Melanoma antigen-a11 (mage-a11) enhances transcriptional activity by linking androgen receptor dimers

Journal of Biological Chemistry

Volumn 288, Issue 3, 2013, Pages 1939-1952

  Minges, John T ^a   Su, Shifeng ^b   Grossman, Gail ^b   Blackwelder, Amanda J ^a   Pop, Elena A ^b   Mohler, James L ^a,b,c   Wilson, Elizabeth M ^a,b,c,d  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTORS; ANDROGEN-DEPENDENT; AR DIMER; CARBOXYL-TERMINAL; CO-IMMUNOPRECIPITATIONS; DUAL FUNCTION; MOLECULAR BRIDGES; PROSTATE CANCER CELLS; PROSTATE CANCERS; PROTEIN LEVEL; SPLICE VARIANTS; STEROID RECEPTORS; STIMULATORY EFFECTS; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL MECHANISMS; TRANSCRIPTIONALLY ACTIVE;

ANTIGENS; DERMATOLOGY; DIMERS; ONCOLOGY; PROTEINS;

DISEASES;

ANDROGEN; ANDROGEN RECEPTOR; CYCLIC AMP; MELANOMA ANTIGEN; MELANOMA ANTIGEN A11; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL; CANCER GROWTH; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; MUTANT; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN INTERACTION; PROTEIN MOTIF; RECURRENT CANCER; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; ANTIGENS, NEOPLASM; BINDING SITES; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP; HUMANS; MALE; MELANOMA; NEOPLASM PROTEINS; PLASMIDS; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTORS, ANDROGEN; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TUMOR CELLS, CULTURED;

PRIMATES;

EID: 84872697730     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.428409     Document Type: Article

References (67)

