Endometrial Decidualization: Of Mice and Men (original) (raw)
Semin Reprod Med 2010; 28(1): 017-026
DOI: 10.1055/s-0029-1242989
© Thieme Medical Publishers
Cyril Y. Ramathal1 , Indrani C. Bagchi2 , Robert N. Taylor4 , Milan K. Bagchi3
- 1Department of Cell and Developmental Biology, University of Illinois-Urbana-Champaign, Urbana, Illinois
- 2Department of Veterinary Biosciences, University of Illinois-Urbana-Champaign, Urbana, Illinois
- 3Molecular and Integrative Physiology, University of Illinois-Urbana-Champaign, Urbana, Illinois
- 4Department of Gyn/Ob, Emory University School of Medicine, Atlanta, Georgia
Further Information
Publication History
Publication Date:
26 January 2010 (online)
ABSTRACT
In murine and human pregnancies, embryos implant by attaching to the luminal epithelium and invading into the stroma of the endometrium. Under the influence of the steroid hormones estrogen and progesterone, the stromal cells surrounding the implanting embryo undergo a remarkable transformation event. This process, known as decidualization, is an essential prerequisite for implantation. It comprises morphogenetic, biochemical, and vascular changes driven by the estrogen and progesterone receptors. The development of mutant mouse models lacking these receptors has firmly established the necessity of steroid signaling for decidualization. Genomic profiling of mouse and human endometrium has uncovered a complex yet highly conserved network of steroid-regulated genes that supports decidualization. To advance our understanding of the mechanisms regulating implantation and better address the clinical challenges of infertility and endometrial diseases such as endometriosis, it is important to integrate the information gained from the mouse and human models.
KEYWORDS
Decidualization - implantation - progesterone receptor - endometriosis
REFERENCES
- 1 Finn C A. The implantation reaction. In: Wynn RM Biology of the Uterus. New York, NY; Plenum Press 1977: 246-308
- 2 Dey S K, Lim H, Das S K et al.. Molecular cues to implantation. Endocr Rev. 2004; 25(3) 341-373
- 3 Carson D D, Bagchi I, Dey S K et al.. Embryo implantation. Dev Biol. 2000; 223(2) 217-237
- 4 Sharkey A M, Smith S K. The endometrium as a cause of implantation failure. Best Pract Res Clin Obstet Gynaecol. 2003; 17(2) 289-307
- 5 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 U S A. 1993; 90(21) 10159-10162
- 6 Psychoyos A. Uterine receptivity for nidation. Ann N Y Acad Sci. 1986; 476 36-42
- 7 Glasser S R, Mulholland J, Mani S K et al.. Blastocyst-endometrial relationships: reciprocal interactions between uterine epithelial and stromal cells and blastocysts. Trophoblast Res. 1991; 5 229-280
- 8 Irwin J C, Giudice L C. Decidua. In: Knobil E, Neill JD Encyclopedia of Reproduction. San Diego, CA; Academic Press 1999: 823-835
- 9 Gu Y, Gibori G. Deciduoma. In: Knobil E, Neill JD Encyclopedia of Reproduction. San Diego, CA; Academic Press 1999: 836-842
- 10 Ansell J D, Barlow P W, McLaren A. Binucleate and polyploid cells in the deciduas of the mouse. J Embryol Exp Morphol. 1974; 31 223-227
- 11 Maruyama T, Yoshimura Y. Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium. Endocr J. 2008; 55(5) 795-810
- 12 Bell S C. Decidualization and relevance to menstruation. In: D' Arcangues C, Fraser IS, Newton JR, Odlind V Contraception and Mechanisms of Endometrial Bleeding. Cambridge, United Kingdom; Cambridge University Press 1990
- 13 Giudice L C. Endometrium. In: Knobil E, Neill JD Encyclopedia of Reproduction. San Diego, CA; Academic Press 1999: 1067-1078
- 14 Strauss J F, Gurpide E. The endometrium: regulation and dysfunction. In: Yen SSC, Jaffe RB Reproductive Endocrinology. Philadelphia, PA; WB Saunders 1991: 309-356
- 15 Tsai M J, O'Malley B W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem. 1994; 63 451-486
- 16 Lubahn D B, Moyer J S, Golding T S, Couse J F, Korach K S, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A. 1993; 90(23) 11162-11166
- 17 Lydon J P, DeMayo F J, Funk C R et al.. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995; 9(18) 2266-2278
- 18 Soyal S M, Mukherjee A, Lee K Y et al.. Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis. 2005; 41(2) 58-66
