Targeting GPR30 with G-1: A new therapeutic target for castration-resistant prostate cancer

Endocrine-Related Cancer

Volumn 21, Issue 6, 2014, Pages 903-914

  Lam, Hung Ming ^a,d   Ouyang, Bin ^a   Chen, Jing ^a   Ying, Jun ^a   Wang, Jiang ^a   Wu, Chin Lee ^b   Jia, Li ^c,g   Medvedovic, Mario ^a   Vessella, Robert L ^d   Ho, Shuk Mei ^a,e,f  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f INTERNATIONAL PAPER   (United States)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Androgen deprivation therapy; Androgen repressed gene; Metastases; Tumor infiltrating Neutrophils

Indexed keywords

1-(4-(6-BROMOBENZO(1,3)DIOXOL-5-YL)-3A,4,5,9B-TETRAHYDRO-3H-CYCLOPENTA(C)QUINOLIN-8-YL)ETHANONE; ANDROGEN; ANDROGEN RECEPTOR; AR PROTEIN, HUMAN; CYCLOPENTANE DERIVATIVE; ESTROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; GPER PROTEIN, HUMAN; MESSENGER RNA; QUINOLINE DERIVATIVE; SMALL INTERFERING RNA; TUMOR MARKER;

ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STAGING; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; COHORT ANALYSIS; DRUG EFFECTS; DRUG SCREENING; ENZYME IMMUNOASSAY; FOLLOW UP; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; METASTASIS; MOUSE; PATHOLOGY; PROGNOSIS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANDROGENS; ANIMALS; BLOTTING, WESTERN; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; COHORT STUDIES; CYCLOPENTANES; FOLLOW-UP STUDIES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MICE; NEOPLASM METASTASIS; NEOPLASM STAGING; PROGNOSIS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; QUINOLINES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84919643170     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-14-0402     Document Type: Article

References (59)

