Physiologic Events of Embryo Implantation and Decidualization in Human and Non-Human Primates

Maria Ariadna Ochoa-Bernal, Asgerally T Fazleabas, Maria Ariadna Ochoa-Bernal, Asgerally T Fazleabas

Abstract

Reproduction is a fundamental process for the preservation of the human species. This process requires a sequence of orchestrated events that are necessary for a successful pregnancy. Two of the most critical steps in the establishment of human pregnancy are implantation and decidualization, which are required for maternal interactions with the developing embryo. This review primarily highlights the physiological aspects of these two events and the adverse pregnancy outcomes from defective implantation and decidualization. The focus of this review is to provide a general concept of the mechanisms involved during the window of implantation, description of components involved in the process and possible pathologies that could disrupt the embryo implantation and decidualization and specifically as it applies to women and non-human primates.

Keywords: Notch; cytokines; decidualization; embryo; endometrium; gynecological pathologies; implantation; miRNA; primates.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Human implantation is a process that could be divided into apposition, adhesion/attachment and invasion/penetration. During apposition (A), the blastocyst expresses L-selectins. The presence of Mucin-1 (MUC-1) repels the blastocyst and prevents it from attaching outside of the window of uterine receptivity. The L-selectins interact with the L-selectin ligands, which are expressed mainly on the pinopodes during the implantation window. At the beginning of the adhesion phase (B), the blastocyst promotes the cleavage of MUC-1 at the implantation site to ensure successful attachment. Cytokines such as Leukemia inhibitory factor (LIF), play an important role during human implantation by supporting the embryo-endometrial interactions. During the invasion or penetration phase (C), the trophoblast cells from the blastocyst penetrate the endometrial epithelium into the stroma. The extra-villous trophoblast cells start proliferating and differentiate into inner cytotrophoblast and outer syncytiotrophoblast. Once implantation is initiated and the embryo breaches the luminal epithelium, the stromal cells surrounding the embryo transform into decidualized cells (D). Immune cells such as macrophages and uterine natural killer (uNK) cells play an important role during decidualization to promote an environment that is conducive to successful implantation. Some art elements used in this figure were obtained from Servier Medical art (http://smart.servier.com). Servier Medical Art by Servier is licensed under a Creative Commons Attribution 3.0 Unported License.

References

    1. Cha J., Sun X., Dey S.K. Mechanisms of implantation: Strategies for successful pregnancy. Nat. Med. 2012;18:1754–1767. doi: 10.1038/nm.3012.
    1. Achache H., Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum. Reprod. Update. 2006;12:731–746. doi: 10.1093/humupd/dml004.
    1. Mor G., Aldo P., Alvero A.B. The unique immunological and microbial aspects of pregnancy. Nat. Rev. Immunol. 2017;17:469–482. doi: 10.1038/nri.2017.64.
    1. Edwards R.G. Human implantation: The last barrier in assisted reproduction technologies? Reprod. Biomed. Online. 2006;13:887–904. doi: 10.1016/S1472-6483(10)61039-5.
    1. Georgadaki K., Khoury N., Spandidos D.A., Zoumpourlis V. The molecular basis of fertilization (Review) Int. J. Mol. Med. 2016;38:979–986. doi: 10.3892/ijmm.2016.2723.
    1. Gilbert S. Developmental Biology. 6th ed. Sinauer Associates; Sunderland, MA, USA: 2000. [(accessed on 10 January 2020)]. The Developmental Mechanics of Cell Specification Sunderland (MA) Available online: .
    1. Kodaman P.H., Taylor H.S. Hormonal regulation of implantation. Obstet. Gynecol. Clin. North. Am. 2004;31:745–766. doi: 10.1016/j.ogc.2004.08.008.
    1. Mazur E.C., Large M.J., DeMayo F.J. Knobil and Neill’s Physiology of Reproduction. Elsevier; Amsterdam, The Netherlands: 2015. Human Oviduct and Endometrium; pp. 1077–1097.
    1. Ashary N., Tiwari A., Modi D. Embryo Implantation: War in Times of Love. Endocrinology. 2018;159:1188–1198. doi: 10.1210/en.2017-03082.
    1. Coppens M.T., Dhont M.A., De Boever J.G., Serreyn R.F., Vandekerckhove D.A., Roels H.J. The distribution of oestrogen and progesterone receptors in the human endometrial basal and functional layer during the normal menstrual cycle. An immunocytochemical study. Histochemistry. 1993;99:121–126. doi: 10.1007/BF00571872.
    1. Alexandra P., Hess N.R.N., Giudice L.C. Oviduct and Endometrium: Cyclic Changes in the Primate Oviduct and Endometrium. In: Jimmy D., editor. Knobil and Neill’s Physiology of Reproduction. 3rd ed. Elsevier; Amsterdam, The Netherlands: 2006.
    1. Simon C., Martin J.C., Pellicer A. Paracrine regulators of implantation. Baillieres Best Pract Res. Clin. Obstet. Gynaecol. 2000;14:815–826. doi: 10.1053/beog.2000.0121.
    1. Fazleabas A.T., Kim J.J. Development. What makes an embryo stick? Science. 2003;299:355–356. doi: 10.1126/science.1081277.
    1. Lessey B.A., Young S.L. What exactly is endometrial receptivity? Fertil. Steril. 2019;111:611–617. doi: 10.1016/j.fertnstert.2019.02.009.
    1. Nikas G., Makrigiannakis A. Endometrial pinopodes and uterine receptivity. Ann. N. Y. Acad. Sci. 2003;997:120–123. doi: 10.1196/annals.1290.042.
    1. Nikas G., Aghajanova L. Endometrial pinopodes: Some more understanding on human implantation? Reprod. BioMedicine Online. 2002;4:18–23. doi: 10.1016/S1472-6483(12)60111-4.
