Mechanisms of implantation: strategies for successful pregnancy (original) (raw)
Dey, S.K. et al. Molecular cues to implantation. Endocr. Rev.25, 341–373 (2004). CASPubMed Google Scholar
Wang, H. & Dey, S.K. Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet.7, 185–199 (2006). PubMed Google Scholar
Carson, D.D. et al. Embryo implantation. Dev. Biol.223, 217–237 (2000). CASPubMed Google Scholar
Norwitz, E.R., Schust, D.J. & Fisher, S.J. Implantation and the survival of early pregnancy. N. Engl. J. Med.345, 1400–1408 (2001). CASPubMed Google Scholar
Wilcox, A.J., Baird, D.D. & Weinberg, C.R. Time of implantation of the conceptus and loss of pregnancy. N. Engl. J. Med.340, 1796–1799 (1999). CASPubMed Google Scholar
Nagaoka, S.I., Hassold, T.J. & Hunt, P.A. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet.13, 493–504 (2012). CASPubMedPubMed Central Google Scholar
Psychoyos, A. Endocrine Control of Egg Implantation (American Physiology Society, Washington, D.C., 1973).
Paria, B.C., Huet-Hudson, Y.M. & Dey, S.K. Blastocyst's state of activity determines the “window” of implantation in the receptive mouse uterus. Proc. Natl. Acad. Sci. USA90, 10159–10162 (1993). CASPubMedPubMed Central Google Scholar
Daikoku, T. et al. Conditional deletion of MSX homeobox genes in the uterus inhibits blastocyst implantation by altering uterine receptivity. Dev. Cell21, 1014–1024 (2011). CASPubMedPubMed Central Google Scholar
Nikas, G. & Psychoyos, A. Uterine pinopodes in peri-implantation human endometrium. Clinical relevance. Ann. NY Acad. Sci.816, 129–142 (1997). CASPubMed Google Scholar
Ma, W.G., Song, H., Das, S.K., Paria, B.C. & Dey, S.K. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc. Natl. Acad. Sci. USA100, 2963–2968 (2003). CASPubMedPubMed Central Google Scholar
Giudice, L.C. Potential biochemical markers of uterine receptivity. Hum. Reprod.14 (suppl. 2), 3–16 (1999). CASPubMed Google Scholar
Song, H., Lim, H., Das, S.K., Paria, B.C. & Dey, S.K. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol. Endocrinol.14, 1147–1161 (2000). CASPubMed Google Scholar
Winuthayanon, W., Hewitt, S.C., Orvis, G.D., Behringer, R.R. & Korach, K.S. Uterine epithelial estrogen receptor α is dispensable for proliferation but essential for complete biological and biochemical responses. Proc. Natl. Acad. Sci. USA107, 19272–19277 (2010). CASPubMedPubMed Central Google Scholar
Franco, H.L. et al. Epithelial progesterone receptor exhibits pleiotropic roles in uterine development and function. FASEB J.26, 1218–1227 (2012). CASPubMedPubMed Central Google Scholar
Simon, L. et al. Stromal progesterone receptors mediate induction of Indian Hedgehog (IHH) in uterine epithelium and its downstream targets in uterine stroma. Endocrinology150, 3871–3876 (2009). CASPubMedPubMed Central Google Scholar
Stewart, C.L. et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature359, 76–79 (1992). CASPubMed Google Scholar
Niwa, H., Burdon, T., Chambers, I. & Smith, A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev.12, 2048–2060 (1998). CASPubMedPubMed Central Google Scholar
Laird, S.M. et al. The production of leukaemia inhibitory factor by human endometrium: presence in uterine flushings and production by cells in culture. Hum. Reprod.12, 569–574 (1997). CASPubMed Google Scholar
Piccinni, M.P. et al. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med.4, 1020–1024 (1998). CASPubMed Google Scholar
Hambartsoumian, E. Endometrial leukemia inhibitory factor (LIF) as a possible cause of unexplained infertility and multiple failures of implantation. Am. J. Reprod. Immunol.39, 137–143 (1998). CASPubMed Google Scholar
Brinsden, P.R., 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.91, 1445–1447 (2009). CASPubMed Google Scholar
