RNA helicase Ddx5 and the noncoding RNA SRA act as coactivators in the Notch signaling pathway

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 5, 2013, Pages 1180-1189

  Jung, Claudia ^a,b   Mittler, Gerhard ^a   Oswald, Franz ^c   Borggrefe, Tilman ^a  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

Coactivator; Lymphocyte development; Non coding RNA; Notch signaling; Transcriptional regulation

Indexed keywords

DEAD BOX PROTEIN; E1A ASSOCIATED P300 PROTEIN; NOTCH RECEPTOR; RNA HELICASE; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOTINYLATION; CHROMATIN; DOWN REGULATION; GENE TARGETING; HISTONE ACETYLATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MICE; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; RECEPTORS, NOTCH; RNA, LONG UNTRANSLATED; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION;

EID: 84874534749     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.01.032     Document Type: Article

References (36)

1. Kopan R., Ilagan M.X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009, 137:216-233.
2. Borggrefe T., Liefke R. Fine-tuning of the intracellular canonical Notch signaling pathway. Cell Cycle 2012, 11:264-276.
3. Hamaguchi Y., Yamamoto Y., Iwanari H., Maruyama S., Furukawa T., Matsunami N., Honjo T. Biochemical and immunological characterization of the DNA binding protein (RBP-J kappa) to mouse J kappa recombination signal sequence. J. Biochem. 1992, 112:314-320.
4. Wu L., Aster J.C., Blacklow S.C., Lake R., Artavanis-Tsakonas S., Griffin J.D. MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat. Genet. 2000, 26:484-489.
5. Kovall R.A. More complicated than it looks: assembly of Notch pathway transcription complexes. Oncogene 2008, 27:5099-5109.
6. Oswald F., Tauber B., Dobner T., Bourteele S., Kostezka U., Adler G., Liptay S., Schmid R.M. p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol. Cell. Biol. 2001, 21:7761-7774.
7. Kurooka H., Honjo T. Functional interaction between the mouse notch1 intracellular region and histone acetyltransferases PCAF and GCN5. J. Biol. Chem. 2000, 275:17211-17220.
8. Jeffries S., Robbins D.J., Capobianco A.J. Characterization of a high-molecular-weight Notch complex in the nucleus of Notch(ic)-transformed RKE cells and in a human T-cell leukemia cell line. Mol. Cell. Biol. 2002, 22:3927-3941.
9. Maillard I., Weng A.P., Carpenter A.C., Rodriguez C.G., Sai H., Xu L., Allman D., Aster J.C., Pear W.S. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 2004, 104:1696-1702.
10. Koch U., Radtke F. Notch signaling in solid tumors. Curr. Top. Dev. Biol. 2010, 92:411-455.
11. Janknecht R. Multi-talented DEAD-box proteins and potential tumor promoters: p68 RNA helicase (DDX5) and its paralog, p72 RNA helicase (DDX17). Am. J. Transl. Res. 2010, 2:223-234.
12. Fuller-Pace F.V., Moore H.C. RNA helicases p68 and p72: multifunctional proteins with important implications for cancer development. Future Oncol. 2011, 7:239-251.
13. Lanz R.B., McKenna N.J., Onate S.A., Albrecht U., Wong J., Tsai S.Y., Tsai M.J., O'Malley B.W. A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 1999, 97:17-27.
14. 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.
15. Yao H., Brick K., Evrard Y., Xiao T., Camerini-Otero R.D., Felsenfeld G. Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev. 2010, 24:2543-2555.
16. Liefke R., Oswald F., Alvarado C., Ferres-Marco D., Mittler G., Rodriguez P., Dominguez M., Borggrefe T. Histone demethylase KDM5A is an integral part of the core Notch-RBP-J repressor complex. Genes Dev. 2010, 24:590-601.
17. Mooney S.M., Goel A., D'Assoro A.B., Salisbury J.L., Janknecht R. Pleiotropic effects of p300-mediated acetylation on p68 and p72 RNA helicase. J. Biol. Chem. 2010, 285:30443-30452.
18. Oswald F., Winkler M., Cao Y., Astrahantseff K., Bourteele S., Knochel W., Borggrefe T. RBP-Jkappa/SHARP recruits CtIP/CtBP corepressors to silence Notch target genes. Mol. Cell. Biol. 2005, 25:10379-10390.