    1. Stavreus-Evers A., Nikas G., Sahlin L., Eriksson H., Landgren B.M. Formation of pinopodes in human endometrium is associated with the concentrations of progesterone and progesterone receptors. Fertil. Steril. 2001;76:782–791. doi: 10.1016/S0015-0282(01)01993-8.
    1. Nikas G. Endometrial receptivity: Changes in cell-surface morphology. Semin. Reprod. Med. 2000;18:229–235. doi: 10.1055/s-2000-12561.
    1. Psychoyos A. Uterine receptivity for nidation. Ann. N. Y. Acad. Sci. 1986;476:36–42. doi: 10.1111/j.1749-6632.1986.tb20920.x.
    1. Nikas G. Cell-surface morphological events relevant to human implantation. Hum. Reprod. 1999;14:37–44. doi: 10.1093/humrep/14.suppl_2.37.
    1. Nikas G. Pinopodes as markers of endometrial receptivity in clinical practice. Hum. Reprod. 1999;14:99–106. doi: 10.1093/humrep/14.suppl_2.99.
    1. Lessey B.A., Damjanovich L., Coutifaris C., Castelbaum A., Albelda S.M., Buck C.A. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J. Clin. Investig. 1992;90:188–195. doi: 10.1172/JCI115835.
    1. Aghajanova L. Coexpression of pinopodes and leukemia inhibitory factor, as well as its receptor, in human endometrium*1. Fertil. Steril. 2003;79:808–814. doi: 10.1016/S0015-0282(02)04830-6.
    1. Jana S.K., Banerjee P., Thangaraju S., Chakravarty B., Chaudhury K. Alteration in Endometrial Remodeling: A Cause for Implantation Failure in Endometriosis? InTech; Rijeka, Croatia: 2012.
    1. Strug M., Fazleabas A. Encyclopedia of Reproduction. Elsevier; Amsterdam, The Netherlands: 2018. Chorionic Gonadotropin; pp. 388–393.
    1. Makrigiannakis A., Vrekoussis T., Zoumakis E., Kalantaridou S.N., Jeschke U. The Role of HCG in Implantation: A Mini-Review of Molecular and Clinical Evidence. Int. J. Mol. Sci. 2017;18:1305. doi: 10.3390/ijms18061305.
    1. Cameo P., Srisuparp S., Strakova Z., Fazleabas A.T. Chorionic gonadotropin and uterine dialogue in the primate. Reprod. Biol. Endocrinol. 2004;2:50. doi: 10.1186/1477-7827-2-50.
    1. Cole L.A. Biological functions of hCG and hCG-related molecules. Reprod. Biol. Endocrinol. 2010;8:102. doi: 10.1186/1477-7827-8-102.
    1. Srisuparp S., Strakova Z., Fazleabas A.T. The role of chorionic gonadotropin (CG) in blastocyst implantation. Arch. Med. Res. 2001;32:627–634. doi: 10.1016/S0188-4409(01)00330-7.
    1. Afshar Y., Stanculescu A., Miele L., Fazleabas A.T. The role of chorionic gonadotropin and Notch1 in implantation. J. Assist. Reprod. Genet. 2007;24:296–302. doi: 10.1007/s10815-007-9149-2.
    1. Schumacher A., Brachwitz N., Sohr S., Engeland K., Langwisch S., Dolaptchieva M., Alexander T., Taran A., Malfertheiner S.F., Costa S.D., et al. Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J. Immunol. 2009;182:5488–5497. doi: 10.4049/jimmunol.0803177.
    1. Banerjee P., Fazleabas A.T. Endometrial responses to embryonic signals in the primate. Int. J. Dev. Biol. 2010;54:295–302. doi: 10.1387/ijdb.082829pb.
    1. Cameo P., Szmidt M., Strakova Z., Mavrogianis P., Sharpe-Timms K.L., Fazleabas A.T. Decidualization regulates the expression of the endometrial chorionic gonadotropin receptor in the primate. Biol. Reprod. 2006;75:681–689. doi: 10.1095/biolreprod.106.051805.
    1. Strug M.R., Su R., Young J.E., Dodds W.G., Shavell V.I., Diaz-Gimeno P., Ruiz-Alonso M., Simon C., Lessey B.A., Leach R.E., et al. Intrauterine human chorionic gonadotropin infusion in oocyte donors promotes endometrial synchrony and induction of early decidual markers for stromal survival: A randomized clinical trial. Hum. Reprod. 2016;31:1552–1561. doi: 10.1093/humrep/dew080.
    1. Kim J.J., Jaffe R.C., Fazleabas A.T. Blastocyst invasion and the stromal response in primates. Hum. Reprod. 1999;14:45–55. doi: 10.1093/humrep/14.suppl_2.45.
    1. Afshar Y., Miele L., Fazleabas A.T. Notch1 is regulated by chorionic gonadotropin and progesterone in endometrial stromal cells and modulates decidualization in primates. Endocrinology. 2012;153:2884–2896. doi: 10.1210/en.2011-2122.
    1. Theofanakis C., Drakakis P., Besharat A., Loutradis D. Human Chorionic Gonadotropin: The Pregnancy Hormone and More. Int. J. Mol. Sci. 2017;18:1059. doi: 10.3390/ijms18051059.
    1. Sasaki Y., Ladner D.G., Cole L.A. Hyperglycosylated human chorionic gonadotropin and the source of pregnancy failures. Fertil. Steril. 2008;89:1781–1786. doi: 10.1016/j.fertnstert.2007.03.010.
    1. Bashiri A., Halper K.I., Orvieto R. Recurrent Implantation Failure-update overview on etiology, diagnosis, treatment and future directions. Reprod. Biol. Endocrinol. 2018;16:121. doi: 10.1186/s12958-018-0414-2.
