Chromatin binding by the androgen receptor in prostate cancer

Molecular and Cellular Endocrinology

Volumn 360, Issue 1-2, 2012, Pages 44-51

  Itkonen, Harri ^a   Mills, Ian G ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Androgen receptor; Chromatin immunoprecipitation; Cistrome; Epigenetics; Prostate cancer; Transcription

Indexed keywords

ANDROGEN RECEPTOR; STEROID RECEPTOR; TUMOR MARKER;

AMINO TERMINAL SEQUENCE; CANCER CELL; CARCINOGENESIS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CLINICAL DECISION MAKING; DNA BINDING MOTIF; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INSERTION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE; PROSTATE CANCER; PROSTATE TUMOR; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; RNA SPLICING;

ANIMALS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; NUCLEIC ACID CONFORMATION; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, ANDROGEN; TRANSCRIPTION, GENETIC;

EID: 84864025407     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.09.037     Document Type: Review

References (86)

1. Abel A., Walcott J., Woods J., Duda J., Merry D.E. Expression of expanded repeat androgen receptor produces neurologic disease in transgenic mice. Hum. Mol. Genet. 2001, 10:107-116.
2. Acevedo L.G., Iniguez A.L., Holster H.L., Zhang X., Green R., Farnham P.J. Genome-scale ChIP-chip analysis using 10,000 human cells. BioTechniques 2007, 43:791-797.
3. Augello M.A., Hickey T.E., Knudsen K.E. FOXA1: master of steroid receptor function in cancer. EMBO J. 2011, 30:3885-3894.
4. Baek S.H., Ohgi K.A., Nelson C.A., Welsbie D., Chen C., Sawyers C.L., Rose D.W., Rosenfeld M.G. Ligand-specific allosteric regulation of coactivator functions of androgen receptor in prostate cancer cells. Proc Natl Acad Sci USA 2006, 103:3100-3105.
5. Baek S.H., Ohgi K.A., Rose D.W., Koo E.H., Glass C.K., Rosenfeld M.G. Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 2002, 110:55-67.
6. Berger S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447:407-412.
7. Blok L.J., de Ruiter P.E., Brinkmann A.O. Androgen receptor phosphorylation. Endocr. Res. 1996, 22:197-219.
8. Bolton E.C., So A.Y., Chaivorapol C., Haqq C.M., Li H., Yamamoto K.R. Cell- and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev. 2007, 21:2005-2017.
9. Buschhorn H.M., Klein R.R., Chambers S.M., Hardy M.C., Green S., Bearss D., Nagle R.B. Aurora-A over-expression in high-grade PIN lesions and prostate cancer. Prostate 2005, 64:341-346.
10. Buszczak M., Spradling A.C. The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes Dev. 2006, 20:977-989.
11. Chamberlain N.L., Driver E.D., Miesfeld R.L. The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucleic Acids Res. 1994, 22:3181-3186.
12. Chaturvedi N.K., Kumar S., Negi S., Tyagi R.K. Endocrine disruptors provoke differential modulatory responses on androgen receptor and pregnane and xenobiotic receptor: potential implications in metabolic disorders. Mol. Cell Biochem. 2010, 345:291-308.
13. Chen S., Kesler C.T., Paschal B.M., Balk S.P. Androgen receptor phosphorylation and activity are regulated by an association with protein phosphatase 1. J. Biol. Chem. 2009, 284:25576-25584.
14. Chen S., Xu Y., Yuan X., Bubley G.J., Balk S.P. Androgen receptor phosphorylation and stabilization in prostate cancer by cyclin-dependent kinase 1. Proc. Natl. Acad. Sci. USA 2006, 103:15969-15974.
15. Chi P., Chen Y., Zhang L., Guo X., Wongvipat J., Shamu T., Fletcher J.A., Dewell S., Maki R.G., Zheng D., Antonescu C.R., Allis C.D., Sawyers C.L. ETV1 is a lineage survival factor that cooperates with KIT in gastrointestinal stromal tumours. Nature 2010, 467:849-853.
