Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 11/2020

01-11-2020 | Commentary

The unknown human trophectoderm: implication for biopsy at the blastocyst stage

Author: Angelo Tocci

Published in: Journal of Assisted Reproduction and Genetics | Issue 11/2020

Login to get access

Abstract

Trophectoderm biopsy is increasingly performed for pre-implantation genetic testing of aneuploidies and considered a safe procedure on short-term clinical outcome, without strong assessment of long-term consequences. Poor biological information on human trophectoderm is available due to ethical restrictions. Therefore, most studies have been conducted in vitro (choriocarcinoma cell lines, embryonic and pluripotent stem cells) and on murine models that nevertheless poorly reflect the human counterpart. Polarization, compaction, and blastomere differentiation (e.g., the basis to ascertain trophectoderm origin) are poorly known in humans. In addition, the trophectoderm function is poorly known from a biological point of view, although a panoply of questionable and controversial microarray studies suggest that important genes overexpressed in trophectoderm are involved in pluripotency, metabolism, cell cycle, endocrine function, and implantation. The intercellular communication system between the trophectoderm cells and the inner cell mass, modulated by cell junctions and filopodia in the murine model, is obscure in humans. For the purpose of this paper, data mainly on primary cells from human and murine embryos has been reviewed. This review suggests that the trophectoderm origin and functions have been insufficiently ascertained in humans so far. Therefore, trophectoderm biopsy should be considered an experimental procedure to be undertaken only under approved rigorous experimental protocols in academic contexts.
Literature
1.
go back to reference Adjaye J, Huntriss J, Herwig R, BenKahla A, Brink TC, Wierling C, et al. Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells. 2005;23:1514–25. Adjaye J, Huntriss J, Herwig R, BenKahla A, Brink TC, Wierling C, et al. Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells. 2005;23:1514–25.
2.
go back to reference Assou S, Boumela I, Haouzi D, Monzo C, Dechaud H, Kadoch IJ, et al. Transcriptome analysis during human trophectoderm specification suggests new roles of metabolic and epigenetic genes. PLoS One. 2012;7:e39306. Assou S, Boumela I, Haouzi D, Monzo C, Dechaud H, Kadoch IJ, et al. Transcriptome analysis during human trophectoderm specification suggests new roles of metabolic and epigenetic genes. PLoS One. 2012;7:e39306.
3.
go back to reference Bai Q, Assou S, Haouzi D, Ramirez JM, Monzo C, Becker F, et al. Dissecting the first transcriptional divergence during human embryonic development. Stem Cell Rev Rep. 2012;8:150–62. Bai Q, Assou S, Haouzi D, Ramirez JM, Monzo C, Becker F, et al. Dissecting the first transcriptional divergence during human embryonic development. Stem Cell Rev Rep. 2012;8:150–62.
4.
go back to reference Cauffman G, De Rycke M, Sermon K, et al. Markers that define stemness in ESC are unable to identify the totipotent cells in human preimplantation embryos. Hum Reprod. 2009;24:63–70. Cauffman G, De Rycke M, Sermon K, et al. Markers that define stemness in ESC are unable to identify the totipotent cells in human preimplantation embryos. Hum Reprod. 2009;24:63–70.
5.
go back to reference Cauffman G, Van de Velde H, Liebaers I, et al. Oct-4 mRNA and protein expression during human preimplantation development. Mol Hum Reprod. 2005;11:173–81. Cauffman G, Van de Velde H, Liebaers I, et al. Oct-4 mRNA and protein expression during human preimplantation development. Mol Hum Reprod. 2005;11:173–81.
6.
go back to reference Niakan KK, Han J, Pedersen RA, Simon C, Pera RAR. Human pre-implantation embryo development. Development. 2012;139:829–41. Niakan KK, Han J, Pedersen RA, Simon C, Pera RAR. Human pre-implantation embryo development. Development. 2012;139:829–41.
7.
go back to reference Niakan KK, Eggan K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol. 2013;375:54–64. Niakan KK, Eggan K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol. 2013;375:54–64.
8.
go back to reference Fogarty NME, McCarthy A, Snijders KE, Powell BE, Kubikova N, Blakeley P, et al. Genome editing reveals a role for OCT4 in human embryogenesis. Nature. 2017;550:67–73. Fogarty NME, McCarthy A, Snijders KE, Powell BE, Kubikova N, Blakeley P, et al. Genome editing reveals a role for OCT4 in human embryogenesis. Nature. 2017;550:67–73.
9.
go back to reference Rossant J, Tam PPL. New insights into early human development: lessons for stem cell derivation and differentiation. Cell Stem Cell. 2017;20:18–28. Rossant J, Tam PPL. New insights into early human development: lessons for stem cell derivation and differentiation. Cell Stem Cell. 2017;20:18–28.
10.
go back to reference Scott RT Jr, Upham KM, Forman EJ, Zhao T, Treff NR. Cleavage-stage biopsy significantly impairs human embryonic implantation potential while blastocyst biopsy does not: a randomized and paired clinical trial. Fertil Steril. 2013;100:624–30. Scott RT Jr, Upham KM, Forman EJ, Zhao T, Treff NR. Cleavage-stage biopsy significantly impairs human embryonic implantation potential while blastocyst biopsy does not: a randomized and paired clinical trial. Fertil Steril. 2013;100:624–30.
11.
go back to reference Munné S, Kaplan B, Frattarelli JL, Child T, Nakhuda G, Shamma FN, et al. Preimplantation genetic testing for aneuploidy versus morphology as selection criteria for single frozen-thawed embryo transfer in good-prognosis patients: a multicenter randomized clinical trial. Fertil Steril. 2019;112:1071–9. Munné S, Kaplan B, Frattarelli JL, Child T, Nakhuda G, Shamma FN, et al. Preimplantation genetic testing for aneuploidy versus morphology as selection criteria for single frozen-thawed embryo transfer in good-prognosis patients: a multicenter randomized clinical trial. Fertil Steril. 2019;112:1071–9.
12.
go back to reference Pagliardini L, Viganò P, Alteri A, Corti L, Somigliana E, Papaleo E. Shooting STAR: reinterpreting the data from the ‘Single Embryo TrAnsfeR of Euploid Embryo’ randomized clinical trial. Reprod BioMed Online. 2020;40(4):475–8. Pagliardini L, Viganò P, Alteri A, Corti L, Somigliana E, Papaleo E. Shooting STAR: reinterpreting the data from the ‘Single Embryo TrAnsfeR of Euploid Embryo’ randomized clinical trial. Reprod BioMed Online. 2020;40(4):475–8.
13.
go back to reference Dahdouh EM, Balayla J, García-Velasco JA. Impact of blastocyst biopsy and comprehensive chromosome screening technology on preimplantation genetic screening: a systematic review of randomized controlled trials. Reprod BioMed Online. 2015;30:281–9. Dahdouh EM, Balayla J, García-Velasco JA. Impact of blastocyst biopsy and comprehensive chromosome screening technology on preimplantation genetic screening: a systematic review of randomized controlled trials. Reprod BioMed Online. 2015;30:281–9.
14.
go back to reference Gleicher N, Orvieto R. Is the hypothesis of preimplantation genetic screening (PGS) still supportable? A review. J Ovarian Res. 2017;10:21. Gleicher N, Orvieto R. Is the hypothesis of preimplantation genetic screening (PGS) still supportable? A review. J Ovarian Res. 2017;10:21.
15.
go back to reference Humięcka M, Szpila M, Kłoś P, Maleszewski M, Szczepańska K. Mouse blastomeres acquire ability to divide asymmetrically before compaction. PLoS One. 2017;12:e0175032. Humięcka M, Szpila M, Kłoś P, Maleszewski M, Szczepańska K. Mouse blastomeres acquire ability to divide asymmetrically before compaction. PLoS One. 2017;12:e0175032.
