryopreserved ovarian tissue: endocrine studies, in vitro fertilization cycles, and live birth. Fertil. Steril. 87, 418.e7–418.e15.
Crossref | GoogleScholarGoogle Scholar |

Nisolle, M. , Casanas-Roux, F. , Qu, J. , Motta, P. , and Donnez, J. (2000). Histologic and ultrastructural evaluation of fresh and frozen–thawed human ovarian xenografts in nude mice. Fertil. Steril. 74, 122–129.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nogueira, D. , Staessen, C. , Van de Velde, H. , and Van Steirteghem, A. (2000). Nuclear status and cytogenetics of embryos derived from in vitro-matured oocytes. Fertil. Steril. 74, 295–298.
Crossref | GoogleScholarGoogle Scholar | PubMed |

O’Brien, M. J. , Pendola, J. K. , and Eppig, J. J. (2003). A revised protocol for in vitro decelopment of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–1686.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oktay, K. , and Karlikaya, G. (2000). Ovarian function after transplantation of frozen, banked autologous ovarian tissue. N. Engl. J. Med. 342, 1919.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oktay, K. , Newton, H. , Mullan, J. , and Gosden, R. (1998). Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum. Reprod. 13, 1133–1138.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oktay, K. , Aydin, B. A. , and Karlikaya, G. (2001a). A technique for laparoscopic transplantation of frozen-banked ovarian tissue. Fertil. Steril. 75, 1212–1216.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oktay, K. , Economos, K. , Kan, M. , Rucinski, J. , Veeck, L. , and Rosenwaks, Z. (2001b). Endocrine function and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm. JAMA 286, 1490–1493.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oktay, K. , Buyuk, E. , Veeck, L. , Zaninovic, N. , Xu, K. , Takeuchi, T. , Opsahl, M. , and Rosenwaks, Z. (2004). Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. Lancet 363, 837–840.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sirard, M. A. , and Lambert, R. D. (1985). In vitro fertilization of bovine follicular oocytes obtained by laparoscopy. Biol. Reprod. 33, 487–494.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tryde Schmidt, K. L. , Yding Andersen, C. , Starup, J. , Loft, A. , Byskov, A. G. , and Nyboe Andersen, A. (2004). Orthotopic autotransplantation of cryopreserved ovarian tissue to a woman cured of cancer: follicular growth, steroid production and oocyte retrieval. Reprod. Biomed. Online 8, 448–453.
PubMed |

Wølner-Hanssen, P. , Hägglund, L. , Ploman, F. , Ramirez, A. , Manthorpe, R. , and Thuring, A. (2005). Autotransplantation of cryopreserved ovarian tissue to the right forearm 4½ years after autologous stem cell transplantation. Acta Obstet. Gynecol. Scand. 84, 695–698.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yoshimura, Y. , Hosoi, Y. , Iritani, A. , Nakamura, Y. , Atlas, S. J. , and Wallach, E. E. (1989). Developmental potential of rabbit oocyte matured in vitro: the possible contribution of prolactin. Biol. Reprod. 41, 26–33.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yoshimura, Y. , Ando, M. , Nagamatsu, S. , Iwashita, M. , Adachi, T. , Sueoka, K. , Miyazaki, T. , Kuji, N. , and Tanaka, M. (1996). Effects of insulin-like growth factor-I on follicle growth, oocyte maturation, and ovarian steroidogenesis and plasminogen activator activity in the rabbit. Biol. Reprod. 55, 152–160.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zeng, S. M. , Zhu, S. E. , Wang, Y. S. , Chen, X. I. , Zhang, Z. C. , and Chen, Y. F. (1999). An efficient method for in vitro fertilization in rabbits. Anim. Biotechnol. 10, 15–23.
PubMed |