RWDD1 interacts with the ligand binding domain of the androgen receptor and acts as a coactivator of androgen-dependent transactivation

Molecular and Cellular Endocrinology

Volumn 358, Issue 1, 2012, Pages 53-62

  Grötsch, Helga ^a   Kunert, Marlene ^a   Mooslehner, Katrin A ^b   Gao, Zhigang ^a,c   Struve, Dagmar ^a   Hughes, Ieuan A ^b   Hiort, Olaf ^a   Werner, Ralf ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Androgen receptor; Coactivator; Genital tubercle; RWDD1; Sexual differentiation; Transcription

Indexed keywords

ANDROGEN RECEPTOR; MEMBRANE PROTEIN; RWD DOMAIN CONTAINING 1 PROTEIN; UNCLASSIFIED DRUG;

ANDROGEN INSENSITIVITY SYNDROME; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIMERIZATION; EMBRYO; EMBRYO DEVELOPMENT; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; HYDROPHOBICITY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION; UBIQUITINATION; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA, MALE; HELA CELLS; HUMANS; MALE; MICE; PROTEINS; RECEPTORS, ANDROGEN; TRANSCRIPTIONAL ACTIVATION;

EID: 84860459265     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.02.020     Document Type: Article

References (51)

1. Alpi A.F., Pace P.E., Babu M.M., Patel K.J. Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol. Cell 2008, 32:767-777.
2. Araki Y., Suzuki K., Matusik R.J., Obinata M., Orgebin-Crist M.C. Immortalized epididymal cell lines from transgenic mice overexpressing temperature-sensitive simian virus 40 large T-antigen gene. J. Androl. 2002, 23:854-869.
3. Bevan C.L., Hoare S., Claessens F., Heery D.M., Parker M.G. The AF1 and AF2 domains of the androgen receptor interact with distinct regions of SRC1. Mol. Cell. Biol. 1999, 19:8383-8392.
4. Brinkmann A.O., Faber P.W., van Rooij H.C., Kuiper G.G., Ris C., Klaassen P., van der Korput J.A., Voorhorst M.M., van Laar J.H., Mulder E. The human androgen receptor: domain structure, genomic organization and regulation of expression. J. Steroid Biochem. 1989, 34:307-310.
5. Bulynko Y.A., O'Malley B.W. Nuclear receptor coactivators: structural and functional biochemistry. Biochemistry 2011, 50:313-328.
6. Carbia-Nagashima A., Gerez J., Perez-Castro C., Paez-Pereda M., Silberstein S., Stalla G.K., Holsboer F., Arzt E. RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell 2007, 131:309-323.
7. Claessens F., Denayer S., Van Tilborgh N., Kerkhofs S., Helsen C., Haelens A. Diverse roles of androgen receptor (AR) domains in AR-mediated signaling. Nucl. Recept. Signal. 2008, 6:e008.
8. Cole A.R., Lewis L.P., Walden H. The structure of the catalytic subunit FANCL of the Fanconi anemia core complex. Nat. Struct. Mol. Biol. 2010, 17:294-298.
9. Daugeron M.C., Prouteau M., Lacroute F., Seraphin B. The highly conserved eukaryotic DRG factors are required for efficient translation in a manner redundant with the putative RNA helicase Slh1. Nucleic Acids Res. 2011, 39:2221-2233.
10. Deeb A., Mason C., Lee Y.S., Hughes I.A. Correlation between genotype, phenotype and sex of rearing in 111 patients with partial androgen insensitivity syndrome. Clin. Endocrinol. (Oxf.) 2005, 63:56-62.
11. Doerks T., Copley R.R., Schultz J., Ponting C.P., Bork P. Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 2002, 12:47-56.
12. Doesburg P., Kuil C.W., Berrevoets C.A., Steketee K., Faber P.W., Mulder E., Brinkmann A.O., Trapman J. Functional in vivo interaction between the amino-terminal, transactivation domain and the ligand binding domain of the androgen receptor. Biochemistry 1997, 36:1052-1064.
13. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
14. Gioeli D., Paschal B.M. Post-translational modification of the androgen receptor. Mol. Cell. Endocrinol. 2012, 352:70-78.
