How to Cite
Abstract
Blastocyst implantation requires the best communication between the mother’s uterus and a competent embryo. Even before the embryo enter the uterus, the endometrial tissue undergoes the process of decidualization to support the anchoring of the blastocyst and provides the blastocyst with nutrition until the fully functional placenta is formed. In this review, I summarize all the molecular and morphological events necessary for the decidualization in mice and human.
References
Lundkvist O, Nilsson BO. Endometrial ultrastructure in the early uterine response to blastocysts and artificial deciduogenic stimuli in rats. Cell Tissue Res 1982; 225: 355-364.
Huet YM, Andrews GK, Dey SK. Modulation of c-myc protein in the mouse uterus during pregnancy and by steroid hormones. Prog Clin Biol Res 1989; 294: 401-412.
Alexander CM, Hansell EJ, Behrendtsen O, Flannery ML, Kishnani NS, Hawkes SP, Werb Z. Expression and function of matrix metalloproteinases and their inhibitors at the maternal-embryonic boundary during mouse embryo implantation. Development 1996; 122: 1723-1736.
Tung HN, Parr MB, Parr EL. The permeability of the primary decidual zone in the rat uterus: an ultrastructural tracer and freeze-fracture study. Biol Reprod 1986; 35: 1045-1058.
Parr MB, Parr EL. Permeability of the primary decidual zone in the rat uterus: studies using fluorescein-labeled proteins and dextrans. Biol Reprod 1986; 34: 393-403.
SK D. Implantation. In: Adashi EY, Rock JA, Rosenwaks Z, eds. Reproductive endocrinology, surgery and technology. New York. Lippincott-Raven; 421–434 1996.
Herington JL, Bany BM. Do molecular signals from the conceptus influence endometrium decidualization in rodents? J Exp Zool B Mol Dev Evol 2009; 312: 797-816.
Herington JL, Underwood T, McConaha M, Bany BM. Paracrine signals from the mouse conceptus are not required for the normal progression of decidualization. Endocrinology 2009; 150: 4404-4413.
PsychoyosA. Endocrine control of egg implantation. In: Greep RO, Astwood EG, Geiger SR, eds. Handbook of physiology. Washington, DC: . American Physiology Society; 187–215 1973.
Paria BC, Huet-Hudson YM, Dey SK. Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci U S A 1993; 90: 10159-10162.
Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol 2003; 178: 357-372.
Lejeune B, Van Hoeck J, Leroy F. Transmitter role of the luminal uterine epithelium in the induction of decidualization in rats. J Reprod Fertil 1981; 61: 235-240.
Wynn RM. Ultrastructural development of the human decidua. Am J Obstet Gynecol 1974; 118: 652-670.
Yee GM, Kennedy TG. Prostaglandin E2, cAMP and cAMP-dependent protein kinase isozymes during decidualization of rat endometrial stromal cells in vitro. Prostaglandins 1993; 46: 117-138.
DiMattia GE, Gellersen B, Duckworth ML, Friesen HG. Human prolactin gene expression. The use of an alternative noncoding exon in decidua and the IM-9-P3 lymphoblast cell line. J Biol Chem 1990; 265: 16412-16421.
Handwerger S, Richards RG, Markoff E. The physiology of decidual prolactin and other decidual protein hormones. Trends Endocrinol Metab 1992; 3: 91-95.
Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, Le Shay N, Nezhat CN, Kempson R, Lessey BA, Nayak NR, Giudice LC. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006; 147: 1097-1121.
Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, Osteen K, Taylor RN, Lessey BA, Giudice LC. Global gene profiling in human endometrium during the window of implantation. Endocrinology 2002; 143: 2119-2138.
Borthwick JM, Charnock-Jones DS, Tom BD, Hull ML, Teirney R, Phillips SC, Smith SK. Determination of the transcript profile of human endometrium. Mol Hum Reprod 2003; 9: 19-33.
