Skip to main content
Erschienen in: Journal of Assisted Reproduction and Genetics 4/2020

27.03.2020 | Fertility Preservation

The growth and development conditions in mouse offspring derived from ovarian tissue cryopreservation and orthotopic transplantation

verfasst von: Zhe Yan, Qing Li, Long Zhang, Beijia Kang, Wei Fan, Tang Deng, Jiang Zhu, Yan Wang

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 4/2020

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To investigate the potential development or metabolic risk in offspring derived from mice with transplanted frozen-thawed ovarian tissue.

Methods

Mice ovaries were intervened by vitrification (group V) and slow-freezing (group S) cryopreservation and orthotopic transplantation. Orthotopic transplantation of fresh ovarian (group F) and natural mating (group C) served as control groups. The fertility restoration and health conditions of generations were assessed by offspring counts, anti-fatigue and motor ability, and organ morphology. The methylation rate and expression level of imprinted genes (IGF2R, H19, SNRPN, and PLAGL1) were used to predict the potential risk of development in transplanted generations.

Results

Both the percentage of normal morphological follicles in different developmental periods and the litter size of receipt mice were comparable in all three transplanted groups. There was no significant difference in offspring mice’s birth defects, body weight gain, anti-fatigue ability, or exercise capacity among the four groups. The methylation rate of IGF2R, H19, and PLAGL1 showed a significant variation in cryopreservation groups as compared with control groups, as well as a difference in gene expression. The SNRPN appeared to be stable in methylation status. There were no differences in mRNA expression in all groups.

