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. 1999 Jun 15;18(12):3392–3403. doi: 10.1093/emboj/18.12.3392

Net, a negative Ras-switchable TCF, contains a second inhibition domain, the CID, that mediates repression through interactions with CtBP and de-acetylation.

P Criqui-Filipe 1, C Ducret 1, S M Maira 1, B Wasylyk 1
PMCID: PMC1171419  PMID: 10369679

Abstract

Signalling cascades are integrated at the transcriptional level by the interplay between factors such as the ternary complex factors (TCFs) that interact with serum response factor (SRF) and the serum response element (SRE) of the fos promoter. Net is a negative TCF that is switched to a positive regulator by the Ras signal. To understand the mechanisms of repression by Net, we used a yeast two-hybrid screen to identify factors that interact with its inhibitory domain. We isolated mCtBP1, the murine homologue of huCtBP1, a factor implicated in negative regulation of transformation by E1A plus Ras. We show that mCtBP1 interacts strongly with Net both in vitro and in vivo. The CtBP interaction domain of Net, the CID, mediates repression independently of the previously identified negative element, the NID. The CID inhibits by recruiting the co-repressor mCtBP1. The CID and mCtBP1 need to use de-acetylase activity for repression, whereas the NID apparently represses by other mechanisms. Finally, we provide evidence that CtBP and de-acetylation repress the c-fos SRE in low serum when it is inactive, but not in high serum when it is active. These results provide insights into the cross-talk between pathways that inhibit and stimulate transformation at the level of Net, a regulator of gene expression.

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Selected References

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  1. Alberts A. S., Geneste O., Treisman R. Activation of SRF-regulated chromosomal templates by Rho-family GTPases requires a signal that also induces H4 hyperacetylation. Cell. 1998 Feb 20;92(4):475–487. doi: 10.1016/s0092-8674(00)80941-1. [DOI] [PubMed] [Google Scholar]
  2. Alland L., Muhle R., Hou H., Jr, Potes J., Chin L., Schreiber-Agus N., DePinho R. A. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature. 1997 May 1;387(6628):49–55. doi: 10.1038/387049a0. [DOI] [PubMed] [Google Scholar]
  3. Ashraf S. I., Ip Y. T. Transcriptional control: repression by local chromatin modification. Curr Biol. 1998 Sep 24;8(19):R683–R686. doi: 10.1016/s0960-9822(98)70435-x. [DOI] [PubMed] [Google Scholar]
  4. Baniahmad A., Ha I., Reinberg D., Tsai S., Tsai M. J., O'Malley B. W. Interaction of human thyroid hormone receptor beta with transcription factor TFIIB may mediate target gene derepression and activation by thyroid hormone. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8832–8836. doi: 10.1073/pnas.90.19.8832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boulay J. L., Dennefeld C., Alberga A. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. 1987 Nov 26-Dec 2Nature. 330(6146):395–398. doi: 10.1038/330395a0. [DOI] [PubMed] [Google Scholar]
  6. Boyd J. M., Subramanian T., Schaeper U., La Regina M., Bayley S., Chinnadurai G. A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. EMBO J. 1993 Feb;12(2):469–478. doi: 10.1002/j.1460-2075.1993.tb05679.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brehm A., Miska E. A., McCance D. J., Reid J. L., Bannister A. J., Kouzarides T. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature. 1998 Feb 5;391(6667):597–601. doi: 10.1038/35404. [DOI] [PubMed] [Google Scholar]
  8. Chatton B., Bahr A., Acker J., Kedinger C. Eukaryotic GST fusion vector for the study of protein-protein associations in vivo: application to interaction of ATFa with Jun and Fos. Biotechniques. 1995 Jan;18(1):142–145. [PubMed] [Google Scholar]