16.
go back to reference Ziomek CA, Johnson MH. Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell. 1980;21:935–42. Ziomek CA, Johnson MH. Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell. 1980;21:935–42.
17.
go back to reference Fleming TP, Pickering SJ. Maturation and polarisation of the endocytotic system in outside blastomeres during mouse preimplantation development. J Embryol Exp Morphol. 1985;89:175–208. Fleming TP, Pickering SJ. Maturation and polarisation of the endocytotic system in outside blastomeres during mouse preimplantation development. J Embryol Exp Morphol. 1985;89:175–208.
18.
go back to reference Johnson MH, Maro B. A dissection of the mechanisms generating and stabilizing polarity in mouse 8- and 16-cell blastomeres: the role of cytoskeletal elements. J Embryol Exp Morphol. 1985;90:311–34. Johnson MH, Maro B. A dissection of the mechanisms generating and stabilizing polarity in mouse 8- and 16-cell blastomeres: the role of cytoskeletal elements. J Embryol Exp Morphol. 1985;90:311–34.
19.
go back to reference Shirayoshi Y, Okada TS, Takeichi M. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell. 1983;35:631–8. Shirayoshi Y, Okada TS, Takeichi M. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell. 1983;35:631–8.
20.
go back to reference Kimber SJ, Surani MA, Barton SC. Interactions of blastomeres suggest changes in cell surface adhesiveness during the formation of inner cell mass and trophectoderm in the preimplantation mouse embryo. J Embryol Exp Morphol. 1982;70:133–52. Kimber SJ, Surani MA, Barton SC. Interactions of blastomeres suggest changes in cell surface adhesiveness during the formation of inner cell mass and trophectoderm in the preimplantation mouse embryo. J Embryol Exp Morphol. 1982;70:133–52.
21.
go back to reference Zhu M, Zernicka-Goetz M. Building an apical domain in the early mouse embryo: lessons, challenges and perspectives. Curr Opin Cell Biol. 2020;62:144–9. Zhu M, Zernicka-Goetz M. Building an apical domain in the early mouse embryo: lessons, challenges and perspectives. Curr Opin Cell Biol. 2020;62:144–9.
22.
go back to reference Hirate Y, Hirahara S, Inoue K, Kiyonari H, Niwa H, Sasaki H. Par-aPKC-dependent and -independent mechanisms cooperatively control cell polarity, Hippo signaling, and cell positioning in 16-cell stage mouse embryos. Develop Growth Differ. 2015;57:544–56. Hirate Y, Hirahara S, Inoue K, Kiyonari H, Niwa H, Sasaki H. Par-aPKC-dependent and -independent mechanisms cooperatively control cell polarity, Hippo signaling, and cell positioning in 16-cell stage mouse embryos. Develop Growth Differ. 2015;57:544–56.
23.
go back to reference Doe CQ. Cell polarity: the PARty expands. Nat Cell Biol. 2001;3:E7–9. Doe CQ. Cell polarity: the PARty expands. Nat Cell Biol. 2001;3:E7–9.
24.
go back to reference Pey R, Vial C, Schatten G, Hafner M. Increase in intracellular Ca2+ and relocation of E-cadherin during experimental decompaction of mouse embryos. Proc Natl Acad Sci U S A. 1998;95:12977–82. Pey R, Vial C, Schatten G, Hafner M. Increase in intracellular Ca2+ and relocation of E-cadherin during experimental decompaction of mouse embryos. Proc Natl Acad Sci U S A. 1998;95:12977–82.
25.
go back to reference Aberle H, Schwartz H, Kemler R. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J Cell Biochem. 1996;61:514–23. Aberle H, Schwartz H, Kemler R. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J Cell Biochem. 1996;61:514–23.
26.
go back to reference Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M, Cockburn K, et al. Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev Cell. 2014;30:410–22. Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M, Cockburn K, et al. Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev Cell. 2014;30:410–22.
27.
go back to reference Watanabe Y, Miyasaka KY, Kubo A, Kida YS, Nakagawa O, Hirate Y, et al. Notch and Hippo signaling converge on Strawberry Notch 1 (Sbno1) to synergistically activate Cdx2 during specification of the trophectoderm. Sci Rep. 2017;7:46135. Watanabe Y, Miyasaka KY, Kubo A, Kida YS, Nakagawa O, Hirate Y, et al. Notch and Hippo signaling converge on Strawberry Notch 1 (Sbno1) to synergistically activate Cdx2 during specification of the trophectoderm. Sci Rep. 2017;7:46135.
28.
go back to reference Anani S, Bhat S, Honma-Yamanaka N, Krawchuk D, Yamanaka Y. Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. Development. 2014;141:2813–24. Anani S, Bhat S, Honma-Yamanaka N, Krawchuk D, Yamanaka Y. Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. Development. 2014;141:2813–24.
29.
go back to reference Leung CY, Zernicka-Goetz M. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and –independent mechanisms. Nat Commun. 2013;4:2251. Leung CY, Zernicka-Goetz M. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and –independent mechanisms. Nat Commun. 2013;4:2251.
30.
go back to reference Kameyama Y, Ohnishi H, Shimoi G, Hashizume R, Ito M, Smith LC. Asymmetrical allocation of mitochondrial DNA to blastomeres during the first two cleavages in mouse embryos. Reprod Fertil Dev. 2010;22:1247–53. Kameyama Y, Ohnishi H, Shimoi G, Hashizume R, Ito M, Smith LC. Asymmetrical allocation of mitochondrial DNA to blastomeres during the first two cleavages in mouse embryos. Reprod Fertil Dev. 2010;22:1247–53.
31.
go back to reference Antczak M, Van Blerkom J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol Hum Reprod. 1997;3:1067–86. Antczak M, Van Blerkom J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol Hum Reprod. 1997;3:1067–86.
32.
go back to reference Tesarík J. Involvement of oocyte-coded message in cell differentiation control of early human embryos. Development. 1989;105:317–22. Tesarík J. Involvement of oocyte-coded message in cell differentiation control of early human embryos. Development. 1989;105:317–22.
33.
go back to reference Nikas G, Ao A, Winston RM, et al. Compaction and surface polarity in the human embryo in vitro. Biol Reprod. 1996;55:32–7. Nikas G, Ao A, Winston RM, et al. Compaction and surface polarity in the human embryo in vitro. Biol Reprod. 1996;55:32–7.
34.
go back to reference Dale B, Tosti E, Iaccarino M. Is the plasma membrane of the human oocyte reorganised following fertilisation and early cleavage? Zygote. 1995;3:31–6. Dale B, Tosti E, Iaccarino M. Is the plasma membrane of the human oocyte reorganised following fertilisation and early cleavage? Zygote. 1995;3:31–6.
35.
go back to reference Alikani M. Epithelial cadherin distribution in abnormal human pre-implantation embryos. Hum Reprod. 2005;20:3369–75. Alikani M. Epithelial cadherin distribution in abnormal human pre-implantation embryos. Hum Reprod. 2005;20:3369–75.
36.
go back to reference Ghassemifar MR, Eckert JJ, Houghton FD, Picton HM, Leese HJ, Fleming TP. Gene expression regulating epithelial intercellular junction biogenesis during human blastocyst development in vitro. Mol Hum Reprod. 2003;9:245–52. Ghassemifar MR, Eckert JJ, Houghton FD, Picton HM, Leese HJ, Fleming TP. Gene expression regulating epithelial intercellular junction biogenesis during human blastocyst development in vitro. Mol Hum Reprod. 2003;9:245–52.
