Androgen receptor acetylation sites differentially regulate gene control

Journal of Cellular Biochemistry

Volumn 104, Issue 2, 2008, Pages 511-524

  Faus, Hortensia ^a,b   Haendler, Bernard ^a  

^a BAYER PHARMA AG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Acetylation; Androgen receptor; Nuclear localization; Promoter

Indexed keywords

ANDROGEN RECEPTOR;

ACETYLATION; ARTICLE; CELLULAR DISTRIBUTION; GENE CONTROL; GENE TRANSLOCATION; GENETIC DIFFERENCE; IMMUNOPRECIPITATION; MUTANT; NUCLEOLUS; PRIORITY JOURNAL; RECEPTOR BINDING; WILD TYPE;

ACETYLATION; AMINO ACID MOTIFS; BINDING SITES; CELL LINE; HUMANS; MUTATION; PROMOTER REGIONS (GENETICS); RECEPTORS, ANDROGEN; RESPONSE ELEMENTS;

MOUSE MAMMARY TUMOR VIRUS;

EID: 43449108865     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21640     Document Type: Article

References (67)

1. An W. 2007. Histone acetylation and methylation: Combinatorial players for transcriptional regulation. Subcell Biochem 41:351-369.
2. Barbulescu K, Geserick C, Schüttke I, Schleuning WD, Haendler B. 2001. New androgen response elements in the murine pem promoter mediate selective transactivation. Mol Endocrinol 15:1803-1816.
3. Buchanan G, Yang M, Harris JM, Nahm HS, Han G, Moore N, Bentel JM, Matusik RJ, Horsfall DJ, Marshall VR, Greenberg NM, Tilley WD. 2001. Mutations at the boundary of the hinge and ligand binding domain of the androgen receptor confer increased transactivation function. Mol Endocrinol 15:46-56.
4. Callewaert L, Verrijdt G, Christiaens V, Haelens A, Claessens F. 2003. Dual function of an amino-terminal amphipatic helix in androgen receptor-mediated transactivation through specific and nonspecific response elements. J Biol Chem 278:8212-8218.
5. Cato AC, Henderson D, Ponta H. 1987. The hormone response element of the mouse mammary tumour virus DNA mediates the progestin and androgen induction of transcription in the proviral long terminal repeat region. EMBO J 6:363-368.
6. Chen L, Meng S, Wang H, Bali P, Bai W, Li B, Atadja P, Bhalla KN, Wu J. 2005. Chemical ablation of androgen receptor in prostate cancer cells by the histone deacetylase inhibitor L AQ824. Mol Cancer Ther 4:1311-1319.
7. Cleutjens KB, van Eekelen CC, van der Korput HA, Brinkmann AO, Trapman J. 1996. Two androgen response regions cooperate in steroid hormone regulated activity of the prostate-specific antigen promoter. J Biol Chem 271:6379-6388.
8. Conway K, Parrish E, Edmiston SN, Tolbert D, Tse CK, Geradts J, Livasy CA, Singh H, Newman B, Millikan RC. 2005. The estrogen receptor-alpha A908G (K303R) mutation occurs at a low frequency in invasive breast tumors: Results from a population-based study. Breast Cancer Res 7:R871-R880.
9. Cui Y, Zhang M, Pestell R, Curran EM, Welshons WV, Fuqua SA. 2004. Phosphorylation of estrogen receptor alpha blocks its acetylation and regulates estrogen sensitivity. Cancer Res 64:9199-9208.
10. Dai Y, Ngo D, Forman LW, Qin DC, Jacob J, Faller DV. 2007. Sirt1 is required for antagonist-induced transcriptional repression of androgen-responsive genes by the androgen receptor. Mol Endocrinol 21:1807-1821.
11. Eakin CM, Maccoss MJ, Finney GL, Klevit RE. 2007. Estrogen receptor alpha is a putative substrate for the BRCA1 ubiquitin ligase. Proc Natl Acad Sci USA 104: 5794-5799.
12. Faus H, Haendler B. 2006. Post-translational modifications of steroid receptors. Biomed Pharmacother 60:520-528.
13. Fiskus W, Ren Y, Mohapatra A, Bali P, Mandawat A, Rao R, Herger B, Yang Y, Atadja P, Wu J, Bhalla K. 2007. Hydroxamic acid analogue histone deacetylase inhibitors attenuate estrogen receptor-alpha levels and transcriptional activity: A result of hyperacetylation and inhibition of chaperone function of heat shock protein 90. Clin Cancer Res 13:4882-4890.
