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Published in: Journal of Assisted Reproduction and Genetics 1/2020

01-01-2020 | Infertility | Reproductive Physiology and Disease

A novel “embryo-endometrial” adhesion model can potentially predict “receptive” or “non-receptive” endometrium

Authors: Jemma Evans, Kathryn J. Walker, Maree Bilandzic, Sophie Kinnear, Lois A. Salamonsen

Published in: Journal of Assisted Reproduction and Genetics | Issue 1/2020

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Abstract

Objective

To establish a model of human implantation that responds to hormonal stimuli and can differentiate between endometrium from fertile women and those with idiopathic infertility.

Design

A trophoblast stem cell (trophectodermal) line (TSC; derived from human pre-implantation embryo) was used to form trophectodermal spheroids (TS). TS attachment to monolayers of endometrial epithelial cell lines or primary endometrial epithelial cells (pHEECs) was determined.

Setting

Independent Medical Research Institute with close clinical linkages

Interventions

Spheroid attachment and outgrowth was determined with added hormones (estradiol 17β (E), E + medroxyprogesterone acetate (MPA) or E + MPA + human chorionic gonadotropin (hCG)). Spheroid attachment to E/MPA treated pHEEC prepared from fertile women or those with idiopathic infertility tested.

Main outcome measure

Firmly attached spheroids counted after co-culture for 6 h. Outgrowth was determined by quantitation of area covered by spheroid after firm adhesion.

Results

Functional adhesion of TS to two endometrial epithelial cell lines, Ishikawa and ECC-1 cells, was hormonally responsive, with adhesion/outgrowth increased by E/MPA (ECC-1; p < 0.01, Ishikawa; p < 0.01) and E/MPA/hCG (ECC-1; p < 0.001, Ishikawa p < 0.01) versus E alone. The same pattern of hormone responsiveness was observed in pHEEC obtained from fertile women (E vs, E/MPA; p < 0.01, E vs. E/MPA/hCG; p < 0.001). TS adhered to 85% of pHEEC obtained from fertile women (11/13) and 11% of pHEEC obtained from women with unexplained infertility (2/18, p < 0.001).

