GPR30 activation opposes estrogen-dependent uterine growth via inhibition of stromal ERK1/2 and Estrogen receptor alpha (ERα) phosphorylation signals

Endocrinology

Volumn 152, Issue 4, 2011, Pages 1434-1447

  Gao, Fei ^a,b   Ma, Xinghong ^a   Ostmann, Alicia B ^a   Das, Sanjoy K ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b NORTHEAST FORESTRY UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 30; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENDOMETRIUM; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; GROWTH REGULATION; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; UTERUS GROWTH;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CYCLOPENTANES; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; IMMUNOHISTOCHEMISTRY; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; OVARIECTOMY; PHOSPHORYLATION; QUINOLINES; RECEPTORS, G-PROTEIN-COUPLED; UTERUS;

EID: 79953168739     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1368     Document Type: Article

References (65)

1. Couse JF, Korach KS 1999 Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358-417
2. Stampfer MJ, Colditz GA, Willett WC, Manson JE, Rosner B, Speizer FE, Hennekens CH 1991 Postmenopausal estrogen therapy and cardiovascular disease. Ten-year follow-up from the Nurses' Health Study. N Engl J Med 325:756-762
3. McDonnell DP, Norris JD 2002 Connections and regulation of the human estrogen receptor. Science 296:1642-1644 (Pubitemid 34579150)
4. Tsai MJ, O'Malley BW 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63:451-486 (Pubitemid 24218640)
5. Beato M, Herrlich P, Schütz G 1995 Steroid hormone receptors: many actors in search of a plot. Cell 83:851-857 (Pubitemid 26006527)
6. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H 2004 Molecular cues to implantation. Endocr Rev 25:341-373 (Pubitemid 38780665)
7. Das SK, Tan J, Raja S, Halder J, Paria BC, Dey SK 2000 Estrogen targets genes involved in the protein processing, calcium homeostasis, and Wnt signaling in the mouse uterus independent of estrogen receptor-α and -α. J Biol Chem 275:28834-28842
8. Hewitt SC, Deroo BJ, Hansen K, Collins J, Grissom S, Afshari CA, Korach KS 2003 Estrogen receptor-dependent genomic responses in the uterus mirror the biphasic physiological response to estrogen. Mol Endocrinol 17:2070-2083 (Pubitemid 37281798)
9. Das SK, Taylor JA, Korach KS, Paria BC, Dey SK, Lubahn DB 1997 Estrogenic responses in estrogen receptor-α deficient mice reveal a distinct estrogen signaling pathway. Proc Natl Acad Sci USA 94: 12786-12791 (Pubitemid 27518429)
10. Das SK, Tan J, Johnson DC, Dey SK 1998 Differential spatiotemporal regulation of lactoferrin and progesterone receptor genes in the mouse uterus by primary estrogen, catechol estrogen, and xenoestrogen. Endocrinology 139:2905-2915 (Pubitemid 28512403)
11. Hou X, Tan Y, Li M, Dey SK, Das SK 2004 Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol 18:3035-3049 (Pubitemid 39577924)
12. Ray S, Hou X, Zhou HE, Wang H, Das SK 2006 Bip is a molecular link between the phase I and phase II estrogenic responses in uterus. Mol Endocrinol 20:1825-1837 (Pubitemid 44148087)
13. O'Brien JE, Peterson TJ, Tong MH, Lee EJ, Pfaff LE, Hewitt SC, Korach KS, Weiss J, Jameson JL 2006 Estrogen-induced proliferation of uterine epithelial cells is independent of estrogen receptor α binding to classical estrogen response elements. J Biol Chem 281:26683-26692 (Pubitemid 44401877)
