DDX5 is a multifunctional co-activator of steroid hormone receptors

Molecular and Cellular Endocrinology

Volumn 361, Issue 1-2, 2012, Pages 80-91

  Wagner, Martin ^a   Rid, Raphaela ^a   Maier, Christina J ^a   Maier, Richard H ^a   Laimer, Martin ^a   Hintner, Helmut ^a   Bauer, Johann W ^a   Onder, Kamil ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

DDX5; PPI; Steroid hormones; Transcriptional co activation; VDR; Vitamin D signaling

Indexed keywords

ANDROGEN RECEPTOR; CALCITRIOL; DDX5 PROTEIN; ESTROGEN RECEPTOR ALPHA; SHORT HAIRPIN RNA; STEROID RECEPTOR; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

ARTICLE; BINDING AFFINITY; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; KERATINOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; TRANSCRIPTION REGULATION;

CALCITRIOL; CELL LINE; CELL NUCLEUS; CHROMOSOMES, HUMAN; DEAD-BOX RNA HELICASES; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; GENOME, HUMAN; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CALCITRIOL; RECEPTORS, STEROID; RNA, SMALL INTERFERING; SUBCELLULAR FRACTIONS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84864336607     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.03.014     Document Type: Article

References (81)

1. Aranda A., Pascual A. Nuclear hormone receptors and gene expression. Physiol. Rev. 2001, 81:1269-1304.
2. Ares M., Proudfoot N.J. The Spanish connection: transcription and mRNA processing get even closer. Cell 2005, 120:163-166.
3. Auboeuf D., Dowhan D.H., Dutertre M., Martin N., Berget S.M., O'Malley B.W. A subset of nuclear receptor coregulators act as coupling proteins during synthesis and maturation of RNA transcripts. Mol. Cell Biol. 2005, 25:5307-5316.
4. Auboeuf D., Honig A., Berget S.M., O'Malley B.W. Coordinate regulation of transcription and splicing by steroid receptor coregulators. Science 2002, 298:416-419.
5. Avila E., Diaz L., Barrera D., Halhali A., Mendez I., Gonzalez L., Zuegel U., Steinmeyer A., Larrea F. Regulation of Vitamin D hydroxylases gene expression by 1,25-dihydroxyvitamin D3 and cyclic AMP in cultured human syncytiotrophoblasts. J. Steroid Biochem. Mol. Biol. 2007, 103:90-96.
6. Barsony J., Renyi I., McKoy W. Subcellular distribution of normal and mutant vitamin D receptors in living cells. Studies with a novel fluorescent ligand. J. Biol. Chem. 1997, 272:5774-5782.
7. Bates G.J., Nicol S.M., Wilson B.J., Jacobs A.M., Bourdon J.C., Wardrop J., Gregory D.J., Lane D.P., Perkins N.D., Fuller-Pace F.V. The DEAD box protein p68: a novel transcriptional coactivator of the p53 tumour suppressor. EMBO J. 2005, 24:543-553.
8. Bikle D. Nonclassic actions of vitamin D. J. Clin. Endocrinol. Metab. 2009, 94:26-34.
9. Bikle D., Teichert A., Hawker N., Xie Z., Oda Y. Sequential regulation of keratinocyte differentiation by 1,25(OH)2D3, VDR, and its coregulators. J. Steroid Biochem. Mol. Biol. 2007, 103:396-404.
10. Bikle D.D., Ng D., Tu C.L., Oda Y., Xie Z. Calcium- and vitamin D-regulated keratinocyte differentiation. Mol. Cell Endocrinol. 2001, 177:161-171.
11. Bikle D.D., Oda Y., Xie Z. Vitamin D and skin cancer: a problem in gene regulation. J. Steroid Biochem. Mol. Biol. 2005, 97:83-91.
12. Bond A.T., Mangus D.A., He F., Jacobson A. Absence of Dbp2p alters both nonsense-mediated mRNA decay and rRNA processing. Mol. Cell Biol. 2001, 21:7366-7379.
13. 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.
14. Caretti G., Schiltz R.L., Dilworth F.J., Di Padova M., Zhao P., Ogryzko V., Fuller-Pace F.V., Hoffman E.P., Tapscott S.J., Sartorelli V. The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev. Cell. 2006, 11:547-560.
15. Carlberg C. Ligand-mediated conformational changes of the VDR are required for gene transactivation. J. Steroid Biochem. Mol. Biol. 2004, 89-90:227-232.
16. Carlberg C., Dunlop T.W., Saramaki A., Sinkkonen L., Matilainen M., Vaisanen S. Controlling the chromatin organization of vitamin D target genes by multiple vitamin D receptor binding sites. J. Steroid Biochem. Mol. Biol. 2007, 103:338-343.