Conclusion

This new model of “embryo” implantation largely discriminates between endometrial epithelial cells obtained from fertile vs. infertile women based on adhesion; this holds potential as an in vitro “diagnostic” tool of endometrial infertility.
Literature
1.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
2.
go back to reference Macklon NS, Geraedts JP, Fauser BC. Conception to ongoing pregnancy: the ‘black box’ of early pregnancy loss. Hum Reprod Update. 2002;8:333–43.PubMedCrossRef Macklon NS, Geraedts JP, Fauser BC. Conception to ongoing pregnancy: the ‘black box’ of early pregnancy loss. Hum Reprod Update. 2002;8:333–43.PubMedCrossRef
3.
go back to reference Harton GL, Munne S, Surrey M, Grifo J, Kaplan B, McCulloh DH, et al. Diminished effect of maternal age on implantation after preimplantation genetic diagnosis with array comparative genomic hybridization. Fertil Steril. 2013;100:1695–703.PubMedCrossRef Harton GL, Munne S, Surrey M, Grifo J, Kaplan B, McCulloh DH, et al. Diminished effect of maternal age on implantation after preimplantation genetic diagnosis with array comparative genomic hybridization. Fertil Steril. 2013;100:1695–703.PubMedCrossRef
4.
go back to reference Hannan NJ, Paiva P, Dimitriadis E, Salamonsen LA. Models for study of human embryo implantation: choice of cell lines? Biol Reprod. 2010;82:235–45.PubMedCrossRef Hannan NJ, Paiva P, Dimitriadis E, Salamonsen LA. Models for study of human embryo implantation: choice of cell lines? Biol Reprod. 2010;82:235–45.PubMedCrossRef
5.
go back to reference Weimar CH, Post Uiterweer ED, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo-endometrium interactions. Reprod BioMed Online. 2013;27:461–76.PubMedCrossRef Weimar CH, Post Uiterweer ED, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo-endometrium interactions. Reprod BioMed Online. 2013;27:461–76.PubMedCrossRef
6.
go back to reference Ho H, Singh H, Aljofan M, Nie G. A high-throughput in vitro model of human embryo attachment. Fertil Steril. 2012;97:974–8.PubMedCrossRef Ho H, Singh H, Aljofan M, Nie G. A high-throughput in vitro model of human embryo attachment. Fertil Steril. 2012;97:974–8.PubMedCrossRef
7.
go back to reference Boggavarapu NR, Berger C, von Grothusen C, Menezes J, Gemzell-Danielsson K, Lalitkumar PG. Effects of low doses of mifepristone on human embryo implantation process in a three-dimensional human endometrial in vitro co-culture system. Contraception. 2016;94:143–51.PubMedCrossRef Boggavarapu NR, Berger C, von Grothusen C, Menezes J, Gemzell-Danielsson K, Lalitkumar PG. Effects of low doses of mifepristone on human embryo implantation process in a three-dimensional human endometrial in vitro co-culture system. Contraception. 2016;94:143–51.PubMedCrossRef
8.
go back to reference Galan A, O’Connor JE, Valbuena D, Herrer R, Remohi J, Pampfer S, et al. The human blastocyst regulates endometrial epithelial apoptosis in embryonic adhesion. Biol Reprod. 2000;63:430–9.PubMedCrossRef Galan A, O’Connor JE, Valbuena D, Herrer R, Remohi J, Pampfer S, et al. The human blastocyst regulates endometrial epithelial apoptosis in embryonic adhesion. Biol Reprod. 2000;63:430–9.PubMedCrossRef
9.
go back to reference Lalitkumar PG, Lalitkumar S, Meng CX, Stavreus-Evers A, Hambiliki F, Bentin-Ley U, et al. Mifepristone, but not levonorgestrel, inhibits human blastocyst attachment to an in vitro endometrial three-dimensional cell culture model. Hum Reprod. 2007;22:3031–7.PubMedCrossRef Lalitkumar PG, Lalitkumar S, Meng CX, Stavreus-Evers A, Hambiliki F, Bentin-Ley U, et al. Mifepristone, but not levonorgestrel, inhibits human blastocyst attachment to an in vitro endometrial three-dimensional cell culture model. Hum Reprod. 2007;22:3031–7.PubMedCrossRef
10.
go back to reference Lalitkumar S, Boggavarapu NR, Menezes J, Dimitriadis E, Zhang JG, Nicola NA, et al. Polyethylene glycated leukemia inhibitory factor antagonist inhibits human blastocyst implantation and triggers apoptosis by down-regulating embryonic AKT. Fertil Steril. 2013;100:1160–9.PubMedCrossRef Lalitkumar S, Boggavarapu NR, Menezes J, Dimitriadis E, Zhang JG, Nicola NA, et al. Polyethylene glycated leukemia inhibitory factor antagonist inhibits human blastocyst implantation and triggers apoptosis by down-regulating embryonic AKT. Fertil Steril. 2013;100:1160–9.PubMedCrossRef