    1. Jasper M.J., Tremellen K.P., Robertson S.A. Reduced expression of IL-6 and IL-1alpha mRNAs in secretory phase endometrium of women with recurrent miscarriage. J. Reprod. Immunol. 2007;73:74–84. doi: 10.1016/j.jri.2006.06.003.
    1. Chen J.R., Cheng J.G., Shatzer T., Sewell L., Hernandez L., Stewart C.L. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology. 2000;141:4365–4372. doi: 10.1210/endo.141.12.7855.
    1. Cullinan E.B., Abbondanzo S.J., Anderson P.S., Pollard J.W., Lessey B.A., Stewart C.L. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc. Natl. Acad. Sci. USA. 1996;93:3115–3120. doi: 10.1073/pnas.93.7.3115.
    1. Murakami M., Kamimura D., Hirano T. Pleiotropy and Specificity: Insights from the Interleukin 6 Family of Cytokines. Immunity. 2019;50:812–831. doi: 10.1016/j.immuni.2019.03.027.
    1. Aghajanova L. Leukemia inhibitory factor and human embryo implantation. Ann. NY Acad. Sci. 2004;1034:176–183. doi: 10.1196/annals.1335.020.
    1. Hambartsoumian E. Endometrial leukemia inhibitory factor (LIF) as a possible cause of unexplained infertility and multiple failures of implantation. Am. J. Reprod. Immunol. 1998;39:137–143. doi: 10.1111/j.1600-0897.1998.tb00345.x.
    1. Seli E., Kayisli U.A., Cakmak H., Bukulmez O., Bildirici I., Guzeloglu-Kayisli O., Arici A. Removal of hydrosalpinges increases endometrial leukaemia inhibitory factor (LIF) expression at the time of the implantation window. Hum. Reprod. 2005;20:3012–3017. doi: 10.1093/humrep/dei188.
    1. Prins J.R., Gomez-Lopez N., Robertson S.A. Interleukin-6 in pregnancy and gestational disorders. J. Reprod. Immunol. 2012;95:1–14. doi: 10.1016/j.jri.2012.05.004.
    1. Heinrich P.C., Behrmann I., Haan S., Hermanns H.M., Muller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 2003;374:1–20. doi: 10.1042/bj20030407.
    1. Kameda T., Matsuzaki N., Sawai K., Okada T., Saji F., Matsuda T., Hirano T., Kishimoto T., Tanizawa O. Production of interleukin-6 by normal human trophoblast. Placenta. 1990;11:205–213. doi: 10.1016/S0143-4004(05)80266-8.
    1. Tanaka T., Narazaki M., Kishimoto T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb. Perspect. Biol. 2014;6:a016295. doi: 10.1101/cshperspect.a016295.
    1. Cork B.A., Tuckerman E.M., Li T.C., Laird S.M. Expression of interleukin (IL)-11 receptor by the human endometrium in vivo and effects of IL-11, IL-6 and LIF on the production of MMP and cytokines by human endometrial cells in vitro. Mol. Hum. Reprod. 2002;8:841–848. doi: 10.1093/molehr/8.9.841.
    1. Perrier d’Hauterive S., Charlet-Renard C., Berndt S., Dubois M., Munaut C., Goffin F., Hagelstein M.T., Noel A., Hazout A., Foidart J.M., et al. Human chorionic gonadotropin and growth factors at the embryonic-endometrial interface control leukemia inhibitory factor (LIF) and interleukin 6 (IL-6) secretion by human endometrial epithelium. Hum. Reprod. 2004;19:2633–2643. doi: 10.1093/humrep/deh450.
    1. Vandermolen D.T., Gu Y. Human endometrial interleukin-6 (IL-6): In vivo messenger ribonucleic acid expression, in vitro protein production, and stimulation thereof by IL-1β*†*Supported in part by National Institutes of Health grant GCRCM01 RR00065, Bethesda, Maryland, and the Medical College of Virginia, A.D. Williams Foundation, Richmond, Virginia.†Presented in part at the Society for Gynecologic Investigation, Philadelphia, Pennsylvania, March 20 to 23, 1996. Fertil. Steril. 1996;66:741–747. doi: 10.1016/s0015-0282(16)58628-2.
    1. Tabibzadeh S., Kong Q.F., Babaknia A., May L.T. Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum. Reprod. 1995;10:2793–2799. doi: 10.1093/oxfordjournals.humrep.a135793.
    1. Dower S.K., Kronheim S.R., Hopp T.P., Cantrell M., Deeley M., Gillis S., Henney C.S., Urdal D.L. The cell surface receptors for interleukin-1 alpha and interleukin-1 beta are identical. Nature. 1986;324:266–268. doi: 10.1038/324266a0.
    1. Simon C., Mercader A., Gimeno M.J., Pellicer A. The interleukin-1 system and human implantation. Am. J. Reprod. Immunol. 1997;37:64–72. doi: 10.1111/j.1600-0897.1997.tb00193.x.
    1. Tabibzadeh S., Sun X.Z. Cytokine expression in human endometrium throughout the menstrual cycle. Hum. Reprod. 1992;7:1214–1221. doi: 10.1093/oxfordjournals.humrep.a137829.
    1. Strakova Z., Szmidt M., Srisuparp S., Fazleabas A.T. Inhibition of matrix metalloproteinases prevents the synthesis of insulin-like growth factor binding protein-1 during decidualization in the baboon. Endocrinology. 2003;144:5339–5346. doi: 10.1210/en.2003-0471.
    1. Strakova Z., Mavrogianis P., Meng X., Hastings J.M., Jackson K.S., Cameo P., Brudney A., Knight O., Fazleabas A.T. In vivo infusion of interleukin-1beta and chorionic gonadotropin induces endometrial changes that mimic early pregnancy events in the baboon. Endocrinology. 2005;146:4097–4104. doi: 10.1210/en.2005-0380.
