Estrogen receptor alpha drives proliferation in PTEN-deficient prostate carcinoma by stimulating survival signaling, MYC expression and altering glucose sensitivity

Oncotarget

Volumn 6, Issue 2, 2015, Pages 604-616

  Takizawa, Itsuhiro ^a   Lawrence, Mitchell G ^a   Balanathan, Preetika ^a   Rebello, Richard ^a   Pearson, Helen B ^b,c   Garg, Elika ^d,e   Pedersen, John ^f   Pouliot, Normand ^b,c   Nadon, Robert ^e   Watt, Matthew J ^a   Taylor, Renea A ^a   Humbert, Patrick ^b,c   Topisirovic, Ivan ^d   Larsson, Ola ^g   Risbridger, Gail P ^a   Furic, Luc ^a  

^a MONASH UNIVERSITY   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MCGILL UNIVERSITY   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f Tissupath Pty Ltd   (Australia)

^g KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Estrogen receptor alpha; Metabolism; MYC; Prostate cancer; PTEN

Indexed keywords

ESTROGEN RECEPTOR ALPHA; GLUCOSE TRANSPORTER 1; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; GLUCOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER GRADING; CANCER GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ERALPHA GENE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; GENE SILENCING; GLUCOSE METABOLISM; KNOCKOUT GENE; MALE; MOUSE; MOUSE MODEL; NONHUMAN; ONCOGENE; ONCOGENE MYC; PROSTATE CARCINOMA; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PTEN GENE; TISSUE DISTRIBUTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; DEFICIENCY; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; PHYSIOLOGY; PROSTATE TUMOR; SIGNAL TRANSDUCTION; SURVIVAL; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; ESTROGEN RECEPTOR ALPHA; GENE KNOCKDOWN TECHNIQUES; GENES, MYC; GLUCOSE; HUMANS; MALE; MCF-7 CELLS; MICE; MICE, TRANSGENIC; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS;

EID: 84921749540     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2820     Document Type: Article

References (58)

1. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64(1):9-29.
2. Travison TG, Araujo AB, Kupelian V, O'Donnell AB and McKinlay JB. The relative contributions of aging, health, and lifestyle factors to serum testosterone decline in men. J Clin Endocrinol Metab. 2007; 92(2):549-555.
3. Risbridger GP, Davis ID, Birrell SN and Tilley W. Breast and prostate cancer: more similar than different. Nature Review Cancer. 2010; 10(3):205-212.
4. Ricke WA, McPherson SJ, Bianco JJ, Cunha GR, Wang Y and Risbridger GP. Prostatic hormonal carcinogenesis is mediated by in situ estrogen production and estrogen receptor alpha signaling. FASEB J. 2008; 22(5):1512-1520.
5. Wang Y, Sudilovsky D, Zhang B, Haughney PC, Rosen MA, Wu DS, Cunha TJ, Dahiya R, Cunha GR and Hayward SW. A human prostatic epithelial model of hormonal carcinogenesis. Cancer Res. 2001; 61(16):6064-6072.
6. Ellem SJ and Risbridger GP. Treating prostate cancer: a rationale for targeting local oestrogens. Nat Rev Cancer. 2007; 7(8):621-627.
7. Sugiyama N, Barros RP, Warner M and Gustafsson JA. ERbeta: recent understanding of estrogen signaling. Trends Endocrinol Metab. 2010; 21(9):545-552.
8. Hussain S, Lawrence MG, Taylor RA, Lo CY, Frydenberg M, Ellem SJ, Furic L and Risbridger GP. Estrogen receptor beta activation impairs prostatic regeneration by inducing apoptosis in murine and human stem/progenitor enriched cell populations. PLoS ONE. 2012; 7(7):e40732.
9. McPherson SJ, Hussain S, Balanathan P, Hedwards SL, Niranjan B, Grant M, Chandrasiri UP, Toivanen R, Wang Y, Taylor RA and Risbridger GP. Estrogen receptor-beta activated apoptosis in benign hyperplasia and cancer of the prostate is androgen independent and TNFalpha mediated. Proc Natl Acad Sci USA. 2010; 107(7):3123-3128.
10. Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA, Gouvin LM, Sharma VM and Mercurio AM. ERbeta impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell. 2010; 17(4):319-332.
11. Bonkhoff H, Fixemer T, Hunsicker I and Remberger K. Estrogen receptor expression in prostate cancer and premalignant prostatic lesions. Am J Pathol. 1999; 155(2):641-647.
12. Leav I, Lau, K. M, Adams, J. Y, McNeal, J. E, Taplin, M. E, Wang, J, Singh, H, Ho, S. M. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol. 2001; 159(1):79-92.
13. Royuela M, de Miguel MP, Bethencourt FR, Sanchez-Chapado M, Fraile B, Arenas MI and Paniagua R. Estrogen receptors alpha and beta in the normal, hyperplastic and carcinomatous human prostate. J Endocrinol. 2001; 168(3):447-454.
14. Hobisch A, Hittmair A, Daxenbichler G, Wille S, Radmayr C, Hobisch-Hagen P, Bartsch G, Klocker H and Culig Z. Metastatic lesions from prostate cancer do not express oestrogen and progesterone receptors. J Pathol. 1997; 182(3):356-361.
15. Celhay O, Yacoub M, Irani J, Dore B, Cussenot O and Fromont G. Expression of estrogen related proteins in hormone refractory prostate cancer: association with tumor progression. J Urol. 2010; 184(5):2172-2178.
16. Hetzl AC, Montico F, Lorencini RM, Kido L, Candido E, Billis A, Ferreira U and Cagnon VH. Fibroblast growth factor, estrogen, and prolactin receptor features in different grades of prostatic adenocarcinoma in elderly men. Microsc Res Tech. 2013; 76(3):321-330.
17. Megas G, Chrisofos M, Anastasiou I, Tsitlidou A, Choreftaki T and Deliveliotis C. Estrogen receptor (alpha and beta) but not androgen receptor expression is correlated with recurrence, progression and survival in post prostatectomy T3N0M0 locally advanced prostate cancer in an urban Greek population. Asian J Androl. 2014.
18. Linja MJ, Savinainen KJ, Tammela TL, Isola JJ and Visakorpi T. Expression of ERalpha and ERbeta in prostate cancer. Prostate. 2003; 55(3):180-186.
19. Sasaki M, Tanaka Y, Perinchery G, Dharia A, Kotcherguina I, Fujimoto S and Dahiya R. Methylation and inactivation of estrogen, progesterone, and androgen receptors in prostate cancer. J Natl Cancer Inst. 2002; 94(5):384-390.