11.
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.PubMedCrossRef 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.PubMedCrossRef
12.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
13.
go back to reference Kirby DR. The development of mouse blastocysts transplanted to the scrotal and cryptorchid testis. J Anat. 1963;97:119–30.PubMedPubMedCentral Kirby DR. The development of mouse blastocysts transplanted to the scrotal and cryptorchid testis. J Anat. 1963;97:119–30.PubMedPubMedCentral
14.
go back to reference Kirby DR. Development of the mouse 9lastocyst transplanted to the spleen. J Reprod Fertil. 1963;5:1–12.PubMedCrossRef Kirby DR. Development of the mouse 9lastocyst transplanted to the spleen. J Reprod Fertil. 1963;5:1–12.PubMedCrossRef
15.
16.
go back to reference Panelli DM, Phillips CH, Brady PC. Incidence, diagnosis and management of tubal and nontubal ectopic pregnancies: a review. Fertil Res Pract. 2015;1:15.PubMedPubMedCentralCrossRef Panelli DM, Phillips CH, Brady PC. Incidence, diagnosis and management of tubal and nontubal ectopic pregnancies: a review. Fertil Res Pract. 2015;1:15.PubMedPubMedCentralCrossRef
17.
go back to reference Valdes CT, Schutt A, Simon C. Implantation failure of endometrial origin: it is not pathology, but our failure to synchronize the developing embryo with a receptive endometrium. Fertil Steril. 2017;108:15–8.PubMedCrossRef Valdes CT, Schutt A, Simon C. Implantation failure of endometrial origin: it is not pathology, but our failure to synchronize the developing embryo with a receptive endometrium. Fertil Steril. 2017;108:15–8.PubMedCrossRef
18.
go back to reference Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod. 2010;16:135–52.PubMedCrossRef Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod. 2010;16:135–52.PubMedCrossRef
19.
20.
go back to reference Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet. 2006;7:185–99.PubMedCrossRef Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet. 2006;7:185–99.PubMedCrossRef
21.
go back to reference Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature. 1992;359:76–9.PubMedCrossRef Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature. 1992;359:76–9.PubMedCrossRef
22.
go back to reference Oliveira JB, Vagnini LD, Petersen CG, Renzi A, Oliveira-Pelegrin GR, Mauri AL, et al. Association between leukaemia inhibitory factor gene polymorphism and pregnancy outcomes after assisted reproduction techniques. Reprod BioMed Online. 2016;32:66–78.PubMedCrossRef Oliveira JB, Vagnini LD, Petersen CG, Renzi A, Oliveira-Pelegrin GR, Mauri AL, et al. Association between leukaemia inhibitory factor gene polymorphism and pregnancy outcomes after assisted reproduction techniques. Reprod BioMed Online. 2016;32:66–78.PubMedCrossRef
23.
go back to reference Paiva P, Menkhorst E, Salamonsen L, Dimitriadis E. Leukemia inhibitory factor and interleukin-11: critical regulators in the establishment of pregnancy. Cytokine Growth Factor Rev. 2009;20:319–28.PubMedCrossRef Paiva P, Menkhorst E, Salamonsen L, Dimitriadis E. Leukemia inhibitory factor and interleukin-11: critical regulators in the establishment of pregnancy. Cytokine Growth Factor Rev. 2009;20:319–28.PubMedCrossRef
24.
go back to reference Brinsden PR, Alam V, de Moustier B, Engrand P. Recombinant human leukemia inhibitory factor does not improve implantation and pregnancy outcomes after assisted reproductive techniques in women with recurrent unexplained implantation failure. Fertil Steril. 2009;91:1445–7.PubMedCrossRef Brinsden PR, Alam V, de Moustier B, Engrand P. Recombinant human leukemia inhibitory factor does not improve implantation and pregnancy outcomes after assisted reproductive techniques in women with recurrent unexplained implantation failure. Fertil Steril. 2009;91:1445–7.PubMedCrossRef
25.
