Transcriptional cross talk between the forkhead transcription factor forkhead box O1A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells

Molecular Endocrinology

Volumn 21, Issue 10, 2007, Pages 2334-2349

  Takano, Masashi ^a   Lu, Zhenxiao ^d   Goto, Tomoko ^a   Fusi, Luca ^a   Higham, Jenny ^b   Francis, Julia ^a   Withey, Anna ^a   Hardt, Jennifer ^d   Cloke, Brianna ^a   Stavropoulou, Alexandra V ^a   Ishihara, Osamu ^c   Lam, Eric W F ^a   Unterman, Terry G ^e   Brosens, Jan J ^a,f   Kim, J Julie ^d  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b ST MARY S HOSPITAL   (United Kingdom)

^c SAITAMA MEDICAL UNIVERSITY   (Japan)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF ILLINOIS   (United States)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; FORKHEAD TRANSCRIPTION FACTOR O1A; OLIGONUCLEOTIDE; PROGESTERONE RECEPTOR; PROTEIN WNT16; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; WNT4 PROTEIN;

ARTICLE; CELL CYCLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; ENDOMETRIUM CELL; GENE IDENTIFICATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; STROMA CELL;

CELL CYCLE; CELL DIFFERENTIATION; CELLS, CULTURED; ENDOMETRIUM; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, PROGESTERONE; STROMAL CELLS; TRANSCRIPTION, GENETIC;

EID: 34948872466     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2007-0058     Document Type: Article

References (68)