37.
go back to reference Eckert JJ, Houghton FD, Hawkhead JA, Balen AH, Leese HJ, Picton HM, et al. Human embryos developing in vitro are susceptible to impaired epithelial junction biogenesis correlating with abnormal metabolic activity. Hum Reprod. 2007;22:2214–24. Eckert JJ, Houghton FD, Hawkhead JA, Balen AH, Leese HJ, Picton HM, et al. Human embryos developing in vitro are susceptible to impaired epithelial junction biogenesis correlating with abnormal metabolic activity. Hum Reprod. 2007;22:2214–24.
38.
go back to reference Campbell S, Swann HR, Seif MW, Kimber SJ, Aplin JD. Cell adhesion molecules on the oocyte and preimplantation human embryo. Hum Reprod. 1995;10:1571–8. Campbell S, Swann HR, Seif MW, Kimber SJ, Aplin JD. Cell adhesion molecules on the oocyte and preimplantation human embryo. Hum Reprod. 1995;10:1571–8.
39.
go back to reference Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell. 2009;16:398–410. Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell. 2009;16:398–410.
40.
go back to reference Qin H, Hejna M, Liu Y, Percharde M, Wossidlo M, Blouin L, et al. YAP induces human naive pluripotency. Cell Rep. 2016;14:2301–12. Qin H, Hejna M, Liu Y, Percharde M, Wossidlo M, Blouin L, et al. YAP induces human naive pluripotency. Cell Rep. 2016;14:2301–12.
41.
go back to reference Hildebrand S, Hultin S, Subramani A, Petropoulos S, Zhang Y, Cao X, et al. The E-cadherin/AmotL2 complex organizes actin filaments required for epithelial hexagonal packing and blastocyst hatching. Sci Rep. 2017;7:9540. Hildebrand S, Hultin S, Subramani A, Petropoulos S, Zhang Y, Cao X, et al. The E-cadherin/AmotL2 complex organizes actin filaments required for epithelial hexagonal packing and blastocyst hatching. Sci Rep. 2017;7:9540.
42.
go back to reference Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum Reprod. 2000;15(12):2621–33. Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum Reprod. 2000;15(12):2621–33.
43.
go back to reference Antczak M, Van Blerkom J. Temporal and spatial aspects of fragmentation in early human embryos: possible effects on developmental competence and association with the differential elimination of regulatory proteins from polarized domains. Hum Reprod. 1999;14:429–47. Antczak M, Van Blerkom J. Temporal and spatial aspects of fragmentation in early human embryos: possible effects on developmental competence and association with the differential elimination of regulatory proteins from polarized domains. Hum Reprod. 1999;14:429–47.
44.
go back to reference Fierro-González JC, White MD, Silva JC, Plachta N. Cadherin-dependent filopodia control preimplantation embryo compaction. Nat Cell Biol. 2013;15:1424–33. Fierro-González JC, White MD, Silva JC, Plachta N. Cadherin-dependent filopodia control preimplantation embryo compaction. Nat Cell Biol. 2013;15:1424–33.
45.
go back to reference Maître JL, Niwayama R, Turlier H, Nédélec F, Hiiragi T. Pulsatile cell-autonomous contractility drives compaction in the mouse embryo. Nat Cell Biol. 2015;17:849–55. Maître JL, Niwayama R, Turlier H, Nédélec F, Hiiragi T. Pulsatile cell-autonomous contractility drives compaction in the mouse embryo. Nat Cell Biol. 2015;17:849–55.
46.
go back to reference Larue L, Ohsugi M, Hirchenhain J, Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci U S A. 1994;91:8263–7. Larue L, Ohsugi M, Hirchenhain J, Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci U S A. 1994;91:8263–7.
47.
go back to reference Riethmacher D, Brinkmann V, Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci U S A. 1995;92:855–9. Riethmacher D, Brinkmann V, Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci U S A. 1995;92:855–9.
48.
go back to reference Ebner T, Moser M, Shebl O, Sommergruber M, Gaiswinkler U, Tews G. Morphological analysis at compacting stage is a valuable prognostic tool for ICSI patients. Reprod BioMed Online. 2009;18:61–6. Ebner T, Moser M, Shebl O, Sommergruber M, Gaiswinkler U, Tews G. Morphological analysis at compacting stage is a valuable prognostic tool for ICSI patients. Reprod BioMed Online. 2009;18:61–6.
49.
go back to reference Landry DW, Zucker HA, Sauer MV, Reznik M, Wiebe L. Hypocellularity and absence of compaction as criteria for embryonic death. Regen Med. 2006;1:367–71. Landry DW, Zucker HA, Sauer MV, Reznik M, Wiebe L. Hypocellularity and absence of compaction as criteria for embryonic death. Regen Med. 2006;1:367–71.
50.
go back to reference Ivec M, Kovacic B, Vlaisavljevic V. Prediction of human blastocyst development from morulas with delayed and/or incomplete compaction. Fertil Steril. 2011;96:1473–8. Ivec M, Kovacic B, Vlaisavljevic V. Prediction of human blastocyst development from morulas with delayed and/or incomplete compaction. Fertil Steril. 2011;96:1473–8.
51.
go back to reference Skiadas CC, Jackson KV, Racowsky C. Early compaction on day 3 may be associated with increased implantation potential. Fertil Steril. 2006;86:1386–91. Skiadas CC, Jackson KV, Racowsky C. Early compaction on day 3 may be associated with increased implantation potential. Fertil Steril. 2006;86:1386–91.
52.
go back to reference Le Cruguel S, Ferre-L’Hotellier V, Moriniere C, et al. Early compaction at day 3 may be a useful additional criterion for embryo transfer. J Assist Reprod Genet. 2013;30:683–90. Le Cruguel S, Ferre-L’Hotellier V, Moriniere C, et al. Early compaction at day 3 may be a useful additional criterion for embryo transfer. J Assist Reprod Genet. 2013;30:683–90.
53.
go back to reference Iwata K, Mio Y. Observation of human embryonic behavior in vitro by high-resolution time-lapse cinematography. Reprod Med Biol. 2016;15:145–54. Iwata K, Mio Y. Observation of human embryonic behavior in vitro by high-resolution time-lapse cinematography. Reprod Med Biol. 2016;15:145–54.
54.
go back to reference Campbell A, Fishel S, Bowman N, Duffy S, Sedler M, Hickman CFL. Modelling a risk classification of aneuploidy in human embryos using non-invasive morphokinetics. Reprod BioMed Online. 2013;26:477–85. Campbell A, Fishel S, Bowman N, Duffy S, Sedler M, Hickman CFL. Modelling a risk classification of aneuploidy in human embryos using non-invasive morphokinetics. Reprod BioMed Online. 2013;26:477–85.
55.
go back to reference Desai N, Abdelhafez F, Bedaiwy MA, et al. Clinical pregnancy and live births after transfer of embryos vitrified on day 3. Reprod BioMed Online. 2010;20:808–13. Desai N, Abdelhafez F, Bedaiwy MA, et al. Clinical pregnancy and live births after transfer of embryos vitrified on day 3. Reprod BioMed Online. 2010;20:808–13.
56.
go back to reference Fernandez Gallardo E, Spiessens, D’Hooghe T, et al. Effect of day 3 embryo morphometrics and morphokinetics on survival and implantation after slow freezing-thawing and after vitrification-warming: a retrospective cohort study. Reprod Biol Endocrinol. 2017;15:79. Fernandez Gallardo E, Spiessens, D’Hooghe T, et al. Effect of day 3 embryo morphometrics and morphokinetics on survival and implantation after slow freezing-thawing and after vitrification-warming: a retrospective cohort study. Reprod Biol Endocrinol. 2017;15:79.