go back to reference Lee YL, Fong SW, Chen AC, Li T, Yue C, Lee CL, et al. Establishment of a novel human embryonic stem cell-derived trophoblastic spheroid implantation model. Hum Reprod. 2015;30:2614–26.PubMedCrossRef Lee YL, Fong SW, Chen AC, Li T, Yue C, Lee CL, et al. Establishment of a novel human embryonic stem cell-derived trophoblastic spheroid implantation model. Hum Reprod. 2015;30:2614–26.PubMedCrossRef
26.
go back to reference Rivron NC, Frias-Aldeguer J, Vrij EJ, Boisset JC, Korving J, Vivie J, et al. Blastocyst-like structures generated solely from stem cells. Nature. 2018;557:106–11.PubMedCrossRef Rivron NC, Frias-Aldeguer J, Vrij EJ, Boisset JC, Korving J, Vivie J, et al. Blastocyst-like structures generated solely from stem cells. Nature. 2018;557:106–11.PubMedCrossRef
27.
go back to reference Zdravkovic T, Nazor KL, Larocque N, Gormley M, Donne M, Hunkapillar N, et al. Human stem cells from single blastomeres reveal pathways of embryonic or trophoblast fate specification. Development. 2015;142:4010–25.PubMedPubMedCentral Zdravkovic T, Nazor KL, Larocque N, Gormley M, Donne M, Hunkapillar N, et al. Human stem cells from single blastomeres reveal pathways of embryonic or trophoblast fate specification. Development. 2015;142:4010–25.PubMedPubMedCentral
28.
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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference Paiva P, Hannan NJ, Hincks C, Meehan KL, Pruysers E, Dimitriadis E, et al. Human chorionic gonadotrophin regulates FGF2 and other cytokines produced by human endometrial epithelial cells, providing a mechanism for enhancing endometrial receptivity. Hum Reprod. 2011;26:1153–62.PubMedCrossRef Paiva P, Hannan NJ, Hincks C, Meehan KL, Pruysers E, Dimitriadis E, et al. Human chorionic gonadotrophin regulates FGF2 and other cytokines produced by human endometrial epithelial cells, providing a mechanism for enhancing endometrial receptivity. Hum Reprod. 2011;26:1153–62.PubMedCrossRef
31.
go back to reference Nepomnaschy PA, Weinberg CR, Wilcox AJ, Baird DD. Urinary hCG patterns during the week following implantation. Hum Reprod. 2008;23:271–7.PubMedCrossRef Nepomnaschy PA, Weinberg CR, Wilcox AJ, Baird DD. Urinary hCG patterns during the week following implantation. Hum Reprod. 2008;23:271–7.PubMedCrossRef
32.
go back to reference Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med. 1999;340:1796–9.PubMedCrossRef Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med. 1999;340:1796–9.PubMedCrossRef
33.
go back to reference Thie M, Harrach-Ruprecht B, Sauer H, Fuchs P, Albers A, Denker HW. Cell adhesion to the apical pole of epithelium: a function of cell polarity. Eur J Cell Biol. 1995;66:180–91.PubMed Thie M, Harrach-Ruprecht B, Sauer H, Fuchs P, Albers A, Denker HW. Cell adhesion to the apical pole of epithelium: a function of cell polarity. Eur J Cell Biol. 1995;66:180–91.PubMed
34.
go back to reference Martin JC, Jasper MJ, Valbuena D, Meseguer M, Remohi J, Pellicer A, et al. Increased adhesiveness in cultured endometrial-derived cells is related to the absence of moesin expression. Biol Reprod. 2000;63:1370–6.PubMedCrossRef Martin JC, Jasper MJ, Valbuena D, Meseguer M, Remohi J, Pellicer A, et al. Increased adhesiveness in cultured endometrial-derived cells is related to the absence of moesin expression. Biol Reprod. 2000;63:1370–6.PubMedCrossRef
35.
go back to reference Thie M, Denker HW. In vitro studies on endometrial adhesiveness for trophoblast: cellular dynamics in uterine epithelial cells. Cells Tissues Organs. 2002;172:237–52.PubMedCrossRef Thie M, Denker HW. In vitro studies on endometrial adhesiveness for trophoblast: cellular dynamics in uterine epithelial cells. Cells Tissues Organs. 2002;172:237–52.PubMedCrossRef
36.
go back to reference Whitby S, Salamonsen LA, Evans J. The endometrial polarity paradox: differential regulation of polarity within secretory-phase human endometrium. Endocrinology. 2018;159:506–18.PubMedCrossRef Whitby S, Salamonsen LA, Evans J. The endometrial polarity paradox: differential regulation of polarity within secretory-phase human endometrium. Endocrinology. 2018;159:506–18.PubMedCrossRef
37.
go back to reference Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99:673–9.PubMedCrossRef Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99:673–9.PubMedCrossRef
38.