17. Carlberg, C., Seuter, S., 2007. The vitamin D receptor. Dermatol. Clin. 25, 515-23 (viii).
18. 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.
19. Clark E.L., Fuller-Pace F.V., Elliott D.J., Robson C.N. Coupling transcription to RNA processing via the p68 DEAD box RNA helicase androgen receptor co-activator in prostate cancer. Biochem. Soc. Trans. 2008, 36:546-547.
20. Darimont B.D., Wagner R.L., Apriletti J.W., Stallcup M.R., Kushner P.J., Baxter J.D., Fletterick R.J., Yamamoto K.R. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 1998, 12:3343-3356.
21. Demay M.B. Mechanism of vitamin D receptor action. Ann. NY Acad. Sci. 2006, 1068:204-213.
22. Dusso A.S., Brown A.J., Slatopolsky E. Vitamin D. Am. J. Physiol. Renal. Physiol. 2005, 289:F8-F28.
23. Ebert R., Schutze N., Adamski J., Jakob F. Vitamin D signaling is modulated on multiple levels in health and disease. Mol. Cell Endocrinol. 2006, 248:149-159.
24. Endoh H., Maruyama K., Masuhiro Y., Kobayashi Y., Goto M., Tai H., Yanagisawa J., Metzger D., Hashimoto S., Kato S. Purification and identification of p68 RNA helicase acting as a transcriptional coactivator specific for the activation function 1 of human estrogen receptor alpha. Mol. Cell Biol. 1999, 19:5363-5372.
25. 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.
26. Fuller-Pace F.V. DExD/H box RNA helicases: multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Res. 2006, 34:4206-4215.
27. Fuller-Pace F.V., Ali S. The DEAD box RNA helicases p68 (Ddx5) and p72 (Ddx17): novel transcriptional co-regulators. Biochem. Soc. Trans. 2008, 36:609-612.
28. Gubler U., Hoffman B.J. A simple and very efficient method for generating cDNA libraries. Gene 1983, 25:263-269.
29. Haussler M.R., Haussler C.A., Jurutka P.W., Thompson P.D., Hsieh J.C., Remus L.S., Selznick S.H., Whitfield G.K. The vitamin D hormone and its nuclear receptor: molecular actions and disease states. J. Endocrinol. 1997, 154(Suppl.):S57-S73.
30. Heery D.M., Kalkhoven E., Hoare S., Parker M.G. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 1997, 387:733-736.
31. Hirling H., Scheffner M., Restle T., Stahl H. RNA helicase activity associated with the human p68 protein. Nature 1989, 339:562-564.
32. Iggo R.D., Jamieson D.J., MacNeill S.A., Southgate J., McPheat J., Lane D.P. P68 RNA helicase: identification of a nucleolar form and cloning of related genes containing a conserved intron in yeasts. Mol. Cell Biol. 1991, 11:1326-1333.
33. Iggo R.D., Lane D.P. Nuclear protein p68 is an RNA-dependent ATPase. EMBO J. 1989, 8:1827-1831.
34. Jacobs A.M., Nicol S.M., Hislop R.G., Jaffray E.G., Hay R.T., Fuller-Pace F.V. SUMO modification of the DEAD box protein p68 modulates its transcriptional activity and promotes its interaction with HDAC1. Oncogene 2007, 26:5866-5876.
35. Jalal C., Uhlmann-Schiffler H., Stahl H. Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res. 2007, 35:3590-3601.
36. Jensen E.D., Niu L., Caretti G., Nicol S.M., Teplyuk N., Stein G.S., Sartorelli V., van Wijnen A.J., Fuller-Pace F.V., Westendorf J.J. P68 (Ddx5) interacts with Runx2 and regulates osteoblast differentiation. J. Cell Biochem. 2008, 103:1438-1451.
37. Jimenez-Lara A.M., Aranda A. Lysine 246 of the vitamin D receptor is crucial for ligand-dependent interaction with coactivators and transcriptional activity. J. Biol. Chem. 1999, 274:13503-13510.
38. Kahlina K., Goren I., Pfeilschifter J., Frank S. P68 DEAD box RNA helicase expression in keratinocytes. Regulation, nucleolar localization, and functional connection to proliferation and vascular endothelial growth factor gene expression. J. Biol. Chem. 2004, 279:44872-44882.
39. Lehmann B. HaCaT cell line as a model system for vitamin D3 metabolism in human skin. J. Invest. Dermatol. 1997, 108:78-82.
40. Lehmann B., Knuschke P., Meurer M. UVB-induced conversion of 7-dehydrocholesterol to 1 alpha,25-dihydroxyvitamin D3 (calcitriol) in the human keratinocyte line HaCaT. Photochem. Photobiol. 2000, 72:803-809.