- 19 Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol. 2003; 178(3) 357-372
- 20 Tranguch S, Cheung-Flynn J, Daikoku T et al.. Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc Natl Acad Sci U S A. 2005; 102(40) 14326-14331
- 21 Yang Z, Wolf I M, Chen H et al.. FK506-binding protein 52 is essential to uterine reproductive physiology controlled by the progesterone receptor A isoform. Mol Endocrinol. 2006; 20(11) 2682-2694
- 22 Cheon Y P, Li Q, Xu X, DeMayo F J, Bagchi I C, Bagchi M K. A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol Endocrinol. 2002; 16(12) 2853-2871
- 23 Reese J, Das S K, Paria B C et al.. Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J Biol Chem. 2001; 276(47) 44137-44145
- 24 Ramji D P, Foka P. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J. 2002; 365(Pt 3) 561-575
- 25 Mantena S R, Kannan A, Cheon Y P et al.. C/EBPbeta is a critical mediator of steroid hormone-regulated cell proliferation and differentiation in the uterine epithelium and stroma. Proc Natl Acad Sci U S A. 2006; 103(6) 1870-1875
- 26 Sterneck E, Tessarollo L, Johnson P F. An essential role for C/EBPbeta in female reproduction. Genes Dev. 1997; 11(17) 2153-2162
- 27 Plante B J, Kannan A, Bagchi M K, Yuan L, Young S L. Cyclic regulation of transcription factor C/EBP beta in human endometrium. Reprod Biol Endocrinol. 2009; 7(1) 15
- 28 Tang B, Guller S, Gurpide E. Cyclic adenosine 3′,5′-monophosphate induces prolactin expression in stromal cells isolated from human proliferative endometrium. Endocrinology. 1993; 133(5) 2197-2203
- 29 Irwin J C, Kirk D, King R J, Quigley M M, Gwatkin R B. Hormonal regulation of human endometrial stromal cells in culture: an in vitro model for decidualization. Fertil Steril. 1989; 52(5) 761-768
- 30 Bell S C, Jackson J A, Ashmore J, Zhu H H, Tseng L. Regulation of insulin-like growth factor-binding protein-1 synthesis and secretion by progestin and relaxin in long term cultures of human endometrial stromal cells. J Clin Endocrinol Metab. 1991; 72(5) 1014-1024
- 31 Giudice L C, Milkowski D A, Lamson G, Rosenfeld R G, Irwin J C. Insulin-like growth factor binding proteins in human endometrium: steroid-dependent messenger ribonucleic acid expression and protein synthesis. J Clin Endocrinol Metab. 1991; 72(4) 779-787
- 32 Christian M, Pohnke Y, Kempf R, Gellersen B, Brosens J J. Functional association of PR and CCAAT/enhancer-binding protein beta isoforms: promoter-dependent cooperation between PR-B and liver-enriched inhibitory protein, or liver-enriched activatory protein and PR-A in human endometrial stromal cells. Mol Endocrinol. 2002; 16(1) 141-154
- 33 Benson G V, Lim H, Paria B C, Satokata I, Dey S K, Maas R L. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development. 1996; 122(9) 2687-2696
- 34 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. 1999; 13(6) 1005-1017
- 35 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. 1998; 101(7) 1379-1384
- 36 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. 1999; 84(3) 1129-1135
- 37 Hogan B L. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 1996; 10(13) 1580-1594
- 38 Ying Y, Zhao G Q. Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, Smad1, during mouse decidualization. Biol Reprod. 2000; 63(6) 1781-1786
- 39 Lee K Y, Jeong J-W, Wang J et al.. Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol. 2007; 27(15) 5468-5478
- 40 Paria B C, Ma W, Tan J et al.. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci U S A. 2001; 98(3) 1047-1052
- 41 Li Q, Kannan A, Wang W et al.. Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. J Biol Chem. 2007; 282(43) 31725-31732
- 42 Logan C Y, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004; 20 781-810
- 43 Tulac S, Nayak N R, Kao L C et al.. Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium. J Clin Endocrinol Metab. 2003; 88(8) 3860-3866
- 44 Matsumoto H, Zhao X, Das S K, Hogan B LM, Dey S K. Indian hedgehog as a progesterone-responsive factor mediating epithelial-mesenchymal interactions in the mouse uterus. Dev Biol. 2002; 245(2) 280-290
- 45 Takamoto N, Zhao B, Tsai S Y, DeMayo F J. Identification of Indian hedgehog as a progesterone-responsive gene in the murine uterus. Mol Endocrinol. 2002; 16(10) 2338-2348