go back to reference Yedwab GA, Paz G, Homonnai TZ, David MP, Kraicer PF. The temperature, pH, and partial pressure of oxygen in the cervix and uterus of women and uterus of rats during the cycle. Fertil Steril. 1976;27:304–9.PubMedCrossRef Yedwab GA, Paz G, Homonnai TZ, David MP, Kraicer PF. The temperature, pH, and partial pressure of oxygen in the cervix and uterus of women and uterus of rats during the cycle. Fertil Steril. 1976;27:304–9.PubMedCrossRef
40.
go back to reference Graham JD, Clarke CL. Physiological action of progesterone in target tissues. Endocr Rev. 1997;18:502–19.PubMed Graham JD, Clarke CL. Physiological action of progesterone in target tissues. Endocr Rev. 1997;18:502–19.PubMed
41.
go back to reference Evans J, Catalano RD, Brown P, Sherwin R, Critchley HO, Fazleabas AT, et al. Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB J. 2009;23:2165–75.PubMedPubMedCentralCrossRef Evans J, Catalano RD, Brown P, Sherwin R, Critchley HO, Fazleabas AT, et al. Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB J. 2009;23:2165–75.PubMedPubMedCentralCrossRef
42.
go back to reference Fazleabas AT, Donnelly KM, Srinivasan S, Fortman JD, Miller JB. Modulation of the baboon (Papio anubis) uterine endometrium by chorionic gonadotrophin during the period of uterine receptivity. Proc Natl Acad Sci U S A. 1999;96:2543–8.PubMedPubMedCentralCrossRef Fazleabas AT, Donnelly KM, Srinivasan S, Fortman JD, Miller JB. Modulation of the baboon (Papio anubis) uterine endometrium by chorionic gonadotrophin during the period of uterine receptivity. Proc Natl Acad Sci U S A. 1999;96:2543–8.PubMedPubMedCentralCrossRef
43.
go back to reference Licht P, Fluhr H, Neuwinger J, Wallwiener D, Wildt L. Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol Cell Endocrinol. 2007;269:85–92.PubMedCrossRef Licht P, Fluhr H, Neuwinger J, Wallwiener D, Wildt L. Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol Cell Endocrinol. 2007;269:85–92.PubMedCrossRef
44.
go back to reference Licht P, Russu V, Lehmeyer S, Moll J, Siebzehnrubl E, Wildt L. Intrauterine microdialysis reveals cycle-dependent regulation of endometrial insulin-like growth factor binding protein-1 secretion by human chorionic gonadotropin. Fertil Steril. 2002;78:252–8.PubMedCrossRef Licht P, Russu V, Lehmeyer S, Moll J, Siebzehnrubl E, Wildt L. Intrauterine microdialysis reveals cycle-dependent regulation of endometrial insulin-like growth factor binding protein-1 secretion by human chorionic gonadotropin. Fertil Steril. 2002;78:252–8.PubMedCrossRef
45.
go back to reference Sherwin JR, Sharkey AM, Cameo P, Mavrogianis PM, Catalano RD, Edassery S, et al. Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology. 2007;148:618–26.PubMedCrossRef Sherwin JR, Sharkey AM, Cameo P, Mavrogianis PM, Catalano RD, Edassery S, et al. Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology. 2007;148:618–26.PubMedCrossRef
46.
go back to reference Greening DW, Nguyen HP, Evans J, Simpson RJ, Salamonsen LA. Modulating the endometrial epithelial proteome and secretome in preparation for pregnancy: The role of ovarian steroid and pregnancy hormones. J Proteome. 2016;144:99–112.CrossRef Greening DW, Nguyen HP, Evans J, Simpson RJ, Salamonsen LA. Modulating the endometrial epithelial proteome and secretome in preparation for pregnancy: The role of ovarian steroid and pregnancy hormones. J Proteome. 2016;144:99–112.CrossRef
48.
go back to reference Macklon NS, Brosens JJ. The human endometrium as a sensor of embryo quality. Biol Reprod. 2014;91:98.PubMedCrossRef Macklon NS, Brosens JJ. The human endometrium as a sensor of embryo quality. Biol Reprod. 2014;91:98.PubMedCrossRef
49.
go back to reference Diaz-Gimeno P, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Alama P, Pellicer A, et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2011;95:50–60 60 e51-15.PubMedCrossRef Diaz-Gimeno P, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Alama P, Pellicer A, et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2011;95:50–60 60 e51-15.PubMedCrossRef
50.
