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  • Print publication year: 2020
  • Online publication date: December 2019

Chapter 6 - Implantation and Early Stages of Fetal Development

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Summary

During the transition from morula to blastocyst the embryo enters the uterus, where it is sustained by oxygen and a rich supply of metabolic substrates in uterine secretions. The subsequent sequence of events that lead to implantation is a crucial milestone in mammalian embryo development. Carefully orchestrated programs are set into action, which establish diverse cell lines, specify cell fate and major remodeling that will generate the embryo and its extraembryonic tissues: during gastrulation, the three primary germ layers that lead to body formation are formed. The critical conditions that are created in this early stage will pave the way to a successful pregnancy.

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Baines, KJ, Renaud, SJ (2017) Transcription factors that regulate trophoblast development and function. In: Huckle, WR (ed.) Progress in Molecular Biology and Translational Science, vol. 145. Academic Press, Burlington, MA pp. 39–88.
Bourgain, C, Devroey, P (2007) Histologic and functional aspects of the endometrium in the implantatory phase. Gynecologic and Obstetric Investigation 64(3): 131–133.
Campbell, S, Swan, HR, Seif, MW, Kimber, SJ, Aplin, JD (1995) Cell adhesion molecules on the oocyte and preimplantation human embryo. Molecular Human Reproduction 1(4): 171–178.
Cheon, YP, Xu, X, Bagchi, MK, Bagchi, IC (2003) IRG1 is a novel target of progesterone receptor and plays a critical role during implantation in the mouse. Endocrinology 144(12): 5623–5630.
Duc-Goiran, P, Mignot, TM, Bourgeois, C, Ferré, F (1999) Embryo-maternal interactions at the implantation site: a delicate equilibrium (Review). European Journal of Obstetrics, Gynecology, and Reproductive Biology 83(1): 85–100.
Grewal, S, Carver, JG, Ridley, AJ, Mardon, HJ (2008) Implantation of the human embryo requires Rac1 dependent endometrial stromal migration. Proceedings of the National Academy of Sciences USA 105: 16189–16194.
Hempstock, J, Cindrova-Davies, T, Jauniaux, E, Burton, G (2004) Endometrial glands as a source of nutrients, growth factors and cytokines during the first trimester of human pregnancy: a morphological and immunohistochemical study. Reproductive Biology and Endocrinology 2: 58. DOI:10.1186/1477-7827-2-58.
Horcajadas, JA, Pellicer, A, Simón, C (2007) Wide genomic analysis of human endometrial receptivity: new times, new opportunities. Human Reproduction Update 13(1): 77–86.
King, A, Burrows, T, Verma, S, Hiby, S, Loke, YW (1998) Human uterine lymphocytes. Human Reproduction Update 4(5): 480–485.
Kliman, HJ (2000) The story of decidualization, menstruation, and trophoblast invasion. American Journal of Pathology 157: 1759–1768.
Lee, CQE, Gardner, L, Turco, M, Zhao, N, et al. (2016) What is trophoblast? A combination of criteria define human first trimester trophoblast. Stem Cell Reports 6: 257–272.
Lee, K, Jeong, J, Kwak, I, et al. (2006) Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nature Genetics 38: 1204–1209.
Mardon, H, Grewal, S (2007) Experimental models for investigating implantation of the human embryo. Seminars in Reproductive Medicine 25: 410–417.
Moffett, A, Shreeve, N (2015) First do no harm: uterine natural killer (NK) cells in assisted reproduction. Human Reproduction 30(7): 1519–1525.
Nikas, G, Drakakis, P, Loutradis, D, et al. (1995) Uterine pinopodes as markers of the ‘nidation window’ in cycling women receiving exogenous oestradiol and progesterone. Human Reproduction 10(5): 1208–1213.
Parr, MB, Parr, EL (1964) Uterine luminal epithelium: protrusions mediate endocytosis, not apocrine secretion, in the rat. Biology of Reproduction 11(2): 220–233.
Psychoyos, A (1986) Uterine receptivity for nidation. Annals of the New York Academy of Sciences 476: 36–42.
Psychoyos, A, Nikas, G, Gravanis, A (1995) The role of prostaglandins in blastocyst implantation. Human Reproduction 10(Suppl. 2): 30–42.
