Skip to main content
Erschienen in: Journal of Assisted Reproduction and Genetics 5/2017

11.02.2017 | Technological Innovations

Polar body transfer restores the developmental potential of oocytes to blastocyst stage in a case of repeated embryo fragmentation

verfasst von: Shuo-Ping Zhang, Chang-Fu Lu, Fei Gong, Ping-Yuan Xie, Liang Hu, Shun-Ji Zhang, Guang-Xiu Lu, Ge Lin

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 5/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose

We aimed to determine the developmental potential of human reconstructed oocytes after polar body genome transfer (PBT) and to report the case of a woman with multiple cycles of severe embryo fragmentation.

Methods

Fresh and cryopreserved first polar bodies (PB1s) were transferred to enucleated metaphase II oocytes (PB1T), while fresh PB2s were removed from fertilized oocytes and used instead of the female pronucleus in donor zygotes. Reconstructed oocytes underwent intracytoplasmic sperm injection (ICSI) and were cultured to blastocyst. Biopsied trophectoderm cells of PBT-derived blastocysts were screened for chromosomes by next-generation sequencing (NGS). Then, cryopreserved PB1T was carried out in one woman with a history of several cycles of extensive embryo fragmentation, and the blastocysts derived from PB1T were screened for aneuploidy but not transferred to the patient.

Results

There were no significant differences in the rates of normal fertilization and blastocyst formation between fresh and cryopreserved PB1T and control oocytes. Of the three fresh and three cryopreserved PB1T-derived blastocysts, two and one blastocysts exhibited normal diploidy respectively. In contrast, 17 PB2 transfers yielded 16 two pronuclei (2PN) zygotes with one normal and one small-sized pronucleus each and no blastocyst formation. In the female patient, 18 oocytes were inseminated by ICSI in the fourth cycle and the PB1s were biopsied. Although the embryos developed from the patient’s own oocytes showed severe fragmentation, the oocytes reconstructed after PB1T produced three chromosomally normal blastocysts.