15. He B., Wilson E.M. Electrostatic modulation in steroid receptor recruitment of LXXLL and FXXLF motifs. Mol. Cell. Biol. 2003, 23:2135-2150.
16. 2-terminal interaction with the ligand binding domain of the androgen receptor. J. Biol. Chem. 2000, 275:22986-22994.
17. He B., Minges J.T., Lee L.W., Wilson E.M. The FXXLF motif mediates androgen receptor-specific interactions with coregulators. J. Biol. Chem. 2002, 277:10226-10235.
18. He B., Gampe R.T., Hnat A.T., Faggart J.L., Minges J.T., French F.S., Wilson E.M. Probing the functional link between androgen receptor coactivator and ligand-binding sites in prostate cancer and androgen insensitivity. J. Biol. Chem. 2006, 281:6648-6663.
19. Heemers H.V., Tindall D.J. Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr. Rev. 2007, 28:778-808.
20. Holterhus P.M., Sinnecker G.H., Hiort O. Phenotypic diversity and testosterone-induced normalization of mutant L712F androgen receptor function in a kindred with androgen insensitivity. J. Clin. Endocrinol. Metab. 2000, 85:3245-3250.
21. Hur E., Pfaff S.J., Payne E.S., Gron H., Buehrer B.M., Fletterick R.J. Recognition and accommodation at the androgen receptor coactivator binding interface. PLoS Biol. 2004, 2:E274.
22. Ishikawa K., Azuma S., Ikawa S., Semba K., Inoue J. Identification of DRG family regulatory proteins (DFRPs): specific regulation of DRG1 and DRG2. Genes Cells 2005, 10:139-150.
23. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 1983, 153:163-168.
24. Kang N., Chen D., Wang L., Duan L., Liu S., Tang L., Liu Q., Cui L., He W. Rwdd1, a thymus aging related molecule, is a new member of the intrinsically unstructured protein family. Cell. Mol. Immunol. 2008, 5:333-339.
25. Kang N., Duan L., Tang L., Liu S., Li C., Li Y., Liu Q., Hu Y., Cui L., He W. Identification and characterization of a novel thymus aging related protein Rwdd1. Cell. Mol. Immunol. 2008, 5:279-285.
26. Kesler C.T., Gioeli D., Conaway M.R., Weber M.J., Paschal B.M. Subcellular localization modulates activation function 1 domain phosphorylation in the androgen receptor. Mol. Endocrinol. 2007, 21:2071-2084.
27. Langley E., Zhou Z.X., Wilson E.M. Evidence for an anti-parallel orientation of the ligand-activated human androgen receptor dimer. J. Biol. Chem. 1995, 270:29983-29990.
28. Li J., Willingham E., Baskin L.S. Gene expression profiles in mouse urethral development. BJU Int. 2006, 98:880-885.
29. Marshall T.W., Link K.A., Petre-Draviam C.E., Knudsen K.E. Differential requirement of SWI/SNF for androgen receptor activity. J. Biol. Chem. 2003, 278:30605-30613.
30. Mendonca B.B., Costa E.M., Belgorosky A., Rivarola M.A., Domenice S. 46,XY DSD due to impaired androgen production. Best Pract. Res. Clin. Endocrinol. Metab. 2010, 24:243-262.
31. Miyagawa S., Satoh Y., Haraguchi R., Suzuki K., Iguchi T., Taketo M.M., Nakagata N., Matsumoto T., Takeyama K., Kato S., Yamada G. Genetic interactions of the androgen and Wnt/{beta}-catenin pathways for the masculinization of external genitalia. Mol. Endocrinol. 2009, 23:871-880.
32. Miyagawa S., Matsumaru D., Murashima A., Omori A., Satoh Y., Haraguchi R., Motoyama J., Iguchi T., Nakagata N., Hui C.C., Yamada G. The role of sonic hedgehog-gli2 pathway in the masculinization of external genitalia. Endocrinology 2011, 152:2894-2903.
33. Mooslehner K.A., Davies J.D., Hughes I.A. A cell model for conditional profiling of androgen receptor interacting proteins. Int. J. Endocrinol 2012, Article ID 381824. doi:10.1155/2012/381824.