1. Askew, E. B., Gampe, R. T., Jr., Stanley, T. B., Faggart, J. L., and Wilson, E. M. (2007) Modulation of androgen receptor activation function 2 by testosterone and dihydrotestosterone. J. Biol. Chem. 282, 25801-25816 (Pubitemid 47372778)
2. Langley, E., Zhou, Z. X., and Wilson, E. M. (1995) Evidence for an antiparallel orientation of the ligand activated human androgen receptor dimer. J. Biol. Chem. 270, 29983-29990 (Pubitemid 26001674)
3. He, B., Kemppainen, J. A., and Wilson, E. M. (2000) FXXLF andWXXLF sequences mediate the NH2-terminal interaction with the ligand binding domain of the androgen receptor. J. Biol. Chem. 275, 22986-22994 (Pubitemid 30646187)
4. Bai, S., He, B., and Wilson E. M. (2005) Melanoma antigen gene protein MAGE-11 regulates androgen receptor function by modulating the interdomain interaction. Mol. Cell. Biol. 25, 1238-1257 (Pubitemid 40204904)
5. Su, S., Blackwelder, A. J., Grossman, G., Minges, J. T., Yuan, L., Young, S. L., and Wilson, E. M. (2012) Primate-specific melanoma antigen-A11 regulates isoform-specific human progesterone receptor-B transactivation. J. Biol. Chem. 287, 34809-34824
6. Askew, E. B., Bai, S., Blackwelder, A. J., and Wilson, E. M. (2010) Transcriptional synergy between melanoma antigen gene protein-A11 (MAGE-11) and p300 in androgen receptor signaling. J. Biol. Chem. 285, 21824-21836
7. Askew, E. B., Bai, S., Hnat, A. T., Minges, J. T., and Wilson, E. M. (2009) Melanoma antigen gene protein-A11 (MAGE-11) F-box links the androgen receptor NH2-terminal transactivation domain to p160 coactivators. J. Biol. Chem. 284, 34793-34808
8. Karpf, A. R., Bai, S., James, S. R., Mohler, J. L., and Wilson, E. M. (2009) Increased expression of androgen receptor coregulator MAGE-11 in prostate cancer byDNAhypomethylation and cyclic AMP. Mol. Cancer Res. 7, 523-535
9. Gregory, C. W., Hamil, K. G., Kim, D., Hall, S. H., Pretlow, T. G., Mohler, J. L., and French, F. S. (1998) Androgen receptor expression in androgenindependent prostate cancer is associated with increased expression of androgen-regulated genes. Cancer Res. 58, 5718-5724 (Pubitemid 29006412)
10. Watson, P. A., Chen, Y. F., Balbas, M. D., Wongvipat, J., Socci, N. D., Viale, A., Kim, K., and Sawyers, C. L. (2010) Constitutively active androgen receptor splice variants expressed in castration-resistant prostate cancer require full-length androgen receptor. Proc. Natl. Acad. Sci. U.S.A. 107, 16759-16765
11. Chen, C. D., Welsbie, D. S., Tran, C., Baek, S. H., Chen, R., Vessella, R., Rosenfeld, M. G., and Sawyers, C. L. (2004) Molecular determinants of resistance to antiandrogen therapy. Nat. Med. 10, 33-39 (Pubitemid 38524696)
12. Wilson, E. M. (2010) Androgen receptor molecular biology and potential targets in prostate cancer. Ther. Adv. Urol. 2, 105-117
13. Wong, C. I., Zhou, Z. X., Sar, M., and Wilson, E. M. (1993) Steroid requirement for androgen receptor dimerization and DNA binding: modulation by intramolecular interactions between the NH2-terminal and steroid binding domains. J. Biol. Chem. 268, 19004-19012 (Pubitemid 23273853)
14. Bai, S., and Wilson, E. M. (2008) Epidermal growth factor-dependent phosphorylation and ubiquitinylation of MAGE-11 regulates its interaction with the androgen receptor. Mol. Cell. Biol. 28, 1947-1963 (Pubitemid 351342626)
15. Lubahn, D. B., Joseph, D. R., Sar, M., Tan, J., Higgs, H. N., Larson, R. E., French, F. S., and Wilson, E. M. (1988) The human androgen receptor: complementary DNA cloning, sequence analysis and gene expression in prostate. Mol. Endocrinol. 2, 1265-1275 (Pubitemid 19005939)
16. De Bellis, A., Quigley, C. A., Cariello, N. F., el-Awady, M. K., Sar, M., Lane, M. V., Wilson, E. M., and French, F. S. (1992) Single base mutations in the human androgen receptor gene causing complete androgen insensitivity: rapid detection by a modified denaturing gradient gel electrophoresis technique. Mol. Endocrinol. 6, 1909-1920