1. Ahola TM, Purmonen S, Pennanen P, Zhuang YH, Tuohimaa P & Ylikomi T 2002 Progestin upregulates G-protein-coupled receptor 30 in breast cancer cells. European Journal of Biochemistry 269 2485-2490. (doi:10.1046/j.1432-1033.2002.02912.x)
2. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Ando S et al. 2007 G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17b-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Research 67 1859-1866. (doi:10.1158/0008-5472.CAN-06-2909)
3. Albanito L, Sisci D, Aquila S, Brunelli E, Vivacqua A, Madeo A, Lappano R, Pandey DP, Picard D, Mauro L et al. 2008 Epidermal growth factor induces G protein-coupled receptor 30 expression in estrogen receptor-negative breast cancer cells. Endocrinology 149 3799-3808. (doi:10.1210/en.2008-0117)
4. Blasko E, Haskell CA, Leung S, Gualtieri G, Halks-Miller M, Mahmoudi M, Dennis MK, Prossnitz ER, Karpus WJ & Horuk R 2009 Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis. Journal of Neuroimmunology 214 67-77. (doi:10.1016/j.jneuroim.2009.06.023)
5. Bologa CG, RevankarCM, Young SM, Edwards BS, Arterburn JB, Kiselyov AS, Parker MA, Tkachenko SE, Savchuck NP, Sklar LA et al. 2006 Virtual and biomolecular screening converge on a selective agonist for GPR30. Nature Chemical Biology 2 207-212. (doi:10.1038/nchembio775)
6. de Bono JS, Oudard S, OzgurogluM, Hansen S, Machiels JP, Kocak I, GravisG, Bodrogi I, Mackenzie MJ, Shen L et al. 2010 Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 376 1147-1154. (doi:10.1016/S0140-6736(10)61389-X)
7. deBonoJS, LogothetisCJ,Molina A, FizaziK,NorthS,Chu L,ChiKN, JonesRJ, Goodman OB Jr, Saad F et al. 2011 Abiraterone and increased survival in metastatic prostate cancer. New England Journal of Medicine 364 1995-2005. (doi:10.1056/NEJMoa1014618)
8. Cacalano G, Lee J, Kikly K, Ryan AM, Pitts-Meek S, Hultgren B, Wood WI & Moore MW 1994 Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265 682-684. (doi:10.1126/science.8036519)
9. Caruso RA, Bellocco R, Pagano M, Bertoli G, Rigoli L & Inferrera C 2002 Prognostic value of intratumoral neutrophils in advanced gastric carcinoma in a high-risk area in northern Italy. Modern Pathology 15 831-837. (doi:10.1097/01.MP.0000020391.98998.6B)
10. 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 G2 cell-cycle arrest. Cell Death and Differentiation 17 1511-1523. (doi:10.1038/cdd.2010.20)
11. Cheng SB, Graeber CT, Quinn JA & Filardo EJ 2011 Retrograde transport of the transmembrane estrogen receptor, G-protein-coupled-receptor-30 (GPR30/GPER) from the plasma membrane towards the nucleus. Steroids 76 892-896. (doi:10.1016/j.steroids.2011.02.018)
12. Claessens F & Tilley W 2014 Androgen signaling and steroid receptor crosstalk in endocrine cancers. Endocrine-Related Cancer 21 E3-E5. (doi:10.1530/ERC-14-0274)
13. Cox RL & Crawford ED 1995 Estrogens in the treatment of prostate cancer. Journal of Urology 154 1991-1998. (doi:10.1016/S0022-5347(01)66670-9)
14. Decker KF, Zheng D, He Y, Bowman T, Edwards JR & Jia L 2012 Persistent androgen receptor-mediated transcription in castration-resistant prostate cancer under androgen-deprived conditions. Nucleic Acids Research 40 10765-10779. (doi:10.1093/nar/gks888)
15. De Marco P, Bartella V, Vivacqua A, Lappano R, Santolla MF, Morcavallo A, Pezzi V, Belfiore A & Maggiolini M 2013 Insulin-like growth factor-I regulates GPER expression and function in cancer cells. Oncogene 32 678-688. (doi:10.1038/onc.2012.97)
16. Dennis MK, Burai R, Ramesh C, Petrie WK, Alcon SN, Nayak TK, Bologa CG, Leitao A, Brailoiu E,Deliu E et al. 2009 In vivo effects of aGPR30 antagonist. Nature Chemical Biology 5 421-427. (doi:10.1038/nchembio.168)
17. Di Carlo E, Forni G, Lollini P, Colombo MP, Modesti A & Musiani P 2001 The intriguing role of polymorphonuclear neutrophils in antitumor reactions. Blood 97 339-345. (doi:10.1182/blood.V97.2.339)
18. Eash KJ, Greenbaum AM, Gopalan PK & Link DC 2010 CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. Journal of Clinical Investigation 120 2423-2431. (doi:10.1172/JCI41649)
19. 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. Molecular Endocrinology 14 1649-1660. (doi:10.1210/mend.14.10.0532)
20. Fu X, Tao L, Rivera A, Xu H & Zhang X 2011 Virotherapy induces massive infiltration of neutrophils in a subset of tumors defined by a strong endogenous interferon response activity. Cancer Gene Therapy 18 785-794. (doi:10.1038/cgt.2011.46)