16. Choong C.S., Kemppainen J.A., Wilson E.M. Evolution of the primate androgen receptor: a structural basis for disease. J. Mol. Evol. 1998, 47:334-342.
17. Clark E.L., Coulson A., Dalgliesh C., Rajan P., Nicol S.M., Fleming S., Heer R., Gaughan L., Leung H.Y., Elliott D.J., Fuller-Pace F.V., Robson C.N. The RNA helicase p68 is a novel androgen receptor coactivator involved in splicing and is overexpressed in prostate cancer. Cancer Res. 2008, 68:7938-7946.
18. Dahl J.A., Collas P. MicroChIP: chromatin immunoprecipitation for small cell numbers. Methods Mol. Biol. 2009, 567:59-74.
19. de Cristofaro T., Affaitati A., Feliciello A., Avvedimento E.V., Varrone S. Polyglutamine-mediated aggregation and cell death. Biochem. Biophys. Res. Commun. 2000, 272:816-821.
20. De Vos P., Claessens F., Peeters B., Rombauts W., Heyns W., Verhoeven G. Interaction of androgen and glucocorticoid receptor DNA-binding domains with their response elements. Mol. Cell Endocrinol. 1993, 90:R11-16.
21. Dhanasekaran S.M., Barrette T.R., Ghosh D., Shah R., Varambally S., Kurachi K., Pienta K.J., Rubin M.A., Chinnaiyan A.M. Delineation of prognostic biomarkers in prostate cancer. Nature 2001, 412:822-826.
22. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 1988, 240:889-895.
23. Fanelli, M., Amatori, S., Barozzi, I., Soncini, M., Dal Zuffo, R., Bucci, G., Capra, M., Quarto, M., Dellino, G.I., Mercurio, C., Alcalay, M., Viale, G., Pelicci, P.G., Minucci, S., 2010. Pathology tissue-chromatin immunoprecipitation, coupled with high-throughput sequencing, allows the epigenetic profiling of patient samples. Proc. Natl. Acad. Sci. USA.
24. Feinberg A.P. Epigenomics reveals a functional genome anatomy and a new approach to common disease. Nat. Biotechnol. 2010, 28:1049-1052.
25. Feng S., Jacobsen S.E., Reik W. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
26. Fitzwater T., Polisky B. A SELEX primer. Methods Enzymol. 1996, 267:275-301.
27. Friedman J.R., Kaestner K.H. The Foxa family of transcription factors in development and metabolism. Cell. Mol. Life Sci. 2006, 63:2317-2328.
28. Fukuda T., Yamagata K., Fujiyama S., Matsumoto T., Koshida I., Yoshimura K., Mihara M., Naitou M., Endoh H., Nakamura T., Akimoto C., Yamamoto Y., Katagiri T., Foulds C., Takezawa S., Kitagawa H., Takeyama K., O'Malley B.W., Kato S. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat. Cell Biol. 2007, 9:604-611.
29. Fullwood. M.J., Han. Y., Wei. C.L., Ruan. X., Ruan. Y., 2010. Chromatin interaction analysis using paired-end tag sequencing. Curr. Protoc. Mol. Biol. Chap. 21: Unit 21 15 21-25.
30. Gaughan, L., Stockley, J., Wang, N., McCracken, S.R., Treumann, A., Armstrong, K., Shaheen, F., Watt, K., McEwan, I.J., Wang, C., Pestell, R.G., Robson, C.N., 2010. Regulation of the androgen receptor by SET9-mediated methylation. Nucleic Acids Res.
31. Griekspoor A., Zwart W., Neefjes J., Michalides R. Visualizing the action of steroid hormone receptors in living cells. Nucl. Recept. Signal. 2007, 5:e003.
32. Haffner M.C., Aryee M.J., Toubaji A., Esopi D.M., Albadine R., Gurel B., Isaacs W.B., Bova G.S., Liu W., Xu J., Meeker A.K., Netto G., De Marzo A.M., Nelson W.G., Yegnasubramanian S. Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat. Genet. 2010, 42:668-675.
33. Hakimi J.M., Schoenberg M.P., Rondinelli R.H., Piantadosi S., Barrack E.R. Androgen receptor variants with short glutamine or glycine repeats may identify unique subpopulations of men with prostate cancer. Clin. Cancer Res. 1997, 3:1599-1608.