  9. Chatton B., Bocco J. L., Gaire M., Hauss C., Reimund B., Goetz J., Kedinger C. Transcriptional activation by the adenovirus larger E1a product is mediated by members of the cellular transcription factor ATF family which can directly associate with E1a. Mol Cell Biol. 1993 Jan;13(1):561–570. doi: 10.1128/mcb.13.1.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chen J. D., Evans R. M. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature. 1995 Oct 5;377(6548):454–457. doi: 10.1038/377454a0. [DOI] [PubMed] [Google Scholar]
  12. David G., Alland L., Hong S. H., Wong C. W., DePinho R. A., Dejean A. Histone deacetylase associated with mSin3A mediates repression by the acute promyelocytic leukemia-associated PLZF protein. Oncogene. 1998 May 14;16(19):2549–2556. doi: 10.1038/sj.onc.1202043. [DOI] [PubMed] [Google Scholar]
  13. Davie J. R. Covalent modifications of histones: expression from chromatin templates. Curr Opin Genet Dev. 1998 Apr;8(2):173–178. doi: 10.1016/s0959-437x(98)80138-x. [DOI] [PubMed] [Google Scholar]
  14. DePinho R. A. Transcriptional repression. The cancer-chromatin connection. Nature. 1998 Feb 5;391(6667):533, 535-6. doi: 10.1038/35257. [DOI] [PubMed] [Google Scholar]
  15. Dhordain P., Albagli O., Lin R. J., Ansieau S., Quief S., Leutz A., Kerckaert J. P., Evans R. M., Leprince D. Corepressor SMRT binds the BTB/POZ repressing domain of the LAZ3/BCL6 oncoprotein. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10762–10767. doi: 10.1073/pnas.94.20.10762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dittmer J., Nordheim A. Ets transcription factors and human disease. Biochim Biophys Acta. 1998 Apr 17;1377(2):F1–11. doi: 10.1016/s0304-419x(97)00039-5. [DOI] [PubMed] [Google Scholar]
  17. Ferreira R., Magnaghi-Jaulin L., Robin P., Harel-Bellan A., Trouche D. The three members of the pocket proteins family share the ability to repress E2F activity through recruitment of a histone deacetylase. Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10493–10498. doi: 10.1073/pnas.95.18.10493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fisher A. L., Caudy M. Groucho proteins: transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates. Genes Dev. 1998 Jul 1;12(13):1931–1940. doi: 10.1101/gad.12.13.1931. [DOI] [PubMed] [Google Scholar]
  19. Fisher A., Caudy M. The function of hairy-related bHLH repressor proteins in cell fate decisions. Bioessays. 1998 Apr;20(4):298–306. doi: 10.1002/(SICI)1521-1878(199804)20:4<298::AID-BIES6>3.0.CO;2-M. [DOI] [PubMed] [Google Scholar]
  20. Fondell J. D., Brunel F., Hisatake K., Roeder R. G. Unliganded thyroid hormone receptor alpha can target TATA-binding protein for transcriptional repression. Mol Cell Biol. 1996 Jan;16(1):281–287. doi: 10.1128/mcb.16.1.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fondell J. D., Roy A. L., Roeder R. G. Unliganded thyroid hormone receptor inhibits formation of a functional preinitiation complex: implications for active repression. Genes Dev. 1993 Jul;7(7B):1400–1410. doi: 10.1101/gad.7.7b.1400. [DOI] [PubMed] [Google Scholar]
  22. Frisch S. M., Reich R., Collier I. E., Genrich L. T., Martin G., Goldberg G. I. Adenovirus E1A represses protease gene expression and inhibits metastasis of human tumor cells. Oncogene. 1990 Jan;5(1):75–83. [PubMed] [Google Scholar]
  23. Futamura M., Monden Y., Okabe T., Fujita-Yoshigaki J., Yokoyama S., Nishimura S. Trichostatin A inhibits both ras-induced neurite outgrowth of PC12 cells and morphological transformation of NIH3T3 cells. Oncogene. 1995 Mar 16;10(6):1119–1123. [PubMed] [Google Scholar]
  24. Giles R. H., Peters D. J., Breuning M. H. Conjunction dysfunction: CBP/p300 in human disease. Trends Genet. 1998 May;14(5):178–183. doi: 10.1016/s0168-9525(98)01438-3. [DOI] [PubMed] [Google Scholar]
  25. Giovane A., Pintzas A., Maira S. M., Sobieszczuk P., Wasylyk B. Net, a new ets transcription factor that is activated by Ras. Genes Dev. 1994 Jul 1;8(13):1502–1513. doi: 10.1101/gad.8.13.1502. [DOI] [PubMed] [Google Scholar]
  26. Graves B. J., Petersen J. M. Specificity within the ets family of transcription factors. Adv Cancer Res. 1998;75:1–55. doi: 10.1016/s0065-230x(08)60738-1. [DOI] [PubMed] [Google Scholar]
