The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis

EMBO Journal

Volumn 30, Issue 13, 2011, Pages 2719-2733

  Massie, Charles E ^a   Lynch, Andy ^a   Ramos Montoya, Antonio ^a   Boren, Joan ^a   Stark, Rory ^a   Fazli, Ladan ^b   Warren, Anne ^c   Scott, Helen ^a   Madhu, Basetti ^a   Sharma, Naomi ^a   Bon, Helene ^a   Zecchini, Vinny ^a   Smith, Donna Michelle ^a   Denicola, Gina M ^a   Mathews, Nik ^a   Osborne, Michelle ^a   Hadfield, James ^a   MacArthur, Stewart ^a   Adryan, Boris ^d   Lyons, Scott K ^a   Brindle, Kevin M ^a   Griffiths, John ^b   Gleave, Martin E ^b   Rennie, Paul S ^a   Neal, David E ^a   Mills, Ian G ^a,e   more..

^a CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^b VANCOUVER PROSTATE CENTRE   (Canada)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

androgen receptor; chromatin; metabolism; prostate cancer; transcription

Indexed keywords

ANDROGEN RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CANCER GROWTH; CONTROLLED STUDY; GENOMICS; HUMAN; HUMAN CELL; INTERDISCIPLINARY RESEARCH; METABOLIC REGULATION; METABOLOMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION;

ANIMALS; BASE SEQUENCE; BINDING SITES; BIOSYNTHETIC PATHWAYS; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; METABOLISM; MICE; MODELS, BIOLOGICAL; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; RESPONSE ELEMENTS; TRANSPLANTATION, HETEROLOGOUS;

EID: 79960071366     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.158     Document Type: Article

References (72)