Sherwin, JR, Sharkey, AM, Cameo, P, et al. (2007) Identification of novel genes regulated by hCG in baboon endometrium. Endocrinology 148: 618–626.
Simon, C, Gimeno, MJ, Mercader, A, et al. (1997) Embryonic regulation of integrins in endometrial epithelial cells. Journal of Clinical Endocrinology and Metabolism 82: 2607–2616.
Simon, L, Spiewak, KA, Ekman, GC, et al. (2009) Stromal progesterone receptors mediate induction of IHH in uterine epithelium. Endocrinology 150: 3871–3876.
Turco, M, Gardner, L, Hughes, J, et al. (2017) Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nature Cell Biology 19(5): 568–577.
Wang, H, Dey, SK (2006) Roadmap to embryo implantation. Nature Reviews Genetics 7: 185–199.
Wilcox, AJ, Baird, DD, Dunson, D, McChesney, R, Weinberg, CR (2001) Natural limits of pregnancy testing in relation to the expected menstrual period. Journal of the American Medical Association 286(14): 1759–1761. Erratum in: JAMA 2002; 287(2): 192.
Wilcox, AJ, Baird, DD, Weinberg, CR (1999) Time of implantation of the conceptus and loss of pregnancy. New England Journal of Medicine 340(23): 1796–1799.
Deglincerti, A, Croft, GF, Pietila, LN, Zernicka-Goetz, M, Siggia, ED, Brivanlou, AH (2016) Self-organization of the in vitro attached human embryo. Nature 533: 251–254.
Dorus, S, Anderson, JR, Vallender, EJ, et al. (2006) Sonic Hedgehog, a key development gene, experienced intensified molecular evolution in primates. Human Molecular Genetics 15(13): 2031–2037.
Gilbert, SF (2000) Developmental Biology. Sinauer Associates, Sunderland, MA.
Herzog, W, Zeng, X, Lele, Z, et al. (2003) Adenohypophysis formation in the zebrafish and its dependence on sonic hedgehog. Developmental Biology 254: 1.
O’Rahilly, RF, Müller, F (1987) Developmental Stages in Human Embryos. Carnegie Institution of Washington, Washington, DC.
Shabazi, MN, Jedrusik, A, Vuoristo, S et al. (2016) Self-organization of the human embryo in the absence of maternal tissues. Nature Cell Biology 18(6): 700–708.
Baines, KJ, Renaud, SJ (2017) Transcription factors that regulate trophoblast development and function. In: Huckle, WR (ed.) Progress in Molecular Biology and Translational Science, vol. 145. Academic Press, Burlington, MA pp. 39–88.
Bourgain, C, Devroey, P (2007) Histologic and functional aspects of the endometrium in the implantatory phase. Gynecologic and Obstetric Investigation 64(3): 131–133.
Campbell, S, Swan, HR, Seif, MW, Kimber, SJ, Aplin, JD (1995) Cell adhesion molecules on the oocyte and preimplantation human embryo. Molecular Human Reproduction 1(4): 171–178.
Cheon, YP, Xu, X, Bagchi, MK, Bagchi, IC (2003) IRG1 is a novel target of progesterone receptor and plays a critical role during implantation in the mouse. Endocrinology 144(12): 5623–5630.
Duc-Goiran, P, Mignot, TM, Bourgeois, C, Ferré, F (1999) Embryo-maternal interactions at the implantation site: a delicate equilibrium (Review). European Journal of Obstetrics, Gynecology, and Reproductive Biology 83(1): 85–100.
Grewal, S, Carver, JG, Ridley, AJ, Mardon, HJ (2008) Implantation of the human embryo requires Rac1 dependent endometrial stromal migration. Proceedings of the National Academy of Sciences USA 105: 16189–16194.
Hempstock, J, Cindrova-Davies, T, Jauniaux, E, Burton, G (2004) Endometrial glands as a source of nutrients, growth factors and cytokines during the first trimester of human pregnancy: a morphological and immunohistochemical study. Reproductive Biology and Endocrinology 2: 58. DOI:10.1186/1477-7827-2-58.
