Home LiteratureArticle Details
PMID: 15743818 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

BAF57 governs androgen receptor action and androgen-dependent proliferation through SWI/SNF.

Molecular and cellular biology ·Vol. 25 ·No. 6 ·2005-03-00 ·Pages 2200-15

Link KA, Burd CJ, Williams E, Marshall T, Rosson G, Henry E, Weissman B, Knudsen KE

Abstract

Androgen receptor (AR) activity is required for prostate cancer development and progression. Thus, there is a major impetus to understand the regulation of AR action. We and others have previously shown that AR transactivation potential is dependent on the presence of an active SWI/SNF chromatin remodeling complex. However, the mechanisms underlying SWI/SNF regulation of the AR remained unsolved. We show here that the BAF57 subunit, an accessory component of the remodeling complex, is a critical regulator of AR function. We show that BAF57 is expressed in the luminal epithelia of the prostate and is required for AR-dependent transactivation in prostatic adenocarcinoma cells. Our data reveal that BAF57 can directly bind to the AR and is recruited to endogenous AR targets upon ligand activation. Loss of BAF57 or inhibition of BAF57 function severely compromised AR activity, as observed with both exogenous and endogenous AR targets. Rescue of BAF57 function restored AR activity, thus demonstrating a specific requirement of BAF57 for AR activity. This action of BAF57 proved to be dependent on SWI/SNF ATPase function. BAF57 has previously been implicated in nuclear receptor coactivator function, and we show that, although BAF57 facilitated coactivator activity, only a selected subset required BAF57 for coactivator function. Lastly, we demonstrate that both BAF57 and BRM are required for the proliferation of AR-dependent prostatic adenocarcinoma cells. In summary, these findings identify BAF57 as a critical modulator of the AR that is capable of altering AR activity, coactivator function, and AR-dependent proliferation.

MeSH Terms
Adenocarcinoma/metabolism Adenosine Triphosphatases/genetics,metabolism,physiology Animals Carrier Proteins/physiology Cell Line, Tumor Cell Proliferation Chromatin Assembly and Disassembly/genetics,physiology Chromatin Immunoprecipitation Chromosomal Proteins, Non-Histone/genetics,metabolism,physiology DNA-Binding Proteins Epithelium/metabolism Gene Silencing Ligands Male Mice Nuclear Proteins/physiology Prostate/cytology Prostatic Neoplasms/metabolism RNA-Binding Proteins Receptors, Androgen/physiology Transcription Factors/genetics,metabolism,physiology
Chemicals
Carrier Proteins Chromosomal Proteins, Non-Histone DNA-Binding Proteins Ligands Mybbp1a protein, mouse Nuclear Proteins RNA-Binding Proteins Receptors, Androgen Smarca2 protein, mouse Smarce1 protein, mouse Transcription Factors Adenosine Triphosphatases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Link Kevin A
Department of Cell Biology, Vontz Center for Molecular Studies, University of Cincinnati College of Medicine, Cincinnati, OH 45267-0521, USA.
Burd Craig J
Williams Erin
Marshall Thomas
Rosson Gary
Henry Erin
Weissman Bernard
Knudsen Karen E
References (76)
76 references, click to expand
  1. Co-activators and co-repressors in the integration of transcriptional responses.
    Curr Opin Cell Biol. 1998 Jun;10(3):373-83 PMID: 9640539
  2. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer.
    Nature. 1998 Jul 9;394(6689):203-6 PMID: 9671307
  3. Multiple G1 regulatory elements control the androgen-dependent proliferation of prostatic carcinoma cells.
    J Biol Chem. 1998 Aug 7;273(32):20213-22 PMID: 9685369
  4. Roles of histone acetyltransferases and deacetylases in gene regulation.
    Bioessays. 1998 Aug;20(8):615-26 PMID: 9780836
  5. Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha).
    EMBO J. 1998 Dec 1;17(23):6979-91 PMID: 9843504
  6. Cloning and characterization of androgen receptor coactivator, ARA55, in human prostate.
    J Biol Chem. 1999 Mar 19;274(12):8316-21 PMID: 10075738
  7. Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by p16INK4a, TGFbeta, and contact inhibition.
