GPER functions as a tumor suppressor in MCF-7 and SK-BR-3 breast cancer cells

Journal of Cancer Research and Clinical Oncology

Volumn 140, Issue 4, 2014, Pages 663-671

  Weißenborn, Christine ^a   Ignatov, Tanja ^a   Poehlmann, Angela ^a   Wege, Anja K ^b   Costa, Serban D ^a   Zenclussen, Ana Claudia ^a   Ignatov, Atanas ^a  

^a OVG University Clinic Magdeburg   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Breast cancer; GPER; GPR30; Tumor suppressor

Indexed keywords

CHEMOKINE RECEPTOR AGONIST; G 1; G PROTEIN COUPLED RECEPTOR 30; HISTONE H3; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CANCER PATIENT; CELL CYCLE M PHASE; CELL PROLIFERATION; CELL SURFACE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HUMAN; HUMAN CELL; MCF 7 CELL LINE; METHYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRIPLE NEGATIVE BREAST CANCER;

APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CYCLOPENTANES; DNA METHYLATION; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; PROMOTER REGIONS, GENETIC; QUINOLINES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 84899477541     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-014-1598-2     Document Type: Article

References (51)

1. Ahola TM, Alkio N, Manninen T, Ylikomi T (2002a) Progestin and G protein-coupled receptor 30 inhibit mitogen-activated protein kinase activity in MCF-7 breast cancer cells. Endocrinology 143:4620-4626 (Pubitemid 35397603)
2. Ahola TM, Manninen T, Alkio N, Ylikomi T (2002b) 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)
3. Aihara M, Yamamoto S, Nishioka H, Inoue Y, Hamano K, Oka M, Mizukami Y (2012) Optimizing high-resolution melting analysis for the detection of mutations of GPR30/GPER-1 in breast cancer. Gene 501:118-126
4. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Ando S, Maggiolini M (2007) G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17 beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67:1859-1866 (Pubitemid 46383413)
5. Albanito L, Sisci D, Aquila S, Brunelli E, Vivacqua A, Madeo A, Lappano R, Pandey DP, Picard D, Mauro L, Ando 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
6. Arias-Pulido H, Royce M, Gong Y, Joste N, Lomo L, Lee SJ, Chaher N, Verschraegen C, Lara J, Prossnitz ER, Cristofanilli M (2010) GPR30 and estrogen receptor expression: new insights into hormone dependence of inflammatory breast cancer. Breast Cancer Res Treat 123:51-58
7. 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
8. 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
9. 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
10. Chimento A, Casaburi I, Bartucci M, Patrizii M, Dattilo R, Avena P, Ando S, Pezzi V, Sirianni R (2013) Selective GPER activation decreases proliferation and activates apoptosis in tumor Leydig cells. Cell Death Dis 4:e747
11. Choi HJ, Fukui M, Zhu BT (2011) Role of cyclin B1/Cdc2 up-regulation in the development of mitotic prometaphase arrest in human breast cancer cells treated with nocodazole. PLoS ONE 6:e24312
12. De Marco P, Bartella V, Vivacqua A, Lappano R, Santolla MF, Morcavallo A, Pezzi V, Belfiore A, Maggiolini M (2012) Insulin-like growth factor-I regulates GPER expression and function in cancer cells. Oncogene 32(6):678-688
13. 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
14. Dorsam RT, Gutkind JS (2007) G-protein-coupled receptors and cancer. Nat Rev Cancer 7:79-94 (Pubitemid 46164746)
15. Du GQ, Zhou L, Chen XY, Wan XP, He YY (2012) The G protein-coupled receptor GPR30 mediates the proliferative and invasive effects induced by hydroxytamoxifen in endometrial cancer cells. Biochem Biophys Res Commun 420:343-349
16. Esteller M, Corn PG, Baylin SB, Herman JG (2001) A gene hypermethylation profile of human cancer. Cancer Res 61:3225-3229 (Pubitemid 32695003)
17. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr (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
18. Filardo EJ, Graeber CT, Quinn JA, Resnick MB, Giri D, DeLellis RA, Steinhoff MM, Sabo E (2006) Distribution of GPR30, a seven membrane-spanning estrogen receptor, in primary breast cancer and its association with clinicopathologic determinants of tumor progression. Clin Cancer Res 12:6359-6366 (Pubitemid 44799705)
19. Gao F, Ma X, Ostmann AB, Das SK (2011) GPR30 activation opposes estrogen-dependent uterine growth via inhibition of stromal ERK1/2 and estrogen receptor alpha (ERalpha) phosphorylation signals. Endocrinology 152:1434-1447
20. Hans F, Dimitrov S (2001) Histone H3 phosphorylation and cell division. Oncogene 20:3021-3027 (Pubitemid 32553556)
21. Holm A, Baldetorp B, Olde B, Leeb-Lundberg LM, Nilsson BO (2011) The GPER1 agonist G-1 attenuates endothelial cell proliferation by inhibiting DNA synthesis and accumulating cells in the S and G2 phases of the cell cycle. J Vasc Res 48:327-335
22. 2+ release by activating the sphingosine-kinase pathway. Biochem Biophys Res Commun 311:329-336
23. Ignatov A, Bischoff J, Schwarzenau C, Krebs T, Kuester D, Herrmann K, Costa SD, Roessner A, Semczuk A, Schneider-Stock R (2008) P16 alterations increase the metastatic potential of endometrial carcinoma. Gynecol Oncol 111:365-371
