TRIM24 Is an Oncogenic Transcriptional Activator in Prostate Cancer

Cancer Cell

Volumn 29, Issue 6, 2016, Pages 846-858

  Groner, Anna C ^a   Cato, Laura ^a   de Tribolet Hardy, Jonas ^a   Bernasocchi, Tiziano ^b   Janouskova, Hana ^b   Melchers, Diana ^c   Houtman, René ^c   Cato, Andrew C B ^d   Tschopp, Patrick ^a   Gu, Lei ^a   Corsinotti, Andrea ^e,f   Zhong, Qing ^g   Fankhauser, Christian ^g   Fritz, Christine ^g   Poyet, Cédric ^g   Wagner, Ulrich ^g   Guo, Tiannan ^h   Aebersold, Ruedi ^h,i   Garraway, Levi A ^a,j   Wild, Peter J ^g   Theurillat, Jean Philippe ^b,j,k   Brown, Myles ^a   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b INSTITUTE OF ONCOLOGY RESEARCH   (Switzerland)

^c PamGene International   (Netherlands)

^d KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f UNIVERSITY OF TSUKUBA   (Japan)

^g UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^h ETH ZURICH   (Switzerland)

ⁱ UNIVERSITY OF ZURICH   (Switzerland)

^j BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^k LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; SPECKLE TYPE POZ PROTEIN; TRANSCRIPTION FACTOR; TRIPARTITE MOTIF CONTAINING PROTEIN 24; UNCLASSIFIED DRUG; AR PROTEIN, HUMAN; CARRIER PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SPOP PROTEIN, HUMAN; TRIM24 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CASTRATION RESISTANT PROSTATE CANCER; CELL GROWTH; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; EC50; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LNCAP CELL LINE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TUMOR GROWTH; UBIQUITINATION; UPREGULATION; ANIMAL; CANCER TRANSPLANTATION; CHEMISTRY; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; PATHOLOGY; PROSTATE TUMOR;

ANIMALS; CARRIER PROTEINS; CELL PROLIFERATION; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RECEPTORS, ANDROGEN; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84969793941     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2016.04.012     Document Type: Article

References (58)