Schatz F, Krikun G, Caze R, Rahman M, Lockwood CJ. Progestin-regulated expression of tissue factor in decidual cells: implications in endometrial hemostasis, menstruation and angiogenesis. Steroids 2003; 68: 849-860.
Dimitriadis E, White CA, Jones RL, Salamonsen LA. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 2005; 11: 613-630.
Dimitriadis E, Stoikos C, Stafford-Bell M, Clark I, Paiva P, Kovacs G, Salamonsen LA. Interleukin-11, IL-11 receptoralpha and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J Reprod Immunol 2006; 69: 53-64.
Kudo Y, Hara T, Katsuki T, Toyofuku A, Katsura Y, Takikawa O, Fujii T, Ohama K. Mechanisms regulating the expression of indoleamine 2,3-dioxygenase during decidualization of human endometrium. Hum Reprod 2004; 19: 1222-1230.
Makrigiannakis A ZE, Kalantaridou S, Chrousos G. Endometrial and placental CRH as regulators of human embryo implantation. J Reprod Immunol 2004; 62: 53-59.
Farrar JD, Carson DD. Differential temporal and spatial expression of mRNA encoding extracellular matrix components in decidua during the peri-implantation period. Biol Reprod 1992; 46: 1095-1108.
Giudice LC. Maternal-fetal conflict--lessons from a transgene. J Clin Invest 2002; 110: 307-309.
Chen L, Belton RJ, Jr., Nowak RA. Basigin-mediated gene expression changes in mouse uterine stromal cells during implantation. Endocrinology 2009; 150: 966-976.
Bany BM, Cross JC. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev Biol 2006; 294: 445-456.
Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK. Endometrial decidualization: of mice and men. Semin Reprod Med; 28: 17-26.
Devi YS, Shehu A, Halperin J, Stocco C, Le J, Seibold AM, Gibori G. Prolactin signaling through the short isoform of the mouse prolactin receptor regulates DNA binding of specific transcription factors, often with opposite effects in different reproductive issues. Reprod Biol Endocrinol 2009; 7: 87.
Aplin JD, Charlton AK, Ayad S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res 1988; 253: 231-240.
Das SK, Yano S, Wang J, Edwards DR, Nagase H, Dey SK. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse uterus during the peri-implantation period. Dev Genet 1997; 21: 44-54.
Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000; 14: 2123-2133.
Folkman J. Tumor angiogenesis in women with node-positive breast cancer. Cancer J Sci Am 1995; 1: 106-108.
Haddad R, Romero R, Gould BR, Tromp G, Gotsch F, Edwin SS, Zingg HH. Angiogenesis gene expression in mouse uterus during the common pathway of parturition. Am J Obstet Gynecol 2008; 198: 539 e531-538.
Halder JB, Zhao X, Soker S, Paria BC, Klagsbrun M, Das SK, Dey SK. Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 2000; 26: 213-224.
Hyder SM, Stancel GM. Regulation of angiogenic growth factors in the female reproductive tract by estrogens and progestins. Mol Endocrinol 1999; 13: 806-811.
Chakraborty I, Das SK, Dey SK. Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 1995; 147: 339-352.
Ferrara N, Keyt B. Vascular endothelial growth factor: basic biology and clinical implications. Exs 1997; 79: 209-232.
Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380: 435-439.
Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996; 380: 439-442.
Hyder SM, Nawaz Z, Chiappetta C, Stancel GM. Identification of functional estrogen response elements in the gene coding for the potent angiogenic factor vascular endothelial growth factor. Cancer Res 2000; 60: 3183-3190.
Ma W, Tan J, Matsumoto H, Robert B, Abrahamson DR, Das SK, Dey SK. Adult tissue angiogenesis: evidence for negative regulation by estrogen in the uterus. Mol Endocrinol 2001; 15: 1983-1992.
Nigg EA. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 1995; 17: 471-480.
Sherr CJ. Mammalian G1 cyclins. Cell 1993; 73: 1059-1065.