Conclusions

The different ovarian tissue cryopreservation methods did not influence either maternal fertility function or offspring growth. However, these technologies could affect the methylation rate and expression level of some development-related imprinting genes in the offspring, which may lead to some indeterminacy risk.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Wallace WH, Anderson RA, Irvine DS. Fertility preservation for young patients with cancer: who is at risk and what can be offered? Lancet Oncol. 2005;6:209–18.CrossRef Wallace WH, Anderson RA, Irvine DS. Fertility preservation for young patients with cancer: who is at risk and what can be offered? Lancet Oncol. 2005;6:209–18.CrossRef
2.
Zurück zum Zitat Letourneau JM, Ebbel EE, Katz PP, Oktay KH, McCulloch CE, Ai WZ, et al. Acute ovarian failure underestimates age-specific reproductive impairment for young women undergoing chemotherapy for cancer. Cancer. 2012a;118:1933–9.CrossRef Letourneau JM, Ebbel EE, Katz PP, Oktay KH, McCulloch CE, Ai WZ, et al. Acute ovarian failure underestimates age-specific reproductive impairment for young women undergoing chemotherapy for cancer. Cancer. 2012a;118:1933–9.CrossRef
3.
Zurück zum Zitat Chen SU, Chien CL, Wu MY, Chen TH, Lai SM, Lin CW, et al. Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Hum Reprod. 2006;21:2794–800.CrossRef Chen SU, Chien CL, Wu MY, Chen TH, Lai SM, Lin CW, et al. Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Hum Reprod. 2006;21:2794–800.CrossRef
4.
Zurück zum Zitat Li S, Wang Y. A carrier to vitrify the tissue slides and a new method of ovarian tissue vitrification. Patent for invention of China: ZL200810045568.X. 2012. Li S, Wang Y. A carrier to vitrify the tissue slides and a new method of ovarian tissue vitrification. Patent for invention of China: ZL200810045568.X. 2012.
5.
Zurück zum Zitat Wang Y, Xiao Z, Li L, Fan W, Li SW. Novel needle immersed vitrification: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation. Hum Reprod. 2008;23:2256–65.CrossRef Wang Y, Xiao Z, Li L, Fan W, Li SW. Novel needle immersed vitrification: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation. Hum Reprod. 2008;23:2256–65.CrossRef
6.
Zurück zum Zitat Xiao Z, Wang Y, Li L, Li SW. Needle immersed vitrification can lower the concentration of cryoprotectant in human ovarian tissue cryopreservation. Fertil Steril. 2010;94:2323–8.CrossRef Xiao Z, Wang Y, Li L, Li SW. Needle immersed vitrification can lower the concentration of cryoprotectant in human ovarian tissue cryopreservation. Fertil Steril. 2010;94:2323–8.CrossRef
7.
Zurück zum Zitat Li Q, Szatmary P, Liu Y, Ding Z, Zhou J, Sun Y, et al. Orthotopic transplantation of cryopreserved mouse ovaries and gonadotrophin releasing hormone analogues in the restoration of function following chemotherapy-induced ovarian damage. PLoS One. 2015;10:e0120736.CrossRef Li Q, Szatmary P, Liu Y, Ding Z, Zhou J, Sun Y, et al. Orthotopic transplantation of cryopreserved mouse ovaries and gonadotrophin releasing hormone analogues in the restoration of function following chemotherapy-induced ovarian damage. PLoS One. 2015;10:e0120736.CrossRef
8.
Zurück zum Zitat Practice Committees of American Society for Reproductive Medicine, Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril. 2013;99:37–43.CrossRef Practice Committees of American Society for Reproductive Medicine, Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril. 2013;99:37–43.CrossRef
9.
Zurück zum Zitat Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ, Patridge AH, et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31:2500–10.CrossRef Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ, Patridge AH, et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31:2500–10.CrossRef
10.
Zurück zum Zitat Hoekman EJ, Louwe LA, Rooijers M, van der Westerlaken LAJ, Klijn NF, Pilgram GSK, et al. Ovarian tissue cryopreservation: low usage rates and high live-birth rate after transplantation. Acta Obstet Gynecol Scand. 2019;00:1–9. Hoekman EJ, Louwe LA, Rooijers M, van der Westerlaken LAJ, Klijn NF, Pilgram GSK, et al. Ovarian tissue cryopreservation: low usage rates and high live-birth rate after transplantation. Acta Obstet Gynecol Scand. 2019;00:1–9.
11.
Zurück zum Zitat Liu L, Wood GA, Morikawa L, Ayearst R, Fleming C, McKerlie C. Restoration of fertility by orthotopic transplantation of frozen adult mouse ovaries. Hum Reprod. 2008;23:122–8.CrossRef Liu L, Wood GA, Morikawa L, Ayearst R, Fleming C, McKerlie C. Restoration of fertility by orthotopic transplantation of frozen adult mouse ovaries. Hum Reprod. 2008;23:122–8.CrossRef
12.
Zurück zum Zitat Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod. 1986;1:81–7.CrossRef Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod. 1986;1:81–7.CrossRef
13.
Zurück zum Zitat Imbert R, Moffa F, Tsepelidis S, Simon P, Delbaere A, Devreker F, et al. Safety and usefulness of cryopreservation of ovarian tissue to preserve fertility: a 12-year retrospective analysis. Hum Reprod. 2014;29:1931–40.CrossRef Imbert R, Moffa F, Tsepelidis S, Simon P, Delbaere A, Devreker F, et al. Safety and usefulness of cryopreservation of ovarian tissue to preserve fertility: a 12-year retrospective analysis. Hum Reprod. 2014;29:1931–40.CrossRef