1. Agoulnik, I.U., Vaid, A., Nakka, M., Alvarado, M., Bingman, W.E. 3rd, Erdem, H., Frolov, A., Smith, C.L., Ayala, G.E., Ittmann, M.M., et al. Androgens modulate expression of transcription intermediary factor 2, an androgen receptor coactivator whose expression level correlates with early biochemical recurrence in prostate cancer. Cancer Res. 66 (2006), 10594–10602.
2. Allton, K., Jain, A.K., Herz, H.M., Tsai, W.W., Jung, S.Y., Qin, J., Bergmann, A., Johnson, R.L., Barton, M.C., Trim24 targets endogenous p53 for degradation. Proc. Natl. Acad. Sci. USA 106 (2009), 11612–11616.
3. An, J., Wang, C., Deng, Y., Yu, L., Huang, H., Destruction of full-length androgen receptor by wild-type SPOP, but not prostate-cancer-associated mutants. Cell Rep. 6 (2014), 657–669.
4. Baca, S.C., Prandi, D., Lawrence, M.S., Mosquera, J.M., Romanel, A., Drier, Y., Park, K., Kitabayashi, N., MacDonald, T.Y., Ghandi, M., et al. Punctuated evolution of prostate cancer genomes. Cell 153 (2013), 666–677.
5. Barbieri, C.E., Baca, S.C., Lawrence, M.S., Demichelis, F., Blattner, M., Theurillat, J.P., White, T.A., Stojanov, P., Van Allen, E., Stransky, N., et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat. Genet. 44 (2012), 685–689.
6. Bennett, J., Fedorov, O., Tallant, C., Monteiro, O., Meier, J., Gamble, V., Savitsky, P., Nunez-Alonso, G.A., Haendler, B., Rogers, C., et al. Discovery of a chemical tool inhibitor targeting the bromodomains of TRIM24 and BRPF. J. Med. Chem. 59 (2015), 1642–1647.
7. Blattner, M., Lee, D.J., O'Reilly, C., Park, K., MacDonald, T.Y., Khani, F., Turner, K.R., Chiu, Y.L., Wild, P.J., Dolgalev, I., et al. SPOP mutations in prostate cancer across demographically diverse patient cohorts. Neoplasia 16 (2014), 14–20.
8. Cavailles, V., Dauvois, S., L'Horset, F., Lopez, G., Hoare, S., Kushner, P.J., Parker, M.G., Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 14 (1995), 3741–3751.
9. Chambon, M., Orsetti, B., Berthe, M.L., Bascoul-Mollevi, C., Rodriguez, C., Duong, V., Gleizes, M., Thenot, S., Bibeau, F., Theillet, C., et al. Prognostic significance of TRIM24/TIF-1alpha gene expression in breast cancer. Am. J. Pathol. 178 (2011), 1461–1469.
10. Cui, Z., Cao, W., Li, J., Song, X., Mao, L., Chen, W., TRIM24 overexpression is common in locally advanced head and neck squamous cell carcinoma and correlates with aggressive malignant phenotypes. PLoS One, 8, 2013, e63887.
11. Culig, Z., Hoffmann, J., Erdel, M., Eder, I.E., Hobisch, A., Hittmair, A., Bartsch, G., Utermann, G., Schneider, M.R., Parczyk, K., et al. Switch from antagonist to agonist of the androgen receptor bicalutamide is associated with prostate tumour progression in a new model system. Br. J. Cancer 81 (1999), 242–251.
12. Eder, I.E., Culig, Z., Ramoner, R., Thurnher, M., Putz, T., Nessler-Menardi, C., Tiefenthaler, M., Bartsch, G., Klocker, H., Inhibition of LncaP prostate cancer cells by means of androgen receptor antisense oligonucleotides. Cancer Gene Ther. 7 (2000), 997–1007.
13. Elsadek, B., Graeser, R., Esser, N., Schafer-Obodozie, C., Tsurumi, C., Abu Ajaj, K., Warnecke, A., Unger, C., Saleem, T., Kratz, F., In vivo evaluation of a novel albumin-binding prodrug of doxorubicin in an orthotopic mouse model of prostate cancer (LNCaP). Prostate Cancer Prostatic Dis. 14 (2011), 14–21.
14. Filippakopoulos, P., Knapp, S., Targeting bromodomains: epigenetic readers of lysine acetylation. Nat. Rev. Drug Discov. 13 (2014), 337–356.
15. Geng, C., He, B., Xu, L., Barbieri, C.E., Eedunuri, V.K., Chew, S.A., Zimmermann, M., Bond, R., Shou, J., Li, C., et al. Prostate cancer-associated mutations in speckle-type POZ protein (SPOP) regulate steroid receptor coactivator 3 protein turnover. Proc. Natl. Acad. Sci. USA 110 (2013), 6997–7002.
16. Geng, C., Rajapakshe, K., Shah, S.S., Shou, J., Eedunuri, V.K., Foley, C., Fiskus, W., Rajendran, M., Chew, S.A., Zimmermann, M., et al. Androgen receptor is the key transcriptional mediator of the tumor suppressor SPOP in prostate cancer. Cancer Res. 74 (2014), 5631–5643.
17. Grasso, C.S., Wu, Y.M., Robinson, D.R., Cao, X., Dhanasekaran, S.M., Khan, A.P., Quist, M.J., Jing, X., Lonigro, R.J., Brenner, J.C., et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 487 (2012), 239–243.