20. Li LC, Chui R, Nakajima K, Oh BR, Au HC and Dahiya R. Frequent methylation of estrogen receptor in prostate cancer: correlation with tumor progression. Cancer Res. 2000; 60(3):702-706.
21. Lau KM, LaSpina M, Long J and Ho SM. Expression of estrogen receptor (ER)-alpha and ER-beta in normal and malignant prostatic epithelial cells: regulation by methylation and involvement in growth regulation. Cancer Res. 2000; 60(12):3175-3182.
22. Setlur SR, Mertz KD, Hoshida Y, Demichelis F, Lupien M, Perner S, Sboner A, Pawitan Y, Andren O, Johnson LA, Tang J, Adami HO, Calza S, Chinnaiyan AM, Rhodes D, Tomlins S, et al. Estrogen-dependent signaling in a molecularly distinct subclass of aggressive prostate cancer. J Natl Cancer Inst. 2008; 100(11):815-825.
23. McDevitt MA, Glidewell-Kenney C, Jimenez MA, Ahearn PC, Weiss J, Jameson JL and Levine JE. New insights into the classical and non-classical actions of estrogen: evidence from estrogen receptor knock-out and knock-in mice. Mol Cell Endocrinol. 2008; 290(1-2):24-30.
24. Parsons S, Pritchard J, Fox E and Shupnik M. (2012). Cooperative Interactions Between c-Src, Estrogen Receptors and Receptor Tyrosine Kinases in Breast Cancer. In: Castoria G and Migliaccio A, eds. Advances in Rapid Sex-Steroid Action: Springer New York), pp. 31-59.
25. Pandini G, Genua M, Frasca F, Squatrito S, Vigneri R and Belfiore A. 17beta-estradiol up-regulates the insulin-like growth factor receptor through a nongenotropic pathway in prostate cancer cells. Cancer Res. 2007; 67(18):8932-8941.
26. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW and Liao JK. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature. 2000; 407(6803):538-541.
27. Shupnik MA. Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene. 2004; 23(48):7979-7989.
28. Phin S, Moore MW and Cotter PD. Genomic Rearrangements of PTEN in Prostate Cancer. Front Oncol. 2013; 3:240.
29. Sircar K, Yoshimoto M, Monzon FA, Koumakpayi IH, Katz RL, Khanna A, Alvarez K, Chen G, Darnel AD, Aprikian AG, Saad F, Bismar TA and Squire JA. PTEN genomic deletion is associated with p-Akt and AR signalling in poorer outcome, hormone refractory prostate cancer. J Pathol. 2009; 218(4):505-513.
30. Wang J, Kobayashi T, Floc'h N, Kinkade CW, Aytes A, Dankort D, Lefebvre C, Mitrofanova A, Cardiff RD, McMahon M, Califano A, Shen MM and Abate-Shen C. B-Raf activation cooperates with PTEN loss to drive c-Myc expression in advanced prostate cancer. Cancer Res. 2012; 72(18):4765-4776.
31. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, Koutcher JA, Scher HI, Ludwig T, Gerald W, Cordon-Cardo C and Pandolfi PP. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature. 2005; 436(7051):725-730.
32. Kim J, Roh M, Doubinskaia I, Algarroba GN, Eltoum IE and Abdulkadir SA. A mouse model of heterogeneous, c-MYC-initiated prostate cancer with loss of Pten and p53. Oncogene. 2012; 31(3):322-332.
33. Wang S, Garcia AJ, Wu M, Lawson DA, Witte ON and Wu H. Pten deletion leads to the expansion of a prostatic stem/progenitor cell subpopulation and tumor initiation. Proc Natl Acad Sci USA. 2006; 103(5):1480-1485.
34. Kretzer NM, Cherian MT, Mao C, Aninye IO, Reynolds PD, Schiff R, Hergenrother PJ, Nordeen SK, Wilson EM and Shapiro DJ. A noncompetitive small molecule inhibitor of estrogen-regulated gene expression and breast cancer cell growth that enhances proteasome-dependent degradation of estrogen receptor {alpha}. J Biol Chem. 2010; 285(53):41863-41873.
35. Mulholland DJ, Xin L, Morim A, Lawson D, Witte O and Wu H. Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res. 2009; 69(22):8555-8562.
36. Lin CJ, Malina A and Pelletier J. c-Myc and eIF4F constitute a feedforward loop that regulates cell growth: implications for anticancer therapy. Cancer Res. 2009; 69(19):7491-7494.
37. Krum SA, Miranda-Carboni GA, Lupien M, Eeckhoute J, Carroll JS and Brown M. Unique ERalpha cistromes control cell type-specific gene regulation. Mol Endocrinol. 2008; 22(11):2393-2406.