Hu, W., Feng, Z., Teresky, A.K. & Levine, A.J. p53 regulates maternal reproduction through LIF. Nature450, 721–724 (2007). CASPubMed Google Scholar
Hirota, Y. et al. Uterine-specific p53 deficiency confers premature uterine senescence and promotes preterm birth in mice. J. Clin. Invest.120, 803–815 (2010). CASPubMedPubMed Central Google Scholar
Kang, H.J. et al. Single-nucleotide polymorphisms in the p53 pathway regulate fertility in humans. Proc. Natl. Acad. Sci. USA106, 9761–9766 (2009). CASPubMedPubMed Central Google Scholar
Patounakis, G. et al. The p53 codon 72 single nucleotide polymorphism lacks a significant effect on implantation rate in fresh in vitro fertilization cycles: an analysis of 1,056 patients. Fertil. Steril.92, 1290–1296 (2009). CASPubMed Google Scholar
Tranguch, S. et al. Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc. Natl. Acad. Sci. USA102, 14326–14331 (2005). CASPubMedPubMed Central Google Scholar
Yang, Z. et al. FK506-binding protein 52 is essential to uterine reproductive physiology controlled by the progesterone receptor A isoform. Mol. Endocrinol.20, 2682–2694 (2006). CASPubMed Google Scholar
Tranguch, S. et al. FKBP52 deficiency-conferred uterine progesterone resistance is genetic background and pregnancy stage specific. J. Clin. Invest.117, 1824–1834 (2007). CASPubMedPubMed Central Google Scholar
Hirota, Y. et al. Uterine FK506-binding protein 52 (FKBP52)-peroxiredoxin-6 (PRDX6) signaling protects pregnancy from overt oxidative stress. Proc. Natl. Acad. Sci. USA107, 15577–15582 (2010). CASPubMedPubMed Central Google Scholar
Yang, H. et al. FKBP52 is regulated by HOXA10 during decidualizaton and in endometriosis. Reproduction143, 531–538 (2012). CASPubMed Google Scholar
Xu, J., Wu, R.C. & O'Malley, B.W. Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat. Rev. Cancer9, 615–630 (2009). CASPubMedPubMed Central Google Scholar
Mukherjee, A. et al. Steroid receptor coactivator 2 is critical for progesterone-dependent uterine function and mammary morphogenesis in the mouse. Mol. Cell. Biol.26, 6571–6583 (2006). CASPubMedPubMed Central Google Scholar
Mukherjee, A., Amato, P., Allred, D.C., DeMayo, F.J. & Lydon, J.P. Steroid receptor coactivator 2 is required for female fertility and mammary morphogenesis: insights from the mouse, relevance to the human. Nucl. Recept. Signal.5, e011 (2007). PubMedPubMed Central Google Scholar
Matsumoto, H., Zhao, X., Das, S.K., Hogan, B.L. & Dey, S.K. Indian hedgehog as a progesterone-responsive factor mediating epithelial-mesenchymal interactions in the mouse uterus. Dev. Biol.245, 280–290 (2002). CASPubMed Google Scholar
Lee, K. et al. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat. Genet.38, 1204–1209 (2006). CASPubMed Google Scholar
Wei, Q., Levens, E.D., Stefansson, L. & Nieman, L.K. Indian Hedgehog and its targets in human endometrium: menstrual cycle expression and response to CDB-2914. J. Clin. Endocrinol. Metab.95, 5330–5337 (2010). CASPubMedPubMed Central Google Scholar
Kurihara, I. et al. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet.3, e102 (2007). PubMedPubMed Central Google Scholar
Petit, F.G. et al. Deletion of the orphan nuclear receptor COUP-TFII in uterus leads to placental deficiency. Proc. Natl. Acad. Sci. USA104, 6293–6298 (2007). CASPubMedPubMed Central Google Scholar
Li, Q. et al. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science331, 912–916 (2011). CASPubMedPubMed Central Google Scholar
Huyen, D.V. & Bany, B.M. Evidence for a conserved function of heart and neural crest derivatives expressed transcript 2 in mouse and human decidualization. Reproduction142, 353–368 (2011). CASPubMedPubMed Central Google Scholar
Pavlova, A., Boutin, E., Cunha, G. & Sassoon, D. Msx1 (Hox-7.1) in the adult mouse uterus: cellular interactions underlying regulation of expression. Development120, 335–345 (1994). CASPubMed Google Scholar