18. Gregory, C.W., He, B., Johnson, R.T., Ford, O.H., Mohler, J.L., French, F.S., Wilson, E.M., A mechanism for androgen receptor-mediated prostate cancer recurrence after androgen deprivation therapy. Cancer Res. 61 (2001), 4315–4319.
19. Guo, Z., Dai, B., Jiang, T., Xu, K., Xie, Y., Kim, O., Nesheiwat, I., Kong, X., Melamed, J., Handratta, V.D., et al. Regulation of androgen receptor activity by tyrosine phosphorylation. Cancer Cell 10 (2006), 309–319.
20. Guo, Z., Yang, X., Sun, F., Jiang, R., Linn, D.E., Chen, H., Kong, X., Melamed, J., Tepper, C.G., Kung, H.J., et al. A novel androgen receptor splice variant is up-regulated during prostate cancer progression and promotes androgen depletion-resistant growth. Cancer Res. 69 (2009), 2305–2313.
21. Hatakeyama, S., TRIM proteins and cancer. Nat. Rev. Cancer 11 (2011), 792–804.
22. Hazelett, D.J., Rhie, S.K., Gaddis, M., Yan, C., Lakeland, D.L., Coetzee, S.G., Henderson, B.E., Noushmehr, H., Cozen, W., Kote-Jarai, Z., et al. Comprehensive functional annotation of 77 prostate cancer risk loci. PLoS Genet., 10, 2014, e1004102.
23. Heinlein, C.A., Chang, C., Androgen receptor in prostate cancer. Endocr. Rev. 25 (2004), 276–308.
24. Herquel, B., Ouararhni, K., Davidson, I., The TIF1alpha-related TRIM cofactors couple chromatin modifications to transcriptional regulation, signaling and tumor suppression. Transcription 2 (2011), 231–236.
25. Hu, R., Dunn, T.A., Wei, S., Isharwal, S., Veltri, R.W., Humphreys, E., Han, M., Partin, A.W., Vessella, R.L., Isaacs, W.B., et al. Ligand-independent androgen receptor variants derived from splicing of cryptic exons signify hormone-refractory prostate cancer. Cancer Res. 69 (2009), 16–22.
26. Jain, A.K., Allton, K., Duncan, A.D., Barton, M.C., TRIM24 is a p53-induced E3-ubiquitin ligase that undergoes ATM-mediated phosphorylation and autodegradation during DNA damage. Mol. Cell Biol. 34 (2014), 2695–2709.
27. Jehle, K., Cato, L., Neeb, A., Muhle-Goll, C., Jung, N., Smith, E.W., Buzon, V., Carbo, L.R., Estebanez-Perpina, E., Schmitz, K., et al. Coregulator control of androgen receptor action by a novel nuclear receptor-binding motif. J. Biol. Chem. 289 (2014), 8839–8851.
28. Jemal, A., Bray, F., Center, M.M., Ferlay, J., Ward, E., Forman, D., Global cancer statistics. CA Cancer J. Clin. 61 (2011), 69–90.
29. Ji, X., Li, W., Song, J., Wei, L., Liu, X.S., CEAS: cis-regulatory element annotation system. Nucleic Acids Res. 34 (2006), W551–W554.
30. Kandoth, C., McLellan, M.D., Vandin, F., Ye, K., Niu, B., Lu, C., Xie, M., Zhang, Q., McMichael, J.F., Wyczalkowski, M.A., et al. Mutational landscape and significance across 12 major cancer types. Nature 502 (2013), 333–339.
31. Kikuchi, M., Okumura, F., Tsukiyama, T., Watanabe, M., Miyajima, N., Tanaka, J., Imamura, M., Hatakeyama, S., TRIM24 mediates ligand-dependent activation of androgen receptor and is repressed by a bromodomain-containing protein, BRD7, in prostate cancer cells. Biochim. Biophys. Acta 1793 (2009), 1828–1836.
32. Lamont, K.R., Tindall, D.J., Minireview: Alternative activation pathways for the androgen receptor in prostate cancer. Mol. Endocrinol. 25 (2011), 897–907.
33. Le Douarin, B., Nielsen, A.L., Garnier, J.M., Ichinose, H., Jeanmougin, F., Losson, R., Chambon, P., A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J. 15 (1996), 6701–6715.
34. Li, H., Sun, L., Tang, Z., Fu, L., Xu, Y., Li, Z., Luo, W., Qiu, X., Wang, E., Overexpression of TRIM24 correlates with tumor progression in non-small cell lung cancer. PLoS One, 7, 2012, e37657.
35. Linja, M.J., Porkka, K.P., Kang, Z., Savinainen, K.J., Janne, O.A., Tammela, T.L., Vessella, R.L., Palvimo, J.J., Visakorpi, T., Expression of androgen receptor coregulators in prostate cancer. Clin. Cancer Res. 10 (2004), 1032–1040.
36. Liu, X., Huang, Y., Yang, D., Li, X., Liang, J., Lin, L., Zhang, M., Zhong, K., Liang, B., Li, J., Overexpression of TRIM24 is associated with the onset and progress of human hepatocellular carcinoma. PLoS One, 9, 2014, e85462.
37. Matsumoto, T., Sakari, M., Okada, M., Yokoyama, A., Takahashi, S., Kouzmenko, A., Kato, S., The androgen receptor in health and disease. Annu. Rev. Physiol. 75 (2013), 201–224.
38. Miao, Z.F., Wang, Z.N., Zhao, T.T., Xu, Y.Y., Wu, J.H., Liu, X.Y., Xu, H., You, Y., Xu, H.M., TRIM24 is upregulated in human gastric cancer and promotes gastric cancer cell growth and chemoresistance. Virchows Arch. 466 (2015), 525–532.