14.
Zurück zum Zitat Dolmans M-M, Jadoul P, Gilliaux S, Amorim CA, Luyckx V, Squifflet J, et al. A review of 15 years of ovarian tissue bank activities. J Assist Reprod Genet. 2013;30:305–14.CrossRef Dolmans M-M, Jadoul P, Gilliaux S, Amorim CA, Luyckx V, Squifflet J, et al. A review of 15 years of ovarian tissue bank activities. J Assist Reprod Genet. 2013;30:305–14.CrossRef
15.
Zurück zum Zitat Rodriguez-Wallberg KA, Tanbo T, Tinkanen H, Thurin-Kjellberg A, Nedstrand E, Kitlinski ML, et al. Ovarian tissue cryopreservation and transplantation among alternatives for fertility preservation in the Nordic countries - compilation of 20 years of multicenter experience. Acta Obstet Gynecol Scand. 2016;95:1015–26.CrossRef Rodriguez-Wallberg KA, Tanbo T, Tinkanen H, Thurin-Kjellberg A, Nedstrand E, Kitlinski ML, et al. Ovarian tissue cryopreservation and transplantation among alternatives for fertility preservation in the Nordic countries - compilation of 20 years of multicenter experience. Acta Obstet Gynecol Scand. 2016;95:1015–26.CrossRef
16.
Zurück zum Zitat Donnez J, Dolmans M-M, Pellicer A, Diaz-Garcia C, Sanchez Serrano M, Schmidt KT, et al. Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil Steril. 2013;99:1503–13.CrossRef Donnez J, Dolmans M-M, Pellicer A, Diaz-Garcia C, Sanchez Serrano M, Schmidt KT, et al. Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil Steril. 2013;99:1503–13.CrossRef
17.
Zurück zum Zitat Dittrich R, Hackl J, Lotz L, Hoffmann I, Beckmann MW. Pregnancies and live births after 20 transplantations of cryopreserved ovarian tissue in a single center. Fertil Steril. 2015;103:462–8.CrossRef Dittrich R, Hackl J, Lotz L, Hoffmann I, Beckmann MW. Pregnancies and live births after 20 transplantations of cryopreserved ovarian tissue in a single center. Fertil Steril. 2015;103:462–8.CrossRef
18.
Zurück zum Zitat Jensen AK, Kristensen SG, Macklon KT, Jeppesen JV, Fedder J, Ernst E, et al. Outcomes of transplantations of cryopreserved ovarian tissue to 41 women in Denmark. Hum Reprod. 2015;30:2838–45.CrossRef Jensen AK, Kristensen SG, Macklon KT, Jeppesen JV, Fedder J, Ernst E, et al. Outcomes of transplantations of cryopreserved ovarian tissue to 41 women in Denmark. Hum Reprod. 2015;30:2838–45.CrossRef
19.
Zurück zum Zitat Takae S, Suzuki N. Current state and future possibilities of ovarian tissue transplantation. Reprod Med Biol. 2019;18:217–24.CrossRef Takae S, Suzuki N. Current state and future possibilities of ovarian tissue transplantation. Reprod Med Biol. 2019;18:217–24.CrossRef
20.
Zurück zum Zitat Zhang L, Yan LY, Zhi X, Yan J, Qiao J. Female fertility: is it safe to “freeze?”. Chin Med J. 2015;128:390–7.CrossRef Zhang L, Yan LY, Zhi X, Yan J, Qiao J. Female fertility: is it safe to “freeze?”. Chin Med J. 2015;128:390–7.CrossRef
21.
Zurück zum Zitat Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril. 2011;96:277–85.CrossRef Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril. 2011;96:277–85.CrossRef
22.
Zurück zum Zitat Cao YX, Xing Q, Li L, Cong L, Zhang ZG, Wei ZL, et al. Comparison of survival and embryonic development in human oocytes cryopreserved by slow-freezing and vitrification. Fertil Steril. 2009;92:1306–11.CrossRef Cao YX, Xing Q, Li L, Cong L, Zhang ZG, Wei ZL, et al. Comparison of survival and embryonic development in human oocytes cryopreserved by slow-freezing and vitrification. Fertil Steril. 2009;92:1306–11.CrossRef
23.
Zurück zum Zitat Cobo A, Meseguer M, Remohí J, Pellicer A. Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod. 2010;25:2239–46.CrossRef Cobo A, Meseguer M, Remohí J, Pellicer A. Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod. 2010;25:2239–46.CrossRef
24.
Zurück zum Zitat Loutradi KE, Kolibianakis EM, Venetis CA, Papanikolaou EG, Pados G, Bontis I, et al. Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertil Steril. 2008;90:186–93.CrossRef Loutradi KE, Kolibianakis EM, Venetis CA, Papanikolaou EG, Pados G, Bontis I, et al. Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertil Steril. 2008;90:186–93.CrossRef
25.
Zurück zum Zitat AbdelHafez FF, Desai N, Abou-Setta AM, Falcone T, Goldfarb J. Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. Reprod BioMed Online. 2010;20:209–22.CrossRef AbdelHafez FF, Desai N, Abou-Setta AM, Falcone T, Goldfarb J. Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. Reprod BioMed Online. 2010;20:209–22.CrossRef
26.
Zurück zum Zitat Poirot CJ, Martelli H, Genestie C, Golmard JL, Valteau-Couanet D, Helardot P, et al. Feasibility of ovarian tissue cryopreservation for prepubertal females with cancer. Pediatr Blood Cancer. 2007;49:74–8.CrossRef Poirot CJ, Martelli H, Genestie C, Golmard JL, Valteau-Couanet D, Helardot P, et al. Feasibility of ovarian tissue cryopreservation for prepubertal females with cancer. Pediatr Blood Cancer. 2007;49:74–8.CrossRef
27.