    1. Librach C.L., Feigenbaum S.L., Bass K.E., Cui T.Y., Verastas N., Sadovsky Y., Quigley J.P., French D.L., Fisher S.J. Interleukin-1 beta regulates human cytotrophoblast metalloproteinase activity and invasion in vitro. J. Biol. Chem. 1994;269:17125–17131.
    1. Strakova Z., Srisuparp S., Fazleabas A.T. Interleukin-1beta induces the expression of insulin-like growth factor binding protein-1 during decidualization in the primate. Endocrinology. 2000;141:4664–4670. doi: 10.1210/endo.141.12.7810.
    1. Fazleabas A.T., Bell S.C., Fleming S., Sun J., Lessey B.A. Distribution of integrins and the extracellular matrix proteins in the baboon endometrium during the menstrual cycle and early pregnancy. Biol. Reprod. 1997;56:348–356. doi: 10.1095/biolreprod56.2.348.
    1. Wang J., Armant D.R. Integrin-mediated adhesion and signaling during blastocyst implantation. Cells Tissues Organs. 2002;172:190–201. doi: 10.1159/000066970.
    1. Ruoslahti E., Reed J.C. Anchorage dependence, integrins, and apoptosis. Cell. 1994;77:477–478. doi: 10.1016/0092-8674(94)90209-7.
    1. Lessey B.A. Endometrial integrins and the establishment of uterine receptivity. Hum. Reprod. 1998;13:247–258. doi: 10.1093/humrep/13.suppl_3.247.
    1. Lessey B.A. Adhesion molecules and implantation. J. Reprod. Immunol. 2002;55:101–112. doi: 10.1016/S0165-0378(01)00139-5.
    1. Aplin J.D., Spanswick C., Behzad F., Kimber S.J., Vicovac L. Integrins beta 5, beta 3 and alpha v are apically distributed in endometrial epithelium. Mol. Hum. Reprod. 1996;2:527–534. doi: 10.1093/molehr/2.7.527.
    1. Lessey B.A. Assessment of endometrial receptivity. Fertil. Steril. 2011;96:522–529. doi: 10.1016/j.fertnstert.2011.07.1095.
    1. Shih I.-M., Hsu M.-Y., Oldt R.J., Herlyn M., Gearhart J.D., Kurman R.J. The Role of E-cadherin in the Motility and Invasion of Implantation Site Intermediate Trophoblast. Placenta. 2002;23:706–715. doi: 10.1053/plac.2002.0864.
    1. Alikani M. Epithelial cadherin distribution in abnormal human pre-implantation embryos. Hum. Reprod. 2005;20:3369–3375. doi: 10.1093/humrep/dei242.
    1. Zhou Y., Fisher S.J., Janatpour M., Genbacev O., Dejana E., Wheelock M., Damsky C.H. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Investig. 1997:2139–2151. doi: 10.1172/JCI119387.
    1. Ley K. The role of selectins in inflammation and disease. Trends Mol. Med. 2003;9:263–268. doi: 10.1016/S1471-4914(03)00071-6.
    1. Feng Y., Ma X., Deng L., Yao B., Xiong Y., Wu Y., Wang L., Ma Q., Ma F. Role of selectins and their ligands in human implantation stage. Glycobiology. 2017;27:385–391. doi: 10.1093/glycob/cwx009.
    1. Genbacev O.D., Prakobphol A., Foulk R.A., Krtolica A.R., Ilic D., Singer M.S., Yang Z.Q., Kiessling L.L., Rosen S.D., Fisher S.J. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science. 2003;299:405–408. doi: 10.1126/science.1079546.
    1. Lai T.H., Shih Ie M., Vlahos N., Ho C.L., Wallach E., Zhao Y. Differential expression of L-selectin ligand in the endometrium during the menstrual cycle. Fertil. Steril. 2005;83:1297–1302. doi: 10.1016/j.fertnstert.2004.11.040.
    1. Brayman M., Thathiah A., Carson D.D. MUC1: A multifunctional cell surface component of reproductive tissue epithelia. Reprod. Biol. Endocrinol. 2004;2:4. doi: 10.1186/1477-7827-2-4.
    1. Hey N.A., Graham R.A., Seif M.W., Aplin J.D. The polymorphic epithelial mucin MUC1 in human endometrium is regulated with maximal expression in the implantation phase. J. Clin. Endocrinol. Metab. 1994;78:337–342. doi: 10.1210/jcem.78.2.8106621.
    1. Meseguer M., Aplin J.D., Caballero-Campo P., O’Connor J.E., Martin J.C., Remohi J., Pellicer A., Simon C. Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biol. Reprod. 2001;64:590–601. doi: 10.1095/biolreprod64.2.590.
    1. Hild-Petito S., Fazleabas A.T., Julian J., Carson D.D. Mucin (Muc-1) expression is differentially regulated in uterine luminal and glandular epithelia of the baboon (Papio anubis) Biol Reprod. 1996;54:939–947. doi: 10.1095/biolreprod54.5.939.
    1. Kimber S.J., Spanswick C. Blastocyst implantation: The adhesion cascade. Semin. Cell Dev. Biol. 2000;11:77–92. doi: 10.1006/scdb.2000.0154.
    1. Norwitz E.R., Schust D.J., Fisher S.J. Implantation and the survival of early pregnancy. N. Engl. J. Med. 2001;345:1400–1408. doi: 10.1056/NEJMra000763.
    1. Su R.W., Fazleabas A.T. Implantation and Establishment of Pregnancy in Human and Nonhuman Primates. Adv. Anat Embryol. Cell Biol. 2015;216:189–213. doi: 10.1007/978-3-319-15856-3_10.
    1. Gnainsky Y., Granot I., Aldo P., Barash A., Or Y., Mor G., Dekel N. Biopsy-induced inflammatory conditions improve endometrial receptivity: The mechanism of action. Reproduction. 2015;149:75–85. doi: 10.1530/REP-14-0395.