14. Watanabe H, Suzuki A, Kobayashi M, Takahashi E, Itamoto M, Lubahn DB, Handa H, Iguchi T 2003 Analysis of temporal changes in the expression of estrogen-regulated genes in the uterus. J Mol Endocrinol 30:347-358 (Pubitemid 36722623)
15. Ray S, Xu F, Wang H, Das SK 2008 Cooperative control via lymphoid enhancer factor 1/T cell factor 3 and estrogen receptor-α for uterine gene regulation by estrogen. Mol Endocrinol 22:1125-1140 (Pubitemid 351629613)
16. Stewart PJ, Webster RA 1983 Intrauterine injection of cholera toxin induces estrogen-like uterine growth. Biol Reprod 29:671-679 (Pubitemid 14249433)
17. Aronica SM, Kraus WL, Katzenellenbogen BS 1994 Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc Natl Acad Sci USA 91:8517-8521 (Pubitemid 24273695)
18. Rajkumar K 1993 Effect of protein kinase-C inhibitor on estradiol-induced deoxyribonucleic acid synthesis in rats. Steroids 58:100-10
19. Pietras RJ, Szego CM 1977 Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265:69-72 (Pubitemid 8004314)
20. Hammes SR, Levin ER 2007 Extranuclear steroid receptors: nature and actions. Endocr Rev 28:726-741 (Pubitemid 350294293)
21. Valverde MA, Rojas P, Amigo J, Cosmelli D, Orio P, Bahamonde MI, Mann GE, Vergara C, Latorre R 1999 Acute activation of Maxi-K channels (hSlo) by estradiol binding to the β subunit. Science 285:1929-1931
22. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER 2005 A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307:1625-1630 (Pubitemid 40354745)
23. Thomas P, Pang Y, Filardo EJ, Dong J 2005 Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146:624-632 (Pubitemid 40129818)
24. Filardo EJ, Quinn JA, Bland KI, Frackelton Jr AR 2000 Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14:1649-1660
25. Filardo EJ, Quinn JA, Frackelton Jr AR, Bland KI 2002 Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol 16:70-84
26. Vivacqua A, Bonofiglio D, Albanito L, Madeo A, Rago V, Carpino A, Musti AM, Picard D, Andò S, Maggiolini M 2006 17β-estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the g protein-coupled receptor GPR30. Mol Pharmacol 70:1414-1423 (Pubitemid 44435994)
27. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Andò S, Maggiolini M 2006 The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17β-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol 20:631-646 (Pubitemid 43291214)
28. Albanito L, Sisci D, Aquila S, Brunelli E, Vivacqua A, Madeo A, Lappano R, Pandey DP, Picard D, Mauro L, Andò S, Maggiolini M 2008 Epidermal growth factor induces G protein-coupled receptor 30 expression in estrogen receptor-negative breast cancer cells. Endocrinology 149:3799-3808
29. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Andò S, Maggiolini M 2007 G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67:1859-1866 (Pubitemid 46383413)
30. Wang C, Dehghani B, Magrisso IJ, Rick EA, Bonhomme E, Cody DB, Elenich LA, Subramanian S, Murphy SJ, Kelly MJ, Rosenbaum JS, Vandenbark AA, Offner H 2008 GPR30 contributes to estrogen-induced thymic atrophy. Mol Endocrinol 22:636-648 (Pubitemid 351397791)
31. Otto C, Fuchs I, Kauselmann G, Kern H, Zevnik B, Andreasen P, Schwarz G, Altmann H, Klewer M, Schoor M, Vonk R, Fritzemeier KH 2009 GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol Reprod 80:34-41
32. Mårtensson UE, Salehi SA, Windahl S, Gomez MF, Swärd K, Daszkiewicz-Nilsson J, Wendt A, Andersson N, Hellstrand P, Grände PO, Owman C, Rosen CJ, Adamo ML, Lundquist I, Rorsman P, Nilsson BO, Ohlsson C, Olde B, Leeb-Lundberg LM 2009 Deletion of the G protein-coupled receptor 30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice. Endocrinology 150:687-698