Zurück zum Zitat Amorim CA, Curaba M, Van Langendonckt A, Dolmans MM, Donnez J. Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod BioMed Online. 2011;23:160–86.CrossRef Amorim CA, Curaba M, Van Langendonckt A, Dolmans MM, Donnez J. Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod BioMed Online. 2011;23:160–86.CrossRef
28.
Zurück zum Zitat Sanfilippo S, Canis M, Smitz J, Sion B, Darcha C, Janny L, et al. Vitrification of human ovarian tissue: a practical and relevant alternative to slow freezing. Reprod Biol Endocrinol. 2015;13:67.CrossRef Sanfilippo S, Canis M, Smitz J, Sion B, Darcha C, Janny L, et al. Vitrification of human ovarian tissue: a practical and relevant alternative to slow freezing. Reprod Biol Endocrinol. 2015;13:67.CrossRef
29.
Zurück zum Zitat Pinborg A, Loft A, Aaris Henningsen AK, Rasmussen S, Andersen AN. Infant outcome of 957 singletons born after frozen embryo replacement: the Danish National Cohort Study 1995–2006. Fertil Steril. 2010a;94:1320–7.CrossRef Pinborg A, Loft A, Aaris Henningsen AK, Rasmussen S, Andersen AN. Infant outcome of 957 singletons born after frozen embryo replacement: the Danish National Cohort Study 1995–2006. Fertil Steril. 2010a;94:1320–7.CrossRef
30.
Zurück zum Zitat Pinborg A, Loft A, Henningsen AK, Ziebe S. Does assisted reproductive treatment increase the risk of birth defects in the offspring? Acta Obstet Gynecol Scand. 2012b;91:1245–6.CrossRef Pinborg A, Loft A, Henningsen AK, Ziebe S. Does assisted reproductive treatment increase the risk of birth defects in the offspring? Acta Obstet Gynecol Scand. 2012b;91:1245–6.CrossRef
31.
Zurück zum Zitat SanMiguel JM, Bartolomei MS. DNA methylation dynamics of genomic imprinting in mouse development. Biol Reprod. 2018;99:252–62.CrossRef SanMiguel JM, Bartolomei MS. DNA methylation dynamics of genomic imprinting in mouse development. Biol Reprod. 2018;99:252–62.CrossRef
32.
Zurück zum Zitat Cassidy FC, Charalambous M. Genomic imprinting, growth and maternal-fetal interactions. J Exp Biol. 2018;221(Suppl 1):jeb164517.CrossRef Cassidy FC, Charalambous M. Genomic imprinting, growth and maternal-fetal interactions. J Exp Biol. 2018;221(Suppl 1):jeb164517.CrossRef
33.
Zurück zum Zitat Negrón-Pérez VM, Echevarría FD, Huffman SR, Rivera RM. Determination of allelic expression of H19 in pre- and peri-implantation mouse embryos. Biol Reprod. 2013;88:1–11.CrossRef Negrón-Pérez VM, Echevarría FD, Huffman SR, Rivera RM. Determination of allelic expression of H19 in pre- and peri-implantation mouse embryos. Biol Reprod. 2013;88:1–11.CrossRef
34.
Zurück zum Zitat Le F, Wang LY, Wang N, Li L, le Li J, Zheng YM, et al. In vitro fertilization alters growth and expression of Igf2/H19 and their epigenetic mechanisms in the liver and skeletal muscle of newborn and elder mice. Biol Reprod. 2013;88:1–10.CrossRef Le F, Wang LY, Wang N, Li L, le Li J, Zheng YM, et al. In vitro fertilization alters growth and expression of Igf2/H19 and their epigenetic mechanisms in the liver and skeletal muscle of newborn and elder mice. Biol Reprod. 2013;88:1–10.CrossRef
35.
Zurück zum Zitat Saenz-de-Juano MD, Billooye K, Smitz J, Anckaert E. The loss of imprinted DNA methylation in mouse blastocysts is inflicted to a similar extent by in vitro follicle culture and ovulation induction. Mol Hum Reprod. 2016;22:427–41.CrossRef Saenz-de-Juano MD, Billooye K, Smitz J, Anckaert E. The loss of imprinted DNA methylation in mouse blastocysts is inflicted to a similar extent by in vitro follicle culture and ovulation induction. Mol Hum Reprod. 2016;22:427–41.CrossRef
36.
Zurück zum Zitat Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet. 2001;27:153–4.CrossRef Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet. 2001;27:153–4.CrossRef
37.
Zurück zum Zitat Lorgen-Ritchie M, Murray AD, FergusonSmith AC, Richards M, Horgan GW, Phillips LH, et al. Imprinting methylation in SNRPN and MEST1 in adult blood predicts cognitive ability. PLoS One. 2019;14:e0211799.CrossRef Lorgen-Ritchie M, Murray AD, FergusonSmith AC, Richards M, Horgan GW, Phillips LH, et al. Imprinting methylation in SNRPN and MEST1 in adult blood predicts cognitive ability. PLoS One. 2019;14:e0211799.CrossRef
38.
Zurück zum Zitat Santi D, De Vincentis S, Magnani E, Spaggiari G. Impairment of sperm DNA methylation in male infertility: a meta-analytic study. Andrology. 2017;5:695–703.CrossRef Santi D, De Vincentis S, Magnani E, Spaggiari G. Impairment of sperm DNA methylation in male infertility: a meta-analytic study. Andrology. 2017;5:695–703.CrossRef
Metadaten
Titel
The growth and development conditions in mouse offspring derived from ovarian tissue cryopreservation and orthotopic transplantation
verfasst von
Zhe Yan
Qing Li
Long Zhang
Beijia Kang
Wei Fan
Tang Deng
Jiang Zhu
Yan Wang
Publikationsdatum
27.03.2020
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 4/2020
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-020-01734-5

Weitere Artikel der Ausgabe 4/2020

Journal of Assisted Reproduction and Genetics 4/2020 Zur Ausgabe

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.