41. Lehmann B., Pietzsch J., Kampf A., Meurer M. Human keratinocyte line HaCaT metabolizes 1alpha-hydroxyvitamin D3 and vitamin D3 to 1alpha,25-dihydroxyvitamin D3 (calcitriol). J. Dermatol. Sci. 1998, 18:118-127.
42. Leo C., Chen J.D. The SRC family of nuclear receptor coactivators. Gene 2000, 245:1-11.
43. Liu M., Lee M.H., Cohen M., Bommakanti M., Freedman L.P. Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced differentiation of the myelomonocytic cell line U937. Genes Dev. 1996, 10:142-153.
44. Liu Z.R. P68 RNA helicase is an essential human splicing factor that acts at the U1 snRNA-5' splice site duplex. Mol. Cell Biol. 2002, 22:5443-5450.
45. Lorsch J.R. RNA chaperones exist and DEAD box proteins get a life. Cell 2002, 109:797-800.
46. Lu J., Goldstein K.M., Chen P., Huang S., Gelbert L.M., Nagpal S. Transcriptional profiling of keratinocytes reveals a vitamin D-regulated epidermal differentiation network. J. Invest. Dermatol. 2005, 124:778-785.
47. MacDonald P.N., Dowd D.R., Zhang C., Gu C. Emerging insights into the coactivator role of NCoA62/SKIP in Vitamin D-mediated transcription. J. Steroid Biochem. Mol. Biol. 2004, 89-90:179-186.
48. Malloy P.J., Xu R., Peng L., Clark P.A., Feldman D. A novel mutation in helix 12 of the vitamin D receptor impairs coactivator interaction and causes hereditary 1,25-dihydroxyvitamin D-resistant rickets without alopecia. Mol. Endocrinol. 2002, 16:2538-2546.
49. McAlister-Henn L., Gibson N., Panisko E. Applications of the yeast two-hybrid system. Methods 1999, 19:330-337.
50. Metivier R., Penot G., Hubner M.R., Reid G., Brand H., Kos M., Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003, 115:751-763.
51. Miyauchi Y., Michigami T., Sakaguchi N., Sekimoto T., Yoneda Y., Pike J.W., Yamagata M., Ozono K. Importing 4 is responsible for ligand-independent nuclear translocation of vitamin D receptor. J. Biol. Chem. 2005, 280:40901-40908.
52. Moras D., Gronemeyer H. The nuclear receptor ligand-binding domain: structure and function. Curr. Opin. Cell Biol. 1998, 10:384-391.
53. Nicol S.M., Causevic M., Prescott A.R., Fuller-Pace F.V. The nuclear DEAD box RNA helicase p68 interacts with the nucleolar protein fibrillarin and colocalizes specifically in nascent nucleoli during telophase. Exp. Cell Res. 2000, 257:272-280.
54. Oender K., Niedermayr P., Hintner H., Richter K., Koller L., Trost A., Bauer J.W., Hundsberger H. Relative quantitation of protein-protein interaction strength within the yeast two-hybrid system via fluorescence beta-galactosidase activity detection in a high-throughput and low-cost manner. Assay Drug Dev. Technol. 2006, 4:709-719.
55. Ordonez-Moran P., Larriba M.J., Palmer H.G., Valero R.A., Barbachano A., Dunach M., de Herreros A.G., Villalobos C., Berciano M.T., Lafarga M., Munoz A. RhoA-ROCK and p38MAPK-MSK1 mediate vitamin D effects on gene expression, phenotype, and Wnt pathway in colon cancer cells. J. Cell Biol. 2008, 183:697-710.
56. Plevin M.J., Mills M.M., Ikura M. The LxxLL motif: a multifunctional binding sequence in transcriptional regulation. Trends Biochem. Sci. 2005, 30:66-69.
57. Polly P., Herdick M., Moehren U., Baniahmad A., Heinzel T., Carlberg C. VDR-Alien: a novel, DNA-selective vitamin D(3) receptor-corepressor partnership. FASEB J. 2000, 14:1455-1463.
58. Privalsky M.L. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu. Rev. Physiol. 2004, 66:315-360.
59. Proudfoot N.J., Furger A., Dye M.J. Integrating mRNA processing with transcription. Cell 2002, 108:501-512.
60. Prufer K., Racz A., Lin G.C., Barsony J. Dimerization with retinoid X receptors promotes nuclear localization and subnuclear targeting of vitamin D receptors. J. Biol. Chem. 2000, 275:41114-41123.
61. Rachez C., Freedman L.P. Mechanisms of gene regulation by vitamin D(3) receptor: a network of coactivator interactions. Gene 2000, 246:9-21.