    Cell. 1999 Apr 2;97(1):53-61 PMID: 10199402
  8. Ubc9 interacts with the androgen receptor and activates receptor-dependent transcription.
    J Biol Chem. 1999 Jul 2;274(27):19441-6 PMID: 10383460
  9. Mechanisms of androgen receptor activation and function.
    J Steroid Biochem Mol Biol. 1999 Apr-Jun;69(1-6):307-13 PMID: 10419007
  10. The role of the androgen receptor in the development and progression of prostate cancer.
    Semin Oncol. 1999 Aug;26(4):407-21 PMID: 10482183
  11. The expression of the SWI/SNF ATPase subunits BRG1 and BRM in normal human tissues.
    Appl Immunohistochem Mol Morphol. 2005 Mar;13(1):66-74 PMID: 15722796
  12. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase.
    Anal Biochem. 1991 Feb 1;192(2):262-7 PMID: 1852137
  13. ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling.
    Mol Cell Biol. 2002 May;22(10):3255-63 PMID: 11971959
  14. Androgen receptor acetylation governs trans activation and MEKK1-induced apoptosis without affecting in vitro sumoylation and trans-repression function.
    Mol Cell Biol. 2002 May;22(10):3373-88 PMID: 11971970
  15. Novel ATPase of SNF2-like protein family interacts with androgen receptor and modulates androgen-dependent transcription.
    Mol Biol Cell. 2002 Jun;13(6):2106-19 PMID: 12058073
  16. Molecular biology of the androgen receptor.
    J Clin Oncol. 2002 Jul 1;20(13):3001-15 PMID: 12089231
  17. Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes.
    Nature. 2002 Jul 11;418(6894):195-9 PMID: 12110891
  18. Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes.
    EMBO J. 2002 Aug 1;21(15):4094-103 PMID: 12145209
  19. Re-expression of hSNF5/INI1/BAF47 in pediatric tumor cells leads to G1 arrest associated with induction of p16ink4a and activation of RB.
    Oncogene. 2002 Aug 8;21(34):5193-203 PMID: 12149641
  20. Androgen receptor as a target in androgen-independent prostate cancer.
    Urology. 2002 Sep;60(3 Suppl 1):132-8; discussion 138-9 PMID: 12231070
  21. REST repression of neuronal genes requires components of the hSWI.SNF complex.
    J Biol Chem. 2002 Oct 25;277(43):41038-45 PMID: 12192000
  22. Largest subunits of the human SWI/SNF chromatin-remodeling complex promote transcriptional activation by steroid hormone receptors.
    J Biol Chem. 2002 Nov 1;277(44):41674-85 PMID: 12200431
  23. Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5.
    Cancer Cell. 2002 Nov;2(5):415-25 PMID: 12450796
  24. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes.
    Mol Cell. 2003 Feb;11(2):377-89 PMID: 12620226
  25. A role for cofactor-cofactor and cofactor-histone interactions in targeting p300, SWI/SNF and Mediator for transcription.
    EMBO J. 2003 May 1;22(9):2146-55 PMID: 12727881
  26. The chromatin-remodeling complex WINAC targets a nuclear receptor to promoters and is impaired in Williams syndrome.
    Cell. 2003 Jun 27;113(7):905-17 PMID: 12837248
  27. Differential requirement of SWI/SNF for androgen receptor activity.
    J Biol Chem. 2003 Aug 15;278(33):30605-13 PMID: 12775722
  28. Nuclear receptors: a rendezvous for chromatin remodeling factors.
    Cell. 2003 Aug 8;114(3):277-80 PMID: 12914692
  29. BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation.
    Mol Cell Biol. 2003 Sep;23(17):6210-20 PMID: 12917342
  30. Histone deacetylation of RB-responsive promoters: requisite for specific gene repression but dispensable for cell cycle inhibition.