14. Fraga MF, Esteller M. 2005. Towards the human cancer epigenome: A first draft of histone modifications. Cell Cycle 4:1377-1381.
15. Fronsdal K, Saatcioglu F. 2005. Histone deacetylase inhibitors differentially mediate apoptosis in prostate cancer cells. Prostate 62:299-306.
16. Fu M, Wang C, Reutens AT, Wang J, Angeletti RH, Siconolfi-Baez L, Ogryzko V, Avantaggiati ML, Pestell RG. 2000. p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J Biol Chem 275:20853-20860.
17. Fu M, Wang C, Wang J, Zhang X, Sakamaki T, Yeung YG, Chang C, Hopp T, Fuqua SA, Jaffray E, Hay RT, Palvimo JJ, Jänne OA, Pestell RG. 2002. Androgen receptor acetylation governs trans activation and MEKK1-induced apoptosis without affecting in vitro sumoylation and trans-repression function. Mol Cell Biol 22:3373-3388.
18. Fu M, Rao M, Wang C, Sakamaki T, Wang J, Di Vizio D, Zhang X, Albanese C, Balk S, Chang C, Fan S, Rosen E, Palvimo JJ, Jänne OA, Muratoglu S, Avantaggiati ML, Pestell RG. 2003a. Acetylation of androgen receptor enhances coactivator binding and promotes prostate cancer cell growth. Mol Cell Biol 23:8563-8575.
19. Fu M, Wang C, Zhang X, Pestell R. 2003b. Nuclear receptor modifications and endocrine cell proliferation. J Steroid Biochem Mol Biol 85:133-138.
20. Fu M, Rao M, Wu K, Wang C, Zhang X, Hessien M, Yeung YG, Gioeli D, Weber MJ, Pestell RG. 2004a. The androgen receptor acetylation site regulates cAMP and AKT but not ERK-induced activity. J Biol Chem 279: 29436-29449.
21. Fu M, Wang C, Zhang X, Pestell RG. 2004b. Acetylation of nuclear receptors in cellular growth and apoptosis. Biochem Pharmacol 68:1199-1208.
22. Fu M, Liu M, Sauve AA, Jiao X, Zhang X, Wu X, Powell MJ, Yang T, Gu W, Avantaggiati ML, Pattabiraman N, Pestell TG, Wang F, Quong AA, Wang C, Pestell RG. 2006. Hormonal control of androgen receptor function through SI RT1. Mol Cell Biol 26:8122-8135.
23. Gaughan L, Brady ME, Cook S, Neal DE, Robson CN. 2001. Tip60 is a co-activator specific for class I nuclear hormone receptors. J Biol Chem 276:46841-46848.
24. Gaughan L, Logan IR, Cook S, Neal DE, Robson CN. 2002. Tip60 and histone deacetylase 1 regulate androgen receptor activity through changes to the acetylation status of the receptor. J Biol Chem 277:25904-25913.
25. Gaughan L, Logan IR, Neal DE, Robson CN. 2005. Regulation of androgen receptor and histone deacetylase 1 by Mdm2-mediated ubiquitylation. Nucleic Acids Res 33:13-26.
26. Geserick C, Meyer HA, Barbulescu K, Haendler B. 2003. Differential modulation of androgen receptor action by deoxyribonucleic acid response elements. Mol Endocrinol 17:1738-1750.
27. Glozak MA, Sengupta N, Zhang X, Seto E. 2005. Acetylation and deacetylation of non-histone proteins. Gene 363:15-23.
28. Gong J, Zhu J, Goodman OB Jr, Pestell RG, Schlegel PN, Nanus DM, Shen R. 2006. Activation of p300 histone acetyltransferase activity and acetylation of the androgen receptor by bombesin in prostate cancer cells. Oncogene 25:2011-2021.
29. Haelens A, Tanner T, Denayer S, Callewaert L, Claessens F. 2007. The hinge region regulates DNA binding, nuclear translocation, and transactivation of the androgen receptor. Cancer Res 67:4514-4523.
30. He B, Kemppainen JA, Wilson EM. 2000. FXXLF and WXXLF sequences mediate the NH2-terminal interaction with the ligand binding domain of the androgen receptor. J Biol Chem 275:22986-22994.
31. He B, Lee LW, Minges JT, Wilson EM. 2002. Dependence of selective gene activation on the androgen receptor NH2-and COOH-terminal interaction. J Biol Chem 277: 25631-25639.
32. Hong CY, Gong EY, Kim K, Suh JH, Ko HM, Lee HJ, Choi HS, Lee K. 2005. Modulation of the expression and transactivation of androgen receptor by the basic helix-loop-helix transcription factor Pod-1 through recruitment of histone deacetylase 1. Mol Endocrinol 19:2245-2257.