1. Anderson KA, Ribar TJ, Lin F, Noeldner PK, Green MF, Muehlbauer MJ, Witters LA, Kemp BE, Means AR (2008) Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metab 7: 377-388 (Pubitemid 351598022)
2. Attar RM, Jure-Kunkel M, Balog A, Cvijic ME, Dell-John J, Rizzo CA, Schweizer L, Spires TE, Platero JS, Obermeier M, Shan W, Salvati ME, Foster WR, Dinchuk J, Chen SJ, Vite G, Kramer R, Gottardis MM (2009) Discovery of BMS-641988, a novel and potent inhibitor of androgen receptor signaling for the treatment of prostate cancer. Cancer Res 69: 6522-6530
3. Attard G, Reid AH, A'Hern R, Parker C, Oommen NB, Folkerd E, Messiou C, Molife LR, Maier G, Thompson E, Olmos D, Sinha R, Lee G, Dowsett M, Kaye SB, Dearnaley D, Kheoh T, Molina A, de Bono JS (2009) Selective inhibition of CYP17 with abiraterone acetate is highly active in the treatment of castration-resistant prostate cancer. J Clin Oncol 27: 3742-3748
4. Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3: 21-29
5. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837 (Pubitemid 46802390)
6. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326
7. Blankenberg D, Taylor J, Schenck I, He J, Zhang Y, Ghent M, Veeraraghavan N, Albert I, Miller W, Makova KD, Hardison RC, Nekrutenko A (2007) A framework for collaborative analysis of ENCODE data: making large-scale analyses biologist-friendly. Genome Res 17: 960-964 (Pubitemid 46919731)
8. Bolton EC, So AY, Chaivorapol C, Haqq CM, Li H, Yamamoto KR (2007) Cell- and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev 21: 2005-2017 (Pubitemid 47267287)
9. Boren J, Lee W-NP, Bassilian S, Centelles JJ, Lim S, Ahmed S, Boros LG, Cascante M (2003) The stable isotope-based dynamic metabolic profile of butyrate-induced HT29 cell differentiation. J Biol Chem 278: 28395-28402 (Pubitemid 36935740)
10. Brand IA, Soling HD (1974) Rat liver phosphofructokinase. Purification and characterization of its reaction mechanism. J Biol Chem 249: 7824-7831
11. Cairns JM, Dunning MJ, Ritchie ME, Russell R, Lynch AG (2008) BASH: a tool for managing BeadArray spatial artefacts. Bioinformatics 24: 2921-2922
12. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297 (Pubitemid 44646291)
13. Chen C, Sun X, Guo P, Dong XY, Sethi P, Zhou W, Zhou Z, Petros J, Frierson Jr HF, Vessella RL, Atfi A, Dong JT (2007) Ubiquitin E3 ligase WWP1 as an oncogenic factor in human prostate cancer. Oncogene 26: 2386-2394 (Pubitemid 46572813)
14. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-233 (Pubitemid 351380249)
15. Core LJ, Waterfall JJ, Lis JT (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science (New York, NY) 322: 1845-1848
16. Costello LC, Liu Y, Franklin RB, Kennedy MC (1997) Zinc inhibition of mitochondrial aconitase and its importance in citrate metabolism of prostate epithelial cells. J Biol Chem 272: 28875-28881 (Pubitemid 27498168)
17. Craft N, Shostak Y, Carey M, Sawyers CL (1999) A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat Med 5: 280-285 (Pubitemid 29124362)
18. Down TA, Hubbard TJ (2005) NestedMICA: sensitive inference of over-represented motifs in nucleic acid sequence. Nucleic Acids Res 33: 1445-1453 (Pubitemid 41418374)
19. Dunning MJ, Smith ML, Ritchie ME, Tavare S (2007) Beadarray: R classes and methods for Illumina bead-based data. Bioinformatics 23: 2183-2184 (Pubitemid 47394121)
20. Frigo DE, Howe MK, Wittmann BM, Brunner AM, Cushman I, Wang Q, Brown M, Means AR, McDonnell DP (2010) CaM Kinase Kinase {beta}-mediated activation of the growth regulatory kinase AMPK is required for androgen-dependent migration of prostate cancer cells. Cancer Res 71 : 528-537
21. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphoryla-tion of raptor mediates a metabolic checkpoint. Mol Cell 30: 214-226 (Pubitemid 351626684)
22. Haag P, Bektic J, Bartsch G, Klocker H, Eder IE (2005) Androgen receptor down regulation by small interference RNA induces cell growth inhibition in androgen sensitive as well as in androgen independent prostate cancer cells. J Steroid Biochem Mol Biol 96: 251-258 (Pubitemid 41080506)
23. Hara T, Miyazaki H, Lee A, Tran CP, Reiter RE (2008) Androgen receptor and invasion in prostate cancer. Cancer Res 68: 1128-1135 (Pubitemid 351272231)
24. Heemers H, Maes B, Foufelle F, Heyns W, Verhoeven G, Swinnen JV (2001) Androgens stimulate lipogenic gene expression in prostate cancer cells by activation of the sterol regulatory element-binding protein cleavage activating protein/sterol regulatory element-binding protein pathway. Mol Endocrinol (Baltimore, Md) 15: 1817-1828 (Pubitemid 32939311)
25. Heemers H, Verrijdt G, Organe S, Claessens F, Heyns W, Verhoeven G, Swinnen JV (2004) Identification of an androgen response element in intron 8 of the sterol regulatory element-binding protein cleavage-activating protein gene allowing direct regulation by the androgen receptor. J Biol Chem 279: 30880-30887 (Pubitemid 38938024)
26. Hellawell GO, Turner GD, Davies DR, Poulsom R, Brewster SF, Macaulay VM (2002) Expression of the type 1 insulin-like growth factor receptor is up-regulated in primary prostate cancer and commonly persists in metastatic disease. Cancer Res 62: 2942-2950 (Pubitemid 34525783)