Conclusions

Normal blastocysts can develop from human reconstructed oocytes after PB1T. The application of the first PB transfers may be beneficial to patients with a history of poor embryo development and excessive fragmentation.
Literatur
1.
Zurück zum Zitat Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14:141–52.CrossRefPubMed Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14:141–52.CrossRefPubMed
2.
3.
Zurück zum Zitat Verlinsky Y, Ginsberg N, Lifchez A, Valle J, Moise J, Strom CM. Analysis of the first polar body: preconception genetic diagnosis. Hum Reprod. 1990;5:826–9.CrossRefPubMed Verlinsky Y, Ginsberg N, Lifchez A, Valle J, Moise J, Strom CM. Analysis of the first polar body: preconception genetic diagnosis. Hum Reprod. 1990;5:826–9.CrossRefPubMed
4.
Zurück zum Zitat Wakayama T, Hayashi Y, Ogura A. Participation of the female pronucleus derived from the second polar body in full embryonic development of mice. J Reprod Fertil. 1997;110:263–6.CrossRefPubMed Wakayama T, Hayashi Y, Ogura A. Participation of the female pronucleus derived from the second polar body in full embryonic development of mice. J Reprod Fertil. 1997;110:263–6.CrossRefPubMed
5.
Zurück zum Zitat Wakayama T, Yanagimachi R. The first polar body can be used for the production of normal offspring in mice. Biol Reprod. 1998;59:100–4.CrossRefPubMed Wakayama T, Yanagimachi R. The first polar body can be used for the production of normal offspring in mice. Biol Reprod. 1998;59:100–4.CrossRefPubMed
6.
Zurück zum Zitat Wang T, Sha H, Ji D, Zhang HL, Chen D, Cao Y, et al. Polar body genome transfer for preventing the transmission of inherited mitochondrial diseases. Cell. 2014;157:1591–604.CrossRefPubMed Wang T, Sha H, Ji D, Zhang HL, Chen D, Cao Y, et al. Polar body genome transfer for preventing the transmission of inherited mitochondrial diseases. Cell. 2014;157:1591–604.CrossRefPubMed
7.
Zurück zum Zitat Wei Y, Zhang T, Wang YP, Schatten H, Sun QY. Polar bodies in assisted reproductive technology: current progress and future perspectives. Biol Reprod. 2015;92:19.CrossRefPubMed Wei Y, Zhang T, Wang YP, Schatten H, Sun QY. Polar bodies in assisted reproductive technology: current progress and future perspectives. Biol Reprod. 2015;92:19.CrossRefPubMed
8.
Zurück zum Zitat Cohen J, Scott R, Alikani M, Schimmel T, Munné S, Levron J, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4:269–80.CrossRefPubMed Cohen J, Scott R, Alikani M, Schimmel T, Munné S, Levron J, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4:269–80.CrossRefPubMed
9.
Zurück zum Zitat Cohen J, Scott R, Schimmel T, Levron J, Willadsen S. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet. 1997;350:186–7.CrossRefPubMed Cohen J, Scott R, Schimmel T, Levron J, Willadsen S. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet. 1997;350:186–7.CrossRefPubMed
10.
Zurück zum Zitat Dale B, Wilding M, Botta G, Rasile M, Marino M, Di Matteo L, et al. Pregnancy after cytoplasmic transfer in a couple suffering from idiopathic infertility: case report. Hum Reprod. 2001;16:1469–72.CrossRefPubMed Dale B, Wilding M, Botta G, Rasile M, Marino M, Di Matteo L, et al. Pregnancy after cytoplasmic transfer in a couple suffering from idiopathic infertility: case report. Hum Reprod. 2001;16:1469–72.CrossRefPubMed
11.
Zurück zum Zitat Prados FJ, Debrock S, Lemmen JG, Agerholm I. The cleavage stage embryo. Hum Reprod. 2012;27 Suppl 1:i50–71.CrossRefPubMed Prados FJ, Debrock S, Lemmen JG, Agerholm I. The cleavage stage embryo. Hum Reprod. 2012;27 Suppl 1:i50–71.CrossRefPubMed
12.
Zurück zum Zitat Fujimoto VY, Browne RW, Bloom MS, Sakkas D, Alikani M. Pathogenesis, developmental consequences, and clinical correlations of human embryo fragmentation. Fertil Steril. 2011;95:1197–204.CrossRefPubMed Fujimoto VY, Browne RW, Bloom MS, Sakkas D, Alikani M. Pathogenesis, developmental consequences, and clinical correlations of human embryo fragmentation. Fertil Steril. 2011;95:1197–204.CrossRefPubMed
13.