    1. Nejatbakhsh R., Kabir-Salmani M., Dimitriadis E., Hosseini A., Taheripanah R., Sadeghi Y., Akimoto Y., Iwashita M. Subcellular localization of L-selectin ligand in the endometrium implies a novel function for pinopodes in endometrial receptivity. Reprod. Biol. Endocrinol. 2012;10:46. doi: 10.1186/1477-7827-10-46.
    1. Kimber S.J. Leukaemia inhibitory factor in implantation and uterine biology. Reproduction. 2005;130:131–145. doi: 10.1530/rep.1.00304.
    1. Nachtigall M.J., Kliman H.J., Feinberg R.F., Olive D.L., Engin O., Arici A. The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: A potential role in human implantation. J. Clin. Endocrinol. Metab. 1996;81:801–806. doi: 10.1210/jcem.81.2.8636307.
    1. 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;20:319–328. doi: 10.1016/j.cytogfr.2009.07.001.
    1. Singh H., Aplin J.D. Adhesion molecules in endometrial epithelium: Tissue integrity and embryo implantation. J. Anat. 2009;215:3–13. doi: 10.1111/j.1469-7580.2008.01034.x.
    1. Reddy K.V.R., Mangale S.S. Integrin receptors: The dynamic modulators of endometrial function. Tissue Cell. 2003;35:260–273. doi: 10.1016/S0040-8166(03)00039-9.
    1. Lessey B.A., Castelbaum A.J., Sawin S.W., Sun J. Integrins as markers of uterine receptivity in women with primary unexplained infertility**Supported by the National Institutes of Health grants HD-29449 and HD-30476–1 (B.A.L.), Bethesa, Maryland.††Presented at the 40th Annual Meeting of the Society of Gynecologic Investigation, Toronto, Ontario, Canada, 1993. Fertil. Steril. 1995;63:535–542. doi: 10.1016/s0015-0282(16)57422-6.
    1. Carson D.D., Bagchi I., Dey S.K., Enders A.C., Fazleabas A.T., Lessey B.A., Yoshinaga K. Embryo implantation. Dev. Biol. 2000;223:217–237. doi: 10.1006/dbio.2000.9767.
    1. Giudice L.C. Potential biochemical markers of uterine receptivity. Hum. Reprod. 1999;14:3–16. doi: 10.1093/humrep/14.suppl_2.3.
    1. Bischof P., Campana A. A model for implantation of the human blastocyst and early placentation. Hum. Reprod. Update. 1996;2:262–270. doi: 10.1093/humupd/2.3.262.
    1. Fitzgerald J.S., Poehlmann T.G., Schleussner E., Markert U.R. Trophoblast invasion: The role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3) Hum. Reprod. Update. 2008;14:335–344. doi: 10.1093/humupd/dmn010.
    1. Gellersen B., Brosens J.J. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr. Rev. 2014;35:851–905. doi: 10.1210/er.2014-1045.
    1. Okada H., Tsuzuki T., Murata H. Decidualization of the human endometrium. Reprod. Med. Biol. 2018;17:220–227. doi: 10.1002/rmb2.12088.
    1. Coulam C. What about superfertility, decidualization, and natural selection? J. Assist. Reprod. Genet. 2016;33:577–580. doi: 10.1007/s10815-016-0658-8.
    1. Dimitriadis E., Nie G., Hannan N.J., Paiva P., Salamonsen L.A. Local regulation of implantation at the human fetal-maternal interface. Int. J. Dev. Biol. 2010;54:313–322. doi: 10.1387/ijdb.082772ed.
    1. Zhang S., Lin H., Kong S., Wang S., Wang H., Wang H., Armant D.R. Physiological and molecular determinants of embryo implantation. Mol. Aspects Med. 2013;34:939–980. doi: 10.1016/j.mam.2012.12.011.
    1. Dunn C.L., Kelly R.W., Critchley H.O. Decidualization of the human endometrial stromal cell: An enigmatic transformation. Reprod. Biomed. Online. 2003;7:151–161. doi: 10.1016/S1472-6483(10)61745-2.
    1. Smith S.D., Dunk C.E., Aplin J.D., Harris L.K., Jones R.L. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am. J. Pathol. 2009;174:1959–1971. doi: 10.2353/ajpath.2009.080995.
    1. Croy B.A., Chen Z., Hofmann A.P., Lord E.M., Sedlacek A.L., Gerber S.A. Imaging of vascular development in early mouse decidua and its association with leukocytes and trophoblasts. Biol. Reprod. 2012;87:125. doi: 10.1095/biolreprod.112.102830.
    1. Dosiou C., Giudice L.C. Natural killer cells in pregnancy and recurrent pregnancy loss: Endocrine and immunologic perspectives. Endocr. Rev. 2005;26:44–62. doi: 10.1210/er.2003-0021.
    1. Robson A., Harris L.K., Innes B.A., Lash G.E., Aljunaidy M.M., Aplin J.D., Baker P.N., Robson S.C., Bulmer J.N. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J. 2012;26:4876–4885. doi: 10.1096/fj.12-210310.
    1. Smarason A.K., Gunnarsson A., Alfredsson J.H., Valdimarsson H. Monocytosis and monocytic infiltration of decidua in early pregnancy. J. Clin. Lab. Immunol. 1986;21:1–5.
    1. Johnson G.A., Burghardt R.C., Joyce M.M., Spencer T.E., Bazer F.W., Pfarrer C., Gray C.A. Osteopontin expression in uterine stroma indicates a decidualization-like differentiation during ovine pregnancy. Biol. Reprod. 2003;68:1951–1958. doi: 10.1095/biolreprod.102.012948.
    1. Plaisier M. Decidualisation and angiogenesis. Best Pract. Res. Clin. Obstet. Gynaecol. 2011;25:259–271. doi: 10.1016/j.bpobgyn.2010.10.011.