57.
go back to reference Berger DS, Abdelhafez F, Russell H, et al. Severe teratozoospermia and its influence on pronuclear morphology, embryonic cleavage and compaction. Reprod Biol Endocrinol. 2011;9:37. Berger DS, Abdelhafez F, Russell H, et al. Severe teratozoospermia and its influence on pronuclear morphology, embryonic cleavage and compaction. Reprod Biol Endocrinol. 2011;9:37.
58.
go back to reference Desai N, Gill P, Tadros NN, Goldberg JM, Sabanegh E, Falcone T. Azoospermia and embryo morphokinetics: testicular sperm-derived embryos exhibit delays in early cell cycle events and increased arrest prior to compaction. J Assist Reprod Genet. 2018;35:1339–48. Desai N, Gill P, Tadros NN, Goldberg JM, Sabanegh E, Falcone T. Azoospermia and embryo morphokinetics: testicular sperm-derived embryos exhibit delays in early cell cycle events and increased arrest prior to compaction. J Assist Reprod Genet. 2018;35:1339–48.
59.
go back to reference Van Langendonckt A, Demylle D, Wyns C, et al. Comparison of G1.2/G2.2 and Sydney IVF cleavage/blastocyst sequential media for the culture of human embryos: a prospective, randomized, comparative study. Fertil Steril. 2001;76:1023–31. Van Langendonckt A, Demylle D, Wyns C, et al. Comparison of G1.2/G2.2 and Sydney IVF cleavage/blastocyst sequential media for the culture of human embryos: a prospective, randomized, comparative study. Fertil Steril. 2001;76:1023–31.
60.
go back to reference Paternot G, Spiessens M, Verstreken D, van Bauwel J, Debrock S, D’Hooghe T, et al. Is there a link between blastomere contact surfaces of day 3 embryos and live birth rate? Reprod Biol Endocrinol. 2012;10:78. Paternot G, Spiessens M, Verstreken D, van Bauwel J, Debrock S, D’Hooghe T, et al. Is there a link between blastomere contact surfaces of day 3 embryos and live birth rate? Reprod Biol Endocrinol. 2012;10:78.
61.
go back to reference Ebner T, Balaban B, Moser M, Shebl O, Urman B, Ata B, et al. Automatic user-independent zona pellucida imaging at the oocyte stage allows for the prediction of preimplantation development. Fertil Steril. 2010;94:913–20. Ebner T, Balaban B, Moser M, Shebl O, Urman B, Ata B, et al. Automatic user-independent zona pellucida imaging at the oocyte stage allows for the prediction of preimplantation development. Fertil Steril. 2010;94:913–20.
62.
go back to reference Fawzy M, AbdelRahman MY, Zidan MH, et al. Humid versus dry incubator: a prospective, randomized, controlled trial. Fertil Steril. 2017;108:277–83. Fawzy M, AbdelRahman MY, Zidan MH, et al. Humid versus dry incubator: a prospective, randomized, controlled trial. Fertil Steril. 2017;108:277–83.
63.
go back to reference Edwards RG, Purdy JM, Steptoe PC, Walters DE. The growth of human preimplantation embryos in vitro. Am J Obstet Gynecol. 1981;141:408–16. Edwards RG, Purdy JM, Steptoe PC, Walters DE. The growth of human preimplantation embryos in vitro. Am J Obstet Gynecol. 1981;141:408–16.
64.
go back to reference Iwata K, Yumoto K, Sugishima M, Mizoguchi C, Kai Y, Iba Y, et al. Analysis of compaction initiation in human embryos by using time-lapse cinematography. J Assist Reprod Genet. 2014;31:421–6. Iwata K, Yumoto K, Sugishima M, Mizoguchi C, Kai Y, Iba Y, et al. Analysis of compaction initiation in human embryos by using time-lapse cinematography. J Assist Reprod Genet. 2014;31:421–6.
65.
go back to reference Van de Velde H, Cauffman G, Tournaye H, et al. The four blastomeres of a 4-cell stage human embryo are able to develop individually into blastocysts with inner cell mass and trophectoderm. Hum Reprod. 2008;23:1742–7. Van de Velde H, Cauffman G, Tournaye H, et al. The four blastomeres of a 4-cell stage human embryo are able to develop individually into blastocysts with inner cell mass and trophectoderm. Hum Reprod. 2008;23:1742–7.
66.
go back to reference Fléchon JE, Panigel M, Kraemer DC, et al. Surface ultrastructure of preimplantation baboon embryos. Anat Embryol (Berl). 1976;149:289–95. Fléchon JE, Panigel M, Kraemer DC, et al. Surface ultrastructure of preimplantation baboon embryos. Anat Embryol (Berl). 1976;149:289–95.
67.
go back to reference Fleming TP, Sheth B, Fesenko I. Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci. 2001;6:D1000–7. Fleming TP, Sheth B, Fesenko I. Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci. 2001;6:D1000–7.
68.
go back to reference Ducibella T, Albertini DF, Anderson E, Biggers JD. The preimplantation mammalian embryo: characterization of intercellular junctions and their appearance during development. Dev Biol. 1975;45:231–50. Ducibella T, Albertini DF, Anderson E, Biggers JD. The preimplantation mammalian embryo: characterization of intercellular junctions and their appearance during development. Dev Biol. 1975;45:231–50.
69.
go back to reference Fleming TP, Javed Q, Collins J, Hay M. Biogenesis of structural intercellular junctions during cleavage in the mouse embryo. J Cell Sci Suppl. 1993;17:119–25. Fleming TP, Javed Q, Collins J, Hay M. Biogenesis of structural intercellular junctions during cleavage in the mouse embryo. J Cell Sci Suppl. 1993;17:119–25.
70.
go back to reference Wang H, Ding T, Brown N, Yamamoto Y, Prince LS, Reese J, et al. Zonula occludens-1 (ZO-1) is involved in morula to blastocyst transformation in the mouse. Dev Biol. 2008;318:112–25. Wang H, Ding T, Brown N, Yamamoto Y, Prince LS, Reese J, et al. Zonula occludens-1 (ZO-1) is involved in morula to blastocyst transformation in the mouse. Dev Biol. 2008;318:112–25.
71.
go back to reference Kim J, Gye MC, Kim MK. Role of occludin, a tight junction protein, in blastocoel formation, and in the paracellular permeability and differentiation of trophectoderm in preimplantation mouse embryos. Mol Cells. 2004;17:248–54. Kim J, Gye MC, Kim MK. Role of occludin, a tight junction protein, in blastocoel formation, and in the paracellular permeability and differentiation of trophectoderm in preimplantation mouse embryos. Mol Cells. 2004;17:248–54.
72.
go back to reference Zenker J, White MD, Gasnier M, Alvarez YD, Lim HYG, Bissiere S, et al. Expanding actin rings zipper the mouse embryo for blastocyst formation. Cell. 2018;173:776–91. Zenker J, White MD, Gasnier M, Alvarez YD, Lim HYG, Bissiere S, et al. Expanding actin rings zipper the mouse embryo for blastocyst formation. Cell. 2018;173:776–91.
73.
go back to reference Chan CJ, Costanzo M, Ruiz-Herrero T, Mönke G, Petrie RJ, Bergert M, et al. Hydraulic control of mammalian embryo size and cell fate. Nature. 2019;571:112–6. Chan CJ, Costanzo M, Ruiz-Herrero T, Mönke G, Petrie RJ, Bergert M, et al. Hydraulic control of mammalian embryo size and cell fate. Nature. 2019;571:112–6.
74.
go back to reference Beyer EC, Paul DL, Goodenough DA. Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol. 1987;105:2621–9. Beyer EC, Paul DL, Goodenough DA. Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol. 1987;105:2621–9.