27. Horie-Inoue K, Bono H, Okazaki Y, Inoue S (2004) Identification and functional analysis of consensus androgen response elements in human prostate cancer cells. Biochem Biophys Res Commun 325: 1312-1317 (Pubitemid 39535906)
28. Horie-Inoue K, Takayama K, Bono HU, Ouchi Y, Okazaki Y, Inoue S (2006) Identification of novel steroid target genes through the combination of bioinformatics and functional analysis of hormone response elements. Biochem Biophys Res Commun 339: 99-106 (Pubitemid 41697520)
29. Jariwala U, Prescott J, Jia L, Barski A, Pregizer S, Cogan JP, Arasheben A, Tilley WD, Scher HI, Gerald WL, Buchanan G, Coetzee GA, Frenkel B (2007) Identification of novel androgen receptor target genes in prostate cancer. Mol Cancer 6: 39
30. Jia L, Berman BP, Jariwala U, Yan X, Cogan JP, Walters A, Chen T, Buchanan G, Frenkel B, Coetzee GA (2008) Genomic androgen receptor-occupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS One 3: e3645
31. Jiang Z, Woda BA, Rock KL, Xu Y, Savas L, Khan A, Pihan G, Cai F, Babcook JS, Rathanaswami P, Reed SG, Xu J, Fanger GR (2001) P504S: a new molecular marker for the detection of prostate carcinoma. Am J Surg Pathol 25: 1397-1404 (Pubitemid 33022055)
32. Jiang Z, Woda BA, Yang XJ (2002) Alpha-methylacyl coenzyme A racemase as a marker for prostate cancer. JAMA 287: 3080-3081; author reply 3081 (Pubitemid 34633979)
33. Johnson DS, Mortazavi A, Myers RM, Wold B (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science (New York, NY) 316: 1497-1502 (Pubitemid 46906620)
34. Knudsen KE, Arden KC, Cavenee WK (1998) Multiple G1 regulatory elements control the androgen-dependent proliferation of prostatic carcinoma cells. J Biol Chem 273: 20213-20222 (Pubitemid 28377582)
35. Li H, Ruan J, Durbin R (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851-1858
36. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL, Slingerland JM, Mills GB (2007) The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 9: 218-224 (Pubitemid 46420865)
37. Lin B, Wang J, Hong X, Yan X, Hwang D, Cho JH, Yi D, Utleg AG, Fang X, Schones DE, Zhao K, Omenn GS, Hood L (2009) Integrated expression profiling and ChIP-seq analyses of the growth inhibition response program of the androgen receptor. PLoS One 4: e6589
38. Makkonen H, Kauhanen M, Jaaskelainen T, Palvimo JJ (2011) Androgen receptor amplification is reflected in the transcriptional responses of vertebral-cancer of the prostate cells. Mol Cell Endocrinol 331: 57-65
39. Margiotti K, Wafa LA, Cheng H, Novelli G, Nelson CC, Rennie PS (2007) Androgen-regulated genes differentially modulated by the androgen receptor coactivator L-dopa decarboxylase in human prostate cancer cells. Mol Cancer 6: 38
40. Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, Van den Berghe G, Carling D, Hue L (2000) Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 10: 1247-1255
41. Massie CE, Adryan B, Barbosa-Morais NL, Lynch AG, Tran MG, Neal DE, Mills IG (2007) New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep 8: 871-878 (Pubitemid 350001432)
42. Mehta PB, Jenkins BL, McCarthy L, Thilak L, Robson CN, Neal DE, Leung HY (2003) MEK5 overexpression is associated with meta-static prostate cancer, and stimulates proliferation, MMP-9 expression and invasion. Oncogene 22: 1381-1389 (Pubitemid 36384600)
43. Migita T, Ruiz S, Fornari A, Fiorentino M, Priolo C, Zadra G, Inazuka F, Grisanzio C, Palescandolo E, Shin E, Fiore C, Xie W, Kung AL, Febbo PG, Subramanian A, Mucci L, Ma J, Signoretti S, Stampfer M, Hahn WC et al (2009) Fatty acid synthase: a metabolic enzyme and candidate oncogene in prostate cancer. J Natl Cancer Inst 101: 519-532
44. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D et al (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273 (Pubitemid 36792858)
45. Park HU, Suy S, Danner M, Dailey V, Zhang Y, Li H, Hyduke DR, Collins BT, Gagnon G, Kallakury B, Kumar D, Brown ML, Fornace A, Dritschilo A, Collins SP (2009) AMP-activated protein kinase promotes human prostate cancer cell growth and survival. Mol Cancer Ther 8: 733-741
46. Perroud B, Lee J, Valkova N, Dhirapong A, Lin PY, Fiehn O, Kultz D, Weiss RH (2006) Pathway analysis of kidney cancer using pro-teomics and metabolic profiling. Mol Cancer 5: 64
47. Prescott J, Jariwala U, Jia L, Cogan JP, Barski A, Pregizer S, Shen HC, Arasheben A, Neilson JJ, Frenkel B, Coetzee GA (2007) Androgen receptor-mediated repression of novel target genes. Prostate 67: 1371-1383 (Pubitemid 47435785)
48. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A, Chinnaiyan AM (2004) ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6 (Pubitemid 38391943)
49. Roche PJ, Hoare SA, Parker MG (1992) A consensus DNA-binding site for the androgen receptor. Mol Endocrinol (Baltimore, Md) 6: 2229-2235 (Pubitemid 23021573)
50. Schmidt D, Stark R, Wilson MD, Brown GD, Odom DT (2008) Genome-scale validation of deep-sequencing libraries. PLoS One 3: e3713
