Progesterone increases manganese superoxide dismutase expression via a cAMP-dependent signaling mediated by noncanonical Wnt5a pathway in human endometrial stromal cells

Journal of Clinical Endocrinology and Metabolism

Volumn 95, Issue 11, 2010, Pages

  Matsuoka, Aki ^a   Kizuka, Fumie ^a   Lee, Lifa ^a   Tamura, Isao ^a   Taniguchi, Ken ^a   Asada, Hiromi ^a   Taketani, Toshiaki ^a   Tamura, Hiroshi ^a   Sugino, Norihiro ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIBUTYRYLCYTIDINE 3',5' PHOSPHATE; MANGANESE SUPEROXIDE DISMUTASE; MEDROXYPROGESTERONE ACETATE; MESSENGER RNA; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROGESTERONE; SOMATOMEDIN BINDING PROTEIN 1; WNT5A PROTEIN;

ADULT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DECIDUALIZATION; DRUG MECHANISM; ENDOMETRIUM CELL; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; WESTERN BLOTTING;

EID: 78049508632     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2010-0619     Document Type: Article

References (45)

1. Sugino N 2007 The role of oxygen radical-mediated signaling pathways in endometrial function. Placenta 28(Suppl A):S133-S136 (Pubitemid 46506050)
2. Gellersen B, Brosens J 2003 Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol 178:357-372
3. Freeman BA, Crapo JD 1982 Biology of disease: free radicals and tissue injury. Lab Invest 47:412-426
4. Balaban RS, Nemoto S, Finkel T 2005 Mitochondria, oxidants, and aging. Cell 120:483-495
5. Wong GH, Elwell JH, Oberley LW, Goeddel DV 1989 Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58:923-931
6. Lebovitz RM, Zhang H, Vogel H, Cartwright Jr J, Dionne L, Lu N, Huang S, Matzuk MM 1996 Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 93:9782-9787
7. Sugino N, Karube-Harada A, Sakata A, Takiguchi S, Kato H 2002 Nuclear factor-κB is required for tumor necrosis factor-α-induced manganese superoxide dismutase expression in human endometrial stromal cells. J Clin Endocrinol Metab 87:3845-3850
8. Sugino N, Karube-Harada A, Kashida S, Takiguchi S, Kato H 2002 Differential regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase by progesterone withdrawal in human endometrial stromal cells. Mol Hum Reprod 8:68-74 (Pubitemid 34097664)
9. Sugino N, Kashida S, Takiguchi S, Nakamura Y, Kato H 2000 Induction of superoxide dismutase by decidualization in human endometrial stromal cells. Mol Hum Reprod 6:178-184 (Pubitemid 30094281)
10. Telgmann R, Maronde E, Taskén K, Gellersen B 1997 Activated protein kinase A is required for differentiation-dependent transcription of the decidual prolactin gene in human endometrial stromal cells. Endocrinology 138:929-937
11. Brar AK, Frank GR, Kessler CA, Cedars MI, Handwerger S 1997 Progesterone-dependent decidualization of the human endometrium is mediated by cAMP. Endocrine 6:301-307
12. Kasahara K, Takakura K, Takebayashi K, Kimura F, Nakanishi K, Noda Y 2001 The role of human chorionic gonadotropin on decidualization of endometrial stromal cells in vitro. J Clin Endocrinol Metab 86:1281-1286
13. Sugino N, Karube-Harada A, Sakata A, Takiguchi S, Kato H 2002 Different mechanisms for the induction of copper-zinc superoxide dismutase and manganese superoxide dismutase by progesterone in human endometrial stromal cells. Hum Reprod 17:1709-1714 (Pubitemid 34790289)
14. Kim HP, Roe JH, Chock PB, Yim MB 1999 Transcriptional activation of the human manganese superoxide dismutase gene mediated by tetradecanoylphorbol acetate. J Biol Chem 274:37455-37460 (Pubitemid 129513939)
15. Moon RT, Bowerman B, Boutros M, Perrimon N 2002 The promise and perils of Wnt signaling through β-catenin. Science 296:1644-1646
16. Logan CY, Nusse R 2004 The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810
17. Clevers H 2006 Wnt/β-catenin signaling in development and disease. Cell 127:469-480
18. Veeman MT, Axelrod JD, Moon RT 2003 A second canon. Functions and mechanisms of β-catenin-independent Wnt signaling. Dev Cell 5:367-377
19. 2+ non-canonical pathway. J Biol Chem 282:28980-28990
20. Chen AE, Ginty DD, Fan CM 2005 Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433:317-322
21. Hansen C, Howlin J, Tengholm A, Dyachok O, Vogel WF, Nairn AC, Greengard P, Andersson T 2009 Wnt-5a-induced phosphorylation of DARPP-32 inhibits breast cancer cell migration in a CREB-dependent manner. J Biol Chem 284:27533-27543
22. Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, Bagchi MK, Bagchi IC 2007 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 282:31725-31732
23. Chen Q, Zhang Y, Lu J, Wang Q, Wang S, Cao Y, Wang H, Duan E 2009 Embryo-uterine cross-talk during implantation: the role of Wnt signaling. Mol Hum Reprod 15:215-221
24. Hayashi K, Erikson DW, Tilford SA, Bany BM, Maclean 2nd JA, Rucker 3rd EB, Johnson GA, Spencer TE 2009 Wnt genes in the mouse uterus: potential regulation of implantation. Biol Reprod 80:989-1000
25. Bui TD, Zhang L, Rees MC, Bicknell R, Harris AL 1997 Expression and hormone regulation of Wnt2, 3, 4, 5a, 7a, 7b and 10b in normal human endometrium and endometrial carcinoma. Br J Cancer 75:1131-1136
26. Tulac S, Nayak NR, Kao LC, Van Waes M, Huang J, Lobo S, Germeyer A, Lessey BA, Taylor RN, Suchanek E, Giudice LC 2003 Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium. J Clin Endocrinol Metab 88:3860-3866
27. Torii K, Nishizawa K, Kawasaki A, Yamashita Y, Katada M, Ito M, Nishimoto I, Terashita K, Aiso S, Matsuoka M 2008 Anti-apoptotic action of Wnt5a in dermal fibroblasts is mediated by the PKA signaling pathways. Cell Signal 20:1256-1266
28. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S 2005 Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by β-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem 280:41342-41351
29. 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
30. Noyes RW, Hertig AT, Rock J 1975 Dating the endometrial biopsy. Am J Obstet Gynecol 122:262-263
31. Yoshino O, Osuga Y, Hirota Y, Koga K, Yano T, Tsutsumi O, Taketani Y 2003 Akt as a possible intracellular mediator for decidualization in human endometrial stromal cells. Mol Hum Reprod 9:265-269
32. Kummitha CM, Mayle KM, Christman 2nd MA, Deosarkar SP, Schwarz AL, McCall KD, Kohn LD, Malgor R, Goetz DJ 2010 A sandwich ELISA for the detection of Wnt5a. J Immunol Methods 352:38-44
33. Giudice LC, Dsupin BA, Irwin JC 1992 Steroid and peptide regulation of insulin-like growth factor-binding proteins secreted by human endometrial stromal cells is dependent on stromal differentiation. J Clin Endocrinol Metab 75:1235-1241
34. Francis J, Rai R, Sebire NJ, El-Gaddal S, Fernandes MS, Jindal P, Lokugamage A, Regan L, Brosens JJ 2006 Impaired expression of endometrial differentiation markers and complement regulatory proteins in patients with recurrent pregnancy loss associated with antiphospholipid syndrome. Mol Hum Reprod 12:435-442
35. 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
36. Kaneda A, Kaminishi M, Sugimura T, Ushijima T 2004 Decreased expression of the seven ARP2/3 complex genes in human gastric cancers. Cancer Lett 212:203-210
37. Asada H, Yamagata Y, Taketani T, Matsuoka A, Tamura H, Hattori N, Ohgane J, Shiota K, Sugino N 2008 Potential link between estrogen receptor-α gene hypomethylation and uterine fibroid formation. Mol Hum Reprod 14:539-545
38. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ 1951 Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
39. Hunter T, Karin M 1992 The regulation of transcription by phosphorylation. Cell 70:375-387
40. Zhang Q, Liu SH, Erikson M, Lewis M, Unemori E 2002 Relaxin activates the MAP kinase pathway in human endometrial stromal cells. J Cell Biochem 85:536-544
41. Maymo JL, Prez AP, Duenas JL, Calvo JC, Sanchez-Margalet V, Varone CL 2010 Regulation of placental leptin expression by cyclic adenosine 5′-monophosphate involves cross talk between protein kinase A and mitogen-activated protein kinase signaling pathways. Endocrinology 151:3738-3751
42. Zhu Y, Bond J, Thomas P 2003 Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progesterone receptor. Proc Natl Acad Sci USA 100:2237-2242
43. Ni Z, Anini Y, Fang X, Mills G, Brubaker PL, Jin T 2003 Transcriptional activation of the proglucagon gene by lithium and beta-catenin in intestinal endocrine L cells. J Biol Chem 278:1380-1387
44. Roy L, McDonald CA, Jiang C, Maroni D, Zeleznik AJ, Wyatt TA, Hou X, Davis JS 2009 Convergence of 3′,5′-cyclic adenosine 5′-monophosphate/protein kinase A and glycogen synthase kinase-3β/β-catenin signaling in corpus luteum progesterone synthesis. Endocrinology 150:5036-5045
45. Grotewold L, Rüther U 2002 The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and c-Jun and modulates programmed cell death. EMBO J 21:966-975