75.
go back to reference Kidder GM, Winterhager E. Intercellular communication in preimplantation development: the role of gap junctions. Front Biosci. 2001;6:D731–6. Kidder GM, Winterhager E. Intercellular communication in preimplantation development: the role of gap junctions. Front Biosci. 2001;6:D731–6.
76.
go back to reference De Sousa PA, Juneja SC, Caveney S, et al. Normal development of preimplantation mouse embryos deficient in gap junctional coupling. J Cell Sci. 1997;110:1751–8. De Sousa PA, Juneja SC, Caveney S, et al. Normal development of preimplantation mouse embryos deficient in gap junctional coupling. J Cell Sci. 1997;110:1751–8.
77.
go back to reference Lee S, Gilula NB, Warner AE. Gap junctional communication and compaction during preimplantation stages of mouse development. Cell. 1987;51:851–60. Lee S, Gilula NB, Warner AE. Gap junctional communication and compaction during preimplantation stages of mouse development. Cell. 1987;51:851–60.
78.
go back to reference Becker DL, Davies CS. Role of gap junctions in the development of the preimplantation mouse embryo. Microsc Res Tech. 1995;31:364–74. Becker DL, Davies CS. Role of gap junctions in the development of the preimplantation mouse embryo. Microsc Res Tech. 1995;31:364–74.
79.
go back to reference Houghton FD. Role of gap junctions during early embryo development. Reproduction. 2005;129:129–35. Houghton FD. Role of gap junctions during early embryo development. Reproduction. 2005;129:129–35.
80.
go back to reference Gualtieri R, Santella L, Dale B. Tight junctions and cavitation in the human pre-embryo. Mol Reprod Dev. 1992;32:81–7. Gualtieri R, Santella L, Dale B. Tight junctions and cavitation in the human pre-embryo. Mol Reprod Dev. 1992;32:81–7.
81.
go back to reference Krivega M, Geens M, Van de Velde H. CAR expression in human embryos and hESC illustrates its role in pluripotency and tight junctions. Reproduction. 2014;148:531–44. Krivega M, Geens M, Van de Velde H. CAR expression in human embryos and hESC illustrates its role in pluripotency and tight junctions. Reproduction. 2014;148:531–44.
82.
go back to reference Dale B, Gualtieri R, Talevi R, Tosti E, Santella L, Elder K. Intercellular communication in the early human embryo. Mol Reprod Dev. 1991;29:22–8. Dale B, Gualtieri R, Talevi R, Tosti E, Santella L, Elder K. Intercellular communication in the early human embryo. Mol Reprod Dev. 1991;29:22–8.
83.
go back to reference Hardy K, Warner A, Winston RM, et al. Expression of intercellular junctions during preimplantation development of the human embryo. Mol Hum Reprod. 1996;2:621–32. Hardy K, Warner A, Winston RM, et al. Expression of intercellular junctions during preimplantation development of the human embryo. Mol Hum Reprod. 1996;2:621–32.
84.
go back to reference Bloor DJ, Wilson Y, Kibschull M, Traub O, Leese HJ, Winterhager E, et al. Expression of connexins in human preimplantation embryos in vitro. Reprod Biol Endocrinol. 2004;2:25. Bloor DJ, Wilson Y, Kibschull M, Traub O, Leese HJ, Winterhager E, et al. Expression of connexins in human preimplantation embryos in vitro. Reprod Biol Endocrinol. 2004;2:25.
85.
go back to reference Holding C, Bolton V, Monk M. Detection of human novel developmental genes in cDNA derived from replicate individual preimplantation embryos. Mol Hum Reprod. 2000;6:801–9. Holding C, Bolton V, Monk M. Detection of human novel developmental genes in cDNA derived from replicate individual preimplantation embryos. Mol Hum Reprod. 2000;6:801–9.
86.
go back to reference Pereda J, Coppo M. Ultrastructure of a two-cell human embryo. Anat Embryol (Berl). 1987;177:91–6. Pereda J, Coppo M. Ultrastructure of a two-cell human embryo. Anat Embryol (Berl). 1987;177:91–6.
87.
go back to reference Bentin-Ley U, Horn T, Sjogren A, et al. Ultrastructure of human blastocyst-endometrial interactions in vitro. J Reprod Fertil. 2000;120:337–50. Bentin-Ley U, Horn T, Sjogren A, et al. Ultrastructure of human blastocyst-endometrial interactions in vitro. J Reprod Fertil. 2000;120:337–50.
88.
go back to reference Sathananthan H, Menezes J, Gunasheela S. Mechanics of human blastocyst hatching in vitro. Reprod BioMed Online. 2003;7:228–34. Sathananthan H, Menezes J, Gunasheela S. Mechanics of human blastocyst hatching in vitro. Reprod BioMed Online. 2003;7:228–34.
89.
go back to reference Bloor DJ, Metcalfe AD, Rutherford, et al. Expression of cell adhesion molecules during human preimplantation embryo development. Mol Hum Reprod. 2002;8:237–45. Bloor DJ, Metcalfe AD, Rutherford, et al. Expression of cell adhesion molecules during human preimplantation embryo development. Mol Hum Reprod. 2002;8:237–45.
90.
go back to reference Houghton FD, Hawkhead JA, Humpherson PG, et al. Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod. 2002;17:999–1005. Houghton FD, Hawkhead JA, Humpherson PG, et al. Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod. 2002;17:999–1005.
91.
go back to reference Blakeley P, Fogarty NM, del Valle I, et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development. 2015;142:3151–65. Blakeley P, Fogarty NM, del Valle I, et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development. 2015;142:3151–65.
92.
go back to reference Yan L, Yang M, Guo H, Yang L, Wu J, Li R, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013;20:1131–9. Yan L, Yang M, Guo H, Yang L, Wu J, Li R, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013;20:1131–9.
93.
go back to reference Hertig AT, Rock J, Adams EC. A description of 34 human ova within the first 17 days of development. Am J Anat. 1956;98:435–93. Hertig AT, Rock J, Adams EC. A description of 34 human ova within the first 17 days of development. Am J Anat. 1956;98:435–93.
94.
go back to reference Shahbazi MN, Jedrusik A, Vuoristo S, Recher G, Hupalowska A, Bolton V, et al. Self-organization of the human embryo in the absence of maternal tissues. Nat Cell Biol. 2016;18:700–8. Shahbazi MN, Jedrusik A, Vuoristo S, Recher G, Hupalowska A, Bolton V, et al. Self-organization of the human embryo in the absence of maternal tissues. Nat Cell Biol. 2016;18:700–8.
95.
go back to reference Deglincerti A, Croft GF, Pietila LN, Zernicka-Goetz M, Siggia ED, Brivanlou AH. Self-organization of the in vitro attached human embryo. Nature. 2016;533:251–4. Deglincerti A, Croft GF, Pietila LN, Zernicka-Goetz M, Siggia ED, Brivanlou AH. Self-organization of the in vitro attached human embryo. Nature. 2016;533:251–4.
96.
go back to reference Morris SA. Human embryos cultured in vitro to 14 days. Open Biol. 2017;7:170003. Morris SA. Human embryos cultured in vitro to 14 days. Open Biol. 2017;7:170003.
97.
go back to reference Cauffman G, Liebaers I, Van Steirteghem A, et al. POU5F1 isoforms show different expression patterns in human embryonic stem cells and preimplantation embryos. Stem Cells. 2006;24:2685–91. Cauffman G, Liebaers I, Van Steirteghem A, et al. POU5F1 isoforms show different expression patterns in human embryonic stem cells and preimplantation embryos. Stem Cells. 2006;24:2685–91.
