Extended uterine receptivity for blastocyst implantation and full-term fetal development in mice with vitrified–warmed ovarian tissue autotransplantation

Abstract

Purpose

Our previous study demonstrated that vitrified–warmed ovarian tissue autotransplantation (VOAT) into estrus cycle-ceased ovariectomized mice restored fertility to achieve full-term fetal development for transferred embryos, while less steroidogenesis in the corpus luteum was observed in VOAT mice. It has been reported that the window of uterine receptivity for blastocyst implantation is extended at lower estrogen levels. Therefore, we hypothesized that duration of the window in VOAT mice could be extended.

Methods

Blastocysts were transferred into VOAT mice on day 5 of pseudopregnancy. Immunohistochemical analysis was performed to examine the potential in VOAT ovarian tissues.

Results

The rate of live birth pups from embryos transferred on day 5 of pseudopregnant VOAT mice was not different from that of embryos transferred on day 4 of pseudopregnancy in VOAT mice, while embryo transfer on day 5 into intact mice showed no pregnancy. Immunohistochemical analysis of the corpus luteum of day 8 pseudopregnant VOAT mice with uteri having decidualization induced on day 5 showed less steroidogenesis and blood vessel formation as compared to intact mice.

Conclusions

Uterine receptivity was extended in VOAT mice. Less steroidogenesis and blood vessel formation in the transferred ovarian tissues may be associated with the extended uterine receptivity.

References Meirow D, Nugent D. The effects of radiotherapy and chemotherapy on female reproduction. Hum Reprod Update, 2001, 7, 535–543 10.1093/humupd/7.6.535 Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M, Schmidt KL, Andersen AN, Ernst E. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod, 2008, 23, 2266–2272 10.1093/humrep/den244 Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin's disease. Oncologist, 2007, 12, 1437–1442 10.1634/theoncologist.12-12-1437 Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, Martinez-Madrid B, Langendonckt A. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet, 2004, 364, 1405–1410 10.1016/S0140-6736(04)17222-X Meirow D, Levron J, Eldar-Geva T, Hardan I, Fridman E, Zalel Y, Schiff E, Dor J. Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. N Engl J Med, 2005, 353, 318–321 10.1056/NEJMc055237 Rosendahl M, Loft A, Byskov AG, Ziebe S, Schmidt KT, Andersen AN, Ottosen C, Andersen CY. Biochemical pregnancy after fertilization of an oocyte aspirated from a heterotopic autotransplant of cryopreserved ovarian tissue: case report. Hum Reprod, 2006, 21, 2006–2009 10.1093/humrep/del140 Anderson RA, Wallace WH, Baird DT. Ovarian cryopreservation for fertility preservation: indications and outcomes. Reproduction, 2008, 136, 681–689 10.1530/REP-08-0097 Kim SS, Radford J, Harris M, Varley J, Rutherford AJ, Lieberman B, Shalet S, Gosden R. Ovarian tissue harvested from lymphoma patients to preserve fertility may be safe for autotransplantation. Hum Reprod, 2001, 16, 2056–2060 10.1093/humrep/16.10.2056 Kagawa N, Kuwayama M, Nakata K, Vajta G, Silber S, Manabe N, Kato O. Production of the first offspring from oocytes derived from fresh and cryopreserved pre-antral follicles of adult mice. Reprod Biomed Online, 2007, 14, 693–699 10.1016/S1472-6483(10)60670-0 Wang X, Catt S, Pangestu M, Temple-Smith P. Live offspring from vitrified blastocysts derived from fresh and cryopreserved ovarian tissue grafts of adult mice. Reproduction, 2009, 138, 527–535 10.1530/REP-09-0148 Mitsui A, Yoshizawa M. Successful pregnancy in ovariectomized mice using a combination of heterotopic autotransplantation of ovarian tissues and embryo transfer. Reprod Med Biol, 2007, 6, 85–90 10.1111/j.1447-0578.2007.00170.x Matsumoto H, Ezoe K, Mitsui A, Fukui E, Ochi M, Yoshizawa M. Vitrified–warmed ovarian tissue autotransplantation into ovariectomized mice restores sufficient ovarian function to support full-term pregnancy. Reprod Med Biol, 2011, 10, 185–191 10.1007/s12522-011-0090-9 Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet, 2006, 7, 185–199 10.1038/nrg1808 Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H. Molecular cues to implantation. Endocr Rev, 2004, 25, 341–373 10.1210/er.2003-0020 Paria BC, Reese J, Das SK, Dey SK. Deciphering the cross-talk of implantation: advances and challenges. Science, 2002, 296, 2185–2188 10.1126/science.1071601 Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, Fisher SJ. Trophoblast differentiation during embryo implantation and formation of the maternal–fetal interface. J Clin Invest, 2004, 114, 744–754 Paria BC, Huet-Hudson YM, Dey SK. Blastocyst's state of activity determines the “window” of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA, 1993, 90, 10159–10162 10.1073/pnas.90.21.10159 Ma WG, Song H, Das SK, Paria BC, Dey SK. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci USA, 2003, 100, 2963–2968 10.1073/pnas.0530162100 Yoshizawa M, Nakamoto S, Fukui E, Muramatsu T, Okamoto A. Chromosomal analysis of first-cleavage mouse eggs fertilized in caffeine-containing medium. J Reprod Dev, 1992, 38, 107–113 10.1262/jrd.38.107 Matsumoto H, Ma W, Smalley W, Trzaskos J, Breyer RM, Dey SK. Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol Reprod, 2001, 64, 1557–1565 10.1095/biolreprod64.5.1557 Matsumoto H, Ma WG, Daikoku T, Zhao X, Paria BC, Das SK, Trzaskos JM, Dey SK. Cyclooxygenase-2 differentially directs uterine angiogenesis during implantation in mice. J Biol Chem, 2002, 277, 29260–29267 10.1074/jbc.M203996200 Agarwal P, Peluso JJ, White BA. Steroidogenic factor-1 expression is transiently repressed and c-myc expression and deoxyribonucleic acid synthesis are induced in rat granulosa cells during the periovulatory period. Biol Reprod, 1996, 55, 1271–1275 10.1095/biolreprod55.6.1271 Hsieh M, Boerboom D, Shimada M, Lo Y, Parlow AF, Luhmann UF, Berger W, Richards JS. Mice null for Frizzled4 (Fzd4−/−) are infertile and exhibit impaired corpora lutea formation and function. Biol Reprod, 2005, 73, 1135–1146 10.1095/biolreprod.105.042739 Sakurai T, Tamura K, Okamoto S, Hara T, Kogo H. Possible role of cyclooxygenase II in the acquisition of ovarian luteal function in rodents. Biol Reprod, 2003, 69, 835–842 10.1095/biolreprod.102.010710 Sugino N, Suzuki T, Sakata A, Miwa I, Asada H, Taketani T, Yamagata Y, Tamura H. Angiogenesis in the human corpus luteum: changes in expression of angiopoietins in the corpus luteum throughout the menstrual cycle and in early pregnancy. J Clin Endocrinol Metab, 2005, 90, 6141–6148 10.1210/jc.2005-0643 Song H, Lim H, Paria BC, Matsumoto H, Swift LL, Morrow J, Bonventre JV, Dey SK. Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for ‘on-time’ embryo implantation that directs subsequent development. Development, 2002, 129, 2879–2889 Song H, Han K, Lim H. Progesterone supplementation extends uterine receptivity for blastocyst implantation in mice. Reproduction, 2007, 133, 487–493 10.1530/REP-06-0330