17. Zhou, Z. X., Sar, M., Simental, J. A., Lane, M. V., and Wilson, E. M. (1994) A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor: requirement for the DNA binding domain and modulation by the NH2-terminal and carboxyl-terminal sequences. J. Biol. Chem. 269, 13115-13123
18. He, B., Kemppainen, J. A., Voegel, J. J., Gronemeyer, H., and Wilson, E. M. (1999) Activation function 2 in the human androgen receptor ligand binding domain mediates interdomain communication with theNH2-terminal domain. J. Biol. Chem. 274, 37219-37225
19. He, B., and Wilson, E. M. (2003) Electrostatic modulation of steroid receptor recruitment of the LXXLL and FXXLF motifs. Mol. Cell. Biol. 23, 2135-2150 (Pubitemid 36278822)
20. Quigley, C. A., Evans, B. A., Simental, J. A., Marschke, K. B., Sar, M., Lubahn, D. B., Davies, P., Hughes, I. A., Wilson, E. M., and French, F. S. (1992) Complete androgen insensitivity due to deletion of exon C of the androgen receptor gene highlights the functional importance of the second zinc finger of the androgen receptor in vivo. Mol. Endocrinol. 6, 1103-1112
21. Zhou, Z. X., Lane, M. V., Kemppainen, J. A., French, F. S., and Wilson, E. M. (1995) Specificity of ligand dependent androgen receptor stabilization: receptor domain interactions influence ligand dissociation and receptor stability. Mol. Endocrinol. 9, 208-218
22. Zhou, Z. X., Wong, C. I., Sar, M., and Wilson, E. M. (1994) The androgen receptor: An overview. Recent Prog. Horm. Res. 49, 249-274 (Pubitemid 24976631)
23. He, B., Bowen, N. T., Minges, J. T., and Wilson, E. M. (2001) AndrogeninducedNH2-and carboxyl-terminal interaction inhibits p160 coactivator recruitment by activation function 2. J. Biol. Chem. 276, 42293-42301
24. Simental, J. A., Sar, M., Lane, M. V., French, F. S., and Wilson, E. M. (1991) Transcriptional activation and nuclear targeting signals of the human androgen receptor. J. Biol. Chem. 266, 510-518 (Pubitemid 21906153)
25. Huang, W., Shostak, Y., Tarr, P., Sawyers, C., and Carey, M. (1999) Cooperative assembly of androgen receptor into a nucleoprotein complex that regulates the prostate-specific antigen enhancer. J. Biol. Chem. 274, 25756-25768
26. Jain, A., Lam, A., Vivanco, I., Carey, M. F., and Reiter, R. E. (2002) Identification of an androgen-dependent enhancer within the prostate stem cell antigen gene. Mol. Endocrinol. 16, 2323-2337 (Pubitemid 35155543)
27. Evans, R. M. (1988) The steroid and thyroid hormone receptor superfamily. Science 240, 889-895
28. Singh, S. S., Qaqish, B., Johnson, J. L., Ford, O. H., 3rd, Foley, J. F., Maygarden, S. J., and Mohler, J. L. (2004) Sampling strategy for prostate tissue microarrays for Ki-67 and androgen receptor biomarkers. Anal. Quant. Cytol. Histol. 26, 194-200 (Pubitemid 39100905)
29. Godoy, A., Kawinski, E., Li, Y., Oka, D., Alexiev, B., Azzouni, F., Titus, M. A., and Mohler, J. L. (2011) 5α-Reductase type 3 expression in human benign and malignant tissues: A comparative analysis during prostate cancer progression. Prostate 71, 1033-1046
30. Bai, S., Grossman, G., Yuan, L., Lessey, B. A., French, F. S., Young, S. L., and Wilson, E. M. (2008) Hormone control and expression of androgen receptor coregulator MAGE-11 in human endometrium during the window of receptivity to embryo implantation. Mol. Hum. Reprod. 14, 107-116 (Pubitemid 351321171)
31. Mohler, J. L., Titus, M. A., Bai, S., Kennerley, B. J., Lih, F. B., Tomer, K. B., and Wilson, E. M. (2011) Activation of the androgen receptor by intratumoral bioconversion of androstanediol to dihydrotestosterone in prostate cancer. Cancer Res. 71, 1486-1496
32. He, B., Minges, J. T., Lee, L. W., and Wilson, E. M. (2002) The FXXLF motif mediates androgen receptor-specific interactions with coregulators. J. Biol. Chem. 277, 10226-10235 (Pubitemid 34968137)
33. Quarmby, V. E., Kemppainen, J. A., Sar, M., Lubahn, D. B., French, F. S., and Wilson, E. M. (1990) Expression of recombinant androgen receptor in cultured mammalian cells. Mol. Endocrinol. 4, 1399-1407 (Pubitemid 20371440)