34. He B., Kemppainen J.A., Wilson E.M. FXXLF and WXXLF sequences mediate the NH2-terminal interaction with the ligand binding domain of the androgen receptor. J. Biol. Chem. 2000, 275:22986-22994.
35. Heinrich M.C., Corless C.L. Cancer: oncogenes in context. Nature 2010, 467:796-797.
36. Heintzman N.D., Hon G.C., Hawkins R.D., Kheradpour P., Stark A., Harp L.F., Ye Z., Lee L.K., Stuart R.K., Ching C.W., Ching K.A., Antosiewicz-Bourget J.E., Liu H., Zhang X., Green R.D., Lobanenkov V.V., Stewart R., Thomson J.A., Crawford G.E., Kellis M., Ren B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
37. Heintzman N.D., Stuart R.K., Hon G., Fu Y., Ching C.W., Hawkins R.D., Barrera L.O., Van Calcar S., Qu C., Ching K.A., Wang W., Weng Z., Green R.D., Crawford G.E., Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
38. Hollenhorst P.C., Shah A.A., Hopkins C., Graves B.J. Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 2007, 21:1882-1894.
39. Jenster G., van der Korput H.A., Trapman J., Brinkmann A.O. Identification of two transcription activation units in the N-terminal domain of the human androgen receptor. J. Biol. Chem. 1995, 270:7341-7346.
40. Jia L., Berman B.P., Jariwala U., Yan X., Cogan J.P., Walters A., Chen T., Buchanan G., Frenkel B., Coetzee G.A. Genomic androgen receptor-occupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS ONE 2008, 3:e3645.
41. Johnstone S.E., Baylin S.B. Stress and the epigenetic landscape: a link to the pathobiology of human diseases?. Nat. Rev. Genet. 2010, 11:806-812.
42. Kazemi-Esfarjani P., Trifiro M.A., Pinsky L. Evidence for a repressive function of the long polyglutamine tract in the human androgen receptor: possible pathogenetic relevance for the (CAG)n-expanded neuronopathies. Hum. Mol. Genet. 1995, 4:523-527.
43. Keay J., Thornton J.W. Hormone-activated estrogen receptors in annelid invertebrates: implications for evolution and endocrine disruption. Endocrinology 2009, 150:1731-1738.
44. Kim J., Roh M., Abdulkadir S.A. Pim1 promotes human prostate cancer cell tumorigenicity and c-MYC transcriptional activity. BMC Cancer 2010, 10:248.
45. Kuiper G.G., Brinkmann A.O. Phosphotryptic peptide analysis of the human androgen receptor: detection of a hormone-induced phosphopeptide. Biochemistry 1995, 34:1851-1857.
46. Kumar-Sinha C., Tomlins S.A., Chinnaiyan A.M. Recurrent gene fusions in prostate cancer. Nat. Rev. Cancer 2008, 8:497-511.
47. La Spada A.R., Wilson E.M., Lubahn D.B., Harding A.E., Fischbeck K.H. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 1991, 352:77-79.
48. Lalevee S., Ferry C., Rochette-Egly C. Phosphorylation control of nuclear receptors. Methods Mol. Biol. 2010, 647:251-266.
49. Libertini S., Abagnale A., Passaro C., Botta G., Portella G. Aurora A and B kinases - targets of novel anticancer drugs. Recent Pat. Anticancer Drug Discov. 2010, 5:219-241.
50. Magee J.A., Chang L.W., Stormo G.D., Milbrandt J. Direct, androgen receptor-mediated regulation of the FKBP5 gene via a distal enhancer element. Endocrinology 2006, 147:590-598.
51. Majumder S., Liu Y., Ford O.H., Mohler J.L., Whang Y.E. Involvement of arginine methyltransferase CARM1 in androgen receptor function and prostate cancer cell viability. Prostate 2006, 66:1292-1301.
52. Massie C.E., Adryan B., Barbosa-Morais N.L., Lynch A.G., Tran M.G., Neal D.E., Mills I.G. New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep. 2007, 8:871-878.