98.
go back to reference Hansis C, Tang YX, Grifo JA, Krey LC. Analysis of Oct-4 expression and ploidy in individual human blastomeres. Mol Hum Reprod. 2001;7:155–61. Hansis C, Tang YX, Grifo JA, Krey LC. Analysis of Oct-4 expression and ploidy in individual human blastomeres. Mol Hum Reprod. 2001;7:155–61.
99.
go back to reference Hansis C, Grifo JA, Krey LC. Oct-4 expression in inner cell mass and trophectoderm of human blastocysts. Mol Hum Reprod. 2000;6:999–1004. Hansis C, Grifo JA, Krey LC. Oct-4 expression in inner cell mass and trophectoderm of human blastocysts. Mol Hum Reprod. 2000;6:999–1004.
100.
go back to reference De Paepe C, Cauffman G, Verloes A, et al. Human trophectoderm cells are not yet committed. Hum Reprod. 2013;28:740–9. De Paepe C, Cauffman G, Verloes A, et al. Human trophectoderm cells are not yet committed. Hum Reprod. 2013;28:740–9.
101.
go back to reference Mitalipov SM, Kuo HC, Hennebold JD, Wolf DP. Oct-4 expression in pluripotent cells of the rhesus monkey. Biol Reprod. 2003;69:1785–92. Mitalipov SM, Kuo HC, Hennebold JD, Wolf DP. Oct-4 expression in pluripotent cells of the rhesus monkey. Biol Reprod. 2003;69:1785–92.
102.
go back to reference Kirchhof N, Carnwath JW, Lemme E, Anastassiadis K, Schöler H, Niemann H. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod. 2000;63:1698–705. Kirchhof N, Carnwath JW, Lemme E, Anastassiadis K, Schöler H, Niemann H. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod. 2000;63:1698–705.
103.
go back to reference Szczepańska K, Stańczuk L, Maleszewski M. Oct4 protein remains in trophectoderm until late stages of mouse blastocyst development. Reprod Biol. 2011;11:145–56. Szczepańska K, Stańczuk L, Maleszewski M. Oct4 protein remains in trophectoderm until late stages of mouse blastocyst development. Reprod Biol. 2011;11:145–56.
104.
go back to reference Harvey AJ, Armant DR, Bavister BD, Nichols SM, Brenner CA. Inner cell mass localization of NANOG precedes OCT3/4 in rhesus monkey blastocysts. Stem Cells Dev. 2009;18:1451–8. Harvey AJ, Armant DR, Bavister BD, Nichols SM, Brenner CA. Inner cell mass localization of NANOG precedes OCT3/4 in rhesus monkey blastocysts. Stem Cells Dev. 2009;18:1451–8.
105.
go back to reference Hambiliki F, Ström S, Zhang P, Stavreus-Evers A. Co-localization of NANOG and OCT4 in human pre-implantation embryos and in human embryonic stem cells. J Assist Reprod Genet. 2012;29:1021–8. Hambiliki F, Ström S, Zhang P, Stavreus-Evers A. Co-localization of NANOG and OCT4 in human pre-implantation embryos and in human embryonic stem cells. J Assist Reprod Genet. 2012;29:1021–8.
106.
go back to reference Toyooka Y, Oka S, Fujimori T. Early preimplantation cells expressing Cdx2 exhibit plasticity of specification to TE and ICM lineages through positional changes. Dev Biol. 2016;411:50–60. Toyooka Y, Oka S, Fujimori T. Early preimplantation cells expressing Cdx2 exhibit plasticity of specification to TE and ICM lineages through positional changes. Dev Biol. 2016;411:50–60.
107.
go back to reference Krivega MV, Geens M, Heindryckx B, Santos-Ribeiro S, Tournaye H, van de Velde H. Cyclin E1 plays a key role in balancing between totipotency and differentiation in human embryonic cells. Mol Hum Reprod. 2015;21:942–56. Krivega MV, Geens M, Heindryckx B, Santos-Ribeiro S, Tournaye H, van de Velde H. Cyclin E1 plays a key role in balancing between totipotency and differentiation in human embryonic cells. Mol Hum Reprod. 2015;21:942–56.
108.
go back to reference Sritanaudomchai H, Sparman M, Tachibana M, Clepper L, Woodward J, Gokhale S, et al. CDX2 in the formation of the trophectoderm lineage in primate embryos. Dev Biol. 2009;335:179–87. Sritanaudomchai H, Sparman M, Tachibana M, Clepper L, Woodward J, Gokhale S, et al. CDX2 in the formation of the trophectoderm lineage in primate embryos. Dev Biol. 2009;335:179–87.
109.
go back to reference Kunath T, Yamanaka Y, Detmar J, MacPhee D, Caniggia I, Rossant J, et al. Developmental differences in the expression of FGF receptors between human and mouse embryos. Placenta. 2014;35:1079–88. Kunath T, Yamanaka Y, Detmar J, MacPhee D, Caniggia I, Rossant J, et al. Developmental differences in the expression of FGF receptors between human and mouse embryos. Placenta. 2014;35:1079–88.
110.
go back to reference Bridges PJ, Jeoung M, Kim H, Kim JH, Lee DR, Ko CM, et al. Methodology matters: IVF versus ICSI and embryonic gene expression. Reprod BioMed Online. 2011;23:234–44. Bridges PJ, Jeoung M, Kim H, Kim JH, Lee DR, Ko CM, et al. Methodology matters: IVF versus ICSI and embryonic gene expression. Reprod BioMed Online. 2011;23:234–44.
111.
go back to reference Kohda T. Effects of embryonic manipulation and epigenetics. J Hum Genet. 2013;58:416–20. Kohda T. Effects of embryonic manipulation and epigenetics. J Hum Genet. 2013;58:416–20.
112.
go back to reference Aghajanova L, Shen S, Rojas AM, Fisher SJ, Irwin JC, Giudice LC. Comparative transcriptome analysis of human trophectoderm and embryonic stem cell-derived trophoblasts reveal key participants in early implantation. Biol Reprod. 2012;86:1–21. Aghajanova L, Shen S, Rojas AM, Fisher SJ, Irwin JC, Giudice LC. Comparative transcriptome analysis of human trophectoderm and embryonic stem cell-derived trophoblasts reveal key participants in early implantation. Biol Reprod. 2012;86:1–21.
113.
go back to reference Jones GM, Cram DS, Song B, Kokkali G, Pantos K, Trounson AO. Novel strategy with potential to identify developmentally competent IVF blastocysts. Hum Reprod. 2008;23:1748–59. Jones GM, Cram DS, Song B, Kokkali G, Pantos K, Trounson AO. Novel strategy with potential to identify developmentally competent IVF blastocysts. Hum Reprod. 2008;23:1748–59.
114.
go back to reference Ntostis P, Kokkali G, Iles D, Huntriss J, Tzetis M, Picton H, et al. Can trophectoderm RNA analysis predict human blastocyst competency? Syst Biol Reprod Med. 2019;65:312–25. Ntostis P, Kokkali G, Iles D, Huntriss J, Tzetis M, Picton H, et al. Can trophectoderm RNA analysis predict human blastocyst competency? Syst Biol Reprod Med. 2019;65:312–25.
115.
go back to reference Kirkegaard K, Villesen P, Jensen JM, Hindkjær JJ, Kølvraa S, Ingerslev HJ, et al. Distinct differences in global gene expression profiles in non-implanted blastocysts and blastocysts resulting in live birth. Gene. 2015;571:212–20. Kirkegaard K, Villesen P, Jensen JM, Hindkjær JJ, Kølvraa S, Ingerslev HJ, et al. Distinct differences in global gene expression profiles in non-implanted blastocysts and blastocysts resulting in live birth. Gene. 2015;571:212–20.