34. Sadar, M. D. (1999) Androgen-independent induction of prostate-specific antigen gene expression via cross-talk between the androgen receptor and protein kinase A signal transduction pathways. J. Biol. Chem. 274, 7777-7783
35. Wang, G., Jones, S. J., Marra, M. A., and Sadar, M. D. (2006) Identification of genes targeted by the androgen and PKA signaling pathways in prostate cancer cells. Oncogene 25, 7311-7323 (Pubitemid 44809097)
36. Majors, J., and Varmus, H. E. (1983) A small region of the mouse mammary tumor virus long terminal repeat confers glucocorticoid hormone regulation on a linked heterologous gene. Proc. Natl. Acad. Sci. U.S.A. 80, 5866-5870 (Pubitemid 14227574)
37. Archer, T. K., Lee, H. L., Cordingley, M. G., Mymryk, J. S., Fragoso, G., Berard, D. S., and Hager, G. L. (1994) Differential steroid hormone induction of transcription from the mouse mammary tumor virus promoter. Mol. Endocrinol. 8, 568-576 (Pubitemid 24174493)
38. Beato, M. (1996) Chromatin structure and the regulation of gene expression: remodeling at the MMTV promoter. J. Mol. Med. 74, 711-724 (Pubitemid 26405601)
39. Préfontaine, G. G., Walther, R., Giffin, W., Lemieux, M. E., Pope, L., and Haché, R. J. (1999) Selective binding of steroid hormone receptors to octamer transcription factors determines transcriptional synergism at the mouse mammary tumor virus promoter. J. Biol. Chem. 274, 26713-26719
40. Gregory, C. W., Fei, X., Ponguta, L. A., He, B., Bill, H. M., French, F. S., and Wilson, E. M. (2004) Epidermal growth factor increases coactivation of the androgen receptor in recurrent prostate cancer. J. Biol. Chem. 279, 7119-7130 (Pubitemid 38248859)
41. Dehm, S. M., Schmidt, L. J., Heemers, H. V., Vessella, R. L., and Tindall, D. J. (2008) Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res. 68, 5469-5477
42. 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., Nelson, P. S., and Plymate, S. R. (2010) Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant. J. Clin. Investig. 120, 2715-2730
43. Lee, Y. H., Koh, S. S., Zhang, X., Cheng, X., and Stallcup, M. R. (2002) Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol. Cell. Biol. 22, 3621-3632 (Pubitemid 34525206)
44. Tamrazi, A., Carlson, K. E., Daniels, J. R., Hurth, K. M., and Katzenellenbogen, J. A. (2002) Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Mol. Endocrinol. 16, 2706-2719 (Pubitemid 36020652)
45. Zentner, G. E., and Scacheri, P. C. (2012) The chromatin fingerprint of gene enhancer elements. J. Biol. Chem. 287, 30888-30896
46. Massie, C. E., Adryan, B., Barbosa-Morais, N. L., Lynch, A. G., Tran, M. G., Neal, D. E., and Mills, I. G. (2007) New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep. 8, 871-878 (Pubitemid 350001432)
47. Wang, Q., Li, W., Liu, X. S., Carroll, J. S., Jänne, O. A., Keeton, E. K., Chinnaiyan, A. M., Pienta, K. J., and Brown, M. (2007) A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 27, 380-392 (Pubitemid 47126935)
48. Centenera, M. M., Harris, J. M., Tilley, W. D., and Butler, L. M. (2008) The contribution of different androgen receptor domains to receptor dimerization and signaling. Mol. Endocrinol. 22, 2373-2382
49. Schaufele, F., Carbonell, X., Guerbadot, M., Borngraeber, S., Chapman, M. S., Ma, A. A., Miner, J. N., and Diamond, M. I. (2005) The structural basis of androgen receptor activation: intramolecular and intermolecular amino-carboxy interactions. Proc. Natl. Acad. Sci. U.S.A. 102, 9802-9807 (Pubitemid 40993649)
50. van Royen, M. E., Cunha, S. M., Brink, M. C., Mattern, K. A., Nigg, A. L., Dubbink, H. J., Verschure, P. J., Trapman, J., and Houtsmuller, A. B. (2007) Compartmentalization of androgen receptor protein-protein interactions in living cells. J. Cell Biol. 177, 63-72 (Pubitemid 46588402)
51. van Royen, M. E., van Cappellen, W. A., de Vos, C., Houtsmuller, A. B., and Trapman, J. (2012) Stepwise androgen receptor dimerization. J. Cell Sci. 125, 1970-1979
52. Raaijmakers, H. C., Versteegh, J. E., and Uitdehaag, J. C. (2009) The x-ray structure of RU486 bound to the progesterone receptor in a destabilized agonistic conformation. J. Biol. Chem. 284, 19572-19579