Zurück zum Zitat Meseguer M, Martínez-Conejero JA, O'Connor JE, Pellicer A, Remohí J, Garrido N. The significance of sperm DNA oxidation in embryo development and reproductive outcome in an oocyte donation program: a new model to study a male infertility prognostic factor. Fertil Steril. 2008;89:1191–9. Meseguer M, Martínez-Conejero JA, O'Connor JE, Pellicer A, Remohí J, Garrido N. The significance of sperm DNA oxidation in embryo development and reproductive outcome in an oocyte donation program: a new model to study a male infertility prognostic factor. Fertil Steril. 2008;89:1191–9.
14.
Zurück zum Zitat Xia P. Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum Reprod. 1997;12:1750–5.CrossRefPubMed Xia P. Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum Reprod. 1997;12:1750–5.CrossRefPubMed
15.
Zurück zum Zitat Stensen MH, Tanbo TG, Storeng R, Åbyholm T, Fedorcsak P. Fragmentation of human cleavage-stage embryos is related to the progression through meiotic and mitotic cell cycles. Fertil Steril. 2015;103:374–81.CrossRefPubMed Stensen MH, Tanbo TG, Storeng R, Åbyholm T, Fedorcsak P. Fragmentation of human cleavage-stage embryos is related to the progression through meiotic and mitotic cell cycles. Fertil Steril. 2015;103:374–81.CrossRefPubMed
16.
Zurück zum Zitat Jurisicova A, Varmuza S, Casper RF. Programmed cell death and human embryo fragmentation. Mol Hum Reprod. 1996;2:93–8.CrossRefPubMed Jurisicova A, Varmuza S, Casper RF. Programmed cell death and human embryo fragmentation. Mol Hum Reprod. 1996;2:93–8.CrossRefPubMed
17.
Zurück zum Zitat Levy R, Benchaib M, Cordonier H, Souchier C, Guerin JF. Annexin V labelling and terminal transferase-mediated DNA end labelling (TUNEL) assay in human arrested embryos. Mol Hum Reprod. 1998;4:775–83.CrossRefPubMed Levy R, Benchaib M, Cordonier H, Souchier C, Guerin JF. Annexin V labelling and terminal transferase-mediated DNA end labelling (TUNEL) assay in human arrested embryos. Mol Hum Reprod. 1998;4:775–83.CrossRefPubMed
18.
Zurück zum Zitat Bencomo E, Pérez R, Arteaga MF, Acosta E, Pena O, Lopez L, et al. Apoptosis of cultured granulosa-lutein cells is reduced by insulin-like growth factor I and may correlate with embryo fragmentation and pregnancy rate. Fertil Steril. 2006;85:474–80.CrossRefPubMed Bencomo E, Pérez R, Arteaga MF, Acosta E, Pena O, Lopez L, et al. Apoptosis of cultured granulosa-lutein cells is reduced by insulin-like growth factor I and may correlate with embryo fragmentation and pregnancy rate. Fertil Steril. 2006;85:474–80.CrossRefPubMed
19.
Zurück zum Zitat Alikani M, Schimmel T, Willadsen SM. Cytoplasmic fragmentation in activated eggs occurs in the cytokinetic phase of the cell cycle, in lieu of normal cytokinesis, and in response to cytoskeletal disorder. Mol Hum Reprod. 2005;11:335–44.CrossRefPubMed Alikani M, Schimmel T, Willadsen SM. Cytoplasmic fragmentation in activated eggs occurs in the cytokinetic phase of the cell cycle, in lieu of normal cytokinesis, and in response to cytoskeletal disorder. Mol Hum Reprod. 2005;11:335–44.CrossRefPubMed
20.
Zurück zum Zitat Fujimoto VY, Kane JP, Ishida BY, Bloom MS, Browne RW. High-density lipoprotein metabolism and the human embryo. Hum Reprod Update. 2010;16:20–38.CrossRefPubMed Fujimoto VY, Kane JP, Ishida BY, Bloom MS, Browne RW. High-density lipoprotein metabolism and the human embryo. Hum Reprod Update. 2010;16:20–38.CrossRefPubMed
21.
Zurück zum Zitat Alikani M, Cohen J, Tomkin G, Garrisi GJ, Mack C, Scott RT. Human embryo fragmentation in vitro and its implications for pregnancy and implantation. Fertil Steril. 1999;71:836–42.CrossRefPubMed Alikani M, Cohen J, Tomkin G, Garrisi GJ, Mack C, Scott RT. Human embryo fragmentation in vitro and its implications for pregnancy and implantation. Fertil Steril. 1999;71:836–42.CrossRefPubMed
22.
Zurück zum Zitat Ebner T, Yaman C, Moser M, Sommergruber M, Pölz W, Tews G. Embryo fragmentation in vitro and its impact on treatment and pregnancy outcome. Fertil Steril. 2001;76:281–5.CrossRefPubMed Ebner T, Yaman C, Moser M, Sommergruber M, Pölz W, Tews G. Embryo fragmentation in vitro and its impact on treatment and pregnancy outcome. Fertil Steril. 2001;76:281–5.CrossRefPubMed
23.