1. Brosens JJ, Gellersen B 2006 Death or survival-progesterone-dependent cell fate decisions in the human endometrial stroma. J Mol Endocrinol 36:389-398
2. Brosens JJ, Pijnenborg R, Brosens IA 2002 The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 187:1416-1423
3. Ramsey EM, Houston ML, Harris JW 1976 Interactions of the trophoblast and maternal tissues in three closely related primate species. Am J Obstet Gynecol 124:647-652
4. Kliman HJ 2000 Uteroplacental blood flow. The story of decidualization, menstruation, and trophoblast invasion. Am J Pathol 157:1759-1768
5. Kudo Y, Hara T, Katsuki T, Toyofuku A, Katsura Y, Takikawa O, Fujii T, Ohama K 2004 Mechanisms regulating the expression of indoleamine 2,3-dioxygenase during decidualization of human endometrium. Hum Reprod 19:1222-1230
6. Red-Horse K, Drake PM, Fisher SJ 2004 Human pregnancy: the role of chemokine networks at the fetal-maternal interface. Expert Rev Mol Med 2004:1-14
7. Sherwin JR, Sharkey AM, Cameo P, Mavrogianis PM, Catalano RD, Edassery S, Fazleabas AT 2007 Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology 148:618-626
8. Sugino N, Shimamura K, Takiguchi S, Tamura H, Ono M, Nakata M, Nakamura Y, Ogino K, Uda T, Kato H 1996 Changes in activity of superoxide dismutase in the human endometrium throughout the menstrual cycle and in early pregnancy. Hum Reprod 11:1073-1078
9. Gellersen B, Brosens J 2003 Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol 178:357-372
10. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
11. Tseng L, Zhu HH 1997 Regulation of progesterone receptor messenger ribonucleic acid by progestin in human endometrial stromal cells. Biol Reprod 57:1360-1366
12. Rowan BG, Garrison N, Weigel NL, O'Malley BW 2000 8-Bromo-cyclic AMP induces phosphorylation of two sites in SRC-1 that facilitate ligand-independent activation of the chicken progesterone receptor and are critical for functional cooperation between SRC-1 and CREB binding protein. Mol Cell Biol 20:8720-8730
13. Wagner BL, Norris JD, Knotts TA, Weigel NL, McDonnell DP 1998 The nuclear corepressors NCoR and SMRT are key regulators of both ligand- and 8-bromo-cyclic AMP-dependent transcriptional activity of the human progesterone receptor. Mol Cell Biol 18:1369-1378
14. Jones MC, Fusi L, Higham JH, Abdel-Hafiz H, Horwitz KB, Lam EW, Brosens JJ 2006 Regulation of the SUMO pathway sensitizes differentiating human endometrial stromal cells to progesterone. Proc Natl Acad Sci USA 103:16272-16277
15. Christian M, Zhang X, Schneider-Merck T, Unterman TG, Gellersen B, White JO, Brosens JJ 2002 Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein β in differentiating human endometrial stromal cells. J Biol Chem 277:20825-20832
16. Kim JJ, Buzzio OL, Li S, Lu Z 2005 Role of FOXO1A in the regulation of insulin-like growth factor-binding protein-1 in human endometrial cells: interaction with progesterone receptor. Biol Reprod 73:833-839
17. Mak IY, Brosens JJ, Christian M, Hills FA, Chamley L, Regan L, White JO 2002 Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro. J Clin Endocrinol Metab 87:2581-2588
18. Pohnke Y, Schneider-Merck T, Fahnenstich J, Kempf R, Christian M, Milde-Langosch K, Brosens JJ, Gellersen B 2004 Wild-type p53 protein is up-regulated upon cyclic adenosine monophosphate-induced differentiation of human endometrial stromal cells. J Clin Endocrinol Metab 89:5233-5244
19. Brar AK, Handwerger S, Kessler CA, Aronow BJ 2001 Gene induction and categorical reprogramming during in vitro human endometrial fibroblast decidualization. Physiol Genomics 7:135-148
20. Dijkers PF, Medema RH, Pals C, Banerji L, Thomas NS, Lam EW, Burgering BM, Raaijmakers JA, Lammers JW, Koenderman L, Coffer PJ 2000 Forkhead transcription factor FKHR-L1 modulates cytokine-dependent transcriptional regulation of p27(KIP1). Mol Cell Biol 20:9138-9148
21. Modur V, Nagarajan R, Evers BM, Milbrandt J 2002 FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem 277:47928-47937
22. Sunters A, Fernandez de Mattos S, Stahl M, Brosens JJ, Zoumpoulidou G, Saunders CA, Coffer PJ, Medema RH, Coombes RC, Lam EW 2003 FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 278:49795-49805
