Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF

EMBO Journal

Volumn 28, Issue 5, 2009, Pages 523-532

  Pandey, Deo Prakash ^a   Lappano, Rosamaria ^b   Albanito, Lidia ^b   Madeo, Antonio ^b   Maggiolini, Marcello ^b   Picard, Didier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF CALABRIA   (Italy)

Author keywords

G protein coupled receptor; Microarray; Oestrogen; Signal transduction; Tamoxifen resistance

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; ESTROGEN; ESTROGEN RECEPTOR; GPR30 PROTEIN; HYDROXYTAMOXIFEN; PROTEIN DERIVATIVE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BREAST ADENOCARCINOMA; CANCER CELL; CELL MIGRATION; CELL PROLIFERATION; COMPREHENSION; CONTROLLED STUDY; FIBROBLAST; GENE; HORMONAL THERAPY; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; SERUM; TUMOR BIOPSY;

BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CONNECTIVE TISSUE GROWTH FACTOR; ESTROGENS; FIBROBLASTS; HUMANS; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TAMOXIFEN; TUMOR CELLS, CULTURED;

EID: 62049084027     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.304     Document Type: Article

References (60)

1. 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 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67: 1859-1866
2. 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) EGF induces GPR30 expression in estrogen receptor-negative breast cancer cells. Endocrinology 149: 3799-3808
3. Bay BH, Jin R, Huang J, Tan PH (2006) Metallothionein as a prognostic biomarker in breast cancer. Exp Biol Med 231: 1516-1521
4. Bhowmick NA, Moses HL (2005) Tumor-stroma interactions. Curr Opin Genet Dev 15: 97-101
5. Bleau AM, Planque N, Perbal B (2005) CCN proteins and cancer: two to tango. Front Biosci 10: 998-1009
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. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, Dun NJ (2007) Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 193: 311-321
8. Canonaco M, Giusi G, Madeo A, Facciolo RM, Lappano R, Canonaco A, Maggiolini M (2008) A sexually dimorphic distribution pattern of the novel estrogen receptor G-protein-coupled receptor 30 in some brain areas of the hamster. J Endocrinol 196: 131-138
9. Carroll JS, Brown M (2006) Estrogen receptor target gene: an evolving concept. Mol Endocrinol 20: 1707-1714
10. Chaqour B, Yang R, Sha Q (2006) Mechanical stretch modulates the promoter activity of the profibrotic factor CCN2 through increased actin polymerization and NF-kappaB activation. J Biol Chem 281: 20608-20622
11. Chen P-S, Wang M-Y, Wu S-N, Su J-L, Hong C-C, Chuang S-E, Chen M-W, Hua K-T, Wu Y-L, Cha S-T, Babu MS, Chen C-N, Lee P-H, Chang K-J, Kuo M-L (2007) CTGF enhances the motility of breast cancer cells via an integrin-avb3-ERK1/2- dependent S100A4-upregulated pathway. J Cell Sci 120: 2053-2065
12. Cooper SJ, Trinklein ND, Nguyen L, Myers RM (2007) Serum response factor binding sites differ in three human cell types. Genome Res 17: 136-144
13. Dahlman-Wright K, Cavailles V, Fuqua SA, Jordan VC, Katzenellenbogen JA, Korach KS, Maggi A, Muramatsu M, Parker MG, Gustafsson JA (2006) International Union of Pharmacology. LXIV. Estrogen receptors. Pharmacol Rev 58: 773-781
14. De Winter P, Leoni P, Abraham D (2008) Connective tissue growth factor: structure-function relationships of a mosaic, multifunctional protein. Growth Factors 26: 80-91
15. Deng YZ, Chen PP, Wang Y, Yin D, Koeffler HP, Li B, Tong XJ, Xie D (2007) Connective tissue growth factor is overexpressed in esophageal squamous cell carcinoma and promotes tumorigenicity through beta-catenin-T-cell factor/Lef signaling. J Biol Chem 282: 36571-36581
16. Deroo BJ, Korach KS (2006) Estrogen receptors and human disease. J Clin Invest 116: 561-570
17. Dudek P, Picard D (2008) Genomics of signaling crosstalk of estrogen receptor α in breast cancer cells. PLoS ONE 3: e1859
18. Filardo EJ (2002) Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J Steroid Biochem Mol Biol 80: 231-238
19. 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
20. 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
21. Filardo EJ, Quinn JA, Sabo E (2008) Association of the membrane estrogen receptor, GPR30, with breast tumor metastasis and transactivation of the epidermal growth factor receptor. Steroids 73: 870-873
22. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallett M, Park M (2008) Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 14: 518-527
23. Gerdes MJ, Myakishev M, Frost NA, Rishi V, Moitra J, Acharya A, Levy MR, Park S-w, Glick A, Yuspa SH, Vinson C (2006) Activator protein-1 activity regulates epithelial tumor cell identity. Cancer Res 66: 7578-7588
24. Gutierrez-Hartmann A, Duval DL, Bradford AP (2007) ETS transcription factors in endocrine systems. Trends Endocrinol Metab 18: 150-158
25. Han HJ, Russo J, Kohwi Y, Kohwi-Shigematsu T (2008) SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452: 187-193
26. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M, Gustafsson JA (2007) Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87: 905-931
27. Herynk MH, Fuqua SA (2007) Estrogen receptors in resistance to hormone therapy. Adv Exp Med Biol 608: 130-143