39. Montgomery, R.B., Mostaghel, E.A., Vessella, R., Hess, D.L., Kalhorn, T.F., Higano, C.S., True, L.D., Nelson, P.S., Maintenance of intratumoral androgens in metastatic prostate cancer: a mechanism for castration-resistant tumor growth. Cancer Res. 68 (2008), 4447–4454.
40. Mortezavi, A., Hermanns, T., Seifert, H.H., Baumgartner, M.K., Provenzano, M., Sulser, T., Burger, M., Montani, M., Ikenberg, K., Hofstadter, F., et al. KPNA2 expression is an independent adverse predictor of biochemical recurrence after radical prostatectomy. Clin. Cancer Res. 17 (2011), 1111–1121.
41. Niraula, S., Chi, K., Joshua, A.M., Beyond castration-defining future directions in the hormonal treatment of prostate cancer. Horm. Cancer 3 (2012), 3–13.
42. Palmer, W.S., Poncet-Montange, G., Liu, G., Petrocchi, A., Reyna, N., Subramanian, G., Theroff, J., Yau, A., Kost-Alimova, M., Bardenhagen, J.P., et al. Structure-guided design of IACS-9571, a selective high-affinity dual TRIM24-BRPF1 bromodomain inhibitor. J. Med. Chem. 59 (2015), 1440–1454.
43. Robinson, D., Van Allen, E.M., Wu, Y.M., Schultz, N., Lonigro, R.J., Mosquera, J.M., Montgomery, B., Taplin, M.E., Pritchard, C.C., Attard, G., et al. Integrative clinical genomics of advanced prostate cancer. Cell 161 (2015), 1215–1228.
44. Scher, H.I., Sawyers, C.L., Biology of progressive, castration-resistant prostate cancer: directed therapies targeting the androgen-receptor signaling axis. J. Clin. Oncol. 23 (2005), 8253–8261.
45. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
46. Sun, S., Sprenger, C.C., Vessella, R.L., Haugk, K., Soriano, K., Mostaghel, E.A., Page, S.T., Coleman, I.M., Nguyen, H.M., Sun, H., et al. Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant. J. Clin. Invest. 120 (2010), 2715–2730.
47. Taplin, M.E., Bubley, G.J., Shuster, T.D., Frantz, M.E., Spooner, A.E., Ogata, G.K., Keer, H.N., Balk, S.P., Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer. N. Engl. J. Med. 332 (1995), 1393–1398.
48. Taylor, B.S., Schultz, N., Hieronymus, H., Gopalan, A., Xiao, Y., Carver, B.S., Arora, V.K., Kaushik, P., Cerami, E., Reva, B., et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 18 (2010), 11–22.
49. TCGA, The molecular taxonomy of primary prostate cancer. Cell 163 (2015), 1011–1025.
50. Thenot, S., Henriquet, C., Rochefort, H., Cavailles, V., Differential interaction of nuclear receptors with the putative human transcriptional coactivator hTIF1. J. Biol. Chem. 272 (1997), 12062–12068.
51. Theurillat, J.P., Udeshi, N.D., Errington, W.J., Svinkina, T., Baca, S.C., Pop, M., Wild, P.J., Blattner, M., Groner, A.C., Rubin, M.A., et al. Prostate cancer. Ubiquitylome analysis identifies dysregulation of effector substrates in SPOP-mutant prostate cancer. Science 346 (2014), 85–89.
52. Tsai, W.W., Wang, Z., Yiu, T.T., Akdemir, K.C., Xia, W., Winter, S., Tsai, C.Y., Shi, X., Schwarzer, D., Plunkett, W., et al. TRIM24 links a non-canonical histone signature to breast cancer. Nature 468 (2010), 927–932.
53. Visakorpi, T., Hyytinen, E., Koivisto, P., Tanner, M., Keinanen, R., Palmberg, C., Palotie, A., Tammela, T., Isola, J., Kallioniemi, O.P., In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat. Genet. 9 (1995), 401–406.
54. vom Baur, E., Zechel, C., Heery, D., Heine, M.J., Garnier, J.M., Vivat, V., Le Douarin, B., Gronemeyer, H., Chambon, P., Losson, R., Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1. EMBO J. 15 (1996), 110–124.
55. Wang, Q., Li, W., Zhang, Y., Yuan, X., Xu, K., Yu, J., Chen, Z., Beroukhim, R., Wang, H., Lupien, M., et al. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138 (2009), 245–256.
56. Xu, K., Wu, Z.J., Groner, A.C., He, H.H., Cai, C., Lis, R.T., Wu, X., Stack, E.C., Loda, M., Liu, T., et al. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent. Science 338 (2012), 1465–1469.
57. Xue, D., Zhang, X., Liu, J., Li, N., Liu, C., Liu, Y., Wang, P., Clinical significance and biological roles of TRIM24 in human bladder carcinoma. Tumour Biol. 36 (2015), 6849–6855.
58. Zhang, L.H., Yin, A.A., Cheng, J.X., Huang, H.Y., Li, X.M., Zhang, Y.Q., Han, N., Zhang, X., TRIM24 promotes glioma progression and enhances chemoresistance through activation of the PI3K/Akt signaling pathway. Oncogene 34 (2015), 600–610.