116.
go back to reference Martins WP, Nastri CO, Rienzi L, van der Poel SZ, Gracia C, Racowsky C. Blastocyst vs cleavage-stage embryo transfer: systematic review and meta-analysis of reproductive outcomes. Ultrasound Obstet Gynecol. 2017;49:583–91. Martins WP, Nastri CO, Rienzi L, van der Poel SZ, Gracia C, Racowsky C. Blastocyst vs cleavage-stage embryo transfer: systematic review and meta-analysis of reproductive outcomes. Ultrasound Obstet Gynecol. 2017;49:583–91.
117.
go back to reference Lonergan P, Fair T, Corcoran D, Evans ACO. Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology. 2006;65:137–52. Lonergan P, Fair T, Corcoran D, Evans ACO. Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology. 2006;65:137–52.
118.
go back to reference Kleijkers SH, Eijssen LM, Coonen E, et al. Differences in gene expression profiles between human preimplantation embryos cultured in two different IVF culture media. Hum Reprod. 2015;30:2303–11. Kleijkers SH, Eijssen LM, Coonen E, et al. Differences in gene expression profiles between human preimplantation embryos cultured in two different IVF culture media. Hum Reprod. 2015;30:2303–11.
119.
go back to reference McEwen KR, Leitch HG, Amouroux R, et al. The impact of culture on epigenetic properties of pluripotent stem cells and pre-implantation embryos. Biochem Soc Trans. 2013;41:711–9. McEwen KR, Leitch HG, Amouroux R, et al. The impact of culture on epigenetic properties of pluripotent stem cells and pre-implantation embryos. Biochem Soc Trans. 2013;41:711–9.
120.
go back to reference Tachataki M, Winston RML, Taylor DM. Quantitative RT-PCR reveals tuberous sclerosis gene, TSC2, mRNA degradation following cryopreservation in the human preimplantation embryo. Mol Hum Reprod. 2003;9:593–601. Tachataki M, Winston RML, Taylor DM. Quantitative RT-PCR reveals tuberous sclerosis gene, TSC2, mRNA degradation following cryopreservation in the human preimplantation embryo. Mol Hum Reprod. 2003;9:593–601.
121.
go back to reference Shaw L, Sneddon SF, Brison DR, Kimber SJ. Comparison of gene expression in fresh and frozen-thawed human preimplantation embryos. Reproduction. 2012;144:569–82. Shaw L, Sneddon SF, Brison DR, Kimber SJ. Comparison of gene expression in fresh and frozen-thawed human preimplantation embryos. Reproduction. 2012;144:569–82.
122.
go back to reference Houghton FD. Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation. 2006;74:11–8. Houghton FD. Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation. 2006;74:11–8.
123.
go back to reference Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science. 2004;303:1007–10. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science. 2004;303:1007–10.
124.
go back to reference Salas-Vidal E, Lomelí H. Imaging filopodia dynamics in the mouse blastocyst. Dev Biol. 2004;265:75–89. Salas-Vidal E, Lomelí H. Imaging filopodia dynamics in the mouse blastocyst. Dev Biol. 2004;265:75–89.
125.
go back to reference Chai N, Patel Y, Jacobson K, McMahon J, McMahon A, Rappolee DA. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev Biol. 1998;198:105–15. Chai N, Patel Y, Jacobson K, McMahon J, McMahon A, Rappolee DA. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev Biol. 1998;198:105–15.
126.
go back to reference Copp AJ. Interaction between inner cell mass and trophectoderm of the mouse blastocyst. I. A study of cellular proliferation. J Embryol Exp Morphol. 1978;48:109–25. Copp AJ. Interaction between inner cell mass and trophectoderm of the mouse blastocyst. I. A study of cellular proliferation. J Embryol Exp Morphol. 1978;48:109–25.
127.
go back to reference Copp AJ. Interaction between inner cell mass and trophectoderm of the mouse blastocyst. II. The fate of the polar trophectoderm. J Embryol Exp Morphol. 1979;51:109–20. Copp AJ. Interaction between inner cell mass and trophectoderm of the mouse blastocyst. II. The fate of the polar trophectoderm. J Embryol Exp Morphol. 1979;51:109–20.
128.
go back to reference Cruz YP, Pedersen RA. Cell fate in the polar trophectoderm of mouse blastocysts as studied by microinjection of cell lineage tracers. Dev Biol. 1985;112:73–83. Cruz YP, Pedersen RA. Cell fate in the polar trophectoderm of mouse blastocysts as studied by microinjection of cell lineage tracers. Dev Biol. 1985;112:73–83.
129.
go back to reference Fleming TP, Warren PD, Chisholm JC, et al. Trophectodermal processes regulate the expression of totipotency within the inner cell mass of the mouse expanding blastocyst. J Embryol Exp Morphol. 1984;84:63–90. Fleming TP, Warren PD, Chisholm JC, et al. Trophectodermal processes regulate the expression of totipotency within the inner cell mass of the mouse expanding blastocyst. J Embryol Exp Morphol. 1984;84:63–90.
130.
go back to reference Rowson LEA, Moor R. Development of sheep conceptus during the first fourteen days. J Anat. 1966;100:777–85. Rowson LEA, Moor R. Development of sheep conceptus during the first fourteen days. J Anat. 1966;100:777–85.
131.
go back to reference Carson SA, Gentry WL, Smith AL, Buster JE. Trophectoderm microbiopsy in murine blastocysts: comparison of four methods. J Assist Reprod Genet. 1993;10:427–33. Carson SA, Gentry WL, Smith AL, Buster JE. Trophectoderm microbiopsy in murine blastocysts: comparison of four methods. J Assist Reprod Genet. 1993;10:427–33.
132.
go back to reference Burwinkel TH, Kim HN, Buster JE, Minhas BS, Carson SA. Embryo survival after pronuclear microinjection and trophectoderm biopsy. Am J Obstet Gynecol. 1994;170:1199–203. Burwinkel TH, Kim HN, Buster JE, Minhas BS, Carson SA. Embryo survival after pronuclear microinjection and trophectoderm biopsy. Am J Obstet Gynecol. 1994;170:1199–203.
133.
go back to reference Sheardown SA, Findlay I, Turner A, Greaves D, Bolton VN, Mitchell M, et al. Preimplantation diagnosis of a human beta-globin transgene in biopsied trophectoderm cells and blastomeres of the mouse embryo. Hum Reprod. 1992;7:1297–303. Sheardown SA, Findlay I, Turner A, Greaves D, Bolton VN, Mitchell M, et al. Preimplantation diagnosis of a human beta-globin transgene in biopsied trophectoderm cells and blastomeres of the mouse embryo. Hum Reprod. 1992;7:1297–303.
134.
go back to reference Muggleton-Harris AL, Glazier AM, Pickering SJ. Biopsy of the human blastocyst and polymerase chain reaction (PCR) amplification of the beta-globin gene and a dinucleotide repeat motif from 2-6 trophectoderm cells. Hum Reprod. 1993;8:2197–205. Muggleton-Harris AL, Glazier AM, Pickering SJ. Biopsy of the human blastocyst and polymerase chain reaction (PCR) amplification of the beta-globin gene and a dinucleotide repeat motif from 2-6 trophectoderm cells. Hum Reprod. 1993;8:2197–205.
135.
go back to reference McArthur SJ, Leigh D, Marshall JT, et al. Pregnancies and live births after trophectoderm biopsy and preimplantation genetic testing of human blastocysts. Fertil Steril. 2005;84:1628–36. McArthur SJ, Leigh D, Marshall JT, et al. Pregnancies and live births after trophectoderm biopsy and preimplantation genetic testing of human blastocysts. Fertil Steril. 2005;84:1628–36.