Daikoku, T. et al. Uterine Msx-1 and Wnt4 signaling becomes aberrant in mice with the loss of leukemia inhibitory factor or Hoxa-10: evidence for a novel cytokine-homeobox-Wnt signaling in implantation. Mol. Endocrinol.18, 1238–1250 (2004). CASPubMed Google Scholar
Nallasamy, S., Li, Q., Bagchi, M.K. & Bagchi, I.C. Msx homeobox genes critically regulate embryo implantation by controlling paracrine signaling between uterine stroma and epithelium. PLoS Genet.8, e1002500 (2012). CASPubMedPubMed Central Google Scholar
Sun, X. et al. Kruppel-like factor 5 (KLF5) is critical for conferring uterine receptivity to implantation. Proc. Natl. Acad. Sci. USA109, 1145–1150 (2012). CASPubMedPubMed Central Google Scholar
Liu, R., Zhou, Z., Zhao, D. & Chen, C. The induction of KLF5 transcription factor by progesterone contributes to progesterone-induced breast cancer cell proliferation and dedifferentiation. Mol. Endocrinol.25, 1137–1144 (2011). CASPubMedPubMed Central Google Scholar
Ema, M. et al. Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell3, 555–567 (2008). CASPubMed Google Scholar
Lejeune, B., Van Hoeck, J. & Leroy, F. Transmitter role of the luminal uterine epithelium in the induction of decidualization in rats. J. Reprod. Fertil.61, 235–240 (1981). CASPubMed Google Scholar
Das, S.K. et al. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development120, 1071–1083 (1994). CASPubMed Google Scholar
Paria, B.C., Elenius, K., Klagsbrun, M. & Dey, S.K. Heparin-binding EGF-like growth factor interacts with mouse blastocysts independently of ErbB1: a possible role for heparan sulfate proteoglycans and ErbB4 in blastocyst implantation. Development126, 1997–2005 (1999). CASPubMed Google Scholar
Raab, G. et al. Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor. Development122, 637–645 (1996). CASPubMed Google Scholar
Hamatani, T. et al. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc. Natl. Acad. Sci. USA101, 10326–10331 (2004). CASPubMedPubMed Central Google Scholar
Paria, B.C. et al. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc. Natl. Acad. Sci. USA98, 1047–1052 (2001). CASPubMedPubMed Central Google Scholar
Iwamoto, R. et al. Heparin-binding EGF-like growth factor and ErbB signaling is essential for heart function. Proc. Natl. Acad. Sci. USA100, 3221–3226 (2003). CASPubMedPubMed Central Google Scholar
Xie, H. et al. Maternal heparin-binding-EGF deficiency limits pregnancy success in mice. Proc. Natl. Acad. Sci. USA104, 18315–18320 (2007). CASPubMedPubMed Central Google Scholar
Stavreus-Evers, A. et al. Co-existence of heparin-binding epidermal growth factor-like growth factor and pinopodes in human endometrium at the time of implantation. Mol. Hum. Reprod.8, 765–769 (2002). CASPubMed Google Scholar
Yoo, H.J., Barlow, D.H. & Mardon, H.J. Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium: a possible role in blastocyst implantation. Dev. Genet.21, 102–108 (1997). CASPubMed Google Scholar
Chobotova, K. et al. Heparin-binding epidermal growth factor and its receptor ErbB4 mediate implantation of the human blastocyst. Mech. Dev.119, 137–144 (2002). CASPubMed Google Scholar
Genbacev, O.D. et al. Trophoblast L-selectin–mediated adhesion at the maternal-fetal interface. Science299, 405–408 (2003). CASPubMed Google Scholar
Lessey, B.A. Assessment of endometrial receptivity. Fertil. Steril.96, 522–529 (2011). CASPubMed Google Scholar
Prakobphol, A., Genbacev, O., Gormley, M., Kapidzic, M. & Fisher, S.J. A role for the L-selectin adhesion system in mediating cytotrophoblast emigration from the placenta. Dev. Biol.298, 107–117 (2006). CASPubMed Google Scholar
Lim, H. et al. Multiple female reproductive failures in cyclooxygenase 2–deficient mice. Cell91, 197–208 (1997). CASPubMed Google Scholar