  27. Gray S., Levine M. Short-range transcriptional repressors mediate both quenching and direct repression within complex loci in Drosophila. Genes Dev. 1996 Mar 15;10(6):700–710. doi: 10.1101/gad.10.6.700. [DOI] [PubMed] [Google Scholar]
  28. Gregory P. D., Hörz W. Chromatin and transcription--how transcription factors battle with a repressive chromatin environment. Eur J Biochem. 1998 Jan 15;251(1-2):9–18. doi: 10.1046/j.1432-1327.1998.2510009.x. [DOI] [PubMed] [Google Scholar]
  29. Grignani F., De Matteis S., Nervi C., Tomassoni L., Gelmetti V., Cioce M., Fanelli M., Ruthardt M., Ferrara F. F., Zamir I. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature. 1998 Feb 19;391(6669):815–818. doi: 10.1038/35901. [DOI] [PubMed] [Google Scholar]
  30. Gu W., Roeder R. G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 1997 Aug 22;90(4):595–606. doi: 10.1016/s0092-8674(00)80521-8. [DOI] [PubMed] [Google Scholar]
  31. Hanna-Rose W., Hansen U. Active repression mechanisms of eukaryotic transcription repressors. Trends Genet. 1996 Jun;12(6):229–234. doi: 10.1016/0168-9525(96)10022-6. [DOI] [PubMed] [Google Scholar]
  32. Hanna-Rose W., Licht J. D., Hansen U. Two evolutionarily conserved repression domains in the Drosophila Kruppel protein differ in activator specificity. Mol Cell Biol. 1997 Aug;17(8):4820–4829. doi: 10.1128/mcb.17.8.4820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hassig C. A., Fleischer T. C., Billin A. N., Schreiber S. L., Ayer D. E. Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell. 1997 May 2;89(3):341–347. doi: 10.1016/s0092-8674(00)80214-7. [DOI] [PubMed] [Google Scholar]
  34. Herrera R. E., Nordheim A., Stewart A. F. Chromatin structure analysis of the human c-fos promoter reveals a centrally positioned nucleosome. Chromosoma. 1997 Oct;106(5):284–292. doi: 10.1007/s004120050249. [DOI] [PubMed] [Google Scholar]
  35. Hollenberg S. M., Sternglanz R., Cheng P. F., Weintraub H. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol Cell Biol. 1995 Jul;15(7):3813–3822. doi: 10.1128/mcb.15.7.3813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Hörlein A. J., När A. M., Heinzel T., Torchia J., Gloss B., Kurokawa R., Ryan A., Kamei Y., Söderström M., Glass C. K. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature. 1995 Oct 5;377(6548):397–404. doi: 10.1038/377397a0. [DOI] [PubMed] [Google Scholar]
  37. Imhof A., Yang X. J., Ogryzko V. V., Nakatani Y., Wolffe A. P., Ge H. Acetylation of general transcription factors by histone acetyltransferases. Curr Biol. 1997 Sep 1;7(9):689–692. doi: 10.1016/s0960-9822(06)00296-x. [DOI] [PubMed] [Google Scholar]
  38. Janknecht R., Hunter T. Transcription. A growing coactivator network. Nature. 1996 Sep 5;383(6595):22–23. doi: 10.1038/383022a0. [DOI] [PubMed] [Google Scholar]
  39. Janknecht R., Hunter T. Versatile molecular glue. Transcriptional control. Curr Biol. 1996 Aug 1;6(8):951–954. doi: 10.1016/s0960-9822(02)00636-x. [DOI] [PubMed] [Google Scholar]
  40. Janknecht R., Nordheim A. MAP kinase-dependent transcriptional coactivation by Elk-1 and its cofactor CBP. Biochem Biophys Res Commun. 1996 Nov 21;228(3):831–837. doi: 10.1006/bbrc.1996.1740. [DOI] [PubMed] [Google Scholar]
  41. Janknecht R., Nordheim A. Regulation of the c-fos promoter by the ternary complex factor Sap-1a and its coactivator CBP. Oncogene. 1996 May 2;12(9):1961–1969. [PubMed] [Google Scholar]
  42. Jiménez G., Paroush Z., Ish-Horowicz D. Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev. 1997 Nov 15;11(22):3072–3082. doi: 10.1101/gad.11.22.3072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kadosh D., Struhl K. Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol Cell Biol. 1998 Sep;18(9):5121–5127. doi: 10.1128/mcb.18.9.5121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Katsanis N., Fisher E. M. A novel C-terminal binding protein (CTBP2) is closely related to CTBP1, an adenovirus E1A-binding protein, and maps to human chromosome 21q21.3. Genomics. 1998 Jan 15;47(2):294–299. doi: 10.1006/geno.1997.5115. [DOI] [PubMed] [Google Scholar]