53. Massie C.E., Lynch A., Ramos-Montoya A., Boren J., Stark R., Fazli L., Warren A., Scott H., Madhu B., Sharma N., Bon H., Zecchini V., Smith D.M., Denicola G.M., Mathews N., Osborne M., Hadfield J., Macarthur S., Adryan B., Lyons S.K., Brindle K.M., Griffiths J., Gleave M.E., Rennie P.S., Neal D.E., Mills I.G. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011, 30:2719-2733.
54. Massie C.E., Mills I.G. ChIPping away at gene regulation. EMBO Rep. 2008, 9:337-343.
55. Metzger E., Wissmann M., Yin N., Muller J.M., Schneider R., Peters A.H., Gunther T., Buettner R., Schule R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
56. Meyer R., Wolf S.S., Obendorf M. PRMT2, a member of the protein arginine methyltransferase family, is a coactivator of the androgen receptor. J. Steroid Biochem. Mol. Biol. 2007, 107:1-14.
57. Nemoto T., Ohara-Nemoto Y., Ota M. Association of the 90-kDa heat shock protein does not affect the ligand-binding ability of androgen receptor. J. Steroid Biochem. Mol. Biol. 1992, 42:803-812.
58. Papini S., Rosellini A., De Matteis A., Campani D., Selli C., Caporali A., Bettuzzi S., Revoltella R.P. Establishment of an organotypic in vitro culture system and its relevance to the characterization of human prostate epithelial cancer cells and their stromal interactions. Pathol. Res. Pract. 2007, 203:209-216.
59. Passer B.J., Wu C.L., Wu S., Rabkin S.D., Martuza R.L. Analysis of genetically engineered oncolytic herpes simplex viruses in human prostate cancer organotypic cultures. Gene Ther. 2009, 16:1477-1482.
60. Quigley C.A., De Bellis A., Marschke K.B., el-Awady M.K., Wilson E.M., French F.S. Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr. Rev. 1995, 16:271-321.
61. Richly H., Lange M., Simboeck E., Di Croce L. Setting and resetting of epigenetic marks in malignant transformation and development. BioEssays 2010, 32:669-679.
62. Robinson J.L., Macarthur S., Ross-Innes C.S., Tilley W.D., Neal D.E., Mills I.G., Carroll J.S. Androgen receptor driven transcription in molecular apocrine breast cancer is mediated by FoxA1. EMBO J. 2011, 30:3019-3027.
63. Roh T.Y., Cuddapah S., Zhao K. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev. 2005, 19:542-552.
64. Sandelin A., Alkema W., Engstrom P., Wasserman W.W., Lenhard B. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 2004, 32:D91-94.
65. Sahu B., Laakso M., Ovaska K., Mirtti T., Lundin J., Rannikko A., Sankila A., Turunen J.P., Lundin M., Konsti J., Vesterinen T., Nordling S., Kallioniemi O., Hautaniemi S., Janne O.A. Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J. 2011, 30:3962-3976.
66. Shu S.K., Liu Q., Coppola D., Cheng J.Q. Phosphorylation and activation of androgen receptor by Aurora-A. J. Biol. Chem. 2010, 285:33045-33053.
67. Simental J.A., Sar M., Lane M.V., French F.S., Wilson E.M. Transcriptional activation and nuclear targeting signals of the human androgen receptor. J. Biol. Chem. 1991, 266:510-518.
68. Takayama K., Kaneshiro K., Tsutsumi S., Horie-Inoue K., Ikeda K., Urano T., Ijichi N., Ouchi Y., Shirahige K., Aburatani H., Inoue S. Identification of novel androgen response genes in prostate cancer cells by coupling chromatin immunoprecipitation and genomic microarray analysis. Oncogene 2007, 26:4453-4463.
69. Tanner T.M., Denayer S., Geverts B., Van Tilborgh N., Kerkhofs S., Helsen C., Spans L., Dubois V., Houtsmuller A.B., Claessens F., Haelens A. A 629RKLKK633 motif in the hinge region controls the androgen receptor at multiple levels. Cell. Mol. Life Sci. 2010, 67:1919-1927.
70. Tomlins S.A., Rhodes D.R., Perner S., Dhanasekaran S.M., Mehra R., Sun X.W., Varambally S., Cao X., Tchinda J., Kuefer R., Lee C., Montie J.E., Shah R.B., Pienta K.J., Rubin M.A., Chinnaiyan A.M. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310:644-648.
