Androgen signaling in decidualizing human endometrial stromal cells enhances resistance to oxidative stress

Fertility and Sterility

Volumn 97, Issue 1, 2012, Pages 185-191

  Kajihara, Takeshi ^a   Tochigi, Hideno ^a   Prechapanich, Japarath ^a   Uchino, Satomi ^a   Itakura, Atsuo ^a   Brosens, Jan J ^b   Ishihara, Osamu ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

androgen; decidualization; Endometrium; FOXO1; oxidative stress

Indexed keywords

8 BROMO CYCLIC AMP; ANDROGEN; ANDROSTANOLONE; COPPER ZINC SUPEROXIDE DISMUTASE; FLUTAMIDE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; PROLACTIN; SCAVENGER; TRANSCRIPTION FACTOR FKHR;

ADULT; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; ENDOMETRIUM CELL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HYSTERECTOMY; IN VITRO STUDY; OXIDATIVE STRESS; PREMENOPAUSE; PRIORITY JOURNAL; PROLACTIN RELEASE; PROTEIN EXPRESSION; STROMA CELL; UTERUS MYOMA;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ADULT; ANDROGEN ANTAGONISTS; APOPTOSIS; DIHYDROTESTOSTERONE; ENDOMETRIUM; FEMALE; FLUTAMIDE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; HYSTERECTOMY; LEIOMYOMA; MIDDLE AGED; OXIDATIVE STRESS; PREMENOPAUSE; PROLACTIN; SIGNAL TRANSDUCTION; STROMAL CELLS; SUPEROXIDE DISMUTASE; UTERINE NEOPLASMS;

EID: 84155164512     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2011.10.017     Document Type: Article

References (44)