Zurück zum Zitat Alikani M. The origins and consequences of fragmentation in mammalian eggs and embryos. In: Elder K, Cohen J, editors. Human preimplantation embryo selection. London: Informa Healthcare; 2007. p. 51–78.CrossRef Alikani M. The origins and consequences of fragmentation in mammalian eggs and embryos. In: Elder K, Cohen J, editors. Human preimplantation embryo selection. London: Informa Healthcare; 2007. p. 51–78.CrossRef
24.
Zurück zum Zitat Xu X, Duan X, Lu C, Lin G, Lu G. Dynamic distribution of NuMA and microtubules in human fetal fibroblasts, developing oocytes and somatic cell nuclear transferred embryos. Hum Reprod. 2011;26:1052–60.CrossRefPubMed Xu X, Duan X, Lu C, Lin G, Lu G. Dynamic distribution of NuMA and microtubules in human fetal fibroblasts, developing oocytes and somatic cell nuclear transferred embryos. Hum Reprod. 2011;26:1052–60.CrossRefPubMed
25.
Zurück zum Zitat Gong F, Li X, Zhang S, Ma H, Cai S, Li J, et al. A modified ultra-long pituitary downregulation protocol improved endometrial receptivity and clinical outcome for infertile patients with polycystic ovarian syndrome. Exp Ther Med. 2015;10:1865–70.PubMedPubMedCentral Gong F, Li X, Zhang S, Ma H, Cai S, Li J, et al. A modified ultra-long pituitary downregulation protocol improved endometrial receptivity and clinical outcome for infertile patients with polycystic ovarian syndrome. Exp Ther Med. 2015;10:1865–70.PubMedPubMedCentral
26.
Zurück zum Zitat Zhang SP, Tan K, Gong F, Gu YF, Tan YQ, Lu CF, et al. Blastocysts can be rebiopsied for preimplantation genetic diagnosis and screening. Fertil Steril. 2014;102:1641–5.CrossRefPubMed Zhang SP, Tan K, Gong F, Gu YF, Tan YQ, Lu CF, et al. Blastocysts can be rebiopsied for preimplantation genetic diagnosis and screening. Fertil Steril. 2014;102:1641–5.CrossRefPubMed
27.
Zurück zum Zitat Tan YQ, Yin XY, Zhang SP, Jiang H, Tan K, Li J, et al. Clinical outcome of preimplantation genetic diagnosis and screening using next generation sequencing. Gigascience. 2014;3:30.CrossRefPubMedPubMedCentral Tan YQ, Yin XY, Zhang SP, Jiang H, Tan K, Li J, et al. Clinical outcome of preimplantation genetic diagnosis and screening using next generation sequencing. Gigascience. 2014;3:30.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Hou Y, Fan W, Yan L, Li R, Lian Y, Huang J, et al. Genome analyses of single human oocytes. Cell. 2013;155:1492–506.CrossRefPubMed Hou Y, Fan W, Yan L, Li R, Lian Y, Huang J, et al. Genome analyses of single human oocytes. Cell. 2013;155:1492–506.CrossRefPubMed
29.
Zurück zum Zitat Wakayama S, Hikichi T, Suetsugu R, Sakaide Y, Bui HT, Mizutani E, et al. Efficient establishment of mouse embryonic stem cell lines from single blastomeres and polar bodies. Stem Cells. 2007;25:986–93.CrossRefPubMed Wakayama S, Hikichi T, Suetsugu R, Sakaide Y, Bui HT, Mizutani E, et al. Efficient establishment of mouse embryonic stem cell lines from single blastomeres and polar bodies. Stem Cells. 2007;25:986–93.CrossRefPubMed
30.
Zurück zum Zitat Wang GJ, Yu JN, Tan XD, Zhou XL, Xu XB, Fan BQ. Injection of frozen-thawed porcine first polar bodies into enucleated oocytes results in fertilization and embryonic development. Theriogenology. 2011;75:826–31.CrossRefPubMed Wang GJ, Yu JN, Tan XD, Zhou XL, Xu XB, Fan BQ. Injection of frozen-thawed porcine first polar bodies into enucleated oocytes results in fertilization and embryonic development. Theriogenology. 2011;75:826–31.CrossRefPubMed
31.
Zurück zum Zitat Evsikov SV, Evsikov AV. Preimplantation development of manipulated mouse zygotes fused with the second polar bodies: a cytogenetic study. Int J Dev Biol. 1994;38:725–30.PubMed Evsikov SV, Evsikov AV. Preimplantation development of manipulated mouse zygotes fused with the second polar bodies: a cytogenetic study. Int J Dev Biol. 1994;38:725–30.PubMed
32.
Zurück zum Zitat VerMilyea MD, Maneck M, Yoshida N, Blochberger I, Suzuki E, Suzuki T, et al. Transcriptome asymmetry within mouse zygotes but not between early embryonic sister blastomeres. EMBO J. 2011;30:1841–51.CrossRefPubMedPubMedCentral VerMilyea MD, Maneck M, Yoshida N, Blochberger I, Suzuki E, Suzuki T, et al. Transcriptome asymmetry within mouse zygotes but not between early embryonic sister blastomeres. EMBO J. 2011;30:1841–51.CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Barritt J, Willadsen S, Brenner C, Cohen J. Cytoplasmic transfer in assisted reproduction. Hum Reprod Update. 2001;7:428–35.CrossRefPubMed Barritt J, Willadsen S, Brenner C, Cohen J. Cytoplasmic transfer in assisted reproduction. Hum Reprod Update. 2001;7:428–35.CrossRefPubMed