33. Ikonen T, Palvimo JJ, Jänne OA. 1997. Interaction between the amino- and carboxyl-terminal regions of the rat androgen receptor modulates transcriptional activity and is influenced by nuclear receptor coactivators. J Biol Chem 272:29821-29828.
34. Ito K, Yamamura S, Essilfie-Quaye S, Cosio B, Ito M, Barnes PJ, Adcock IM. 2006. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. J Exp Med 203:7-13.
35. Jeong BC, Hong CY, Chattopadhyay S, Park JH, Gong EY, Kim HJ, Chun SY, Lee K. 2004. Androgen receptor corepressor-19 kDa (ARR19), a leucine-rich protein that represses the transcriptional activity of androgen receptor through recruitment of histone deacetylase. Mol Endocrinol 18:13-25.
36. Karvonen U, Jänne OA, Palvimo JJ. 2006. Androgen receptor regulates nuclear trafficking and nuclear domain residency of corepressor HDAC7 in a ligand-dependent fashion. Exp Cell Res 312:3165-3183.
37. Kasper S, Smith JA Jr. 2004. Genetically modified mice and their use in developing therapeutic strategies for prostate cancer. J Urol 172:12-19.
38. Kim MY, Woo EM, Chong YT, Homenko DR, Kraus WL. 2006. Acetylation of estrogen receptor alpha by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol Endocrinol 20:1479-1493.
39. Korkmaz CG, Fronsdal K, Zhang Y, Lorenzo PI, Saatcioglu F. 2004. Potentiation of androgen receptor transcriptional activity by inhibition of histone deacetylation - Rescue of transcriptionally compromised mutants. J Endocrinol 182:377-389.
40. Kouzarides T. 2000. Acetylation: A regulatory modification to rival phosphorylation? EMBO J 19:1176-1179.
41. Lee YS, Kim HJ, Lee HJ, Lee JW, Chun SY, Ko SK, Lee K. 2002. Activating signal cointegrator 1 is highly expressed in murine testicular Leydig cells and enhances the ligand-dependent transactivation of androgen receptor. Biol Reprod 67:1580-1587.
42. Liao G, Chen LY, Zhang A, Godavarthy A, Xia F, Ghosh JC, Li H, Chen JD. 2003. Regulation of androgen receptor activity by the nuclear receptor corepressor SMRT. J Biol Chem 278:5052-5061.
43. Loven MA, Muster N, Yates JR, Nardulli AM. 2003. A novel estrogen receptor alpha-associated protein, template-activating factor I beta, inhibits acetylation and transactivation. Mol Endocrinol 17:67-78.
44. Loven MA, Davis RE, Curtis CD, Muster N, Yates JR, Nardulli AM. 2004. A novel estrogen receptor alpha-associated protein alters receptor- deoxyribonucleic acid interactions and represses receptor-mediated transcription. Mol Endocrinol 18:2649-2659.
45. Loy CJ, Sim KS, Yong EL. 2003. Filamin-A fragment localizes to the nucleus to regulate androgen receptor and coactivator functions. Proc Natl Acad Sci USA 100:4562-4567.
46. Maclean JA II, Chen MA, Wayne CM, Bruce SR, Rao M, Meistrich ML, Macleod C, Wilkinson MF. 2005. Rhox: A new homeobox gene cluster. Cell 120:369-382.
47. Margueron R, Duong V, Castet A, Cavailles V. 2004. Histone deacetylase inhibition and estrogen signalling in human breast cancer cells. Biochem Pharmacol 68: 1239-1246.
48. Marrocco DL, Tilley WD, Bianco-Miotto T, Evdokiou A, Scher HI, Rifkind RA, Marks PA, Richon VM, Butler LM. 2007. Suberoylanilide hydroxamic acid (vorinostat) represses androgen receptor expression and acts synergistically with an androgen receptor antagonist to inhibit prostate cancer cell proliferation. Mol Cancer Ther 6: 51-60.
49. Mishra SK, Mazumdar A, Vadlamudi RK, Li F, Wang RA, Yu W, Jordan VC, Santen RJ, Kumar R. 2003. MICoA, a novel metastasis-associated protein 1 (MTA1) interacting protein coactivator, regulates estrogen receptor-alpha transactivation functions. J Biol Chem 278:19209-19219.
50. Pascual-Le Tallec L, Lombes M. 2005. The mineralocorticoid receptor: A journey exploring its diversity and specificity of action. Mol Endocrinol 19:2211-2221.