Lee, K.Y. et al. Bmp2 is critical for the murine uterine decidual response. Mol. Cell. Biol.27, 5468–5478 (2007). CASPubMedPubMed Central Google Scholar
Benson, G.V. et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development122, 2687–2696 (1996). CASPubMed Google Scholar
Lim, H., Ma, L., Ma, W.G., Maas, R.L. & Dey, S.K. Hoxa-10 regulates uterine stromal cell responsiveness to progesterone during implantation and decidualization in the mouse. Mol. Endocrinol.13, 1005–1017 (1999). CASPubMed Google Scholar
Gendron, R.L. et al. Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol. Reprod.56, 1097–1105 (1997). CASPubMed Google Scholar
Tan, J. et al. Evidence for coordinated interaction of cyclin D3 with p21 and cdk6 in directing the development of uterine stromal cell decidualization and polyploidy during implantation. Mech. Dev.111, 99–113 (2002). CASPubMedPubMed Central Google Scholar
Taylor, H.S., Arici, A., Olive, D. & Igarashi, P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J. Clin. Invest.101, 1379–1384 (1998). CASPubMedPubMed Central Google Scholar
Taylor, H.S., Igarashi, P., Olive, D.L. & Arici, A. Sex steroids mediate HOXA11 expression in the human peri-implantation endometrium. J. Clin. Endocrinol. Metab.84, 1129–1135 (1999). CASPubMed Google Scholar
Popovici, R.M., Kao, L.C. & Giudice, L.C. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology141, 3510–3513 (2000). CASPubMed Google Scholar
Gellersen, B., Brosens, I.A. & Brosens, J.J. Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin. Reprod. Med.25, 445–453 (2007). CASPubMed Google Scholar
Brar, A.K. et al. Laminin decreases PRL and IGFBP-1 expression during in vitro decidualization of human endometrial stromal cells. J. Cell. Physiol.163, 30–37 (1995). CASPubMed Google Scholar
Arias-Stella, J. The Arias-Stella reaction: facts and fancies four decades after. Adv. Anat. Pathol.9, 12–23 (2002). PubMed Google Scholar
Mori, M. et al. Death effector domain-containing protein (DEDD) is required for uterine decidualization during early pregnancy in mice. J. Clin. Invest.121, 318–327 (2011). CASPubMed Google Scholar
Bilinski, P., Roopenian, D. & Gossler, A. Maternal IL-11Rα function is required for normal decidua and fetoplacental development in mice. Genes Dev.12, 2234–2243 (1998). CASPubMedPubMed Central Google Scholar
Robb, L. et al. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat. Med.4, 303–308 (1998). CASPubMed Google Scholar
Mizugishi, K. et al. Maternal disturbance in activated sphingolipid metabolism causes pregnancy loss in mice. J. Clin. Invest.117, 2993–3006 (2007). CASPubMedPubMed Central Google Scholar
Salker, M.S. et al. Deregulation of the serum- and glucocorticoid-inducible kinase SGK1 in the endometrium causes reproductive failure. Nat. Med.17, 1509–1513 (2011). CASPubMed Google Scholar
Kim, J.J. et al. Expression of cyclooxygenase-1 and -2 in the baboon endometrium during the menstrual cycle and pregnancy. Endocrinology140, 2672–2678 (1999). CASPubMed Google Scholar
Critchley, H.O. et al. Role of inflammatory mediators in human endometrium during progesterone withdrawal and early pregnancy. J. Clin. Endocrinol. Metab.84, 240–248 (1999). CASPubMed Google Scholar
Marions, L. & Danielsson, K.G. Expression of cyclo-oxygenase in human endometrium during the implantation period. Mol. Hum. Reprod.5, 961–965 (1999). CASPubMed Google Scholar
Lim, H. et al. Cyclo-oxygenase-2–derived prostacyclin mediates embryo implantation in the mouse via PPARδ. Genes Dev.13, 1561–1574 (1999). CASPubMedPubMed Central Google Scholar
Wang, H. et al. Stage-specific integration of maternal and embryonic peroxisome proliferator-activated receptor δ signaling is critical to pregnancy success. J. Biol. Chem.282, 37770–37782 (2007). CASPubMed Google Scholar
Ruan, Y.C. et al. Activation of the epithelial Na+ channel triggers prostaglandin E2 release and production required for embryo implantation. Nat. Med.18, 1112–1117 (2012). CASPubMed Google Scholar