    1. Plaisier M., Koolwijk P., Willems F., Helmerhorst F.M., van Hinsbergh V.W. Pericellular-acting proteases in human first trimester decidua. Mol. Hum. Reprod. 2008;14:41–51. doi: 10.1093/molehr/gam085.
    1. Henderson T.A., Saunders P.T., Moffett-King A., Groome N.P., Critchley H.O. Steroid receptor expression in uterine natural killer cells. J. Clin. Endocrinol. Metab. 2003;88:440–449. doi: 10.1210/jc.2002-021174.
    1. Naruse K., Lash G.E., Bulmer J.N., Innes B.A., Otun H.A., Searle R.F., Robson S.C. The urokinase plasminogen activator (uPA) system in uterine natural killer cells in the placental bed during early pregnancy. Placenta. 2009;30:398–404. doi: 10.1016/j.placenta.2009.02.002.
    1. Whitley G.S., Cartwright J.E. Cellular and molecular regulation of spiral artery remodelling: Lessons from the cardiovascular field. Placenta. 2010;31:465–474. doi: 10.1016/j.placenta.2010.03.002.
    1. Pijnenborg R., Bland J.M., Robertson W.B., Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta. 1983;4:397–413. doi: 10.1016/S0143-4004(83)80043-5.
    1. Hori K., Sen A., Artavanis-Tsakonas S. Notch signaling at a glance. J. Cell Sci. 2013;126:2135–2140. doi: 10.1242/jcs.127308.
    1. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling: Cell fate control and signal integration in development. Science. 1999;284:770–776. doi: 10.1126/science.284.5415.770.
    1. Kopan R. Notch signaling. Cold Spring Harb. Perspect Biol. 2012;4 doi: 10.1101/cshperspect.a011213.
    1. Strug M.R., Su R.W., Kim T.H., Jeong J.W., Fazleabas A. The Notch Family Transcription Factor, RBPJkappa, Modulates Glucose Transporter and Ovarian Steroid Hormone Receptor Expression During Decidualization. Reprod. Sci. 2019;26:774–784. doi: 10.1177/1933719118799209.
    1. Su R.W., Strug M.R., Joshi N.R., Jeong J.W., Miele L., Lessey B.A., Young S.L., Fazleabas A.T. Decreased Notch pathway signaling in the endometrium of women with endometriosis impairs decidualization. J. Clin. Endocrinol. Metab. 2015;100:E433–E442. doi: 10.1210/jc.2014-3720.
    1. Mikhailik A., Mazella J., Liang S., Tseng L. Notch ligand-dependent gene expression in human endometrial stromal cells. Biochem. Biophys. Res. Commun. 2009;388:479–482. doi: 10.1016/j.bbrc.2009.07.037.
    1. Ghatak S., Sen C.K. MicroRNA Biogenesis in Regenerative Medicine. Sci. Direct. 2015:3–46. doi: 10.1016/b978-0-12-405544-5.00001-0.
    1. Bartel D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297. doi: 10.1016/S0092-8674(04)00045-5.
    1. Winter J., Jung S., Keller S., Gregory R.I., Diederichs S. Many roads to maturity: Microrna biogenesis pathways and their regulation. Nat. Cell Biol. 2009;11 doi: 10.1038/ncb0309-228.
    1. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–854. doi: 10.1016/0092-8674(93)90529-Y.
    1. Mari-Alexandre J., Sanchez-Izquierdo D., Gilabert-Estelles J., Barcelo-Molina M., Braza-Boils A., Sandoval J. miRNAs Regulation and Its Role as Biomarkers in Endometriosis. Int. J. Mol. Sci. 2016;17:93. doi: 10.3390/ijms17010093.
    1. Mohr A.M., Mott J.L. Overview of microRNA biology. Semin. Liver Dis. 2015;35:3–11. doi: 10.1055/s-0034-1397344.
    1. Cannell I.G., Kong Y.W., Bushell M. How do microRNAs regulate gene expression? Biochem. Soc. Trans. 2008;36:1224–1231. doi: 10.1042/BST0361224.
    1. Tesfaye D., Salilew-Wondim D., Gebremedhn S., Sohel M.M., Pandey H.O., Hoelker M., Schellander K. Potential role of microRNAs in mammalian female fertility. Reprod. Fertil. Dev. 2016;29:8–23. doi: 10.1071/RD16266.
    1. Revel A., Achache H., Stevens J., Smith Y., Reich R. MicroRNAs are associated with human embryo implantation defects. Hum. Reprod. 2011;26:2830–2840. doi: 10.1093/humrep/der255.
    1. Teague E.M., Print C.G., Hull M.L. The role of microRNAs in endometriosis and associated reproductive conditions. Hum. Reprod. Update. 2010;16:142–165. doi: 10.1093/humupd/dmp034.
    1. Joshi N.R., Su R.W., Chandramouli G.V., Khoo S.K., Jeong J.W., Young S.L., Lessey B.A., Fazleabas A.T. Altered expression of microRNA-451 in eutopic endometrium of baboons (Papio anubis) with endometriosis. Hum. Reprod. 2015;30:2881–2891. doi: 10.1093/humrep/dev229.
    1. Joshi N.R., Miyadahira E.H., Afshar Y., Jeong J.W., Young S.L., Lessey B.A., Serafini P.C., Fazleabas A.T. Progesterone Resistance in Endometriosis Is Modulated by the Altered Expression of MicroRNA-29c and FKBP4. J. Clin. Endocrinol. Metab. 2017;102:141–149. doi: 10.1210/jc.2016-2076.
    1. Yang Z., Wang L. Regulation of microRNA expression and function by nuclear receptor signaling. Cell Biosci. 2011;1:31. doi: 10.1186/2045-3701-1-31.