34.
Zurück zum Zitat Athayde Wirka K, Chen AA, Conaghan J, Ivani K, Gvakharia M, Behr B, et al. A typical embryo phenotypes identified by time-lapse microscopy: high prevalence and association with embryo development. Fertil Steril. 2014;101:1637–48.CrossRefPubMed Athayde Wirka K, Chen AA, Conaghan J, Ivani K, Gvakharia M, Behr B, et al. A typical embryo phenotypes identified by time-lapse microscopy: high prevalence and association with embryo development. Fertil Steril. 2014;101:1637–48.CrossRefPubMed
35.
Zurück zum Zitat Yang ST, Shi JX, Gong F, Zhang SP, Lu CF, Tan K, et al. Cleavage pattern predicts developmental potential of day 3 human embryos produced by IVF. Reprod Biomed Online. 2015;30:625–34.CrossRefPubMed Yang ST, Shi JX, Gong F, Zhang SP, Lu CF, Tan K, et al. Cleavage pattern predicts developmental potential of day 3 human embryos produced by IVF. Reprod Biomed Online. 2015;30:625–34.CrossRefPubMed
36.
Zurück zum Zitat Fragouli E, Wells D. Aneuploidy in the human blastocyst. Cytogenet Genome Res. 2011;133:149–59.CrossRefPubMed Fragouli E, Wells D. Aneuploidy in the human blastocyst. Cytogenet Genome Res. 2011;133:149–59.CrossRefPubMed
37.
Zurück zum Zitat Capalbo A, Rienzi L, Cimadomo D, Maggiulli R, Elliott T, Wright G, et al. Correlation between standard blastocyst morphology, euploidy and implantation: an observational study in two centers involving 956 screened blastocysts. Hum Reprod. 2014;29:1173–81.CrossRefPubMed Capalbo A, Rienzi L, Cimadomo D, Maggiulli R, Elliott T, Wright G, et al. Correlation between standard blastocyst morphology, euploidy and implantation: an observational study in two centers involving 956 screened blastocysts. Hum Reprod. 2014;29:1173–81.CrossRefPubMed
38.
Zurück zum Zitat Howe K, FitzHarris G. Recent insights into spindle function in mammalian oocytes and early embryos. Biol Reprod. 2013;89:71.CrossRefPubMed Howe K, FitzHarris G. Recent insights into spindle function in mammalian oocytes and early embryos. Biol Reprod. 2013;89:71.CrossRefPubMed
39.
Zurück zum Zitat Jones KT, Lane SI. Molecular causes of aneuploidy in mammalian eggs. Development. 2013;140:3719–30.CrossRefPubMed Jones KT, Lane SI. Molecular causes of aneuploidy in mammalian eggs. Development. 2013;140:3719–30.CrossRefPubMed
40.
Zurück zum Zitat Jones KT. Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum Reprod Update. 2008;14:143–58.CrossRefPubMed Jones KT. Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum Reprod Update. 2008;14:143–58.CrossRefPubMed
41.
Zurück zum Zitat Zhang J, Zhuang G, Zeng Y, Grifo J, Acosta C, Shu Y, et al. Pregnancy derived from human zygote pronuclear transfer in a patient who had arrested embryos after IVF. Reprod Biomed Online. 2016;33:529–33.CrossRefPubMed Zhang J, Zhuang G, Zeng Y, Grifo J, Acosta C, Shu Y, et al. Pregnancy derived from human zygote pronuclear transfer in a patient who had arrested embryos after IVF. Reprod Biomed Online. 2016;33:529–33.CrossRefPubMed
42.
Zurück zum Zitat Zhang J. Revisiting germinal vesicle transfer as a treatment for aneuploidy in infertile women with diminished ovarian reserve. J Assist Reprod Genet. 2015;32:313–7.CrossRefPubMed Zhang J. Revisiting germinal vesicle transfer as a treatment for aneuploidy in infertile women with diminished ovarian reserve. J Assist Reprod Genet. 2015;32:313–7.CrossRefPubMed
Metadaten
Titel
Polar body transfer restores the developmental potential of oocytes to blastocyst stage in a case of repeated embryo fragmentation
verfasst von
Shuo-Ping Zhang
Chang-Fu Lu
Fei Gong
Ping-Yuan Xie
Liang Hu
Shun-Ji Zhang
Guang-Xiu Lu
Ge Lin
Publikationsdatum
11.02.2017
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 5/2017
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-017-0881-y

Weitere Artikel der Ausgabe 5/2017

Journal of Assisted Reproduction and Genetics 5/2017 Zur Ausgabe

Update Gynäkologie

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