go back to reference Fitzgerald HC, Evans J, Johnson N, Infusini G, Webb A, Rombauts LJR, et al. Idiopathic infertility in women is associated with distinct changes in proliferative phase uterine fluid proteins. Biol Reprod. 2018;98:752–64.PubMedCrossRef Fitzgerald HC, Evans J, Johnson N, Infusini G, Webb A, Rombauts LJR, et al. Idiopathic infertility in women is associated with distinct changes in proliferative phase uterine fluid proteins. Biol Reprod. 2018;98:752–64.PubMedCrossRef
51.
go back to reference Fitzgerald HC, Salamonsen LA, Rombauts LJ, Vollenhoven BJ, Edgell TA. The proliferative phase underpins endometrial development: altered cytokine profiles in uterine lavage fluid of women with idiopathic infertility. Cytokine. 2016;88:12–9.PubMedCrossRef Fitzgerald HC, Salamonsen LA, Rombauts LJ, Vollenhoven BJ, Edgell TA. The proliferative phase underpins endometrial development: altered cytokine profiles in uterine lavage fluid of women with idiopathic infertility. Cytokine. 2016;88:12–9.PubMedCrossRef
52.
go back to reference Sebastian-Leon P, Garrido N, Remohi J, Pellicer A, Diaz-Gimeno P. Asynchronous and pathological windows of implantation: two causes of recurrent implantation failure. Hum Reprod. 2018;33:626–35.PubMedCrossRef Sebastian-Leon P, Garrido N, Remohi J, Pellicer A, Diaz-Gimeno P. Asynchronous and pathological windows of implantation: two causes of recurrent implantation failure. Hum Reprod. 2018;33:626–35.PubMedCrossRef
53.
go back to reference Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat Cell Biol. 2017;19:568–77.PubMedPubMedCentralCrossRef Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat Cell Biol. 2017;19:568–77.PubMedPubMedCentralCrossRef
54.
go back to reference Boretto M, Cox B, Noben M, Hendriks N, Fassbender A, Roose H, et al. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development. 2017;144:1775–86.PubMed Boretto M, Cox B, Noben M, Hendriks N, Fassbender A, Roose H, et al. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development. 2017;144:1775–86.PubMed
55.
go back to reference Boretto M, Maenhoudt N, Luo X, Hennes A, Boeckx B, Bui B, et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat Cell Biol. 2019;21:1041–51.PubMedCrossRef Boretto M, Maenhoudt N, Luo X, Hennes A, Boeckx B, Bui B, et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat Cell Biol. 2019;21:1041–51.PubMedCrossRef
56.
go back to reference Gardner DK. Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion? Bioessays. 2015;37:364–71.PubMedPubMedCentralCrossRef Gardner DK. Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion? Bioessays. 2015;37:364–71.PubMedPubMedCentralCrossRef
57.
go back to reference Shahbazi MN, Scialdone A, Skorupska N, Weberling A, Recher G, Zhu M, et al. Pluripotent state transitions coordinate morphogenesis in mouse and human embryos. Nature. 2017;552:239–43.PubMedPubMedCentralCrossRef Shahbazi MN, Scialdone A, Skorupska N, Weberling A, Recher G, Zhu M, et al. Pluripotent state transitions coordinate morphogenesis in mouse and human embryos. Nature. 2017;552:239–43.PubMedPubMedCentralCrossRef
58.
go back to reference Chen X, Jiang L, Wang CC, Huang J, Li TC. Hypoxia inducible factor and microvessels in peri-implantation endometrium of women with recurrent miscarriage. Fertil Steril. 2016;105:1496–502 e1494.PubMedCrossRef Chen X, Jiang L, Wang CC, Huang J, Li TC. Hypoxia inducible factor and microvessels in peri-implantation endometrium of women with recurrent miscarriage. Fertil Steril. 2016;105:1496–502 e1494.PubMedCrossRef
59.
go back to reference Salker M, Teklenburg G, Molokhia M, Lavery S, Trew G, Aojanepong T, et al. Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss. PLoS One. 2010;5:e10287.PubMedPubMedCentralCrossRef Salker M, Teklenburg G, Molokhia M, Lavery S, Trew G, Aojanepong T, et al. Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss. PLoS One. 2010;5:e10287.PubMedPubMedCentralCrossRef
Metadata
Title
A novel “embryo-endometrial” adhesion model can potentially predict “receptive” or “non-receptive” endometrium
Authors
Jemma Evans
Kathryn J. Walker
Maree Bilandzic
Sophie Kinnear
Lois A. Salamonsen
Publication date
01-01-2020
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 1/2020
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-019-01629-0

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