38. Kalaany NY and Sabatini DM. Tumours with PI3K activation are resistant to dietary restriction. Nature. 2009; 458(7239):725-731.
39. Blouin MJ, Zhao Y, Zakikhani M, Algire C, Piura E and Pollak M. Loss of function of PTEN alters the relationship between glucose concentration and cell proliferation, increases glycolysis, and sensitizes cells to 2-deoxyglucose. Cancer Lett. 2010; 289(2):246-253.
40. O'Mahony F, Razandi M, Pedram A, Harvey BJ and Levin ER. Estrogen modulates metabolic pathway adaptation to available glucose in breast cancer cells. Mol Endocrinol. 2012; 26(12):2058-2070.
41. Birsoy K, Possemato R, Lorbeer FK, Bayraktar EC, Thiru P, Yucel B, Wang T, Chen WW, Clish CB and Sabatini DM. Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides. Nature. 2014; 508(7494):108-112.
42. Tai S, Sun Y, Squires JM, Zhang H, Oh WK, Liang CZ and Huang J. PC3 is a cell line characteristic of prostatic small cell carcinoma. Prostate. 2011; 71(15):1668-1679.
43. Mertz KD, Setlur SR, Dhanasekaran SM, Demichelis F, Perner S, Tomlins S, Tchinda J, Laxman B, Vessella RL, Beroukhim R, Lee C, Chinnaiyan AM and Rubin MA. Molecular characterization of TMPRSS2-ERG gene fusion in the NCI-H660 prostate cancer cell line: a new perspective for an old model. Neoplasia. 2007; 9(3):200-206.
44. Fisher G, Yang ZH, Kudahetti S, Moller H, Scardino P, Cuzick J, Berney DM and Transatlantic Prostate G. Prognostic value of Ki-67 for prostate cancer death in a conservatively managed cohort. Br J Cancer. 2013; 108(2):271-277.
45. Shtivelman E, Beer TM and Evans CP. Molecular pathways and targets in prostate cancer. Oncotarget. 2014; 5(17):7217-7259.
46. Cho NY, Choi M, Kim BH, Cho YM, Moon KC and Kang GH. BRAF and KRAS mutations in prostatic adenocarcinoma. Int J Cancer. 2006; 119(8):1858-1862.
47. Kollermann J, Albrecht H, Schlomm T, Huland H, Graefen M, Bokemeyer C, Simon R, Sauter G and Wilczak W. Activating BRAF gene mutations are uncommon in hormone refractory prostate cancer in Caucasian patients. Oncol Lett. 2010; 1(4):729-732.
48. Margel D, Urbach DR, Lipscombe LL, Bell CM, Kulkarni G, Austin PC and Fleshner N. Metformin use and all-cause and prostate cancer-specific mortality among men with diabetes. J Clin Oncol. 2013; 31(25):3069-3075.
49. Jin C, McKeehan K and Wang F. Transgenic mouse with high Cre recombinase activity in all prostate lobes, seminal vesicle, and ductus deferens. Prostate. 2003; 57(2):160-164.
50. Lesche R, Groszer M, Gao J, Wang Y, Messing A, Sun H, Liu X and Wu H. Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis. 2002; 32(2):148-149.
51. Bevitt DJ, Milton ID, Piggot N, Henry L, Carter MJ, Toms GL, Lennard TW, Westley B, Angus B and Horne CH. New monoclonal antibodies to oestrogen and progesterone receptors effective for paraffin section immunohistochemistry. J Pathol. 1997; 183(2):228-232.
52. Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, Bunney WE, Myers RM, Speed TP, Akil H, Watson SJ and Meng F. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 2005; 33(20):e175.
53. Sandberg R and Larsson O. Improved precision and accuracy for microarrays using updated probe set definitions. BMC Bioinformatics. 2007; 8:48.
54. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U and Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4(2):249-264.
55. Wright GW and Simon RM. A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics. 2003; 19(18):2448-2455.
56. Benjamini Y and Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological. 1995; 57(1):289-300.
57. Luo W, Friedman MS, Shedden K, Hankenson KD and Woolf PJ. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics. 2009; 10:161.
58. Gene Ontology C, Blake JA, Dolan M, Drabkin H, Hill DP, Li N, Sitnikov D, Bridges S, Burgess S, Buza T, McCarthy F, Peddinti D, Pillai L, Carbon S, Dietze H, Ireland A, et al. Gene Ontology annotations and resources. Nucleic Acids Res. 2013; 41(Database issue):D530-535.