24. Ignatov A, Bischoff J, Ignatov T, Schwarzenau C, Krebs T, Kuester D, Costa SD, Roessner A, Semczuk A, Schneider-Stock R (2009a) APC promoter hypermethylation is an early event in endometrial tumorigenesis. Cancer Sci 101(2):321-327
25. Ignatov A, Ignatov T, Roessner A, Costa SD, Kalinski T (2009b) Role of GPR30 in the mechanisms of tamoxifen resistance in breast cancer MCF-7 cells. Breast Cancer Res Treat 123(1):87-96
26. Ignatov A, Ignatov T, Weissenborn C, Eggemann H, Bischoff J, Semczuk A, Roessner A, Costa SD, Kalinski T (2011) G-protein-coupled estrogen receptor GPR30 and tamoxifen resistance in breast cancer. Breast Cancer Res Treat 128:457-466
27. Ignatov T, Modl S, Thulig M, Weissenborn C, Treeck O, Ortmann O, Zenclussen A, Costa SD, Kalinski T, Ignatov A (2013a) GPER-1 acts as a tumor suppressor in ovarian cancer. J Ovarian Res 6:51
28. Ignatov T, Weissenborn C, Poehlmann A, Lemke A, Semczuk A, Roessner A, Costa SD, Kalinski T, Ignatov A (2013b) GPER-1 expression decreases during breast cancer tumorigenesis. Cancer Invest 31:309-315
29. Kuo WH, Chang LY, Liu DL, Hwa HL, Lin JJ, Lee PH, Chen CN, Lien HC, Yuan RH, Shun CT, Chang KJ, Hsieh FJ (2007) The interactions between GPR30 and the major biomarkers in infiltrating ductal carcinoma of the breast in an Asian population. Taiwan J Obstet Gynecol 46:135-145 (Pubitemid 47236783)
30. Li LC, Dahiya R (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18:1427-1431
31. Liu Q, Li JG, Zheng XY, Jin F, Dong HT (2009) Expression of CD133, PAX2, ESA, and GPR30 in invasive ductal breast carcinomas. Chin Med J (Engl) 122:2763-2769
32. Lubig J, Lattrich C, Springwald A, Haring J, Schuler S, Ortmann O, Treeck O (2012) Effects of a combined treatment with GPR30 agonist G-1 and herceptin on growth and gene expression of human breast cancer cell lines. Cancer Invest 30:372-379
33. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, Ando S (2004) The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17 beta-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279:27008-27016 (Pubitemid 38812536)
34. Osborne C, Wilson P, Tripathy D (2004) Oncogenes and tumor suppressor genes in breast cancer: potential diagnostic and therapeutic applications. Oncologist 9:361-377 (Pubitemid 39014548)
35. Payne SR, Kemp CJ (2005) Tumor suppressor genetics. Carcinogenesis 26:2031-2045 (Pubitemid 41672190)
36. Poola I, Abraham J, Liu A, Marshalleck JJ, Dewitty RL (2008) The cell surface estrogen receptor, G protein- coupled receptor 30 (GPR30), is markedly down regulated during breast tumorigenesis. Breast Cancer (Auckl) 1:65-78
37. Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ (2008) Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 70:165-190 (Pubitemid 351738176)
38. 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)
39. Ruan SQ, Wang SW, Wang ZH, Zhang SZ (2012a) Regulation of HRG-beta1-induced proliferation, migration and invasion of MCF-7 cells by upregulation of GPR30 expression. Mol Med Rep 6:131-138
40. Ruan SQ, Wang ZH, Wang SW, Fu ZX, Xu KL, Li DB, Zhang SZ (2012b) Heregulin-beta1-induced GPR30 upregulation promotes the migration and invasion potential of SkBr 3 breast cancer cells via ErbB2/ErbB3-MAPK/ERK pathway. Biochem Biophys Res Commun 420:385-390
41. Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, Dolaptchieva M, Alexander T, Taran A, Malfertheiner SF, Costa SD, Zimmermann G, Nitschke C, Volk HD, Alexander H, Gunzer M, Zenclussen AC (2009) Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol 182:5488-5497
42. 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 196:386-389
43. Smith HO, Arias-Pulido H, Kuo DY, Howard T, Qualls CR, Lee SJ, Verschraegen CF, Hathaway HJ, Joste NE, Prossnitz ER (2009) GPR30 predicts poor survival for ovarian cancer. Gynecol Oncol 114:465-471
44. Song SH, Han SW, Bang YJ (2011) Epigenetic-based therapies in cancer: progress to date. Drugs 71:2391-2403
45. Teng J, Wang ZY, Prossnitz ER, Bjorling DE (2008) The G protein-coupled receptor GPR30 inhibits human urothelial cell proliferation. Endocrinology 149:4024-4034
46. 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)
47. Toh WH, Nam SY, Sabapathy K (2010) An essential role for p73 in regulating mitotic cell death. Cell Death Differ 17:787-800
48. Tu G, Hu D, Yang G, Yu T (2009) The correlation between GPR30 and clinicopathologic variables in breast carcinomas. Technol Cancer Res Treat 8:231-234
49. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Ando S, Maggiolini M (2006) The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17beta-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol 20:631-646 (Pubitemid 43291214)
50. Vivacqua A, Romeo E, De Marco P, De Francesco EM, Abonante S, Maggiolini M (2012) GPER mediates the Egr-1 expression induced by 17beta-estradiol and 4-hydroxitamoxifen in breast and endometrial cancer cells. Breast Cancer Res Treat 133:1025-1035
51. Wang C, Lv X, Jiang C, Davis JS (2012) The putative G-protein coupled estrogen receptor agonist G-1 suppresses proliferation of ovarian and breast cancer cells in a GPER-independent manner. Am J Transl Res 4:390-402