    Mol Cell Biol. 2003 Nov;23(21):7719-31 PMID: 14560017
  31. BRG1 controls the activity of the retinoblastoma protein via regulation of p21CIP1/WAF1/SDI.
    Mol Cell Biol. 2004 Feb;24(3):1188-99 PMID: 14729964
  32. P16INK4a is required for hSNF5 chromatin remodeler-induced cellular senescence in malignant rhabdoid tumor cells.
    J Biol Chem. 2004 Jan 30;279(5):3807-16 PMID: 14604992
  33. Modifying chromatin to permit steroid hormone receptor-dependent transcription.
    Biochim Biophys Acta. 2004 Mar 15;1677(1-3):30-45 PMID: 15020043
  34. Dyrk1A potentiates steroid hormone-induced transcription via the chromatin remodeling factor Arip4.
    Mol Cell Biol. 2004 Jul;24(13):5821-34 PMID: 15199138
  35. Functional domain and motif analyses of androgen receptor coregulator ARA70 and its differential expression in prostate cancer.
    J Biol Chem. 2004 Aug 6;279(32):33438-46 PMID: 15166229
  36. High-efficiency transformation of mammalian cells by plasmid DNA.
    Mol Cell Biol. 1987 Aug;7(8):2745-52 PMID: 3670292
  37. Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors.
    Science. 1992 Dec 4;258(5088):1598-604 PMID: 1360703
  38. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor.
    EMBO J. 1993 Nov;12(11):4279-90 PMID: 8223438
  39. Dominant negative regulation of trans-activation by the rat androgen receptor: roles of the N-terminal domain and heterodimer formation.
    Mol Endocrinol. 1993 Nov;7(11):1399-407 PMID: 8114755
  40. Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor.
    Nucleic Acids Res. 1994 May 25;22(10):1815-20 PMID: 8208605
  41. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest.
    Cell. 1994 Oct 7;79(1):119-30 PMID: 7923370
  42. Androgen receptor defects: historical, clinical, and molecular perspectives.
    Endocr Rev. 1995 Jun;16(3):271-321 PMID: 7671849
  43. Transforming growth factor-beta1 is a mediator of androgen-regulated growth arrest in an androgen-responsive prostatic cancer cell line, LNCaP.
    Endocrinology. 1996 Mar;137(3):991-9 PMID: 8603613
  44. Nuclear receptors: coactivators, corepressors and chromatin remodeling in the control of transcription.
    J Mol Endocrinol. 1999 Dec;23(3):255-75 PMID: 10601972
  45. ATP-dependent chromatin-remodeling complexes.
    Mol Cell Biol. 2000 Mar;20(6):1899-910 PMID: 10688638
  46. Promoter targeting and chromatin remodeling by the SWI/SNF complex.
    Curr Opin Genet Dev. 2000 Apr;10(2):187-92 PMID: 10753786
  47. Acetylation of histones and transcription-related factors.
    Microbiol Mol Biol Rev. 2000 Jun;64(2):435-59 PMID: 10839822
  48. BRG-1 is required for RB-mediated cell cycle arrest.
    Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):7748-53 PMID: 10884406
  49. BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation.
    Mol Cell Biol. 2000 Oct;20(20):7541-9 PMID: 11003650
  50. 8-Bromo-cyclic AMP induces phosphorylation of two sites in SRC-1 that facilitate ligand-independent activation of the chicken progesterone receptor and are critical for functional cooperation between SRC-1 and CREB binding protein.
    Mol Cell Biol. 2000 Dec;20(23):8720-30 PMID: 11073973
  51. A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex.
    Mol Cell Biol. 2000 Dec;20(23):8879-88 PMID: 11073988
  52. A small composite probasin promoter confers high levels of prostate-specific gene expression through regulation by androgens and glucocorticoids in vitro and in vivo.
    Endocrinology. 2000 Dec;141(12):4698-710 PMID: 11108285
  53. Characterization of SWI/SNF protein expression in human breast cancer cell lines and other malignancies.
    J Cell Physiol. 2001 Jan;186(1):136-45 PMID: 11147808
  54. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes.
    Mol Cell. 2000 Dec;6(6):1287-95 PMID: 11163203
  55. Mechanisms for ATP-dependent chromatin remodelling.
    Curr Opin Genet Dev. 2001 Apr;11(2):148-54 PMID: 11250137
  56. Identification of SWI.SNF complex subunit BAF60a as a determinant of the transactivation potential of Fos/Jun dimers.