62. Rachez C., Suldan Z., Ward J., Chang C.P., Burakov D., Erdjument-Bromage H., Tempst P., Freedman L.P. A novel protein complex that interacts with the vitamin D3 receptor in a ligand-dependent manner and enhances VDR transactivation in a cell-free system. Genes Dev. 1998, 12:1787-1800.
63. Reichrath J., Lehmann B., Carlberg C., Varani J., Zouboulis C.C. Vitamins as hormones. Horm. Metab. Res. 2007, 39:71-84.
64. Rochel N., Moras D. Ligand binding domain of vitamin D receptors. Curr. Top Med. Chem. 2006, 6:1229-1241.
65. Rochel N., Wurtz J.M., Mitschler A., Klaholz B., Moras D. The crystal structure of the nuclear receptor for vitamin D bound to its natural ligand. Mol Cell. 2000, 5:173-179.
66. Rosenfeld M.G., Glass C.K. Coregulator codes of transcriptional regulation by nuclear receptors. J. Biol. Chem. 2001, 276:36865-36868.
67. Rossler O.G., Straka A., Stahl H. Rearrangement of structured RNA via branch migration structures catalysed by the highly related DEAD-box proteins p68 and p72. Nucleic Acids Res. 2001, 29:2088-2096.
68. Rossow K.L., Janknecht R. Synergism between p68 RNA helicase and the transcriptional coactivators CBP and p300. Oncogene 2003, 22:151-156.
69. Saramaki A., Banwell C.M., Campbell M.J., Carlberg C. Regulation of the human p21(waf1/cip1) gene promoter via multiple binding sites for p53 and the vitamin D3 receptor. Nucleic Acids Res. 2006, 34:543-554.
70. Savkur R.S., Burris T.P. The coactivator LXXLL nuclear receptor recognition motif. J. Pept. Res. 2004, 63:207-212.
71. Schmuth M., Watson R.E., Deplewski D., Dubrac S., Zouboulis C.C., Griffiths C.E. Nuclear hormone receptors in human skin. Horm. Metab. Res. 2007, 39:96-105.
72. Schrader M., Nayeri S., Kahlen J.P., Muller K.M., Carlberg C. Natural vitamin D3 response elements formed by inverted palindromes: polarity-directed ligand sensitivity of vitamin D3 receptor-retinoid X receptor heterodimer-mediated transactivation. Mol. Cell Biol. 1995, 15:1154-1161.
73. Staal A., van Wijnen A.J., Birkenhager J.C., Pols H.A., Prahl J., DeLuca H., Gaub M.P., Lian J.B., Stein G.S., van Leeuwen J.P., Stein J.L. Distinct conformations of vitamin D receptor/retinoid X receptor-alpha heterodimers are specified by dinucleotide differences in the vitamin D-responsive elements of the osteocalcin and osteopontin genes. Mol. Endocrinol. 1996, 10:1444-1456.
74. Su M.J., Bikle D.D., Mancianti M.L., Pillai S. 1,25-Dihydroxyvitamin D3 potentiates the keratinocyte response to calcium. J. Biol. Chem. 1994, 269:14723-14729.
75. Tanner N.K., Linder P. DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell. 2001, 8:251-262.
76. Watanabe M., Yanagisawa J., Kitagawa H., Takeyama K., Ogawa S., Arao Y., Suzawa M., Kobayashi Y., Yano T., Yoshikawa H., Masuhiro Y., Kato S. A subfamily of RNA-binding DEAD-box proteins acts as an estrogen receptor alpha coactivator through the N-terminal activation domain (AF-1) with an RNA coactivator. SRA EMBO J. 2001, 20:1341-1352.
77. Wilson B.J., Bates G.J., Nicol S.M., Gregory D.J., Perkins N.D., Fuller-Pace F.V. The p68 and p72 DEAD box RNA helicases interact with HDAC1 and repress transcription in a promoter-specific manner. BMC Mol. Biol. 2004, 5:11.
78. Xie Z., Komuves L., Yu Q.C., Elalieh H., Ng D.C., Leary C., Chang S., Crumrine D., Yoshizawa T., Kato S., Bikle D.D. Lack of the vitamin D receptor is associated with reduced epidermal differentiation and hair follicle growth. J. Invest. Dermatol. 2002, 118:11-16.
79. Yamamoto K., Masuno H., Choi M., Nakashima K., Taga T., Ooizumi H., Umesono K., Sicinska W., VanHooke J., DeLuca H.F., Yamada S. Three-dimensional modeling of and ligand docking to vitamin D receptor ligand binding domain. Proc. Natl. Acad. Sci. USA 2000, 97:1467-1472.
80. Yamaoka K., Shindo M., Iwasaki K., Yamaoka I., Yamamoto Y., Kitagawa H., Kato S. Multiple co-activator complexes support ligand-induced transactivation function of VDR. Arch. Biochem. Biophys. 2007, 460:166-171.
81. Zella L.A., Chang C.Y., McDonnell D.P., Wesley Pike J. The vitamin D receptor interacts preferentially with DRIP205-like LxxLL motifs. Arch. Biochem. Biophys. 2007, 460:206-212.