21. Funakoshi T, Yanai A, Shinoda K, Kawano MM & Mizukami Y 2006 G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochemical and Biophysical Research Communications 346 904-910. (doi:10.1016/j.bbrc.2006.05.191)
22. 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 (ERa) phosphorylation signals. Endocrinology 152 1434-1447. (doi:10.1210/en.2010-1368)
23. Geiser T, Dewald B, Ehrengruber MU, Clark-Lewis I & Baggiolini M 1993 The interleukin-8-related chemotactic cytokines GROa, GROb, and GROg activate human neutrophil and basophil leukocytes. Journal of Biological Chemistry 268 15419-15424.
24. Gregory AD & Houghton AM 2011 Tumor-associated neutrophils: new targets for cancer therapy. Cancer Research 71 2411-2416. (doi:10.1158/0008-5472.CAN-10-2583)
25. Haas E, Meyer MR, SchurrU, Bhattacharya I, Minotti R, Nguyen HH, Heigl A, Lachat M, Genoni M & Barton M 2007 Differential effects of 17b-estradiol on function and expression of estrogen receptor a, estrogen receptor b, and GPR30 in arteries and veins of patients with atherosclerosis. Hypertension 49 1358-1363. (doi:10.1161/HYPERTENSIONAHA. 107.089995)
26. Harokopakis E & Hajishengallis G 2005 Integrin activation by bacterial fimbriae through a pathway involving CD14, Toll-like receptor 2, and phosphatidylinositol-3-kinase. European Journal of Immunology 35 1201-1210. (doi:10.1002/eji.200425883)
27. Higano CS & Crawford ED 2011 New and emerging agents for the treatment of castration-resistant prostate cancer. Urologic Oncology 29 S1-S8. (doi:10.1016/j.urolonc.2011.08.013)
28. Higano CS, Schellhammer PF, Small EJ, Burch PA, Nemunaitis J, Yuh L, Provost N & Frohlich MW 2009 Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer. Cancer 115 3670-3679. (doi:10.1002/cncr.24429)
29. Hirose K, Hakozaki M, Nyunoya Y, Kobayashi Y, Matsushita K, Takenouchi T, Mikata A, Mukaida N & Matsushima K 1995 Chemokine gene transfection into tumour cells reduced tumorigenicity in nude mice in association with neutrophilic infiltration. British Journal of Cancer 72 708-714. (doi:10.1038/bjc.1995.398)
30. Ho SM, Lee MT, Lam HM & Leung YK 2011 Estrogens and prostate cancer: etiology, mediators, prevention, and management. Endocrinology and Metabolism Clinics of North America 40 591-614. (doi:10.1016/j.ecl.2011.05.002)
31. Huang HJ, Neven P, DrijkoningenM, Paridaens R, Wildiers H, Van Limbergen E, Berteloot P, Amant F, Vergote I & Christiaens MR 2005 Association between tumour characteristics and HER-2/neu by immunohistochemistry in 1362 women with primary operable breast cancer. Journal of Clinical Pathology 58 611-616. (doi:10.1136/jcp.2004.022772)
32. Huggins C & Hodges CV 2002 Studies on prostatic cancer: I. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. 1941. Journal of Urology 168 9-12. (doi:10.1016/S0022-5347(05)64820-3)
33. Jacobi JS, Martin C, Nava G, Jeziorski MC, Clapp C & Martinez de la EG 2007 17-b-estradiol directly regulates the expression of adrenergic receptors and kisspeptin/GPR54 system in GT1-7 GnRH neurons. Neuroendocrinology 86 260-269. (doi:10.1159/000107770)
34. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB et al. 2010 Sipuleucel-T immunotherapy for castration-resistant prostate cancer. New England Journal of Medicine 363 411-422. (doi:10.1056/NEJMoa1001294)
35. Langley RE, Cafferty FH, Alhasso AA, Rosen SD, Sundaram SK, Freeman SC, Pollock P, Jinks RC, Godsland IF, Kockelbergh R et al. 2013 Cardiovascular outcomes in patients with locally advanced and metastatic prostate cancer treated with luteinising-hormone-releasinghormone agonists or transdermal oestrogen: the randomised, phase 2 MRC PATCH trial (PR09). Lancet Oncology 14 306-316. (doi:10.1016/S1470-2045(13)70025-1)
36. Leav I, Lau KM, Adams JY,McNeal JE, Taplin ME, Wang J, Singh H & Ho SM 2001 Comparative studies of the estrogen receptors b and a and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. American Journal of Pathology 159 79-92. (doi:10.1016/S0002-9440(10)61676-8)
37. Leung BP, Culshaw S, Gracie JA, Hunter D, Canetti CA, Campbell C, Cunha F, Liew FY & McInnes IB 2001 A role for IL-18 in neutrophil activation. Journal of Immunology 167 2879-2886. (doi:10.4049/jimmunol.167.5.2879)
38. Leung YK, Lam HM, Wu S, Song D, Levin L, Cheng L, Wu CL & Ho SM2010 Estrogen receptor b2 and b5 are associated with poor prognosis in prostate cancer, and promote cancer cell migration and invasion. Endocrine-Related Cancer 17 675-689. (doi:10.1677/ERC-09-0294)