Shiozawa T, Li SF, Nakayama K, Nikaido T, Fujii S. Relationship between the expression of cyclins/cyclin-dependent kinases and sex-steroid receptors/Ki67 in normal human endometrial glands and stroma during the menstrual cycle. Mol Hum Reprod 1996; 2: 745-752.
Shiozawa T, Nikaido T, Nakayama K, Lu X, Fujii S. Involvement of cyclin-dependent kinase inhibitor p27Kip1 in growth inhibition of endometrium in the secretory phase and of hyperplastic endometrium treated with progesterone. Mol Hum Reprod 1998; 4: 899-905.
Geum D, Sun W, Paik SK, Lee CC, Kim K. Estrogen-induced cyclin D1 and D3 gene expressions during mouse uterine cell proliferation in vivo: differential induction mechanism of cyclin D1 and D3. Mol Reprod Dev 1997; 46: 450-458.
Altucci L, Addeo R, Cicatiello L, Germano D, Pacilio C, Battista T, Cancemi M, Petrizzi VB, Bresciani F, Weisz A. Estrogen induces early and timed activation of cyclin-dependent kinases 4, 5, and 6 and increases cyclin messenger ribonucleic acid expression in rat uterus. Endocrinology 1997; 138: 978-984.
Prall OW, Sarcevic B, Musgrove EA, Watts CK, Sutherland RL. Estrogen-induced activation of Cdk4 and Cdk2 during G1-S phase progression is accompanied by increased cyclin D1 expression and decreased cyclin-dependent kinase inhibitor association with cyclin E-Cdk2. J Biol Chem 1997; 272: 10882-10894.
Musgrove EA, Swarbrick A, Lee CS, Cornish AL, Sutherland RL. Mechanisms of cyclin-dependent kinase inactivation by progestins. Mol Cell Biol 1998; 18: 1812-1825.
Jones SR, Kimler BF, Justice WM, Rider V. Transit of normal rat uterine stromal cells through G1 phase of the cell cycle requires progesterone-growth factor interactions. Endocrinology 2000; 141: 637-648.
Das SK, Lim H, Paria BC, Dey SK. Cyclin D3 in the mouse uterus is associated with the decidualization process during early pregnancy. J Mol Endocrinol 1999; 22: 91-101.
Tan J, Raja S, Davis MK, Tawfik O, Dey SK, Das SK. 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 2002; 111: 99-113.
Tan Y, Li M, Cox S, Davis MK, Tawfik O, Paria BC, Das SK. HB-EGF directs stromal cell polyploidy and decidualization via cyclin D3 during implantation. Dev Biol 2004; 265: 181-195.
Kennedy TG, Ross HE. Effect of prostaglandin E2 on rate of decidualization in rats. Prostaglandins 1993; 46: 243-250.
Parr MB, Parr EL, Munaretto K, Clark MR, Dey SK. Immunohistochemical localization of prostaglandin synthase in the rat uterus and embryo during the peri-implantation period. Biol Reprod 1988; 38: 333-343.
Wang H, Dey SK. Lipid signaling in embryo implantation. Prostaglandins Other Lipid Mediat 2005; 77: 84-102.
Lim H, Gupta RA, Ma WG, Paria BC, Moller DE, Morrow JD, DuBois RN, Trzaskos JM, Dey SK. Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPARdelta. Genes Dev 1999; 13: 1561-1574.
Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 1997; 91: 197-208.
Cheng JG, Stewart CL. Loss of cyclooxygenase-2 retards decidual growth but does not inhibit embryo implantation or development to term. Biol Reprod 2003; 68: 401-404.
Reese J, Zhao X, Ma WG, Brown N, Maziasz TJ, Dey SK. Comparative analysis of pharmacologic and/or genetic disruption of cyclooxygenase-1 and cyclooxygenase-2 function in female reproduction in mice. Endocrinology 2001; 142: 3198-3206.