33. Isensee J, Meoli L, Zazzu V, Nabzdyk C, Witt H, Soewarto D, Effertz K, Fuchs H, Gailus-Durner V, Busch D, Adler T, de Angelis MH, Irgang M, Otto C, Noppinger PR 2009 Expression pattern of G protein-coupled receptor 30 in LacZ reporter mice. Endocrinology 150:1722-1730
34. Bologa CG, Revankar CM, Young SM, Edwards BS, Arterburn JB, Kiselyov AS, Parker MA, Tkachenko SE, Savchuck NP, Sklar LA, Oprea TI, Prossnitz ER 2006 Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol 2:207-212
35. Otto C, Rohde-Schulz B, Schwarz G, Fuchs I, Klewer M, Brittain D, Langer G, Bader B, Prelle K, Nubbemeyer R, Fritzemeier KH 2008 G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology 149:4846-4856
36. Dennis MK, Burai R, Ramesh C, Petrie WK, Alcon SN, Nayak TK, Bologa CG, Leitao A, Brailoiu E, Deliu E, Dun NJ, Sklar LA, Hathaway HJ, Arterburn JB, Oprea TI, Prossnitz ER 2009 In vivo effects of a GPR30 antagonist. Nat Chem Biol 5:421-427
37. Paria BC, Lim H, Wang XN, Liehr J, Das SK, Dey SK 1998 Coordination of differential effects of primary estrogen and catecholestrogen on two distinct targets mediates embryo implantation in the mouse. Endocrinology 139:5235-5246 (Pubitemid 28533473)
38. Tan J, Raja S, Davis MK, Tawfik O, Dey SK, Das SK 2002 Evidence for coordinated interaction of cyclin D3 with p21 and cdk6 in directing the development of uterine stromal cell decidualization and polyploidy during implantation. Mech Dev 111:99-113 (Pubitemid 34136982)
39. Tan Y, Li M, Cox S, Davis MK, Tawfik O, Paria BC, Das SK 2004 HB-EGF directs stromal cell polyploidy and decidualization via cyclin D3 during implantation. Dev Biol 265:181-195 (Pubitemid 38018830)
40. Ray S, Xu F, Li P, Sanchez NS, Wang H, Das SK 2007 Increased level of cellular Bip critically determines estrogenic potency for a xenoestrogen kepone in the mouse uterus. Endocrinology 148:4774-4785 (Pubitemid 47481515)
41. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M 2000 Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852
42. Liu YH, Teng CT 1991 Characterization of estrogen-responsive mouse lactoferrin promoter. J Biol Chem 266:21880-21885 (Pubitemid 121000263)
43. Couse JF, Curtis SW, Washburn TF, Lindzey J, Golding TS, Lubahn DB, Smithies O, Korach KS 1995 Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol Endocrinol 9:1441-1454
44. Kirkland JL, Murthy L, Stancel GM 1992 Progesterone inhibits the estrogen-induced expression of c-fos messenger ribonucleic acid in the uterus. Endocrinology 130:3223-3230
45. Wang XN, Das SK, Damm D, Klagsbrun M, Abraham JA, Dey SK 1994 Differential regulation of heparin-binding epidermal growth factor-like growth factor in the adult ovariectomized mouse uterus by progesterone and estrogen. Endocrinology 135:1264-1271 (Pubitemid 24271225)
46. Migliaccio A, Di Domenico M, Castoria G, de Falco A, Bontempo P, Nola E, Auricchio F 1996 Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 15:1292-1300
47. Song RX, McPherson RA, Adam L, Bao Y, Shupnik M, Kumar R, Santen RJ 2002 Linkage of rapid estrogen action to MAPK activation by ERα-Shc association and Shc pathway activation. Mol Endocrinol 16:116-127 (Pubitemid 34044502)
48. Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H, Metzger D, Chambon P 1995 Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270:1491-1494
49. Chen D, Riedl T, Washbrook E, Pace PE, Coombes RC, Egly JM, Ali S 2000 Activation of estrogen receptor α by S118 phosphorylation involves a ligand-dependent interaction with TFIIH and participation of CDK7. Mol Cell 6:127-137
