GPER functions as a tumor suppressor in triple-negative breast cancer cells

Journal of Cancer Research and Clinical Oncology

Volumn 140, Issue 5, 2014, Pages 713-723

  Weißenborn, Christine ^a   Ignatov, Tanja ^a   Ochel, Hans Joachim ^a   Costa, Serban Dan ^a   Zenclussen, Ana Claudia ^a   Ignatova, Zoya ^b   Ignatov, Atanas ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Breast cancer; GPER; GPR30; TNBC; Tumor suppression

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CASPASE 3; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; CYTOKINE RECEPTOR AGONIST; G 1 AGONIST; G PROTEIN COUPLED RECEPTOR 30; HISTONE H3; PROPIDIUM IODIDE; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; APOPTOSIS ASSAY; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER GROWTH; CANCER RADIOTHERAPY; CELL CYCLE ARREST; CELL CYCLE M PHASE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; EPIGENETICS; G2 PHASE CELL CYCLE CHECKPOINT; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; TRIPLE NEGATIVE BREAST CANCER; WESTERN BLOTTING;

APOPTOSIS; CARCINOGENESIS; CASPASE 3; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLOPENTANES; FEMALE; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; QUINOLINES; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84901587405     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-014-1620-8     Document Type: Article

References (50)

1. 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)
2. 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 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67:1859-1866 (Pubitemid 46383413)
3. 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. 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
10. 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
11. Dorsam RT, Gutkind JS (2007) G-protein-coupled receptors and cancer. Nat Rev Cancer 7:79-94 (Pubitemid 46164746)
12. Esteller M, Corn PG, Baylin SB, Herman JG (2001) A gene hypermethylation profile of human cancer. Cancer Res 61:3225-3229 (Pubitemid 32695003)
13. Fan P, Yue W, Wang JP, Aiyar S, Li Y, Kim TH, Santen RJ (2009) Mechanisms of resistance to structurally diverse antiestrogens differ under premenopausal and postmenopausal conditions: evidence from in vitro breast cancer cell models. Endocrinology 150:2036-2045
14. Fei P, El Deiry WS (2003) P53 and radiation responses. Oncogene 22:5774-5783 (Pubitemid 37176699)
15. 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
16. Filardo EJ, Quinn JA, Frackelton AR Jr, 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 (Pubitemid 34044499)
17. 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)
18. Fujiwara S, Terai Y, Kawaguchi H, Takai M, Yoo S, Tanaka Y, Tanaka T, Tsunetoh S, Sasaki H, Kanemura M, Tanabe A, Yamashita Y, Ohmichi M (2012) GPR30 regulates the EGFR-Akt cascade and predicts lower survival in patients with ovarian cancer. J Ovarian Res 5:35
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. Girgert R, Emons G, Grundker C (2012) Inactivation of GPR30 reduces growth of triple-negative breast cancer cells: possible application in targeted therapy. Breast Cancer Res Treat 134:199-205
21. Hans F, Dimitrov S (2001) Histone H3 phosphorylation and cell division. Oncogene 20:3021-3027 (Pubitemid 32553556)
22. 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
23. Ignatov A, Lintzel J, Kreienkamp HJ, Schaller HC (2003) Sphingosine-1-phosphate is a high-affinity ligand for the G protein-coupled receptor GPR6 from mouse and induces intracellular Ca2+ release by activating the sphingosine-kinase pathway. Biochem Biophys Res Commun 311:329-336 (Pubitemid 37340081)
24. 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
25. Ignatov A, Bischoff J, Ignatov T, Schwarzenau C, Krebs T, Kuester D, Costa SD, Roessner A, Semczuk A, Schneider-Stock R (2010a) APC promoter hypermethylation is an early event in endometrial tumorigenesis. Cancer Sci 101(2):321-327
26. Ignatov T, Eggemann H, Semczuk A, Smith B, Bischoff J, Roessner A, Costa SD, Kalinski T, Ignatov A (2010b) Role of GPR30 in endometrial pathology after tamoxifen for breast cancer. Am J Obstet Gynecol 203:595-16
27. Ignatov A, Ignatov T, Roessner A, Costa SD, Kalinski T (2010c) Role of GPR30 in the mechanisms of tamoxifen resistance in breast cancer MCF-7 cells. Breast Cancer Res Treat 123:87-96
28. 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
29. 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
30. 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
31. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51:6304-6311
32. 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)
33. Leblanc K, Sexton E, Parent S, Belanger G, Dery MC, Boucher V, Asselin E (2007) Effects of 4-hydroxytamoxifen, raloxifene and ICI 182 780 on survival of uterine cancer cell lines in the presence and absence of exogenous estrogens. Int J Oncol 30:477-487
34. Li LC, Dahiya R (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18:1427-1431
35. Lim LY, Vidnovic N, Ellisen LW, Leong CO (2009) Mutant p53 mediates survival of breast cancer cells. Br J Cancer 101:1606-1612
36. 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
37. 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 17beta-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279:27008-27016 (Pubitemid 38812536)
38. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey S, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406:747-752
39. 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)
40. Schneider BP, Winer EP, Foulkes WD, Garber J, Perou CM, Richardson A, Sledge GW, Carey LA (2008) Triple-negative breast cancer: risk factors to potential targets. Clin Cancer Res 14:8010-8018
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. Sun W, Yang J (2010) Functional mechanisms for human tumor suppressors. J Cancer 1:136-140
45. Tam SW, Shay JW, Pagano M (1994) Differential expression and cell cycle regulation of the cyclin-dependent kinase 4 inhibitor p16Ink4. Cancer Res 54:5816-5820
46. Toh WH, Nam SY, Sabapathy K (2010) An essential role for p73 in regulating mitotic cell death. Cell Death Differ 17:787-800
47. 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
48. 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)
49. 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
50. Wang C, Lv X, He C, Hua G, Tsai MY, Davis JS (2013) The G-protein-coupled estrogen receptor agonist G-1 suppresses proliferation of ovarian cancer cells by blocking tubulin polymerization. Cell Death Dis 4:e869