Brar AK, Frank GR, Kessler CA, Cedars MI, Handwerger S. Progesterone-dependent decidualization of the human endometrium is mediated by cAMP. Endocrine 1997; 6: 301-307.
Ivell R, Balvers M, Pohnke Y, Telgmann R, Bartsch O, Milde-Langosch K, Bamberger AM, Einspanier A. Immunoexpression of the relaxin receptor LGR7 in breast and uterine tissues of humans and primates. Reprod Biol Endocrinol 2003; 1: 114.
Gravanis A, Stournaras C, Margioris AN. Paracrinology of endometrial neuropeptides: corticotropin-releasing hormone and opioids. Semin Reprod Endocrinol 1999; 17: 29-38.
Milne SA, Perchick GB, Boddy SC, Jabbour HN. Expression, localization, and signaling of PGE(2) and EP2/EP4 receptors in human nonpregnant endometrium across the menstrual cycle. J Clin Endocrinol Metab 2001; 86: 4453-4459.
Skalhegg BS, Tasken K. Specificity in the cAMP/PKA signaling pathway. Differential expression,regulation, and subcellular localization of subunits of PKA. Front Biosci 2000; 5: D678-693.
Mayr B, Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2001; 2: 599-609.
Voth H, Oberthuer A, Simon T, Kahlert Y, Berthold F, Fischer M. Co-regulated expression of HAND2 and DEIN by a bidirectional promoter with asymmetrical activity in neuroblastoma. BMC Mol Biol 2009; 10: 28.
Lynch VJ, Brayer K, Gellersen B, Wagner GP. HoxA-11 and FOXO1A cooperate to regulate decidual prolactin expression: towards inferring the core transcriptional regulators of decidual genes. PLoS One 2009; 4: e6845.
Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96: 857-868.
Kim JH, Kim MK, Lee HE, Cho SJ, Cho YJ, Lee BL, Lee HS, Nam SY, Lee JS, Kim WH. Constitutive phosphorylation of the FOXO1A transcription factor as a prognostic variable in gastric cancer. Mod Pathol 2007; 20: 835-842.
Buzzio OL, Lu Z, Miller CD, Unterman TG, Kim JJ. FOXO1A differentially regulates genes of decidualization. Endocrinology 2006; 147: 3870-3876.
Kim JJ, Buzzio OL, Li S, Lu Z. Role of FOXO1A in the regulation of insulin-like growth factor-binding protein-1 in human endometrial cells: interaction with progesterone receptor. Biol Reprod 2005; 73: 833-839.
Murre C, McCaw PS, Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 1989; 56: 777-783.
Massari ME, Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 2000; 20: 429-440.
Murakami M, Kataoka K, Tominaga J, Nakagawa O, Kurihara H. Differential cooperation between dHAND and three different E-proteins. Biochem Biophys Res Commun 2004; 323: 168-174.
Murre C, McCaw PS, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN, Hauschka SD, Lassar AB, et al. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 1989; 58: 537-544.
Riley P, Anson-Cartwright L, Cross JC. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 1998; 18: 271-275.
Firulli AB, McFadden DG, Lin Q, Srivastava D, Olson EN. Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nat Genet 1998; 18: 266-270.
Srivastava D, Thomas T, Lin Q, Kirby ML, Brown D, Olson EN. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat Genet 1997; 16: 154-160.
Thomas T, Yamagishi H, Overbeek PA, Olson EN, Srivastava D. The bHLH factors, dHAND and eHAND, specify pulmonary and systemic cardiac ventricles independent of left-right sidedness. Dev Biol 1998; 196: 228-236.
Biben C, Harvey RP. Homeodomain factor Nkx2-5 controls left/right asymmetric expression of bHLH gene eHand during murine heart development. Genes Dev 1997; 11: 1357-1369.
Li Q, Kannan A, DeMayo FJ, Lydon JP, Cooke PS, Yamagishi H, Srivastava D, Bagchi MK, Bagchi IC. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science; 331: 912-916.