51. Sherk AB, Frigo DE, Schnackenberg CG, Bray JD, Laping NJ, Trizna W, Hammond M, Patterson JR, Thompson SK, Kazmin D, Norris JD, McDonnell DP (2008) Development of a small-molecule serum- and glucocorticoid-regulated kinase-1 antagonist and its evaluation as a prostate cancer therapeutic. Cancer Res 68: 7475-7483
52. Snoek R, Cheng H, Margiotti K, Wafa LA, Wong CA, Wong EC, Fazli L, Nelson CC, Gleave ME, Rennie PS (2009) In vivo knockdown of the androgen receptor results in growth inhibition and regression of well-established, castration-resistant prostate tumors. Clin Cancer Res 15: 39-47
53. Steinkamp MP, O'Mahony OA, Brogley M, Rehman H, Lapensee EW, Dhanasekaran S, Hofer MD, Kuefer R, Chinnaiyan A, Rubin MA, Pienta KJ, Robins DM (2009) Treatment-dependent androgen receptor mutations in prostate cancer exploit multiple mechanisms to evade therapy. Cancer Res 69: 4434-4442
54. Takayama K, Kaneshiro K, Tsutsumi S, Horie-Inoue K, Ikeda K, Urano T, Ijichi N, Ouchi Y, Shirahige K, Aburatani H, Inoue S (2007) Identification of novel androgen response genes in prostate cancer cells by coupling chromatin immuno-precipitation and genomic microarray analysis. Oncogene 26: 4453-4463 (Pubitemid 47014467)
55. Taylor J, Schenck I, Blankenberg D, Nekrutenko A (2007) Using galaxy to perform large-scale interactive data analyses. Curr Protoc Bioinformatics 19: 10.5.1-10.5.25
56. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R (2002) STO-609, a specific inhibitor of the Ca(2+)/calmodulin-dependent protein kinase kinase. J Biol Chem 277: 15813-15818 (Pubitemid 34967859)
57. Tong X, Zhao F, Mancuso A, Gruber JJ, Thompson CB (2009) The glucose-responsive transcription factor ChREBP contributes to glucose-dependent anabolic synthesis and cell proliferation. Proc Natl Acad Sci USA 106: 21660-21665
58. Tran C, Ouk S, Clegg NJ, Chen Y, Watson PA, Arora V, Wongvipat J, Smith-Jones PM, Yoo D, Kwon A, Wasielewska T, Welsbie D, Chen CD, Higano CS, Beer TM, Hung DT, Scher HI, Jung ME, Sawyers CL (2009) Development of a second-generation antian-drogen for treatment of advanced prostate cancer. Science (New York, NY) 324: 787-790
59. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033
60. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D, Christofk HR, Wagner G, Rabinowitz JD, Asara JM, Cantley LC (2010) Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science (New York, NY) 329: 1492-1499
61. Varambally S, Yu J, Laxman B, Rhodes DR, Mehra R, Tomlins SA, Shah RB, Chandran U, Monzon FA, Becich MJ, Wei JT, Pienta KJ, Ghosh D, Rubin MA, Chinnaiyan AM (2005) Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 8: 393-406 (Pubitemid 41579834)
62. Velasco AM, Gillis KA, Li Y, Brown EL, Sadler TM, Achilleos M, Greenberger LM, Frost P, Bai W, Zhang Y (2004) Identification and validation of novel androgen-regulated genes in prostate cancer. Endocrinology 145: 3913-3924 (Pubitemid 39037580)
63. Veldscholte J, Ris-Stalpers C, Kuiper GG, Jenster G, Berrevoets C, Claassen E, van Rooij HC, Trapman J, Brinkmann AO, Mulder E (1990) A mutation in the ligand binding domain of the androgen receptor of human LNCaP cells affects steroid binding characteristics and response to anti-androgens. Biochem Biophys Res Commun 173: 534-540
64. Visakorpi T, Hyytinen E, Koivisto P, Tanner M, Keinanen R, Palmberg C, Palotie A, Tammela T, Isola J, Kallioniemi OP (1995) In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet 9: 401-406
65. Wang Q, Li W, Liu XS, Carroll JS, Janne OA, Keeton EK, Chinnaiyan AM, Pienta KJ, Brown M (2007) A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol Cell 27: 380-392 (Pubitemid 47126935)
66. Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J, Chen Z, Beroukhim R, Wang H, Lupien M, Wu T, Regan MM, Meyer CA, Carroll JS, Manrai AK, Janne OA, Balk SP, Mehra R, Han B, Chinnaiyan AM et al (2009) Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138: 245-256
67. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VL, Fisher EM, Tavare S, Odom DT (2008) Species-specific transcription in mice carrying human chromosome 21. Science (New York, NY) 322: 434-438
68. Wu H, Southam AD, Hines A, Viant MR (2008) High-throughput tissue extraction protocol for NMR- and MS-based meta-bolomics. Anal Biochem 372: 204-212 (Pubitemid 350116777)
69. Xu Y, Chen SY, Ross KN, Balk SP (2006) Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and post-transcriptional increases in cyclin D proteins. Cancer Res 66: 7783-7792 (Pubitemid 44289239)
70. Yu J, Mani RS, Cao Q, Brenner CJ, Cao X, Wang X, Wu L, Li J, Hu M, Gong Y, Cheng H, Laxman B, Vellaichamy A, Shankar S, Li Y, Dhanasekaran SM, Morey R, Barrette T, Lonigro RJ, Tomlins SA et al (2010) An integrated network of androgen receptor, poly-comb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 17: 443-454
71. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137
72. Zhou J, Huang W, Tao R, Ibaragi S, Lan F, Ido Y, Wu X, Alekseyev YO, Lenburg ME, Hu GF, Luo Z (2009) Inactivation of AMPK alters gene expression and promotes growth of prostate cancer cells. Oncogene 28: 1993-2002