28. Hishikawa K, Oemar BS, Tanner FC, Nakaki T, Luscher TF, Fujii T (1999) Connective tissue growth factor induces apoptosis in human breast cancer cell line MCF-7. J Biol Chem 274: 37461-37466
29. Holbourn KP, Acharya KR, Perbal B (2008) The CCN family of proteins: structure-function relationships. Trends Biochem Sci 33: 461-473
30. Hsieh YC, Yu HP, Frink M, Suzuki T, Choudhry MA, Schwacha MG, Chaudry IH (2007) G protein-coupled receptor 30-dependent protein kinase A pathway is critical in nongenomic effects of estrogen in attenuating liver injury after trauma-hemorrhage. Am J Pathol 170: 1210-1218
31. Inoki I, Shiomi T, Hashimoto G, Enomoto H, Nakamura H, Makino K, Ikeda E, Takata S, Kobayashi K, Okada Y (2002) Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J 16: 219-221
32. Iyer VR, Eisen MB, Ross DT, Schuler G, Moore T, Lee JC, Trent JM, Staudt LM, Hudson Jr J, Boguski MS, Lashkari D, Shalon D, Botstein D, Brown PO (1999) The transcriptional program in the response of human fibroblasts to serum. Science 283: 83-87
33. Jiang WG, Watkins G, Fodstad O, Douglas-Jones A, Mokbel K, Mansel RE (2004) Differential expression of the CCN family members Cyr61, CTGF and Nov in human breast cancer. Endocr Relat Cancer 11: 781-791
34. Jordan VC (2004) Selective estrogen receptor modulation: concept and consequences in cancer. Cancer Cell 5: 207-213
35. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massagué J (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3: 537-549
36. Kisanga ER, Gjerde J, Guerrieri-Gonzaga A, Pigatto F, Pesci-Feltri A, Robertson C, Serrano D, Pelosi G, Decensi A, Lien EA (2004) Tamoxifen and metabolite concentrations in serum and breast cancer tissue during three dose regimens in a randomized preoperative trial. Clin Cancer Res 10: 2336-2343
37. Kuhn J, Dina OA, Goswami C, Suckow V, Levine JD, Hucho T (2008) GPR30 estrogen receptor agonists induce mechanical hyperalgesia in the rat. Eur J Neurosci 27: 1700-1709
38. 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
39. Leask A, Abraham DJ (2006) All in the CCN family: essential matricellular signaling modulators emerge from the bunker. J Cell Sci 119: 4803-4810
40. Liu LY, Han YC, Wu SH, Lv ZH (2008) Expression of connective tissue growth factor in tumor tissues is an independent predictor of poor prognosis in patients with gastric cancer. World J Gastroenterol 14: 2110-2114
41. Maggiolini M, Donzé O, Picard D (1999) A non-radioactive method for inexpensive quantitative RT-PCR. Biol Chem 380: 695-697
42. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, Andò S (2004) The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17b-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279: 27009-27016
43. Mullis TC, Tang X, Chong KT (2008) Expression of connective tissue growth factor (CTGF/CCN2) in head and neck squamous cell carcinoma. J Clin Pathol 61: 606-610
44. Posern G, Treisman R (2006) Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 16: 588-596
45. 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
46. Qiu J, Bosch MA, Tobias SC, Krust A, Graham SM, Murphy SJ, Korach KS, Chambon P, Scanlan TS, Ronnekleiv OK, Kelly MJ (2006) A G-protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J Neurosci 26: 5649-5655
47. Rachfal AW, Brigstock DR (2005) Structural and functional properties of CCN proteins. Vitam Horm 70: 69-103
48. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307: 1625-1630
49. Riggins RB, Schrecengost RS, Guerrero MS, Bouton AH (2007) Pathways to tamoxifen resistance. Cancer Lett 256: 1-24
50. Schall TJ, Lewis M, Koller KJ, Lee A, Rice GC, Wong GH, Gatanaga T, Granger GA, Lentz R, Raab H, Kohr WJ, Goeddel DV (1990) Molecular cloning and expression of a receptor for human tumor necrosis factor. Cell 61: 361-370
51. Sirianni R, Chimento A, Ruggiero C, De Luca A, Lappano R, Andò S, Maggiolini M, Pezzi V (2008) The novel estrogen receptor GPR30 mediates the proliferative effects induced by 17β-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology 149: 5043-5051
52. 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 e381-389
53. Sotiropoulos A, Gineitis D, Copeland J, Treisman R (1999) Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98: 159-169
54. Teng J, Wang ZY, Prossnitz ER, Bjorling DE (2008) The G protein-coupled receptor GPR30 inhibits human urothelial cell proliferation. Endocrinology 149: 4024-4034
55. Teplyuk NM, Galindo M, Teplyuk VI, Pratap J, Young DW, Lapointe D, Javed A, Stein JL, Lian JB, Stein GS, van Wijnen AJ (2008) Runx2 regulates G protein-coupled signaling pathways to control growth of osteoblast progenitors. J Biol Chem 283: 27585-27597
56. 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
57. Vivacqua A, Bonofiglio D, Albanito L, Madeo A, Rago V, Carpino A, Musti AM, Picard D, Andò S, Maggiolini M (2006a) 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
58. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Andò S, Maggiolini M (2006b) 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
59. 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 (2008a) GPR30 contributes to estrogen-induced thymic atrophy. Mol Endocrinol 22: 636-648
60. Wang C, Prossnitz ER, Roy SK (2008b) G protein-coupled receptor 30 expression is required for estrogen stimulation of primordial follicle formation in the hamster ovary. Endocrinology 149: 4452-4461