    1. Bidarimath M., Khalaj K., Wessels J.M., Tayade C. MicroRNAs, immune cells and pregnancy. Cell Mol. Immunol. 2014;11:538–547. doi: 10.1038/cmi.2014.45.
    1. Oskowitz A.Z., Lu J., Penfornis P., Ylostalo J., McBride J., Flemington E.K., Prockop D.J., Pochampally R. Human multipotent stromal cells from bone marrow and microRNA: Regulation of differentiation and leukemia inhibitory factor expression. Proc. Natl. Acad. Sci. USA. 2008;105:18372–18377. doi: 10.1073/pnas.0809807105.
    1. Kang Y.J., Lees M., Matthews L.C., Kimber S.J., Forbes K., Aplin J.D. MiR-145 suppresses embryo-epithelial juxtacrine communication at implantation by modulating maternal IGF1R. J. Cell Sci. 2015;128:804–814. doi: 10.1242/jcs.164004.
    1. Zhang Q., Zhang H., Jiang Y., Xue B., Diao Z., Ding L., Zhen X., Sun H., Yan G., Hu Y. MicroRNA-181a is involved in the regulation of human endometrial stromal cell decidualization by inhibiting Kruppel-like factor 12. Reprod. Biol. Endocrinol. 2015;13:23. doi: 10.1186/s12958-015-0019-y.
    1. Luo S.S., Ishibashi O., Ishikawa G., Ishikawa T., Katayama A., Mishima T., Takizawa T., Shigihara T., Goto T., Izumi A., et al. Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol. Reprod. 2009;81:717–729. doi: 10.1095/biolreprod.108.075481.
    1. Dreisler E., Stampe Sorensen S., Ibsen P.H., Lose G. Prevalence of endometrial polyps and abnormal uterine bleeding in a Danish population aged 20-74 years. Ultrasound Obstet. Gynecol. 2009;33:102–108. doi: 10.1002/uog.6259.
    1. Lieng M., Istre O., Sandvik L., Qvigstad E. Prevalence, 1-year regression rate, and clinical significance of asymptomatic endometrial polyps: Cross-sectional study. J. Minim. Invasive Gynecol. 2009;16:465–471. doi: 10.1016/j.jmig.2009.04.005.
    1. Perez-Medina T., Bajo-Arenas J., Salazar F., Redondo T., Sanfrutos L., Alvarez P., Engels V. Endometrial polyps and their implication in the pregnancy rates of patients undergoing intrauterine insemination: A prospective, randomized study. Hum. Reprod. 2005;20:1632–1635. doi: 10.1093/humrep/deh822.
    1. Baird D.D., Dunson D.B., Hill M.C., Cousins D., Schectman J.M. High cumulative incidence of uterine leiomyoma in black and white women: Ultrasound evidence. Am. J. Obstet. Gynecol. 2003;188:100–107. doi: 10.1067/mob.2003.99.
    1. Griffiths A., D’Angelo A., Amso N. Surgical treatment of fibroids for subfertility. Cochrane Database Syst Rev. 2006 doi: 10.1002/14651858.CD003857.
    1. Matsuzaki S., Canis M., Darcha C., Pouly J.L., Mage G. HOXA-10 expression in the mid-secretory endometrium of infertile patients with either endometriosis, uterine fibromas or unexplained infertility. Hum. Reprod. 2009;24:3180–3187. doi: 10.1093/humrep/dep306.
    1. Dubuisson J.B., Chapron C., Chavet X., Gregorakis S.S. Fertility after laparoscopic myomectomy of large intramural myomas: Preliminary results. Hum. Reprod. 1996;11:518–522. doi: 10.1093/HUMREP/11.3.518.
    1. Zondervan K.T., Becker C.M., Koga K., Missmer S.A., Taylor R.N., Vigano P. Endometriosis. Nat. Rev. Dis. Primers. 2018;4:9. doi: 10.1038/s41572-018-0008-5.
    1. Giudice L.C., Kao L.C. Endometriosis. The Lancet. 2004;364:1789–1799. doi: 10.1016/S0140-6736(04)17403-5.
    1. Bulun S.E. Endometriosis. N. Engl. J. Med. 2009;360:268–279. doi: 10.1056/NEJMra0804690.
    1. Matsuzaki S., Darcha C., Maleysson E., Canis M., Mage G. Impaired down-regulation of E-cadherin and beta-catenin protein expression in endometrial epithelial cells in the mid-secretory endometrium of infertile patients with endometriosis. J. Clin. Endocrinol. Metab. 2010;95:3437–3445. doi: 10.1210/jc.2009-2713.
    1. Barnhart K., Dunsmoor-Su R., Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil. Steril. 2002;77:1148–1155. doi: 10.1016/S0015-0282(02)03112-6.
    1. Burney R.O., Talbi S., Hamilton A.E., Vo K.C., Nyegaard M., Nezhat C.R., Lessey B.A., Giudice L.C. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007;148:3814–3826. doi: 10.1210/en.2006-1692.
    1. Bulletti C., Coccia M.E., Battistoni S., Borini A. Endometriosis and infertility. J. Assist. Reprod. Genet. 2010;27:441–447. doi: 10.1007/s10815-010-9436-1.
    1. Macer M.L., Taylor H.S. Endometriosis and infertility: A review of the pathogenesis and treatment of endometriosis-associated infertility. Obstet. Gynecol. Clin. North. Am. 2012;39:535–549. doi: 10.1016/j.ogc.2012.10.002.
    1. Patel B.G., Rudnicki M., Yu J., Shu Y., Taylor R.N. Progesterone resistance in endometriosis: Origins, consequences and interventions. Acta Obstet. Gynecol. Scand. 2017;96:623–632. doi: 10.1111/aogs.13156.