136.
go back to reference Muggleton-Harris AL, Findlay I. In-vitro studies on ‘spare’ human preimplantation embryos in culture. Hum Reprod. 1991;6:85–92. Muggleton-Harris AL, Findlay I. In-vitro studies on ‘spare’ human preimplantation embryos in culture. Hum Reprod. 1991;6:85–92.
137.
go back to reference Dokras A, Sargent IL, Ross C, Gardner RL, Barlow DH. Trophectoderm biopsy in human blastocysts. Hum Reprod. 1990;5:821–5. Dokras A, Sargent IL, Ross C, Gardner RL, Barlow DH. Trophectoderm biopsy in human blastocysts. Hum Reprod. 1990;5:821–5.
138.
go back to reference Cimadomo D, Capalbo A, Levi-Setti PE, Soscia D, Orlando G, Albani E, et al. Associations of blastocyst features, trophectoderm biopsy and other laboratory practice with post-warming behavior and implantation. Hum Reprod. 2018;33:1992–2001. Cimadomo D, Capalbo A, Levi-Setti PE, Soscia D, Orlando G, Albani E, et al. Associations of blastocyst features, trophectoderm biopsy and other laboratory practice with post-warming behavior and implantation. Hum Reprod. 2018;33:1992–2001.
139.
go back to reference Fong CY, Bongso A, Sathananthan H, Ho J, Ng SC. Ultrastructural observations of enzymatically treated human blastocysts: zona-free blastocyst transfer and rescue of blastocysts with hatching difficulties. Hum Reprod. 2001;16:540–6. Fong CY, Bongso A, Sathananthan H, Ho J, Ng SC. Ultrastructural observations of enzymatically treated human blastocysts: zona-free blastocyst transfer and rescue of blastocysts with hatching difficulties. Hum Reprod. 2001;16:540–6.
140.
go back to reference Monk M, Muggleton-Harris AL, Rawlings E, Whittingham DG. Pre-implantation diagnosis of HPRT-deficient male and carrier female mouse embryos by trophectoderm biopsy. Hum Reprod. 1988;3:377–81. Monk M, Muggleton-Harris AL, Rawlings E, Whittingham DG. Pre-implantation diagnosis of HPRT-deficient male and carrier female mouse embryos by trophectoderm biopsy. Hum Reprod. 1988;3:377–81.
141.
go back to reference Gardner RL, Edwards RG. Control of the sex ratio at fullterm in the rabbit by transferring sexed blastocysts. Nature. 1968;218:346–9. Gardner RL, Edwards RG. Control of the sex ratio at fullterm in the rabbit by transferring sexed blastocysts. Nature. 1968;218:346–9.
142.
go back to reference Nijs M, Van Steirteghem A. Developmental potential of biopsied mouse blastocysts. J Exp Zool. 1990;256:232–6. Nijs M, Van Steirteghem A. Developmental potential of biopsied mouse blastocysts. J Exp Zool. 1990;256:232–6.
143.
go back to reference Gentry WL, Critser ES. Growth of mouse pups derived from biopsied blastocysts. Obstet Gynecol. 1995;85:1003–6. Gentry WL, Critser ES. Growth of mouse pups derived from biopsied blastocysts. Obstet Gynecol. 1995;85:1003–6.
144.
go back to reference Dokras A, Sargent IL, Gardner RL, Barlow DH. Human trophectoderm biopsy and secretion of chorionic gonadotrophin. Hum Reprod. 1991;6:1453–9. Dokras A, Sargent IL, Gardner RL, Barlow DH. Human trophectoderm biopsy and secretion of chorionic gonadotrophin. Hum Reprod. 1991;6:1453–9.
145.
go back to reference Summers PM, Campbell JM, Miller MW. Normal in-vivo development of marmoset monkey embryos after trophectoderm biopsy. Hum Reprod. 1988;3:389–93. Summers PM, Campbell JM, Miller MW. Normal in-vivo development of marmoset monkey embryos after trophectoderm biopsy. Hum Reprod. 1988;3:389–93.
146.
go back to reference Zhang S, Luo K, Cheng D, Tan Y, Lu C, He H, et al. Number of biopsied trophectoderm cells is likely to affect the implantation potential of blastocysts with poor trophectoderm quality. Fertil Steril. 2016;105:1222–7. Zhang S, Luo K, Cheng D, Tan Y, Lu C, He H, et al. Number of biopsied trophectoderm cells is likely to affect the implantation potential of blastocysts with poor trophectoderm quality. Fertil Steril. 2016;105:1222–7.
147.
go back to reference Molbay M, Kipmen-Korgun D, Korkmaz G, Ozekinci M, Turkay Korgun E. Human trophoblast progenitor cells express and release angiogenic factors. Int J Mol Cell Med. 2018;7:203–11. Molbay M, Kipmen-Korgun D, Korkmaz G, Ozekinci M, Turkay Korgun E. Human trophoblast progenitor cells express and release angiogenic factors. Int J Mol Cell Med. 2018;7:203–11.
148.
go back to reference Neal SA, Franasiak JM, Forman EJ, Werner MD, Morin SJ, Tao X, et al. High relative deoxyribonucleic acid content of trophectoderm biopsy adversely affects pregnancy outcomes. Fertil Steril. 2017;107:731–6. Neal SA, Franasiak JM, Forman EJ, Werner MD, Morin SJ, Tao X, et al. High relative deoxyribonucleic acid content of trophectoderm biopsy adversely affects pregnancy outcomes. Fertil Steril. 2017;107:731–6.
149.
go back to reference Gleicher N, Metzger J, Croft G, Kushnir VA, Albertini DF, Barad DH. A single trophectoderm biopsy at blastocyst stage is mathematically unable to determine embryo ploidy accurately enough for clinical use. Reprod Biol Endocrinol. 2017;15:33. Gleicher N, Metzger J, Croft G, Kushnir VA, Albertini DF, Barad DH. A single trophectoderm biopsy at blastocyst stage is mathematically unable to determine embryo ploidy accurately enough for clinical use. Reprod Biol Endocrinol. 2017;15:33.
150.
go back to reference Berger JJ. Primum non nocere: are we closer to saying that the trophectoderm biopsy does no harm? Fertil Steril. 2019;112:35–6. Berger JJ. Primum non nocere: are we closer to saying that the trophectoderm biopsy does no harm? Fertil Steril. 2019;112:35–6.
151.
go back to reference Vera-Rodriguez M, Diez-Juan A, Jimenez-Almazan J, Martinez S, Navarro R, Peinado V, et al. Origin and composition of cell-free DNA in spent medium from human embryo culture during preimplantation development. Hum Reprod. 2018;33:745–56. Vera-Rodriguez M, Diez-Juan A, Jimenez-Almazan J, Martinez S, Navarro R, Peinado V, et al. Origin and composition of cell-free DNA in spent medium from human embryo culture during preimplantation development. Hum Reprod. 2018;33:745–56.
152.
go back to reference Huang L, Bogale B, Tang Y, Lu S, Xie XS, Racowsky C. Noninvasive preimplantation genetic testing for aneuploidy in spent medium may be more reliable than trophectoderm biopsy. Proc Natl Acad Sci U S A. 2019;116:14105–12. Huang L, Bogale B, Tang Y, Lu S, Xie XS, Racowsky C. Noninvasive preimplantation genetic testing for aneuploidy in spent medium may be more reliable than trophectoderm biopsy. Proc Natl Acad Sci U S A. 2019;116:14105–12.
Metadata
Title
The unknown human trophectoderm: implication for biopsy at the blastocyst stage
Author
Angelo Tocci
Publication date
01-11-2020
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 11/2020
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-020-01925-0

Other articles of this Issue 11/2020

Journal of Assisted Reproduction and Genetics 11/2020 Go to the issue