Endometrial decidualization: Of mice and men

Seminars in Reproductive Medicine

Volumn 28, Issue 1, 2010, Pages 17-26

  Ramathal, Cyril Y ^a   Bagchi, Indrani C ^b   Taylor, Robert N ^c   Bagchi, Milan K ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Decidualization; Endometriosis; Implantation; Progesterone receptor

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CCAAT ENHANCER BINDING PROTEIN BETA; CHAPERONE; CONNEXIN 43; CYTOKINE; ESTROGEN; ESTROGEN RECEPTOR; FK 506 BINDING PROTEIN; INTERLEUKIN 11; INTERLEUKIN 11 RECEPTOR ALPHA; PROGESTERONE; PROGESTERONE RECEPTOR; SMALL INTERFERING RNA; SONIC HEDGEHOG PROTEIN; STEROID HORMONE; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR HOXA10; VASCULOTROPIN; WNT4 PROTEIN;

CELL COMMUNICATION; CYTOKINE PRODUCTION; DECIDUALIZATION; EMBRYO; EMBRYO DEVELOPMENT; ENDOMETRIOSIS; ENDOMETRIUM; ESTROGEN METABOLISM; ESTROGEN SYNTHESIS; FEMALE; FEMALE INFERTILITY; GENE DELETION; HORMONE ACTION; HUMAN; KNOCKOUT MOUSE; MOUSE; NIDATION; NONHUMAN; PREGNANCY; PROTEIN EXPRESSION; REVIEW; STROMA CELL; UTERUS; UTERUS DISEASE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CONNEXIN 43; DECIDUA; DISEASE MODELS, ANIMAL; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; INTERLEUKIN-11; MICE; MOLECULAR CHAPERONES; PREGNANCY; RECEPTORS, STEROID; UTERINE DISEASES;

EID: 76249088857     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0029-1242989     Document Type: Review

References (70)

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 USA 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 USA 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 USA 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 USA 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 USA 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 J E. Jr. Hepatocyte nuclear factor 3/fork head or winged helix proteins: a family of transcription factors of diverse biologic function. Proc Natl Acad Sci USA 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