Hayashi, K. et al. Wnt genes in the mouse uterus: potential regulation of implantation. Biol. Reprod.80, 989–1000 (2009). CASPubMedPubMed Central Google Scholar
Tulac, S. et al. Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium. J. Clin. Endocrinol. Metab.88, 3860–3866 (2003). CASPubMed Google Scholar
Mohamed, O.A. et al. Uterine Wnt/β-catenin signaling is required for implantation. Proc. Natl. Acad. Sci. USA102, 8579–8584 (2005). CASPubMedPubMed Central Google Scholar
Franco, H.L. et al. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J.25, 1176–1187 (2011). CASPubMedPubMed Central Google Scholar
Dunlap, K.A. et al. Postnatal deletion of Wnt7a inhibits uterine gland morphogenesis and compromises adult fertility in mice. Biol. Reprod.85, 386–396 (2011). CASPubMedPubMed Central Google Scholar
Parr, B.A. & McMahon, A.P. Sexually dimorphic development of the mammalian reproductive tract requires Wnt-7a. Nature395, 707–710 (1998). CASPubMed Google Scholar
Jeong, J.W. et al. Foxa2 is essential for mouse endometrial gland development and fertility. Biol. Reprod.83, 396–403 (2010). CASPubMedPubMed Central Google Scholar
Jeong, J.W. et al. β-catenin mediates glandular formation and dysregulation of β-catenin induces hyperplasia formation in the murine uterus. Oncogene28, 31–40 (2009). CASPubMed Google Scholar
Song, H. & Lim, H. Evidence for heterodimeric association of leukemia inhibitory factor (LIF) receptor and gp130 in the mouse uterus for LIF signaling during blastocyst implantation. Reproduction131, 341–349 (2006). CASPubMed Google Scholar
Song, H. et al. Cytosolic phospholipase A2α is crucial [correction of A2α deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development129, 2879–2889 (2002). CASPubMed Google Scholar
Wang, H., Dey, S.K. & Maccarrone, M. Jekyll and Hyde: two faces of cannabinoid signaling in male and female fertility. Endocr. Rev.27, 427–448 (2006). CASPubMed Google Scholar
Sun, X. et al. Endocannabinoid signaling directs differentiation of trophoblast cell lineages and placentation. Proc. Natl. Acad. Sci. USA107, 16887–16892 (2010). CASPubMedPubMed Central Google Scholar
Wang, H. et al. Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat. Med.10, 1074–1080 (2004). CASPubMed Google Scholar
Horne, A.W. et al. CB1 expression is attenuated in Fallopian tube and decidua of women with ectopic pregnancy. PLoS ONE3, e3969 (2008). PubMedPubMed Central Google Scholar
Wang, H. et al. Fatty acid amide hydrolase deficiency limits early pregnancy events. J. Clin. Invest.116, 2122–2131 (2006). CASPubMedPubMed Central Google Scholar
Trabucco, E. et al. Endocannabinoid system in first trimester placenta: low FAAH and high CB1 expression characterize spontaneous miscarriage. Placenta30, 516–522 (2009). CASPubMed Google Scholar
Leach, R.E. et al. Pre-eclampsia and expression of heparin-binding EGF-like growth factor. Lancet360, 1215–1219 (2002). CASPubMed Google Scholar
Stavreus-Evers, A., Koraen, L., Scott, J.E., Zhang, P. & Westlund, P. Distribution of cyclooxygenase-1, cyclooxygenase-2, and cytosolic phospholipase A2 in the luteal phase human endometrium and ovary. Fertil. Steril.83, 156–162 (2005). CASPubMed Google Scholar
Ye, X. et al. LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature435, 104–108 (2005). CASPubMedPubMed Central Google Scholar
Wang, H. et al. Rescue of female infertility from the loss of cyclooxygenase-2 by compensatory up-regulation of cyclooxygenase-1 is a function of genetic makeup. J. Biol. Chem.279, 10649–10658 (2004). CASPubMed Google Scholar
Yotsumoto, S. et al. Expression of adrenomedullin, a hypotensive peptide, in the trophoblast giant cells at the embryo implantation site in mouse. Dev. Biol.203, 264–275 (1998). CASPubMed Google Scholar