Horcajadas, JA, Pellicer, A, Simón, C (2007) Wide genomic analysis of human endometrial receptivity: new times, new opportunities. Human Reproduction Update 13(1): 77–86.
King, A, Burrows, T, Verma, S, Hiby, S, Loke, YW (1998) Human uterine lymphocytes. Human Reproduction Update 4(5): 480–485.
Kliman, HJ (2000) The story of decidualization, menstruation, and trophoblast invasion. American Journal of Pathology 157: 1759–1768.
Lee, CQE, Gardner, L, Turco, M, Zhao, N, et al. (2016) What is trophoblast? A combination of criteria define human first trimester trophoblast. Stem Cell Reports 6: 257–272.
Lee, K, Jeong, J, Kwak, I, et al. (2006) Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nature Genetics 38: 1204–1209.
Mardon, H, Grewal, S (2007) Experimental models for investigating implantation of the human embryo. Seminars in Reproductive Medicine 25: 410–417.
Moffett, A, Shreeve, N (2015) First do no harm: uterine natural killer (NK) cells in assisted reproduction. Human Reproduction 30(7): 1519–1525.
Nikas, G, Drakakis, P, Loutradis, D, et al. (1995) Uterine pinopodes as markers of the ‘nidation window’ in cycling women receiving exogenous oestradiol and progesterone. Human Reproduction 10(5): 1208–1213.
Parr, MB, Parr, EL (1964) Uterine luminal epithelium: protrusions mediate endocytosis, not apocrine secretion, in the rat. Biology of Reproduction 11(2): 220–233.
Psychoyos, A (1986) Uterine receptivity for nidation. Annals of the New York Academy of Sciences 476: 36–42.
Psychoyos, A, Nikas, G, Gravanis, A (1995) The role of prostaglandins in blastocyst implantation. Human Reproduction 10(Suppl. 2): 30–42.
Sherwin, JR, Sharkey, AM, Cameo, P, et al. (2007) Identification of novel genes regulated by hCG in baboon endometrium. Endocrinology 148: 618–626.
Simon, C, Gimeno, MJ, Mercader, A, et al. (1997) Embryonic regulation of integrins in endometrial epithelial cells. Journal of Clinical Endocrinology and Metabolism 82: 2607–2616.
Simon, L, Spiewak, KA, Ekman, GC, et al. (2009) Stromal progesterone receptors mediate induction of IHH in uterine epithelium. Endocrinology 150: 3871–3876.
Turco, M, Gardner, L, Hughes, J, et al. (2017) Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nature Cell Biology 19(5): 568–577.
Wang, H, Dey, SK (2006) Roadmap to embryo implantation. Nature Reviews Genetics 7: 185–199.
Wilcox, AJ, Baird, DD, Dunson, D, McChesney, R, Weinberg, CR (2001) Natural limits of pregnancy testing in relation to the expected menstrual period. Journal of the American Medical Association 286(14): 1759–1761. Erratum in: JAMA 2002; 287(2): 192.
Wilcox, AJ, Baird, DD, Weinberg, CR (1999) Time of implantation of the conceptus and loss of pregnancy. New England Journal of Medicine 340(23): 1796–1799.
Deglincerti, A, Croft, GF, Pietila, LN, Zernicka-Goetz, M, Siggia, ED, Brivanlou, AH (2016) Self-organization of the in vitro attached human embryo. Nature 533: 251–254.
Dorus, S, Anderson, JR, Vallender, EJ, et al. (2006) Sonic Hedgehog, a key development gene, experienced intensified molecular evolution in primates. Human Molecular Genetics 15(13): 2031–2037.
Gilbert, SF (2000) Developmental Biology. Sinauer Associates, Sunderland, MA.
Herzog, W, Zeng, X, Lele, Z, et al. (2003) Adenohypophysis formation in the zebrafish and its dependence on sonic hedgehog. Developmental Biology 254: 1.
O’Rahilly, RF, Müller, F (1987) Developmental Stages in Human Embryos. Carnegie Institution of Washington, Washington, DC.
Shabazi, MN, Jedrusik, A, Vuoristo, S et al. (2016) Self-organization of the human embryo in the absence of maternal tissues. Nature Cell Biology 18(6): 700–708.