Androgens modulate the morphological characteristics of human endometrial stromal cells decidualized in vitro

Reproductive Sciences

Volumn 21, Issue 3, 2014, Pages 372-380

  Kajihara, Takeshi ^a   Tanaka, Kayoko ^a   Oguro, Tatsuo ^b   Tochigi, Hideno ^a   Prechapanich, Japarath ^a   Uchino, Satomi ^a   Itakura, Atsuo ^a   Šućurović, Sandra ^c,d   Murakami, Keisuke ^c   Brosens, Jan J ^c   Ishihara, Osamu ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b NIPPON MEDICAL SCHOOL CHIBA HOKUSOH HOSPITAL   (Japan)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF RIJEKA   (Croatia)

Author keywords

androgen; decidualization; endometrium; ultrastructure

Indexed keywords

8 BROMO CYCLIC AMP; ANDROGEN; FAT DROPLET; PROGESTERONE; ANDROSTANOLONE; BICALUTAMIDE; FLUTAMIDE;

ARTICLE; CELL EXPANSION; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; DECIDUALIZATION; DRUG EFFECT; ELECTRON MICROSCOPY; ENDOMETRIUM CELL; EXTRACELLULAR MATRIX; GAP JUNCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMAGE ANALYSIS; IN VITRO STUDY; PRIORITY JOURNAL; STROMA CELL; ADULT; CELL ENLARGEMENT; CELL JUNCTION; CELL ORGANELLE; CELL TRANSFORMATION; CONFOCAL MICROSCOPY; ENDOMETRIUM; ENDOMETRIUM STROMA CELL; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN CELL CULTURE; MICROFILAMENT; MOLECULAR WEIGHT; MORPHOLOGICAL TRAIT; PROTEIN EXPRESSION; ROUGH ENDOPLASMIC RETICULUM; WESTERN BLOTTING;

ANDROGEN; DECIDUALIZATION; ENDOMETRIUM; ULTRASTRUCTURE;

ADULT; ANDROGENS; CELLS, CULTURED; DECIDUA; ENDOMETRIUM; FEMALE; HUMANS; STROMAL CELLS;

EID: 84896891734     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719113497280     Document Type: Article

References (46)