Li, M., Yee, D., Magnuson, T.R., Smithies, O. & Caron, K.M. Reduced maternal expression of adrenomedullin disrupts fertility, placentation, and fetal growth in mice. J. Clin. Invest.116, 2653–2662 (2006). CASPubMedPubMed Central Google Scholar
Di Iorio, R., Marinoni, E., Scavo, D., Letizia, C. & Cosmi, E.V. Adrenomedullin in pregnancy. Lancet349, 328 (1997). CASPubMed Google Scholar
Li, M., Wu, Y. & Caron, K.M. Haploinsufficiency for adrenomedullin reduces pinopodes and diminishes uterine receptivity in mice. Biol. Reprod.79, 1169–1175 (2008). CASPubMedPubMed Central Google Scholar
Maltepe, E., Bakardjiev, A.I. & Fisher, S.J. The placenta: transcriptional, epigenetic, and physiological integration during development. J. Clin. Invest.120, 1016–1025 (2010). CASPubMedPubMed Central Google Scholar
Hunkapiller, N.M. et al. A role for Notch signaling in trophoblast endovascular invasion and in the pathogenesis of pre-eclampsia. Development138, 2987–2998 (2011). CASPubMedPubMed Central Google Scholar
Cross, J.C. The genetics of pre-eclampsia: a feto-placental or maternal problem? Clin. Genet.64, 96–103 (2003). CASPubMed Google Scholar
Cui, Y. et al. Role of corin in trophoblast invasion and uterine spiral artery remodelling in pregnancy. Nature484, 246–250 (2012). CASPubMedPubMed Central Google Scholar
Dokras, A. et al. Severe feto-placental abnormalities precede the onset of hypertension and proteinuria in a mouse model of preeclampsia. Biol. Reprod.75, 899–907 (2006). CASPubMed Google Scholar
Lam, C., Lim, K.H. & Karumanchi, S.A. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension46, 1077–1085 (2005). CASPubMed Google Scholar
Ormandy, C.J. et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev.11, 167–178 (1997). CASPubMed Google Scholar
Harrison, D.E. et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature460, 392–395 (2009). CASPubMedPubMed Central Google Scholar
Hirota, Y., Cha, J., Yoshie, M., Daikoku, T. & Dey, S.K. Heightened uterine mammalian target of rapamycin complex 1 (mTORC1) signaling provokes preterm birth in mice. Proc. Natl. Acad. Sci. USA108, 18073–18078 (2011). CASPubMedPubMed Central Google Scholar
Cnattingius, S., Forman, M.R., Berendes, H.W. & Isotalo, L. Delayed childbearing and risk of adverse perinatal outcome. A population-based study. J. Am. Med. Assoc.268, 886–890 (1992). CAS Google Scholar
Krieg, S.A., Henne, M.B. & Westphal, L.M. Obstetric outcomes in donor oocyte pregnancies compared with advanced maternal age in in vitro fertilization pregnancies. Fertil. Steril.90, 65–70 (2008). PubMed Google Scholar
Nelson, S.M. & Lawlor, D.A. Predicting live birth, preterm delivery, and low birth weight in infants born from in vitro fertilisation: a prospective study of 144,018 treatment cycles. PLoS Med.8, e1000386 (2011). PubMedPubMed Central Google Scholar
Demidenko, Z.N., Korotchkina, L.G., Gudkov, A.V. & Blagosklonny, M.V. Paradoxical suppression of cellular senescence by p53. Proc. Natl. Acad. Sci. USA107, 9660–9664 (2010). CASPubMedPubMed Central Google Scholar
Paria, B.C. & Dey, S.K. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc. Natl. Acad. Sci. USA87, 4756–4760 (1990). CASPubMedPubMed Central Google Scholar
Melin, J. et al. In vitro embryo culture in defined, sub-microliter volumes. Dev. Dyn.238, 950–955 (2009). PubMedPubMed Central Google Scholar
Sjöblom, C., Wikland, M. & Robertson, S.A. Granulocyte-macrophage colony–stimulating factor promotes human blastocyst development in vitro. Hum. Reprod.14, 3069–3076 (1999). PubMed Google Scholar
Martin, K.L., Barlow, D.H. & Sargent, I.L. Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum. Reprod.13, 1645–1652 (1998). CASPubMed Google Scholar
Lim, H.J. & Dey, S.K. HB-EGF: a unique mediator of embryo-uterine interactions during implantation. Exp. Cell Res.315, 619–626 (2009). CASPubMed Google Scholar