1. B. Gellersen, I.A. Brosens, and J.J. Brosens Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives Semin Reprod Med 25 2007 445 453 (Pubitemid 350058431)
2. T. Kajihara, M. Jones, L. Fusi, M. Takano, F. Feroze-Zaidi, and G. Pirianov Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization Mol Endocrinol 20 2006 2444 2455 (Pubitemid 44496413)
3. H. Shiina, T. Matsumoto, T. Sato, K. Igarashi, J. Miyamoto, and S. Takemasa Premature ovarian failure in androgen receptor-deficient mice Proc Natl Acad Sci USA 103 2006 224 229 (Pubitemid 43076131)
4. S. Yeh, M.Y. Tsai, Q. Xu, X.M. Mu, H. Lardy, and K.E. Huang Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues Proc Natl Acad Sci USA 99 2002 13498 13503 (Pubitemid 35215410)
5. H.J. Mertens, M.J. Heineman, J. Koudstaal, P. Theunissen, and J.L. Evers Androgen receptor expression content in human endometrium Eur J Obstet Gynecol Reprod Biol 70 1996 11 13 (Pubitemid 27041932)
6. O.D. Slayden, N.R. Nayak, K.A. Burton, K. Chwalisz, S.T. Cameron, and H.O. Critchley Progesterone antagonists increase androgen receptor expression in the rhesus macaque and human endometrium J Clin Endocrinol Metab 86 2001 2668 2679 (Pubitemid 32545722)
7. R.C. Bonney, M.J. Scanlon, D.L. Jones, M.J. Reed, and V.H. James Adrenal androgen concentrations in endometrium and plasma during the menstrual cycle J Endocrinol 101 1984 181 188 (Pubitemid 14135332)
8. A. Salonia, M. Pontillo, R.E. Nappi, G. Zanni, F. Fabbri, and M. Scavini Menstrual cycle-related changes in circulating androgens in healthy women with self-reported normal sexual function J Sex Med 5 2008 854 863 (Pubitemid 351472195)
9. C. Vermeulen-Meiners, J. Poortman, M. Nabuurs, and J.H. Thijssen The endogenous concentration and subcellular distribution of androgens in normal human premenopausal endometrium, myometrium and vagina Gynecol Endocrinol 2 1988 121 130
10. B. Cloke, K. Huhtinen, L. Fusi, T. Kajihara, M. Yliheikkila, and K.K. Ho The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium Endocrinology 149 2008 4462 4474
11. B. Leitao, M.C. Jones, L. Fusi, J. Higham, Y. Lee, and M. Takano Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed oxidative stress signals FASEB J 24 2010 1541 1551
12. J.J. Brosens, N. Hayashi, and J.O. White Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cell Endocrinology 140 1999 4809 4820 (Pubitemid 30666151)
13. M. Christian, X. Zhang, T. Schneider-Merck, T.G. Unterman, B. Gellersen, and J.O. White Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein β in differentiating human endometrial stromal cells J Biol Chem 277 2002 20825 20832 (Pubitemid 34967389)
14. T. Kajihara, S. Uchino, M. Suzuki, A. Itakura, J.J. Brosens, and O. Ishihara Human chorionic gonadotropin confers resistance to oxidative stress-induced apoptosis in decidualizing human endometrial stromal cell Fertil Steril 95 2011 1302 1307
15. B. Gellersen, R. Kempf, R. Telgmann, and G.E. DiMattia Nonpituitary human prolactin gene transcription is independent of Pit-1 and differentially controlled in lymphocytes and in endometrial stroma Mol Endocrinol 8 1994 356 373 (Pubitemid 24108363)
16. S. Ajossa, S. Guerriero, A.M. Paoletti, M. Orru, and G.B. Melis The antiandrogenic effect of flutamide improves uterine perfusion in women with polycystic ovary syndrome Fertil Steril 77 2002 1136 1140 (Pubitemid 34626319)
17. S. Labied, T. Kajihara, P.A. Madureria, L. Fusi, M.C. Jones, and J.M. Higham Progestins regulate the expression and activity of the forkhead transcription factor FOXO1 in differentiating human endometrium Mol Endrionl 20 2006 35 44 (Pubitemid 43011668)
18. E.P. Gelmann Molecular biology of the androgen receptor J Clin Oncol 20 2002 3001 3015 (Pubitemid 34728896)
19. D.J. Vnader Griend, I.V. Litvinov, and J.T. Isaacs Stabilizing androgen receptor in mitosis inhibits prostate cancer proliferation Cell Cycle 6 2007 647 651 (Pubitemid 46535673)
20. H.J. Mertens, M.J. Heineman, P.H. Theunissen, F.H. de Jong, and J.L. Evers Androgen, estrogen and progesterone receptor expression in the human uterus during the menstrual cycle Eur J Obstet Gynecol Reprod Biol 98 2001 58 65 (Pubitemid 32758836)
21. K. Ito, T. Suzuki, J. Akahira, T. Moriya, C. Kaneko, and H. Utsunomiya Expression of androgen receptor and 5α-reductases in the human normal endometrium and its disorders Int J Cancer 99 2002 652 657 (Pubitemid 34538743)