19. Oswald F., Kostezka U., Astrahantseff K., Bourteele S., Dillinger K., Zechner U., Ludwig L., Wilda M., Hameister H., Knochel W., Liptay S., Schmid R.M. SHARP is a novel component of the Notch/RBP-Jkappa signalling pathway. EMBO J. 2002, 21:5417-5426.
20. Minoguchi S., Taniguchi Y., Kato H., Okazaki T., Strobl L.J., Zimber-Strobl U., Bornkamm G.W., Honjo T. RBP-L, a transcription factor related to RBP-Jkappa. Mol. Cell. Biol. 1997, 17:2679-2687.
21. de Boer E., Rodriguez P., Bonte E., Krijgsveld J., Katsantoni E., Heck A., Grosveld F., Strouboulis J. Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7480-7485.
22. Rossow K.L., Janknecht R. Synergism between p68 RNA helicase and the transcriptional coactivators CBP and p300. Oncogene 2003, 22:151-156.
23. Wang H., Zou J., Zhao B., Johannsen E., Ashworth T., Wong H., Pear W.S., Schug J., Blacklow S.C., Arnett K.L., Bernstein B.E., Kieff E., Aster J.C. Genome-wide analysis reveals conserved and divergent features of Notch1/RBPJ binding in human and murine T-lymphoblastic leukemia cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14908-14913.
24. Han H., Tanigaki K., Yamamoto N., Kuroda K., Yoshimoto M., Nakahata T., Ikuta K., Honjo T. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 2002, 14:637-645.
25. Mijimolle N., Velasco J., Dubus P., Guerra C., Weinbaum C.A., Casey P.J., Campuzano V., Barbacid M. Protein farnesyltransferase in embryogenesis, adult homeostasis, and tumor development. Cancer Cell 2005, 7:313-324.
26. Salat D., Liefke R., Wiedenmann J., Borggrefe T., Oswald F. ETO, but not leukemogenic fusion protein AML1/ETO, augments RBP-Jkappa/SHARP-mediated repression of notch target genes. Mol. Cell. Biol. 2008, 28:3502-3512.
27. 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.
28. 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.
29. Gill G., Ptashne M. Negative effect of the transcriptional activator GAL4. Nature 1988, 334:721-724.
30. Martin M.L., Lieberman P.M., Curran T. Fos-Jun dimerization promotes interaction of the basic region with TFIIE-34 and TFIIF. Mol. Cell. Biol. 1996, 16:2110-2118.
31. Drewelus I., Gopfert C., Hippel C., Dickmanns A., Damianitsch K., Pieler T., Dobbelstein M. p63 Antagonizes Wnt-induced transcription. Cell Cycle 2010, 9:580-587.
32. Visel A., Blow M.J., Li Z., Zhang T., Akiyama J.A., Holt A., Plajzer-Frick I., Shoukry M., Wright C., Chen F., Afzal V., Ren B., Rubin E.M., Pennacchio L.A. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
33. Jin Q., Yu L.R., Wang L., Zhang Z., Kasper L.H., Lee J.E., Wang C., Brindle P.K., Dent S.Y., Ge K. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 2011, 30:249-262.
34. Puente X.S., Pinyol M., Quesada V., Conde L., Ordonez G.R., Villamor N., Escaramis G., Jares P., Bea S., Gonzalez-Diaz M., Bassaganyas L., Baumann T., Juan M., Lopez-Guerra M., Colomer D., Tubio J.M., Lopez C., Navarro A., Tornador C., Aymerich M., Rozman M., Hernandez J.M., Puente D.A., Freije J.M., Velasco G., Gutierrez-Fernandez A., Costa D., Carrio A., Guijarro S., Enjuanes A., Hernandez L., Yague J., Nicolas P., Romeo-Casabona C.M., Himmelbauer H., Castillo E., Dohm J.C., de Sanjose S., Piris M.A., de Alava E., San Miguel J., Royo R., Gelpi J.L., Torrents D., Orozco M., Pisano D.G., Valencia A., Guigo R., Bayes M., Heath S., Gut M., Klatt P., Marshall J., Raine K., Stebbings L.A., Futreal P.A., Stratton M.R., Campbell P.J., Gut I., Lopez-Guillermo A., Estivill X., Montserrat E., Lopez-Otin C., Campo E. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature 2011, 475:101-105.
35. Lin S., Tian L., Shen H., Gu Y., Li J.L., Chen Z., Sun X., James You M., Wu L. DDX5 is a positive regulator of oncogenic NOTCH1 signaling in T cell acute lymphoblastic leukemia. Oncogene Oct. 29 2012, http://dx.doi.org/10.1038/onc.2012.482 (Electronic publication ahead of print).
36. Nicol S.M., Bray S.E., Derek Black H., Lorimore S.A., Wright E.G., Lane D.P., Meek D.W., Coates P.J., Fuller-Pace F.V. The RNA helicase p68 (DDX5) is selectively required for the induction of p53-dependent p21 expression and cell-cycle arrest after DNA damage. Oncogene Sep. 17 2012, http://dx.doi.org/10.1038/onc.2012.426 (Electronic publication ahead of print).