Diaz-Gimeno, P. et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertility and sterility95 50–60, 60 e51–15 (2011). Google Scholar
Burnum, K.E. et al. Imaging mass spectrometry reveals unique protein profiles during embryo implantation. Endocrinology149, 3274–3278 (2008). CASPubMedPubMed Central Google Scholar
Burnum, K.E. et al. Spatial and temporal alterations of phospholipids determined by mass spectrometry during mouse embryo implantation. J. Lipid Res.50, 2290–2298 (2009). CASPubMedPubMed Central Google Scholar
Simón, C. et al. Increasing uterine receptivity by decreasing estradiol levels during the preimplantation period in high responders with the use of a follicle-stimulating hormone step-down regimen. Fertil. Steril.70, 234–239 (1998). PubMed Google Scholar
Moffett, A. & Loke, C. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol.6, 584–594 (2006). CASPubMed Google Scholar
Munoz-Suano, A., Hamilton, A.B. & Betz, A.G. Gimme shelter: the immune system during pregnancy. Immunol. Rev.241, 20–38 (2011). CASPubMed Google Scholar
Collins, M.K., Tay, C.S. & Erlebacher, A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J. Clin. Invest.119, 2062–2073 (2009). CASPubMedPubMed Central Google Scholar
Samstein, R.M., Josefowicz, S.Z., Arvey, A., Treuting, P.M. & Rudensky, A.Y. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell150, 29–38 (2012). CASPubMedPubMed Central Google Scholar
Nancy, P. et al. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science336, 1317–1321 (2012). CASPubMedPubMed Central Google Scholar
Gluckman, P.D., Hanson, M.A., Cooper, C. & Thornburg, K.L. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med.359, 61–73 (2008). CASPubMedPubMed Central Google Scholar
Ravelli, G.P., Stein, Z.A. & Susser, M.W. Obesity in young men after famine exposure in utero and early infancy. N. Engl. J. Med.295, 349–353 (1976). CASPubMed Google Scholar
Carone, B.R. et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell143, 1084–1096 (2010). CASPubMedPubMed Central Google Scholar
Rosenfeld, C.S. et al. Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc. Natl. Acad. Sci. USA100, 4628–4632 (2003). CASPubMedPubMed Central Google Scholar
Anway, M.D., Cupp, A.S., Uzumcu, M. & Skinner, M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science308, 1466–1469 (2005). CASPubMed Google Scholar
Chakrabarty, A. et al. MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc. Natl. Acad. Sci. USA104, 15144–15149 (2007). CASPubMedPubMed Central Google Scholar
Hu, S.J. et al. MicroRNA expression and regulation in mouse uterus during embryo implantation. J. Biol. Chem.283, 23473–23484 (2008). CASPubMed Google Scholar
Renthal, N.E. et al. miR-200 family and targets, ZEB1 and ZEB2, modulate uterine quiescence and contractility during pregnancy and labor. Proc. Natl. Acad. Sci. USA107, 20828–20833 (2010). CASPubMedPubMed Central Google Scholar
Lynch, V.J., May, G. & Wagner, G.P. Regulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB. Nature480, 383–386 (2011). CASPubMed Google Scholar
Lynch, V.J., Leclerc, R.D., May, G. & Wagner, G.P. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet.43, 1154–1159 (2011). CASPubMed Google Scholar
Lubahn, D.B. et al. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA90, 11162–11166 (1993). CASPubMedPubMed Central Google Scholar
Lydon, J.P. et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev.9, 2266–2278 (1995). CASPubMed Google Scholar
Mulac-Jericevic, B., Mullinax, R.A., DeMayo, F.J., Lydon, J.P. & Conneely, O.M. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science289, 1751–1754 (2000). CASPubMed Google Scholar
Thomas, K., De Hertogh, R., Pizarro, M., Van Exter, C. & Ferin, J. Plasma LH-HCG, 17 -estradiol, estrone and progesterone monitoring around ovulation and subsequent nidation. Int. J. Fertil.18, 65–73 (1973). CASPubMed Google Scholar