22. Y. Chandrasekhar, D.T. Armstrong, and T.G. Kennedy Implantation delay and anti-deciduogenic activity in the rat by the anti-androgen, hydroxyflutamide Biol Reprod 42 1990 120 125 (Pubitemid 20097087)
23. A.D. Mooradian, J.E. Morley, and S.G. Korenman Biological actions of androgens Endocr Rev 8 1987 1 28
24. E.S. Knochenhauer, T.J. Key, M. Kahsar-Miller, W. Waggoner, L.R. Boots, and R. Azziz Prevalence of polycystic ovary syndrome in unselected black and white women of the southeastern United States: a prospective study J Clin Endocrinol Metab 83 1998 3078 3082 (Pubitemid 28500937)
25. M. Tulppala, U.H. Stenman, B. Cacciatore, and O. Ylikorlaka Polycystic ovaries and levels of gonadotropins and androgen in recurrent miscarriage: prospective study in 50 women Br J Obstet Gynaecol 100 1993 348 352 (Pubitemid 23121156)
26. D. Cermik, B. Selam, and H.S. Taylor Regulation of HOXA-10 expression by testosterone in vitro and in the endometrium of patients with polycystic ovary syndrome J Clin Endocrinol Metab 88 2003 238 243 (Pubitemid 36115172)
27. L.C. Giudice Endometrium in PCOS: implantation and predisposition to endocrine CA Best Pract Res Clin Endocrinol Metab 20 2006 235 244 (Pubitemid 43842928)
28. E.M. Tuckerman, M.A. Okon, T. Li, and S.M. Laird Do androgens have a direct effect on endometrial function? An in vitro study Fertil Steril 74 2000 771 779
29. M.A. Okon, S.M. Laird, E.M. Tuckerman, and T.C. Li Serum androgen levels in women who have recurrent miscarriage and their correlation with marker of endometrial function Fertil Steril 69 1998 682 690 (Pubitemid 28188464)
30. S. Bussen, M. Sutterlin, and T. Steck Endocrine abnormalities during the follicular phase in women with recurrent spontaneous abortion Hum Reprod 14 1999 18 20 (Pubitemid 29046305)
31. G. Teklenburg, M. Salker, C. Heijnen, N.S. Macklon, and J.J. Brosens The molecular basis of recurrent pregnancy loss: impaired natural embryo selection Mol Hum Reprod 16 2010 886 895
32. G.J. Kops, N.D. de Ruiter, A.M. De Vries-Smits, D.R. Powell, J.L. Bos, and B.M. Burgering Direct control of the forkhead transcription factor AFX by protein kinase B Nature 398 1999 630 634 (Pubitemid 29183692)
33. Burnet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 199;96:857-68.
34. KIP1 Mol Cell Biol 20 2000 9138 9148 (Pubitemid 32246103)
35. A. Sunters, S. Fernandez de Mottos, M. Stahl, J.J. Brosens, G. Zoumpoulidou, and C.A. Saunders FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines J Biol Chem 278 2003 49795 49805 (Pubitemid 37548813)
36. V. Modur, R. Nagarajan, B.M. Evers, and J. Milbrandt FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer J Biol Chem 277 2002 47928 47937 (Pubitemid 36159321)
37. T. Suhara, H.S. Kim, L.A. Kirshenbaum, and K. Walsh Supression of Akt signaling induces Fas ligand expression: involvement of caspase and Jun kinase activation in Akt-mediated Fas ligand regulation Mol Cell Biol 22 2002 680 691 (Pubitemid 34027511)
38. P.F. Dijkers, R.H. Medema, J.W. Lammers, L. Koenderman, and P.J. Coffer Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1 Curr Biol 10 2000 1201 1204
39. R.H. Medema, G.J. Kops, J.L. Bos, and B.M. Burgering AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1 Nature 404 2000 782 787 (Pubitemid 30212408)
40. S. Nemoto, and T. Finkel Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway Science 295 2002 2450 2452 (Pubitemid 34270258)
41. M.A. Essers, S. Weijzen, A.M. de Vries-Smits, I. Saarloos, N.D. de Ruiter, J.L. Bos, and B.M. Burgering FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK EMBO J 23 2004 4802 4812 (Pubitemid 40069710)
42. Tran H, Brunet A, Grenier JM, Datta SR, Fornace AJ Jr, DiStefano PS, et al. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 2202;296;530-4.
43. H. Huang, D.C. Muddiman, and D.J. Tindall Androgens negative regulate forkhead transcription factor FKHR (FOXO1) through a proteolytic mechanism in prostate cancer cells J Biol Chem 279 2004 13866 13877 (Pubitemid 38468919)
44. P. Li, H. Lee, S. Guo, T.G. Unterman, G. Jenster, and W. Bai AKT-independent protection of prostate cancer cells from apoptosis mediated through complex formation between the androgen receptor and FKHR Mol Cell Biol 23 2003 104 118 (Pubitemid 36008505)