1. Gellersen B, Brosens IA, Brosens JJ. Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin Reprod Med. 2007; 25 (6). 445-453
2. Brosens JJ, Gellersen B. Death or survival: progesterone-dependent cell fate decisions in the human endometrial stroma. J Mol Endcrinol. 2006; 36 (3). 389-398
3. Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in the normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol. 2002; 187 (5). 1416-1423
4. Mertens HJ, Heineman MJ, Koudstaal J, Theunissen P, Evers JL. Androgen receptor expression content in human endometrium. Eur J Obstet Gynecol Reprod Biol. 1996; 70 (1). 11-13
5. Slayden OD, Nayak NR, Burton KA, et al. Progesterone antagonists increase androgen receptor expression in the rhesus macaque and human endometrium. J Clin Endocrinol Metab. 2001; 86 (6). 2668-2679
6. Vermeulen-Meiners C, Poortman J, Nabuurs M, Thijssen JH. The endogenous concentration and subcellular distribution of androgens in normal human premenopausal endometrium, myometrium and vagina. Gynecol Endocrinol. 1988; 2 (2). 121-130
7. Cloke B, Huhtinen K, Fusi L, et al. The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium. Endocrinology. 2008; 149 (9). 4462-4474
8. Kajihara T, Tochigi H, Prechapanich J, et al. Androgen signaling decidualizaing endometrial stromal cells enhances resistance to oxidative stress. Fertil Steril. 2012; 97 (1). 185-191
9. Leitao B, Jones MC, Fusi L, et al. Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed oxidative stress signals. FASEB J. 2010; 24 (5). 1541-1551
10. Brosens JJ, Hayashi N, White JO. Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cell. Endocrinology. 1999; 140 (10). 4809-48020
11. Christian M, Zhang X, Schneider-Merck T, et al. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein β in differentiating human endometrial stromal cells. J Biol Chem. 2002; 277 (23). 20825-20832
12. Kajihara T, Uchino S, Suzuki M, Itakura A, Brosens JJ, Ishihara O. Human chorionic gonadotropin confers resistance to oxidative stress-induced apoptosis in decidualizing human endometrial stromal cells. Fertil Steril. 2011; 95 (4). 1302-1307
13. Schutte SC, Taylor RN. A tissue-engineered human endometrial stroma that responds to cues for secretory differentiation, decidualization, and menstruation. Fertil Steril. 2012; 97 (4). 997-1003
14. Gellersen B, Kempf R, Telgmann R, DiMattia GE. Nonpituitary human prolactin gene transcription is independent of Pit-1 and differentially controlled in lymphocytes and in endometrial stroma. Mol Endocrinol. 1994; 8 (3). 356-373
15. Lane B, Oxberry W, Mazella J, Tseng L. Decidualization of human endometrial stromal cells in vitro: effects of progestin and relaxin on the ultrastructure and production of decidual secretory proteins. Hum Reprod. 1994; 9 (2). 259-266
16. Wynn R. Ultrastructural development of the human decidua. Am J Obstet Gynecol. 1974; 118 (5). 652-670
17. Yu J, Wu J, Bagchi IC, Bagchi MK, Sidell N, Taylor RN. Disruption of gap junctions reduces biomarkers of decidualization and angiogenesis and increases inflammatory mediators in human endometrial stromal cell cultures. Mol Cell Endocrinol. 2011; 344 (1-2). 25-34
18. Shiina H, Matsumoto T, Sato T, et al. Premature ovarian failure in androgen receptor-deficient mice. Proc Natl Acad Sci USA. 2006; 103 (1). 224-229
19. Yeh S, Tsai MY, Xu Q, et al. 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. 2002; 99 (21). 13498-13503
20. Gelmann EP. Molecular biology of the androgen receptor. J Clin Oncol. 2002; 20 (13). 3001-3015
21. Vnader Griend DJ, Litvinov IV, Isaacs JT. Stabilizing androgen receptor in mitosis inhibits prostate cancer proliferation. Cell Cycle. 2007; 6 (6). 647-651
22. Walters KA, Allan CM, Jimenez M, et al. Female mice haploinsufficient for an inactivated androgen receptor (AR) exhibit age-dependent defects that resemble the AR null phenotype of dysfunctional late follicle development, ovulation, and fertility. Endocrinology. 2007; 148 (8). 3674-3684
23. Walters KA, McTavish KJ, Seneviratne MG, et al. Subfertile female androgen receptor knockout mice exhibit defects in neuroendocrine signaling, intraovarian function, and uterine development but not uterine function. Endocrinology. 2009; 150 (7). 3274-3282
24. Hu YC, Wang PH, Yeh S, et al. Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci USA. 2004; 101 (31). 11209-11214
25. Irwin JC, Quigley MM, Kirk D, Gwatkin RB, King RJ. Hormonal regulation of human endometrial cells in culture: an in vitro model for decidualization. Fertil Steril. 1989; 52 (5). 761-768
26. Lawn AM, Wilson EW, Finn CA. The ultrastructure of human decidual and precidual cells. J Reprod Fertil. 1971; 26 (1). 85-90
27. Singh R, Kaushik S, Wang Y, et al. Autophagy regulates lipid metabolism. Nature. 2009; 458 (7242). 1131-1135
28. Greenspan P, Mayer EP, Fowler SD. Nile Red: A selective fluorescent stain for intracellular lipid droplets. J Cell Biol. 1985; 100 (3). 965-973
29. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E. Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab. 2002; 87 (6). 2954-2959
30. Castracane VD, Stewart DR, Gimpel T, Overstreet JW, Lasley BL. Maternal serum androgens in human pregnancy: early increases within the cycle of conception. Hum Reprod. 1998; 13 (2). 460-464
31. Dawood MY, Saxena BB. Plasma testosterone and dihydrotestosterone in ovulatory and anovulatory cycles. Am J Obstet Gynecol. 1976; 126 (4). 430-435
32. Frattarelli JL, Peterson EH. Effect of androgen levels on in vitro fertilization cycles. Fertil Steril. 2004; 81 (6). 1713-1714
33. Abdalla HI, Billett A, Kan AK, et al. Obstetric outcome in 232 ovum donation pregnancies. Br J Obstet Gynaecol. 1998; 105 (3). 332-337
34. Boomsma CM, Fauser BC, Macklon NS. Pregnancy complications in women with polycystic ovary syndrome. Semin Reprod Med. 2008; 26 (1). 72-84
35. Cano F, Simon C, Remohi J, Pellicer A. Effect of aging on the female reproductive system: evidence for a role of uterine senescence in the decline in female fecundity. Fertil Steril. 1995; 64 (3). 584-589
36. Cleary-Goldman J, Malone FD, Vidaver J, et al. Impact of maternal age on obstetric outcome. Obstet Gynecol. 2005; 105 (5 pt 1). 983-990
37. Jacobsson B, Ladfors L, Milsom I. Advanced maternal age and adverse perinatal outcome. Obstet Gynecol. 2004; 104 (4). 727-733
38. Pados G, Camus M, Van Steirteghem A, Bonduelle M, Devroey P. The evolution and outcome of pregnancies from oocyte donation. Hum Reprod. 1994; 9 (3). 538-542
39. Reddy UM, Ko CW, Willinger M. Maternal age and the risk of stillbirth throughout pregnancy in the United States. Am J Obstet Gynecol. 2006; 195 (3). 764-770
40. Sagle M, Bishop K, Ridley N, et al. Recurrent early miscarriage and polycystic ovaries. BMJ. 1988; 297 (6655). 1027-1028
41. Bonney RC, Scanlon MJ, Jones DL, Reed MJ, James VH. Adrenal androgen concentrations in endometrium and plasma during the menstrual cycle. J Endocrinol. 1984; 101 (2). 181-188
42. Callewaert L, Verrijdt G, Haelens A, Claessens F. Differential effect of small ubiquitin-like modifier (SUMO)-ylation of the androgen receptor in the control of cooperativity on selective versus canonical response elements. Mol Endocrinol. 2004; 18 (6). 1438-1449
43. Cloke B, Shah K, Kaneda H, et al. The poly(c)-binding protein-1 regulates expression of the androgen receptor. Endocrinology. 2010; 151 (8). 3954-3964
44. Poukka H, Karvonen U, Janne OA, Palvimo JJ. Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc Natl Acad Sci USA. 2000; 97 (26). 14145-14150
45. Yeap BB, Krueger RG, Leedman PJ. Differential posttranscriptional regulation of androgen receptor gene expression by androgen in prostate and breast cancer cells. Endocrinology. 1999; 140 (7). 3282-3291
46. Yeap BB, Voon DC, Vivian JP, et al. Novel binding of HuR and poly(C)-binding protein to a conserved UC-rich motif within the 3′-untranslated region of the androgen receptor messenger RNA. J Biol Chem. 2002; 277 (30). 27183-27192