Ghosh, D., De, P. & Sengupta, J. Luteal phase ovarian oestrogen is not essential for implantation and maintenance of pregnancy from surrogate embryo transfer in the rhesus monkey. Hum. Reprod.9, 629–637 (1994). CASPubMed Google Scholar
Smitz, J. et al. A prospective randomized study on oestradiol valerate supplementation in addition to intravaginal micronized progesterone in buserelin and HMG induced superovulation. Hum. Reprod.8, 40–45 (1993). CASPubMed Google Scholar
Rao, A.J. et al. Establishment of the need for oestrogen during implantation in non-human primates. Reprod. Biomed. Online14, 563–571 (2007). CASPubMed Google Scholar
McLaren, A. A study of balstocysts during delay and subsequent implantation in lactating mice. J. Endocrinol.42, 453–463 (1968). CASPubMed Google Scholar
Yoshinaga, K. & Adams, C.E. Delayed implantation in the spayed, progesterone treated adult mouse. J. Reprod. Fertil.12, 593–595 (1966). CASPubMed Google Scholar
Lee, J.E. et al. Autophagy regulates embryonic survival during delayed implantation. Endocrinology152, 2067–2075 (2011). CASPubMed Google Scholar
Lopes, F.L., Desmarais, J.A. & Murphy, B.D. Embryonic diapause and its regulation. Reproduction128, 669–678 (2004). CASPubMed Google Scholar
Renfree, M.B. & Shaw, G. Diapause. Annu. Rev. Physiol.62, 353–375 (2000). CASPubMed Google Scholar
Hess, A.P., Nayak, N.R. & Giudice, L.C. Oviduct and endometrium: cyclic changes in the primate oviduct and endometrium. in. Knobil and Neill's Physiology of Reproduction, Vol. 1 (ed. Neill, J.D.) 337–381 (Elsevier Academic Press, 2006).
Schlafke, S. & Enders, A.C. Cellular basis of interaction between trophoblast and uterus at implantation. Biol. Reprod.12, 41–65 (1975). CASPubMed Google Scholar
World Health Organization. Born Too Soon: The Global Action Report on Preterm Birth. (World Health Organization, Geneva, 2012).
Roizen, J.D., Asada, M., Tong, M., Tai, H.H. & Muglia, L.J. Preterm birth without progesterone withdrawal in 15-hydroxyprostaglandin dehydrogenase hypomorphic mice. Mol. Endocrinol.22, 105–112 (2008). CASPubMed Google Scholar
Park, C.B., DeMayo, F.J., Lydon, J.P. & Dufort, D. NODAL in the uterus is necessary for proper placental development and maintenance of pregnancy. Biol. Reprod.86, 194 (2012). PubMedPubMed Central Google Scholar
Hamilton, S. et al. Macrophages infiltrate the human and rat decidua during term and preterm labor: evidence that decidual inflammation precedes labor. Biol. Reprod.86, 39 (2011). Google Scholar
Wang, H. & Hirsch, E. Bacterially-induced preterm labor and regulation of prostaglandin-metabolizing enzyme expression in mice: the role of Toll-like receptor 4. Biol. Reprod.69, 1957–1963 (2003). CASPubMed Google Scholar
Döring, B. et al. Ablation of connexin43 in uterine smooth muscle cells of the mouse causes delayed parturition. J. Cell Sci.119, 1715–1722 (2006). PubMed Google Scholar
Fonseca, E.B., Celik, E., Parra, M., Singh, M. & Nicolaides, K.H. Progesterone and the risk of preterm birth among women with a short cervix. N. Engl. J. Med.357, 462–469 (2007). CASPubMed Google Scholar
Meis, P.J. et al. Prevention of recurrent preterm delivery by 17 α-hydroxyprogesterone caproate. N. Engl. J. Med.348, 2379–2385 (2003). CASPubMed Google Scholar
Groom, K.M., Shennan, A.H., Jones, B.A., Seed, P. & Bennett, P.R. TOCOX–a randomised, double-blind, placebo-controlled trial of rofecoxib (a COX-2-specific prostaglandin inhibitor) for the prevention of preterm delivery in women at high risk. BJOG112, 725–730 (2005). CASPubMed Google Scholar
Kawagoe, J. et al. Nuclear receptor coactivator-6 attenuates uterine estrogen sensitivity to permit embryo implantation. Dev. Cell23, 858–865 (2012). CASPubMedPubMed Central Google Scholar