50. Wang H, Tranguch S, Xie H, Hanley G, Das SK, Dey SK 2005 Variation in commercial rodent diets induces disparate molecular and physiological changes in the mouse uterus. Proc Natl Acad Sci USA 102:9960-9965 (Pubitemid 40993675)
51. Chan QK, Lam HM, Ng CF, Lee AY, Chan ES, Ng HK, Ho SM, Lau KM 2010 Activation of GPR30 inhibits the growth of prostate cancer cells through sustained activation of Erk1/2, c-jun/c-fos-dependent upregulation of p21, and induction of G(2) cell-cycle arrest. Cell Death Differ 17:1511-1523
52. Ahola TM, Manninen T, Alkio N, Ylikomi T 2002 G protein-coupled receptor 30 is critical for a progestin-induced growth inhibition in MCF-7 breast cancer cells. Endocrinology 143:3376-3384 (Pubitemid 34925712)
53. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H 1984 Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133:1710-1715 (Pubitemid 14035254)
54. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O 1993 Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90:11162-11166 (Pubitemid 23354389)
55. Weihua Z, Saji S, Mäkinen S, Cheng G, Jensen EV, Warner M, Gustafsson JA 2000 Estrogen receptor (ER) β, a modulator of ERα in the uterus. Proc Natl Acad Sci USA 97:5936-5941
56. Ariazi EA, Brailoiu E, Yerrum S, Shupp HA, Slifker MJ, Cunliffe HE, Black MA, Donato AL, Arterburn JB, Oprea TI, Prossnitz ER, Dun NJ, Jordan VC 2010 The G protein-coupled receptor GPR30 inhibits proliferation of estrogen receptor-positive breast cancer cells. Cancer Res 70:1184-1194
57. Lupien M, Eeckhoute J, Meyer CA, Krum SA, Rhodes DR, Liu XS, Brown M 2009 Coactivator function defines the active estrogen receptor α cistrome. Mol Cell Biol 29:3413-3423
58. Klotz DM, Hewitt SC, Ciana P, Raviscioni M, Lindzey JK, Foley J, Maggi A, DiAugustine RP, Korach KS 2002 Requirement of estrogen receptor-α in insulin-like growth factor-1 (IGF-1)-induced uterine responses and in vivo evidence for IGF-1/estrogen receptor crosstalk. J Biol Chem 277:8531-8537 (Pubitemid 34968316)
59. Madak-Erdogan Z, Lupien M, Stossi F, Brown M, Katzenellenbogen BS 2011 Genomic collaboration of estrogen receptor α and extracellular signal-regulated kinase 2 in regulating gene and proliferation programs. Mol Cell Biol 31:226-236
60. Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J, Korach KS, Taylor J, Lubahn DB, Cunha GR 1997 Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci USA 94:6535-6540 (Pubitemid 27270720)
61. Buchanan DL, Setiawan T, Lubahn DB, Taylor JA, Kurita T, Cunha GR, Cooke PS 1999 Tissue compartment-specific estrogen receptor- α participation in the mouse uterine epithelial secretory response. Endocrinology 140:484-491 (Pubitemid 29011195)
62. Kolkova Z, Noskova V, Ehinger A, Hansson S, Casslen B 2010 G protein-coupled estrogen receptor 1 (GPER, GPR 30) in normal human endometrium and early pregnancy decidua. Mol Hum Reprod 16:743-751
63. Smith HO, Leslie KK, Singh M, Qualls CR, Revankar CM, Joste NE, Prossnitz ER 2007 GPR30: a novel indicator of poor survival for endometrial carcinoma. Am J Obstet Gynecol 196:386.e381-e389; discussion 386.e389-e311
64. Gingerich S, Kim GL, Chalmers JA, Koletar MM, Wang X, Wang Y, Belsham DD 2010 Estrogen receptor α and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience 170:54-66
65. Weil BR, Manukyan MC, Herrmann JL, Wang Y, Abarbanell AM, Poynter JA, Meldrum DR 2010 Signaling via GPR30 protects the myocardium from ischemia/reperfusion injury. Surgery 148:436-443