34. Nameki N., Yoneyama M., Koshiba S., Tochio N., Inoue M., Seki E., Matsuda T., Tomo Y., Harada T., Saito K., Kobayashi N., Yabuki T., Aoki M., Nunokawa E., Matsuda N., Sakagami N., Terada T., Shirouzu M., Yoshida M., Hirota H., Osanai T., Tanaka A., Arakawa T., Carninci P., Kawai J., Hayashizaki Y., Kinoshita K., Guntert P., Kigawa T., Yokoyama S. Solution structure of the RWD domain of the mouse GCN2 protein. Protein Sci. 2004, 13:2089-2100.
35. Nishida T., Yasuda H. PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. J. Biol. Chem. 2002, 277:41311-41317.
36. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87:953-959.
37. Reddy G.P., Barrack E.R., Dou Q.P., Menon M., Pelley R., Sarkar F.H., Sheng S. Regulatory processes affecting androgen receptor expression, stability, and function: potential targets to treat hormone-refractory prostate cancer. J. Cell. Biochem. 2006, 98:1408-1423.
38. Schaufele F., Carbonell X., Guerbadot M., Borngraeber S., Chapman M.S., Ma A.A., Miner J.N., Diamond M.I. The structural basis of androgen receptor activation: intramolecular and intermolecular amino-carboxy interactions. Proc. Natl. Acad. Sci. USA 2005, 102:9802-9807.
39. Smith D.F., Toft D.O. Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions. Mol. Endocrinol. 2008, 22:2229-2240.
40. Tantos A., Han K.H., Tompa P. Intrinsic disorder in cell signaling and gene transcription. Mol. Cell. Endocrinol. 2012, 348:457-465.
41. van de Wijngaart D.J., van Royen M.E., Hersmus R., Pike A.C., Houtsmuller A.B., Jenster G., Trapman J., Dubbink H.J. Novel FxxFF and FxxMF motifs in androgen receptor cofactors mediate high affinity and specific interactions with the ligand-binding domain. J. Biol. Chem. 2006, 281:19407-19416.
42. van de Wijngaart D.J., Dubbink H.J., Molier M., de Vos C., Trapman J., Jenster G. Functional screening of FxxLF-like peptide motifs identifies SMARCD1/BAF60a as an androgen receptor cofactor that modulates TMPRSS2 expression. Mol. Endocrinol. 2009, 23:1776-1786.
43. van Royen M.E., Cunha S.M., Brink M.C., Mattern K.A., Nigg A.L., Dubbink H.J., Verschure P.J., Trapman J., Houtsmuller A.B. Compartmentalization of androgen receptor protein-protein interactions in living cells. J. Cell Biol. 2007, 177:63-72.
44. Wang J., Mager J., Chen Y., Schneider E., Cross J.C., Nagy A., Magnuson T. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat. Genet. 2001, 28:371-375.
45. Ward R.D., Weigel N.L. Steroid receptor phosphorylation: assigning function to site-specific phosphorylation. BioFactors 2009, 35:528-536.
46. Werner R., Schutt J., Hannema S., Ropke A., Wieacker P., Hiort O., Holterhus P.M. Androgen receptor gene mutations in androgen insensitivity syndrome cause distinct patterns of reduced activation of androgen-responsive promoter constructs. J. Steroid Biochem. Mol. Biol. 2006, 101:1-10.
47. Werner R., Grotsch H., Hiort O. 46,XY disorders of sex development - the undermasculinised male with disorders of androgen action. Best Pract. Res. Clin. Endocrinol. Metab. 2010, 24:263-277.
48. Yamada G., Satoh Y., Baskin L.S., Cunha G.R. Cellular and molecular mechanisms of development of the external genitalia. Differentiation 2003, 71:445-460.
49. Yamada G., Suzuki K., Haraguchi R., Miyagawa S., Satoh Y., Kamimura M., Nakagata N., Kataoka H., Kuroiwa A., Chen Y. Molecular genetic cascades for external genitalia formation: an emerging organogenesis program. Dev. Dyn. 2006, 235:1738-1752.
50. Zhou Z.X., He B., Hall S.H., Wilson E.M., French F.S. Domain interactions between coregulator ARA(70) and the androgen receptor (AR). Mol. Endocrinol. 2002, 16:287-300.
51. Zuccarello D., Ferlin A., Vinanzi C., Prana E., Garolla A., Callewaert L., Claessens F., Brinkmann A.O., Foresta C. Detailed functional studies on androgen receptor mild mutations demonstrate their association with male infertility. Clin. Endocrinol. (Oxf.) 2008, 68:580-588.