    1. Kim T.H., Yoo J.Y., Wang Z., Lydon J.P., Khatri S., Hawkins S.M., Leach R.E., Fazleabas A.T., Young S.L., Lessey B.A., et al. ARID1A Is Essential for Endometrial Function during Early Pregnancy. Plos Genet. 2015;11:e1005537. doi: 10.1371/journal.pgen.1005537.
    1. Kim T.H., Yoo J.Y., Choi K.C., Shin J.H., Leach R.E., Fazleabas A.T., Young S.L., Lessey B.A., Yoon H.G., Jeong J.W. Loss of HDAC3 results in nonreceptive endometrium and female infertility. Sci. Transl. Med. 2019;11 doi: 10.1126/scitranslmed.aaf7533.
    1. Marquardt R.M., Kim T.H., Shin J.H., Jeong J.W. Progesterone and Estrogen Signaling in the Endometrium: What Goes Wrong in Endometriosis? Int. J. Mol. Sci. 2019;20:3822. doi: 10.3390/ijms20153822.
    1. Joshi N., Su R.-W., Fazleabas A. Gene Expression in Endometriosis. In: Kwak-Kim J., editor. Endometrial Gene Expression: An Emerging Paradigm for Reproductive Disorders. Springer International Publishing; Cham, Switzerland: 2020. pp. 159–180.
    1. Hawkins S.M., Creighton C.J., Han D.Y., Zariff A., Anderson M.L., Gunaratne P.H., Matzuk M.M. Functional microRNA involved in endometriosis. Mol. Endocrinol. 2011;25:821–832. doi: 10.1210/me.2010-0371.
    1. Vailhe B., Dietl J., Kapp M., Toth B., Arck P. Increased blood vessel density in decidua parietalis is associated with spontaneous human first trimester abortion. Hum. Reprod. 1999;1999:1628–1634. doi: 10.1093/humrep/14.6.1628.
    1. Mekinian A., Cohen J., Alijotas-Reig J., Carbillon L., Nicaise-Roland P., Kayem G., Darai E., Fain O., Bornes M. Unexplained Recurrent Miscarriage and Recurrent Implantation Failure: Is There a Place for Immunomodulation? Am. J. Reprod. Immunol. 2016;76:8–28. doi: 10.1111/aji.12493.
    1. ESHRE . Recurrent Pregnancy Loss. A guideline of the European Society of Human Reproduction and Embryology. ESHRE; Brussels, Belgium: 2017.
    1. Simon A., Laufer N. Assessment and treatment of repeated implantation failure (RIF) J. Assist. Reprod. Genet. 2012;29:1227–1239. doi: 10.1007/s10815-012-9861-4.
    1. Ticconi C., Pietropolli A., Di Simone N., Piccione E., Fazleabas A. Endometrial Immune Dysfunction in Recurrent Pregnancy Loss. Int. J. Mol. Sci. 2019;20:5332. doi: 10.3390/ijms20215332.
    1. Plaisier M., Dennert I., Rost E., Koolwijk P., van Hinsbergh V.W., Helmerhorst F.M. Decidual vascularization and the expression of angiogenic growth factors and proteases in first trimester spontaneous abortions. Hum. Reprod. 2009;24:185–197. doi: 10.1093/humrep/den296.
    1. Quenby S., Nik H., Innes B., Lash G., Turner M., Drury J., Bulmer J. Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum. Reprod. 2009;24:45–54. doi: 10.1093/humrep/den348.
    1. Calleja-Agius J., Jauniaux E., Pizzey A.R., Muttukrishna S. Investigation of systemic inflammatory response in first trimester pregnancy failure. Hum. Reprod. 2012;27:349–357. doi: 10.1093/humrep/der402.
    1. Fox R., Kitt J., Leeson P., Aye C.Y.L., Lewandowski A.J. Preeclampsia: Risk Factors, Diagnosis, Management, and the Cardiovascular Impact on the Offspring. J. Clin. Med. 2019;8:1625. doi: 10.3390/jcm8101625.
    1. Rana S., Lemoine E., Granger J., Karumanchi S.A. Preeclampsia. Circ. Res. 2019;124:1094–1112. doi: 10.1161/CIRCRESAHA.118.313276.
    1. Dokras A., Hoffmann D.S., Eastvold J.S., Kienzle M.F., Gruman L.M., Kirby P.A., Weiss R.M., Davisson R.L. Severe feto-placental abnormalities precede the onset of hypertension and proteinuria in a mouse model of preeclampsia. Biol. Reprod. 2006;75:899–907. doi: 10.1095/biolreprod.106.053603.
    1. Lam C., Lim K.H., Karumanchi S.A. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension. 2005;46:1077–1085. doi: 10.1161/01.HYP.0000187899.34379.b0.
    1. Rabaglino M.B., Conrad K.P. Evidence for shared molecular pathways of dysregulated decidualization in preeclampsia and endometrial disorders revealed by microarray data integration. Faseb J. 2019;33:11682–11695. doi: 10.1096/fj.201900662R.
    1. Fukui A., Kamoi M., Funamizu A., Fuchinoue K., Chiba H., Yokota M., Fukuhara R., Mizunuma H. NK cell abnormality and its treatment in women with reproductive failures such as recurrent pregnancy loss, implantation failures, preeclampsia, and pelvic endometriosis. Reprod. Med. Biol. 2015;14:151–157. doi: 10.1007/s12522-015-0207-7.
    1. Fu B., Li X., Sun R., Tong X., Ling B., Tian Z., Wei H. Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proc. Natl. Acad. Sci. USA. 2013;110:E231–E240. doi: 10.1073/pnas.1206322110.
    1. Turco M.Y., Gardner L., Hughes J., Cindrova-Davies T., Gomez M.J., Farrell L., Hollinshead M., Marsh S.G.E., Brosens J.J., Critchley H.O., et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat. Cell Biol. 2017;19:568–577. doi: 10.1038/ncb3516.

Source: PubMed

3
購読する