Androgens suppress EZH2 expression via retinoblastoma (RB) and p130-dependent pathways: A potential mechanism of androgen-refractory progression of prostate cancer

Endocrinology

Volumn 151, Issue 11, 2010, Pages 5136-5145

  Bohrer, Laura R ^a   Chen, Shuai ^a   Hallstrom, Timothy C ^a,b   Huang, Haojie ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; DISABLED HOMOLOG 2 INTERACTING PROTEIN; METRIBOLONE; PROTEIN P130; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; UVOMORULIN; ANDROGEN RECEPTOR; EZH2 PROTEIN, MOUSE; HISTONE LYSINE METHYLTRANSFERASE; RBL2 PROTEIN, MOUSE;

ANDROGEN DEPRIVATION THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CASTRATION; CELL CULTURE; CONTROLLED STUDY; GENE TARGETING; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; CELL MOTION; CHROMATIN IMMUNOPRECIPITATION; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; ORCHIECTOMY; PHYSIOLOGY; PROMOTER REGION; PROSTATE TUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; TUMOR CELL LINE; WESTERN BLOTTING;

ANDROGENS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; CHROMATIN IMMUNOPRECIPITATION; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE-LYSINE N-METHYLTRANSFERASE; IMMUNOHISTOCHEMISTRY; MALE; MICE; ORCHIECTOMY; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; RETINOBLASTOMA PROTEIN; RETINOBLASTOMA-LIKE PROTEIN P130; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 78049500122     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0436     Document Type: Article

References (37)

1. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, Higgins SJ, Sugimura Y 1987 The endocrinology and developmental biology of the prostate. Endocr Rev 8:338-362
2. Kyprianou N, Isaacs JT 1988 Activation of programmed cell death in the rat ventral prostate after castration. Endocrinology 122:552-562
3. Huang H, Tindall DJ 2002 The role of the androgen receptor in prostate cancer. Crit Rev Eukar Gene 12:193-207
4. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM 2005 Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310:644-648
5. Tomlins SA, Laxman B, Dhanasekaran SM, Helgeson BE, Cao X, Morris DS, Menon A, Jing X, Cao Q, Han B, Yu J, Wang L, Montie JE, Rubin MA, Pienta KJ, Roulston D, Shah RB, Varambally S, Mehra R, Chinnaiyan AM 2007 Distinct classes of chromosomal rearrangements create oncogenic ETS gene fusions in prostate cancer. Nature 448:595-599 (Pubitemid 47206938)
6. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y 2002 Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039-1043 (Pubitemid 35247314)
7. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D 2002 Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of Zeste protein. Genes Dev 16:2893-2905
8. Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA 2002 Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197-208
9. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K, Odom DT, Otte AP, Volkert TL, Bartel DP, Melton DA, Gifford DK, Jaenisch R, Young RA 2006 Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125:301-313 (Pubitemid 44313811)
10. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R 2006 Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441:349-353 (Pubitemid 44050199)
11. Ezhkova E, Pasolli HA, Parker JS, Stokes N, Su IH, Hannon G, Tarakhovsky A, Fuchs E 2009 Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 136:1122-1135
12. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA, Chinnaiyan AM 2002 The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419:624-629
13. Stanbrough M, Bubley GJ, Ross K, Golub TR, Rubin MA, Penning TM, Febbo PG, Balk SP 2006 Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res 66:2815-2825
14. Yu J, Cao Q, Mehra R, Laxman B, Yu J, Tomlins SA, Creighton CJ, Dhanasekaran SM, Shen R, Chen G, Morris DS, Marquez VE, Shah RB, Ghosh D, Varambally S, Chinnaiyan AM 2007 Integrative genomics analysis reveals silencing of β-adrenergic signaling by polycomb in prostate cancer. Cancer Cell 12:419-431
15. Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B, Laxman B, Cao X, Jing X, Ramnarayanan K, Brenner JC, Yu J, Kim JH, Han B, Tan P, Kumar-Sinha C, Lonigro RJ, Palanisamy N, Maher CA, Chinnaiyan AM 2008 Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322:1695-1699
16. Karanikolas BD, Figueiredo ML, Wu L 2009 Polycomb group protein enhancer of zeste 2 is an oncogene that promotes the neoplastic transformation of a benign prostatic epithelial cell line. Mol Cancer Res 7:1456-1465
17. Min J, Zaslavsky A, Fedele G, McLaughlin SK, Reczek EE, De Raedt T, Guney I, Strochlic DE, Macconaill LE, Beroukhim R, Bronson RT, Ryeom S, Hahn WC, Loda M, Cichowski K 2010 An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-κB. Nat Med 16:286-294
18. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K 2003 EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 22:5323-5335
19. Friedman JM, Liang G, Liu CC, Wolff EM, Tsai YC, Ye W, Zhou X, Jones PA 2009 The putative tumor suppressor microRNA-101 modulates the cancer epigenome by repressing the polycomb group protein EZH2. Cancer Res 69:2623-2629
20. Huang H, Cheville JC, Pan Y, Roche PC, Schmidt LJ, Tindall DJ 2001 PTEN induces chemosensitivity in PTEN-mutated prostate cancer cells by suppression of Bcl-2 expression. J Biol Chem 276:38830-38836
21. Murillo H, Huang H, Schmidt LJ, Smith DI, Tindall DJ 2001 Role of PI3K signaling in survival and progression of LNCaP prostate cancer cells to the androgen refractory state. Endocrinology 142:4795-4805
22. Day KC, McCabe MT, Zhao X, Wang Y, Davis JN, Phillips J, Von Geldern M, Ried T, KuKuruga MA, Cunha GR, Hayward SW, Day ML 2002 Rescue of embryonic epithelium reveals that the homozygous deletion of the retinoblastoma gene confers growth factor independence and immortality but does not influence epithelial differentiation or tissue morphogenesis. J Biol Chem 277:44475-44484
23. Liu SL, Rand A, Kelm Jr RJ, Getz MJ 2000 The retinoblastoma gene family members pRB and p107 coactivate the AP-1-dependent mouse tissue factor promoter in fibroblasts. Oncogene 19:3352-3362
24. Huang H, Zegarra-Moro OL, Benson D, Tindall DJ 2004 Androgens repress Bcl-2 expression via activation of the retinoblastoma (RB) protein in prostate cancer cells. Oncogene 23:2161-2176
25. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, Pathak S, von Eschenbach AC, Chung LW 1994 Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res 54:2577-2581 (Pubitemid 24173741)
26. Li JJ, Li SA, Llombart-Bosch A, eds. 2005 Hormonal carcinogenesis IV. New York: Springer Verlag
27. Liu P, Li S, Gan L, Kao TP, Huang H 2008 A transcription-independent function of FOXO1 in inhibition of androgen-independent activation of the androgen receptor in prostate cancer cells. Cancer Res 68:10290-10299
28. McDonnell TJ, Troncoso P, Brisbay SM, Logothetis C, Chung LW, Hsieh JT, Tu SM, Campbell ML 1992 Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res 52:6940-6944
29. Tsihlias J, Zhang W, Bhattacharya N, Flanagan M, Klotz L, Slingerland J 2000 Involvement of p27Kip1 in G1 arrest by high dose 5α- dihydrotestosterone in LNCaP human prostate cancer cells. Oncogene 19:670-679
30. Jiao J, Wang S, Qiao R, Vivanco I, Watson PA, Sawyers CL, Wu H 2007 Murine cell lines derived from Pten null prostate cancer show the critical role of PTEN in hormone refractory prostate cancer development. Cancer Res 67:6083-6091
31. Dehm SM, Tindall DJ 2007 Androgen receptor structural and functional elements: role and regulation in prostate cancer. Mol Endocrinol 21:2855-2863
32. Takahashi Y, Rayman JB, Dynlacht BD 2000 Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev 14:804-816
33. Cao Q, Yu J, Dhanasekaran SM, Kim JH, Mani RS, Tomlins SA, Mehra R, Laxman B, Cao X, Yu J, Kleer CG, Varambally S, Chinnaiyan AM 2008 Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene 27:7274-7284
34. Hofman K, Swinnen JV, Verhoeven G, Heyns W 2001 E2F activity is biphasically regulated by androgens in LNCaP cells. Biochem Biophys Res Commun 283:97-101
35. Lu S, Liu M, Epner DE, Tsai SY, Tsai MJ 1999 Androgen regulation of the cyclin-dependent kinase inhibitor p21 gene through an androgen response element in the proximal promoter. Mol Endocrinol 13:376-384
36. Simon JA, Kingston RE 2009 Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10:697-708
37. Xie D, Gore C, Liu J, Pong RC, Mason R, Hao G, Long M, Kabbani W, Yu L, Zhang H, Chen H, Sun X, Boothman DA, Min W, Hsieh JT 2010 Role of DAB2IP in modulating epithelial-to-mesenchymal transition and prostate cancer metastasis. Proc Natl Acad Sci USA 107:2485-2490