39. Madeo A & Maggiolini M 2010 Nuclear alternate estrogen receptor GPR30 mediates 17b-estradiol-induced gene expression and migration in breast cancer-associated fibroblasts. Cancer Research 70 6036-6046. (doi:10.1158/0008-5472.CAN-10-0408)
40. Maggiolini M & Picard D 2010 The unfolding stories of GPR30, a new membrane-bound estrogen receptor. Journal of Endocrinology 204 105-114. (doi:10.1677/JOE-09-0242)
41. Musiani P, Allione A, Modica A, Lollini PL, Giovarelli M, Cavallo F, Belardelli F, Forni G & Modesti A 1996 Role of neutrophils and lymphocytes in inhibition of a mouse mammary adenocarcinoma engineered to release IL-2, IL-4, IL-7, IL-10, IFN-a, IFN-g, and TNF-a. Laboratory Investigation 74 146-157.
42. Nelson AW, Tilley WD, Neal DE & Carroll JS 2014 Estrogen receptor beta in prostate cancer: friend or foe? Endocrine-Related Cancer 21 T219-T234. (doi:10.1530/ERC-13-0508)
43. Norman G, Dean ME, Langley RE, Hodges ZC, Ritchie G, Parmar MK, Sydes MR, Abel P & Eastwood AJ 2008 Parenteral oestrogen in the treatment of prostate cancer: a systematic review. British Journal of Cancer 98 697-707. (doi:10.1038/sj.bjc.6604230)
44. Oh WK 2002 The evolving role of estrogen therapy in prostate cancer. Clinical Prostate Cancer 1 81-89. (doi:10.3816/CGC.2002.n.009)
45. Otto C, Rohde-Schulz B, Schwarz G, Fuchs I, Klewer M, Brittain D, Langer G, Bader B, Prelle K, Nubbemeyer R et al. 2008 G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology 149 4846-4856. (doi:10.1210/en.2008-0269)
46. Pandey DP, Lappano R, Albanito L, Madeo A,MaggioliniM& Picard D 2009 Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF. EMBO Journal 28 523-532. (doi:10.1038/emboj.2008.304)
47. Pelleitier M & Montplaisir S 1975 The nude mouse: a model of deficient T-cell function. Methods and Achievements in Experimental Pathology 7 149-166.
48. Prossnitz ER & Barton M 2011 The G-protein-coupled estrogen receptor GPER in health and disease. Nature Reviews. Endocrinology 7 715-726. (doi:10.1038/nrendo.2011.122)
49. Prossnitz ER, Arterburn JB & Sklar LA 2007 GPR30: a G protein-coupled receptor for estrogen. Molecular and Cellular Endocrinology 265 138-142. (doi:10.1016/j.mce.2006.12.010)
50. Recchia AG, De Francesco EM, Vivacqua A, Sisci D, Panno ML, Ando S & Maggiolini M 2011 The G protein-coupled receptor 30 is up-regulated by hypoxia-inducible factor-1a (HIF-1a) in breast cancer cells and cardiomyocytes. Journal of Biological Chemistry 286 10773-10782. (doi:10.1074/jbc.M110.172247)
51. Ryckman C, Vandal K, Rouleau P, Talbot M & Tessier PA 2003 Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. Journal of Immunology 170 3233-3242. (doi:10.4049/jimmunol.170.6.3233)
52. Saenko EL, Skorobogat'ko OV, Tarasenko P, Romashko V, Zhuravetz L, Zadorozhnaya L, Senjuk OF & Yaropolov AI 1994 Modulatory effects of ceruloplasmin on lymphocytes, neutrophils and monocytes of patients with altered immune status. Immunological Investigations 23 99-114. (doi:10.3109/08820139409087792)
53. Schaider H, Oka M, Bogenrieder T, Nesbit M, Satyamoorthy K, Berking C, Matsushima K & Herlyn M 2003 Differential response of primary and metastatic melanomas to neutrophils attracted by IL-8. International Journal of Cancer 103 335-343. (doi:10.1002/ijc.10775)
54. Schellhammer P 2012 Life after failure of traditional androgen deprivation therapy. Urologic Oncology 30 S10-S14. (doi:10.1016/j.urolonc.2012.01.009)
55. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Theodore C, James ND, Turesson I et al. 2004 Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. New England Journal of Medicine 351 1502-1512. (doi:10.1056/NEJMoa040720)
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. (doi:10.1210/en.2004-1064)
57. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Ando S & MaggioliniM2006 TheG protein-coupled receptor GPR30 mediates the proliferative effects induced by 17b-estradiol and hydroxytamoxifen in endometrial cancer cells. Molecular Endocrinology 20 631-646. (doi:10.1210/me.2005-0280)
58. Yang L, Ravindranathan P, Ramanan M, Kapur P, Hammes SR, Hsieh JT & Raj GV 2012 Central role for PELP1 in nonandrogenic activation of the androgen receptor in prostate cancer. Molecular Endocrinology 26 550-561. (doi:10.1210/me.2011-1101)
59. ZhengD,Decker KF, Zhou T, Chen J, Qi Z, Jacobs K,Weilbaecher KN, Corey E, Long F & Jia L 2013 Role of WNT7B-induced noncanonical pathway in advanced prostate cancer. Molecular Cancer Research 11 482-493. (doi:10.1158/1541-7786.MCR-12-0520)