53. Luisi, B., and Freedman, L. (1995) Nuclear receptors. Dymer, dymer binding tight. Nature 375, 359-360
54. Williams, S. P., and Sigler, P. B. (1998) Atomic structure of progesterone complexed with its receptor. Nature 393, 392-396 (Pubitemid 28269716)
55. Wang, L., Zuercher, W. J., Consler, T. G., Lambert, M. H., Miller, A. B., Orband-Miller, L. A., McKee, D. D., Willson, T. M., and Nolte, R. T. (2006) X-ray crystal structures of the estrogen-related receptor-α ligand binding domain in three functional states reveal the molecular basis of small molecule regulation. J. Biol. Chem. 281, 37773-37781 (Pubitemid 46042080)
56. Bledsoe, R. K., Montana, V. G., Stanley, T. B., Delves, C. J., Apolito, C. J., McKee, D. D., Consler, T. G., Parks, D. J., Stewart, E. L., Willson, T. M., Lambert, M. H., Moore, J. T., Pearce, K. H., and Xu, H. E. (2002) Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 110, 93-105 (Pubitemid 34874609)
57. Tanenbaum, D. M., Wang, Y., Williams, S. P., and Sigler, P. B. (1998) Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc. Natl. Acad. Sci. U.S.A. 95, 5998-6003 (Pubitemid 28248953)
58. Sack, J. S., Kish, K. F., Wang, C., Attar, R. M., Kiefer, S. E., An, Y., Wu, G. Y., Scheffler, J. E., Salvati, M. E., Krystek, S. R., Jr., Weinmann, R., and Einspahr, H. M. (2001) Crystallographic structures of the ligand-binding domains of the androgen receptor and its T877A mutant complexed with the natural agonist dihydrotestosterone. Proc. Natl. Acad. Sci. U.S.A. 98, 4904-4909 (Pubitemid 32397055)
59. He, B., Gampe, R. T., Jr., Kole, A. J., Hnat, A. T., Stanley, T. B., An, G., Stewart, E. L., Kalman, R. I., Minges, J. T., and Wilson, E. M. (2004) Structural basis for androgen receptor interdomain and coactivator interactions suggests a transition in nuclear receptor activation function dominance. Mol. Cell 16, 425-438 (Pubitemid 39504796)
60. Askew, E. B., Minges, J. T., Hnat, A. T., and Wilson, E. M. (2012) Structural features discriminate androgen receptor N/C terminal and coactivator interactions. Mol. Cell. Endocrinol. 348, 403-410
61. Steketee, K., Berrevoets, C. A., Dubbink, H. J., Doesburg, P., Hersmus, R., Brinkmann, A. O., and Trapman, J. (2002) Amino acids 3-13 and amino acids in and flanking the 23FxxLF27 motif modulate the interaction between the N-terminal and ligand-binding domain of the androgen receptor. Eur. J. Biochem. 269, 5780-5791 (Pubitemid 35425576)
62. Lagarde, W. H., Blackwelder, A. J., Minges, J. T., Hnat, A. T., French, F. S., and Wilson, E. M. (2012) Androgen receptor exon 1 mutation causes androgen insensitivity by creating a phosphorylation site and inhibiting MAGE-A11 activation ofNH2-and carboxyl-terminal interaction-dependent transactivation. J. Biol. Chem. 287, 10905-10915
63. Nazareth, L. V., and Weigel, N. L. (1996) Activation of the human androgen receptor through a protein kinase A signaling pathway. J. Biol. Chem. 271, 19900-19907 (Pubitemid 26281734)
64. Merkle, D., and Hoffmann, R. (2011) Roles of cAMP and cAMP-dependent protein kinase in the progression of prostate cancer: cross-talk with the androgen receptor. Cell. Signal. 23, 507-515
65. Burchardt, T., Burchardt, M., Chen, M. W., Cao, Y., de la Taille, A., Shabsigh, A., Hayek, O., Dorai, T., and Buttyan, R. (1999) Transdifferentiation of prostate cancer cells to a neuroendocrine cell phenotype in vitro and in vivo. J. Urol. 162, 1800-1805 (Pubitemid 29474732)
66. Kim, J., Jia, L., Stallcup, M. R., and Coetzee, G. A. (2005) The role of protein kinase A pathway and cAMP responsive element-binding protein in androgen receptor-mediated transcription at the prostate-specific antigen locus. J. Mol. Endocrinol. 34, 107-118 (Pubitemid 40305553)
67. He, B., Lee, L. W., Minges, J. T., and Wilson, E. M. (2002) Dependence of selective gene activation on the androgen receptor NH2-and carboxylterminal interaction. J. Biol. Chem. 277, 25631-25639 (Pubitemid 34951881)