23. Kajihara T, Jones M, Fusi L, Takano M, Feroze-Zaidi F, Pirianov G, Mehmet H, Ishihara O, Higham JM, Lam EW, Brosens JJ 2006 Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization. Mol Endocrinol 20:2444-2455
24. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Burgering BM 2002 Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419:316-321
25. Nemoto S, Fergusson MM, Finkel T 2004 Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science 306:2105-2108
26. Biggs 3rd WH, Meisenhelder J, Hunter T, Cavenee WK, Arden KC 1999 Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA 96:7421-7426
27. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME 1999 Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868
28. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME 2001 Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol Cell Biol 21:952-965
29. Rena G, Woods YL, Prescott AR, Peggie M, Unterman TG, Williams MR, Cohen P 2002 Two novel phosphorylation sites on FKHR that are critical for its nuclear exclusion. EMBO J 21:2263-2271
30. Woods YL, Rena G, Morrice N, Barthel A, Becker W, Guo S, Unterman TG, Cohen P 2001 The kinase DYRK1A phosphorylates the transcription factor FKHR at Ser329 in vitro, a novel in vivo phosphorylation site. Biochem J 355:597-607
31. Labied S, Kajihara T, Madureira PA, Fusi L, Jones MC, Higham JM, Varshochi R, Francis JM, Zoumpoulidou G, Essafi A, Fernandez de Mattos S, Lam EW, Brosens JJ 2006 Progestins regulate the expression and activity of the forkhead transcription factor FOXO1 in differentiating human endometrium. Mol Endocrinol 20:35-44
32. Kim JJ, Taylor HS, Akbas GE, Foucher I, Trembleau A, Jaffe RC, Fazleabas AT, Unterman TG 2003 Regulation of insulin-like growth factor binding protein-1 promoter activity by FKHR and HOXA10 in primate endometrial cells. Biol Reprod 68:24-30
33. Buzzio OL, Lu Z, Miller CD, Unterman TG, Kim JJ 2006 FOXO1A differentially regulates genes of decidualization. Endocrinology 147:3870-3876
34. Grinius L, Kessler C, Schroeder J, Handwerger S 2006 Forkhead transcription factor FOXO1A is critical for induction of human decidualization. J Endocrinol 189:179-187
35. Alfaidy N, Li W, MacIntosh T, Yang K, Challis J 2003 Late gestation increase in 11-hydroxysteroid dehydrogenase 1 expression in human fetal membranes: a novel intrauterine source of cortisol. J Clin Endocrinol Metab 88:5033-5038
36. Tierney EP, Tulac S, Huang ST, Giudice LC 2003 Activation of the protein kinase A pathway in human endometrial stromal cells reveals sequential categorical gene regulation. Physiol Genomics 16:47-66
37. Qian K, Chen H, Wei Y, Hu J, Zhu G 2005 Differentiation of endometrial stromal cells in vitro: down-regulation of suppression of the cell cycle inhibitor p57 by HOXA10? Mol Hum Reprod 11:245-251
38. Yao MW, Lim H, Schust DJ, Choe SE, Farago A, Ding Y, Michaud S, Church GM, Maas RL 2003 Gene expression profiling reveals progesterone-mediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. Mol Endocrinol 17:610-627
39. Bjornstedt M, Xue J, Huang W, Akesson B, Holmgren A 1994 The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J Biol Chem 269:29382-29384
40. Tham DM, Whitin JC, Kim KK, Zhu SX, Cohen HJ 1998 Expression of extracellular glutathione peroxidase in human and mouse gastrointestinal tract. Am J Physiol 275:G1463-1471
41. Burton GJ, Jauniaux E 2004 Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 11:342-352
42. Jauniaux E, Burton GJ 2005 Pathophysiology of histological changes in early pregnancy loss. Placenta 26:114-123
43. Jauniaux E, Hempstock J, Teng C, Battaglia FC, Burton GJ 2005 Polyol concentrations in the fluid compartments of the human conceptus during the first trimester of pregnancy: maintenance of redox potential in a low oxygen environment. J Clin Endocrinol Metab 90:1171-1175
44. Apparao KB, Murray MJ, Fritz MA, Meyer WR, Chambers AF, Truong PR, Lessey BA 2001 Osteopontin and its receptor αvβ(3) integrin are coexpressed in the human endometrium during the menstrual cycle but regulated differentially. J Clin Endocrinol Metab 86:4991-5000
45. Brown TL, Moulton BC, Witte DP, Swertfeger DK, Harmony JA 1996 Apolipoprotein J/clusterin expression defines distinct stages of blastocyst implantation in the mouse uterus. Biol Reprod 55:740-747