    J Biol Chem. 2001 Jan 26;276(4):2852-7 PMID: 11053448
  57. A mechanism for androgen receptor-mediated prostate cancer recurrence after androgen deprivation therapy.
    Cancer Res. 2001 Jun 1;61(11):4315-9 PMID: 11389051
  58. Chromatin remodeling and transcriptional activation: the cast (in order of appearance).
    Oncogene. 2001 May 28;20(24):2991-3006 PMID: 11420714
  59. Different expression of androgen receptor coactivators in human prostate.
    Urology. 2001 Aug;58(2):289-94 PMID: 11489729
  60. Estrogen receptor and breast cancer.
    Semin Cancer Biol. 2001 Oct;11(5):339-52 PMID: 11562176
  61. Compensation of BRG-1 function by Brm: insight into the role of the core SWI-SNF subunits in retinoblastoma tumor suppressor signaling.
    J Biol Chem. 2002 Feb 15;277(7):4782-9 PMID: 11719516
  62. Concomitant down-regulation of BRM and BRG1 in human tumor cell lines: differential effects on RB-mediated growth arrest vs CD44 expression.
    Oncogene. 2002 Feb 14;21(8):1196-207 PMID: 11850839
  63. The development of androgen-independent prostate cancer.
    Nat Rev Cancer. 2001 Oct;1(1):34-45 PMID: 11900250
  64. Cooperation between complexes that regulate chromatin structure and transcription.
    Cell. 2002 Feb 22;108(4):475-87 PMID: 11909519
  65. Formation of the androgen receptor transcription complex.
    Mol Cell. 2002 Mar;9(3):601-10 PMID: 11931767
  66. Androgen receptor (AR) coregulators: an overview.
    Endocr Rev. 2002 Apr;23(2):175-200 PMID: 11943742
  67. Cloning and characterization of a specific coactivator, ARA70, for the androgen receptor in human prostate cells.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5517-21 PMID: 8643607
  68. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex.
    EMBO J. 1996 Oct 1;15(19):5370-82 PMID: 8895581
  69. An androgen response element in a far upstream enhancer region is essential for high, androgen-regulated activity of the prostate-specific antigen promoter.
    Mol Endocrinol. 1997 Feb;11(2):148-61 PMID: 9013762
  70. Ligand-dependent interaction between the estrogen receptor and the human homologues of SWI2/SNF2.
    Gene. 1997 Mar 25;188(1):95-100 PMID: 9099865
  71. Stromal-epithelial interactions in the normal and neoplastic prostate.
    Br J Urol. 1997 Apr;79 Suppl 2:18-26 PMID: 9126066
  72. Steroid receptor coactivator-1 is a histone acetyltransferase.
    Nature. 1997 Sep 11;389(6647):194-8 PMID: 9296499
  73. Dual mechanisms for the inhibition of E2F binding to RB by cyclin-dependent kinase-mediated RB phosphorylation.
    Mol Cell Biol. 1997 Oct;17(10):5771-83 PMID: 9315635
  74. Architectural DNA binding by a high-mobility-group/kinesin-like subunit in mammalian SWI/SNF-related complexes.
    Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):492-8 PMID: 9435219
  75. Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex.
    Nature. 1998 May 7;393(6680):88-91 PMID: 9590696
  76. Promotion of agonist activity of antiandrogens by the androgen receptor coactivator, ARA70, in human prostate cancer DU145 cells.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7379-84 PMID: 9636157
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-03-00
Pages
2200-15
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1061596
Subset
IM
Grants
NCI NIH HHS · R01 CA102848 · United States
NIEHS NIH HHS · T32 ES007250 · United States
NIEHS NIH HHS · 2 T32 ES07250-16 · United States
NCI NIH HHS · CA102848 · United States
NCI NIH HHS · CA91048 · United States
NCI NIH HHS · R01CA099996 · United States
NCI NIH HHS · R01 CA091048 · United States
NCI NIH HHS · R01 CA099996 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com