71. Urbanucci A., Sahu B., Seppala J., Larjo A., Latonen L.M., Waltering K.K., Tammela T.L., Vessella R.L., Lahdesmaki H., Janne O.A., Visakorpi T. Overexpression of androgen receptor enhances the binding of the receptor to the chromatin in prostate cancer. Oncogene. 2011, doi: 10.1038/onc.2011.401.
72. van der Poel H.G., Zevenhoven J., Bergman A.M. Pim1 regulates androgen-dependent survival signaling in prostate cancer cells. Urol. Int. 2010, 84:212-220.
73. Vassetzky Y., Gavrilov A., Eivazova E., Priozhkova I., Lipinski M., Razin S. Chromosome conformation capture (from 3C to 5C) and its ChIP-based modification. Methods Mol. Biol. 2009, 567:171-188.
74. Walters K.A., Simanainen U., Handelsman D.J. Molecular insights into androgen actions in male and female reproductive function from androgen receptor knockout models. Hum. Reprod. Update 2010, 16:543-558.
75. Wang Q., Li W., Liu X.S., Carroll J.S., Janne O.A., Keeton E.K., Chinnaiyan A.M., Pienta K.J., Brown M. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 2007, 27:380-392.
76. Wang Q., Li W., Zhang Y., Yuan X., Xu K., Yu J., Chen Z., Beroukhim R., Wang H., Lupien M., Wu T., Regan M.M., Meyer C.A., Carroll J.S., Manrai A.K., Janne O.A., Balk S.P., Mehra R., Han B., Chinnaiyan A.M., Rubin M.A., True L., Fiorentino M., Fiore C., Loda M., Kantoff P.W., Liu X.S., Brown M. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 2009, 138:245-256.
77. Wang Z., Zang C., Rosenfeld J.A., Schones D.E., Barski A., Cuddapah S., Cui K., Roh T.Y., Peng W., Zhang M.Q., Zhao K. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 2008, 40:897-903.
78. Ward R.D., Weigel N.L. Steroid receptor phosphorylation: assigning function to site-specific phosphorylation. BioFactors 2009, 35:528-536.
79. Wingender E., Dietze P., Karas H., Knuppel R. TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res. 1996, 24:238-241.
80. Wissmann M., Yin N., Muller J.M., Greschik H., Fodor B.D., Jenuwein T., Vogler C., Schneider R., Gunther T., Buettner R., Metzger E., Schule R. Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat. Cell Biol. 2007, 9:347-353.
81. Wong H.Y., Demmers J.A., Bezstarosti K., Grootegoed J.A., Brinkmann A.O. DNA dependent recruitment of DDX17 and other interacting proteins by the human androgen receptor. Biochim. Biophys. Acta 2009, 1794:193-198.
82. Xu P.L., Liu Y.Q., Shan S.F., Kong Y.Y., Zhou Q., Li M., Ding J.P., Xie Y.H., Wang Y. Molecular mechanism for the potentiation of the transcriptional activity of human liver receptor homolog 1 by steroid receptor coactivator-1. Mol. Endocrinol. 2004, 18:1887-1905.
83. Ye X., Han S.J., Tsai S.Y., DeMayo F.J., Xu J., Tsai M.J., O'Malley B.W. Roles of steroid receptor coactivator (SRC)-1 and transcriptional intermediary factor (TIF) 2 in androgen receptor activity in mice. Proc. Natl. Acad. Sci. USA 2005, 102:9487-9492.
84. Yu J., Mani R.S., Cao Q., Brenner C.J., Cao X., Wang X., Wu L., Li J., Hu M., Gong Y., Cheng H., Laxman B., Vellaichamy A., Shankar S., Li Y., Dhanasekaran S.M., Morey R., Barrette T., Lonigro R.J., Tomlins S.A., Varambally S., Qin Z.S., Chinnaiyan A.M. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 2010, 17:443-454.
85. Zecchini V., Mills I.G. Putting chromatin immunoprecipitation into context. J. Cell. Biochem. 2009, 107:19-29.
86. Zhou X. Roles of androgen receptor in male and female reproduction: lessons from global and cell-specific androgen receptor knockout (ARKO) mice. J. Androl. 2010, 31:235-243.