- 46 Lee K, Jeong J, Kwak I et al.. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet. 2006; 38(10) 1204-1209
- 47 Simon L, Spiewak K A, Ekman G C et al.. Stromal progesterone receptors mediate induction of Indian Hedgehog (IHH) in uterine epithelium and its downstream targets in uterine stroma. Endocrinology. 2009; 150(8) 3871-3876
- 48 Kurihara I, Lee D-K, Petit F G et al.. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet. 2007; 3(6) e102
- 49 Laws M J, Taylor R N, Sidell N et al.. Gap junction communication between uterine stromal cells plays a critical role in pregnancy-associated neovascularization and embryo survival. Development. 2008; 135(15) 2659-2668
- 50 Kumar N M, Gilula N B. The gap junction communication channel. Cell. 1996; 84(3) 381-388
- 51 Lai E, Clark K L, Burley S K, Darnell Jr J E. Hepatocyte nuclear factor 3/fork head or “winged helix” proteins: a family of transcription factors of diverse biologic function. Proc Natl Acad Sci U S A. 1993; 90(22) 10421-10423
- 52 Christian M, Zhang X, Schneider-Merck T et al.. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein beta in differentiating human endometrial stromal cells. J Biol Chem. 2002; 277(23) 20825-20832
- 53 Buzzio O L, Lu Z, Miller C D, Unterman T G, Kim J J. FOXO1A differentially regulates genes of decidualization. Endocrinology. 2006; 147(8) 3870-3876
- 54 Bilinski P, Roopenian D, Gossler A. Maternal IL-11Ralpha function is required for normal decidua and fetoplacental development in mice. Genes Dev. 1998; 12(14) 2234-2243
- 55 Robb L, Li R, Hartley L et al.. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat Med. 1998; 4(3) 303-308
- 56 Menkhorst E, Salamonsen L, Robb L, Dimitriadis E. IL11 antagonist inhibits uterine stromal differentiation, causing pregnancy failure in mice. Biol Reprod. 2009; 80(5) 920-927
- 57 Karpovich N, Chobotova K, Carver J, Heath J K, Barlow D H, Mardon H J. Expression and function of interleukin-11 and its receptor alpha in the human endometrium. Mol Hum Reprod. 2003; 9(2) 75-80
- 58 Ryan I P, Taylor R N. Endometriosis and infertility: new concepts. Obstet Gynecol Surv. 1997; 52(6) 365-371
- 59 Giudice L C, Kao L C. Endometriosis. Lancet. 2004; 364(9447) 1789-1799
- 60 Giudice L C, Telles T L, Lobo S, Kao L. The molecular basis for implantation failure in endometriosis: on the road to discovery. Ann N Y Acad Sci. 2002; 955 252-264
- 61 Zeitoun K, Takayama K, Sasano H et al.. Deficient 17beta-hydroxysteroid dehydrogenase type 2 expression in endometriosis: failure to metabolize 17beta-estradiol. J Clin Endocrinol Metab. 1998; 83(12) 4474-4480
- 62 Attia G R, Zeitoun K, Edwards D, Johns A, Carr B R, Bulun S E. Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab. 2000; 85(8) 2897-2902
- 63 Klemmt P A, Carver J G, Kennedy S H, Koninckx P R, Mardon H J. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril. 2006; 85(3) 564-572
- 64 Kao L C, Germeyer A, Tulac S et al.. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology. 2003; 144(7) 2870-2881
- 65 Taylor H S, Bagot C, Kardana A, Olive D, Arici A. HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod. 1999; 14(5) 1328-1331
- 66 Taylor R N, Lundeen S G, Giudice L C. Emerging role of genomics in endometriosis research. Fertil Steril. 2002; 78(4) 694-698
- 67 Bulun S E, Yang S, Fang Z et al.. Role of aromatase in endometrial disease. J Steroid Biochem Mol Biol. 2001; 79(1) 19-25
- 68 Yang S, Fang Z, Suzuki T et al.. Regulation of aromatase P450 expression in endometriotic and endometrial stromal cells by CCAAT/enhancer binding proteins (C/EBPs): decreased C/EBPbeta in endometriosis is associated with overexpression of aromatase. J Clin Endocrinol Metab. 2002; 87(5) 2336-2345
- 69 Bulun S E, Utsunomiya H, Lin Z et al.. Steroidogenic factor-1 and endometriosis. Mol Cell Endocrinol. 2009; 300(1-2) 104-108
- 70 Attar E, Tokunaga H, Imir G et al.. Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J Clin Endocrinol Metab. 2009; 94(2) 623-631
Milan K BagchiPh.D.
Molecular and Integrative Physiology, University of Illinois-Urbana-Champaign, Urbana Illinois
524 Burrill Hall, 407 S. Goodwin Ave., Urbana, IL 61801
Email: mbagchi@life.uiuc.edu