51. Pledgie-Tracy A, Sobolewski MD, Davidson NE. 2007. Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol Cancer Ther 6: 1013-1021.
52. Popov VM, Wang C, Shirley LA, Rosenberg A, Li S, Nevalainen M, Fu M, Pestell RG. 2007. The functional significance of nuclear receptor acetylation. Steroids 72:221-230.
53. Poukka H, Aarnisalo P, Karvonen U, Palvimo JJ, Jänne OA. 1999. Ubc9 interacts with the androgen receptor and activates receptor-dependent transcription. J Biol Chem 274:19441-19446.
54. Poukka H, Karvonen U, Yoshikawa N, Tanaka H, Palvimo JJ, Jänne OA. 2000. The RING finger protein SNURF modulates nuclear trafficking of the androgen receptor. J Cell Sci 113(Pt 17):2991-3001.
55. Rokhlin OW, Glover RB, Guseva NV, Taghiyev AF, Kohlgraf KG, Cohen MB. 2006. Mechanisms of cell death induced by histone deacetylase inhibitors in androgen receptor-positive prostate cancer cells. Mol Cancer Res 4:113-123.
56. Salas TR, Kim J, Vakar-Lopez F, Sabichi AL, Troncoso P, Jenster G, Kikuchi A, Chen SY, Shemshedini L, Suraokar M, Logothetis CJ, DiGiovanni J, Lippman SM, Menter DG. 2004. Glycogen synthase kinase-3 beta is involved in the phosphorylation and suppression of androgen receptor activity. J Biol Chem 279:19191-19200.
57. Schauwaers K, De Gendt K, Saunders PT, Atanassova N, Haelens A, Callewaert L, Moehren U, Swinnen JV, Verhoeven G, Verrijdt G, Claessens F. 2007. Loss of androgen receptor binding to selective androgen response elements causes a reproductive phenotype in a knockin mouse model. Proc Natl Acad Sci USA 104: 4961-4966.
58. Scroggins BT, Robzyk K, Wang D, Marcu MG, Tsutsumi S, Beebe K, Cotter RJ, Felts S, Toft D, Karnitz L, Rosen N, Neckers L. 2007. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 25:151-159.
59. Sentis S, Le Romancer M, Bianchin C, Rostan MC, Corbo L. 2005. Sumoylation of the estrogen receptor alpha hinge region regulates its transcriptional activity. Mol Endocrinol 19:2671-2684.
60. Shi XB, Ma AH, Xia L, Kung HJ, de Vere White RW. 2002. Functional analysis of 44 mutant androgen receptors from human prostate cancer. Cancer Res 62:1496-1502.
61. Tanner T, Claessens F, Haelens A. 2004. The hinge region of the androgen receptor plays a role in proteasome-mediated transcriptional activation. Ann NY Acad Sci 1030:587-592.
62. Tao RH, Kawate H, Wu Y, Ohnaka K, Ishizuka M, Inoue A, Hagiwara H, Takayanagi R. 2006. Testicular zinc finger protein recruits histone deacetylase 2 and suppresses the transactivation function and intranuclear foci formation of agonist-bound androgen receptor competitively with T IF2. Mol Cell Endocrinol 247:150-165.
63. Thomas M, Dadgar N, Aphale A, Harrell JM, Kunkel R, Pratt WB, Lieberman AP. 2004. Androgen receptor acetylation site mutations cause trafficking defects, misfolding, and aggregation similar to expanded glutamine tracts. J Biol Chem 279:8389-8395.
64. Thompson J, Hyytinen ER, Haapala K, Rantala I, Helin HJ, Jänne OA, Palvimo JJ, Koivisto PA. 2003. Androgen receptor mutations in high-grade prostate cancer before hormonal therapy. Lab Invest 83:1709-1713.
65. Wang C, Fu M, Angeletti RH, Siconolfi-Baez L, Reutens AT, Albanese C, Lisanti MP, Katzenellenbogen BS, Kato S, Hopp T, Fuqua SA, Lopez GN, Kushner PJ, Pestell RG. 2001a. Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J Biol Chem 276:18375-18383.
66. Wang Q, Lu J, Yong EL. 2001b. Ligand- and coactivator-mediated transactivation function (AF2) of the androgen receptor ligand-binding domain is inhibited by the cognate hinge region. J Biol Chem 276:7493-7499.
67. Zhou ZX, Sar M, Simental JA, Lane MV, Wilson EM. 1994. A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor. Requirement for the DNA-binding domain and modulation by NH2-terminal and carboxyl-terminal sequences. J Biol Chem 269:13115-13123.