46. Henriquez S, Tapia A, Quezada M, Vargas M, Cardenas H, Rios M, Salvatierra AM, Croxatto H, Orihuela P, Zegers-Hochschild F, Munroe DJ, Velasquez L 2006 Deficient expression of monoamine oxidase A in the endometrium is associated with implantation failure in women participating as recipients in oocyte donation. Mol Hum Reprod 12:749-754
47. Sherr CJ, Roberts JM 2004 Living with or without cyclins and cyclin-dependent kinases. Genes Dev 18:2699-2711
48. Steinman RA 2002 Cell cycle regulators and hematopoiesis. Oncogene 21:3403-3413
49. Kuiperij HB, van der Horst A, Raaijmakers J, Weijzen S, Medema RH, Bos JL, Burgering BM, Zwartkruis FJ 2005 Activation of FoxO transcription factors contributes to the antiproliferative effect of cAMP. Oncogene 24:2087-2095
50. Lynch RL, Konicek BW, McNulty AM, Hanna KR, Lewis JE, Neubauer BL, Graff JR 2005 The progression of LNCaP human prostate cancer cells to androgen independence involves decreased FOXO3a expression and reduced p27KIP1 promoter transactivation. Mol Cancer Res 3:163-169
51. Park Y, Maizels ET, Feiger ZJ, Alam H, Peters CA, Woodruff TK, Unterman TG, Lee EJ, Jameson JL, Hunzicker-Dunn M 2005 Induction of cyclin D2 in rat granulosa cells requires FSH-dependent relief from FOXO1 repression coupled with positive signals from Smad. J Biol Chem 280:9135-9148
52. Seoane J, Le HV, Shen L, Anderson SA, Massague J 2004 Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117:211-223
53. Risinger JI, Maxwell GL, Chandramouli GV, Jazaeri A, Aprelikova O, Patterson T, Berchuck A, Barrett JC 2003 Microarray analysis reveals distinct gene expression profiles among different histologic types of endometrial cancer. Cancer Res 63:6-11
54. Shazand K, Baban S, Prive C, Malette B, Croteau P, Lagace M, Racine JB, Hugo P 2004 FOXO1 and c-jun transcription factors mRNA are modulated in endometriosis. Mol Hum Reprod 10:871-877
55. Arden KC 2004 FoxO: linking new signaling pathways. Mol Cell 14:416-418
56. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC 2005 Functional interaction between -catenin and FOXO in oxidative stress signaling. Science 308:1181-1184
57. Brisken C, Heineman A, Chavarria T, Elenbaas B, Tan J, Dey SK, McMahon JA, McMahon AP, Weinberg RA 2000 Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev 14:650-654
58. Sekiya T, Adachi S, Kohu K, Yamada T, Higuchi O, Furukawa Y, Nakamura Y, Nakamura T, Tashiro K, Kuhara S, Ohwada S, Akiyama T 2004 Identification of BMP and activin membrane-bound inhibitor (BAMBI), an inhibitor of transforming growth factor-β signaling, as a target of the β-catenin pathway in colorectal tumor cells. J Biol Chem 279:6840-6846
59. Sekiya T, Oda T, Matsuura K, Akiyama T 2004 Transcriptional regulation of the TGF-β pseudoreceptor BAMBI by TGF-β signaling. Biochem Biophys Res Commun 320:680-684
60. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, Massague J, Niehrs C 1999 Silencing of TGF-β signalling by the pseudoreceptor BAMBI. Nature 401:480-485
61. Jacobsen BM, Schittone SA, Richer JK, Horwitz KB 2005 Progesterone-independent effects of human progesterone receptors (PRs) in estrogen receptor-positive breast cancer: PR isoform-specific gene regulation and tumor biology. Mol Endocrinol 19:574-587
62. Brosens JJ, Hayashi N, White JO 1999 Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 140:4809-4820
63. Christian M, Pohnke Y, Kempf R, Gellersen B, Brosens JJ 2002 Functional association of PR and CCAAT/enhancer-binding protein β 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 16:141-154
64. Dudoit S, Gentleman RC, Quackenbush J 2003 Open source software for the analysis of microarray data. Biotechniques Suppl:45-51
65. Wettenhall JM, Smyth GK 2004 limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20:3705-3706
66. Hosack DA, Dennis Jr G, Sherman BT, Lane HC, Lempicki RA 2003 Identifying biological themes within lists of genes with EASE. Genome Biol 4:R70
67. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔ C(T)) Method. Methods 25:402-408
68. Essafi A, Fernandez de Mattos S, Hassen YA, Soeiro I, Mufti GJ, Thomas NS, Medema RH, Lam EW 2005 Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 24:2317-2329