  45. Kuo M. H., Allis C. D. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays. 1998 Aug;20(8):615–626. doi: 10.1002/(SICI)1521-1878(199808)20:8<615::AID-BIES4>3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
  46. Laherty C. D., Billin A. N., Lavinsky R. M., Yochum G. S., Bush A. C., Sun J. M., Mullen T. M., Davie J. R., Rose D. W., Glass C. K. SAP30, a component of the mSin3 corepressor complex involved in N-CoR-mediated repression by specific transcription factors. Mol Cell. 1998 Jul;2(1):33–42. doi: 10.1016/s1097-2765(00)80111-2. [DOI] [PubMed] [Google Scholar]
  47. Laherty C. D., Yang W. M., Sun J. M., Davie J. R., Seto E., Eisenman R. N. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell. 1997 May 2;89(3):349–356. doi: 10.1016/s0092-8674(00)80215-9. [DOI] [PubMed] [Google Scholar]
  48. Lehming N., Thanos D., Brickman J. M., Ma J., Maniatis T., Ptashne M. An HMG-like protein that can switch a transcriptional activator to a repressor. Nature. 1994 Sep 8;371(6493):175–179. doi: 10.1038/371175a0. [DOI] [PubMed] [Google Scholar]
  49. Lin R. J., Nagy L., Inoue S., Shao W., Miller W. H., Jr, Evans R. M. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature. 1998 Feb 19;391(6669):811–814. doi: 10.1038/35895. [DOI] [PubMed] [Google Scholar]
  50. Linder S., Popowicz P., Svensson C., Marshall H., Bondesson M., Akusjärvi G. Enhanced invasive properties of rat embryo fibroblasts transformed by adenovirus E1A mutants with deletions in the carboxy-terminal exon. Oncogene. 1992 Mar;7(3):439–443. [PubMed] [Google Scholar]
  51. Luger K., Richmond T. J. The histone tails of the nucleosome. Curr Opin Genet Dev. 1998 Apr;8(2):140–146. doi: 10.1016/s0959-437x(98)80134-2. [DOI] [PubMed] [Google Scholar]
  52. Magnaghi-Jaulin L., Groisman R., Naguibneva I., Robin P., Lorain S., Le Villain J. P., Troalen F., Trouche D., Harel-Bellan A. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature. 1998 Feb 5;391(6667):601–605. doi: 10.1038/35410. [DOI] [PubMed] [Google Scholar]
  53. Maira S. M., Wurtz J. M., Wasylyk B. Net (ERP/SAP2) one of the Ras-inducible TCFs, has a novel inhibitory domain with resemblance to the helix-loop-helix motif. EMBO J. 1996 Nov 1;15(21):5849–5865. [PMC free article] [PubMed] [Google Scholar]
  54. Nagy L., Kao H. Y., Chakravarti D., Lin R. J., Hassig C. A., Ayer D. E., Schreiber S. L., Evans R. M. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell. 1997 May 2;89(3):373–380. doi: 10.1016/s0092-8674(00)80218-4. [DOI] [PubMed] [Google Scholar]
  55. Nauber U., Pankratz M. J., Kienlin A., Seifert E., Klemm U., Jäckle H. Abdominal segmentation of the Drosophila embryo requires a hormone receptor-like protein encoded by the gap gene knirps. Nature. 1988 Dec 1;336(6198):489–492. doi: 10.1038/336489a0. [DOI] [PubMed] [Google Scholar]
  56. Nibu Y., Zhang H., Levine M. Interaction of short-range repressors with Drosophila CtBP in the embryo. Science. 1998 Apr 3;280(5360):101–104. doi: 10.1126/science.280.5360.101. [DOI] [PubMed] [Google Scholar]
  57. Parkhurst S. M. Groucho: making its Marx as a transcriptional co-repressor. Trends Genet. 1998 Apr;14(4):130–132. doi: 10.1016/s0168-9525(98)01407-3. [DOI] [PubMed] [Google Scholar]
  58. Paroush Z., Finley R. L., Jr, Kidd T., Wainwright S. M., Ingham P. W., Brent R., Ish-Horowicz D. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell. 1994 Dec 2;79(5):805–815. doi: 10.1016/0092-8674(94)90070-1. [DOI] [PubMed] [Google Scholar]
  59. Poortinga G., Watanabe M., Parkhurst S. M. Drosophila CtBP: a Hairy-interacting protein required for embryonic segmentation and hairy-mediated transcriptional repression. EMBO J. 1998 Apr 1;17(7):2067–2078. doi: 10.1093/emboj/17.7.2067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Rundlett S. E., Carmen A. A., Suka N., Turner B. M., Grunstein M. Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature. 1998 Apr 23;392(6678):831–835. doi: 10.1038/33952. [DOI] [PubMed] [Google Scholar]
  61. Schaeper U., Boyd J. M., Verma S., Uhlmann E., Subramanian T., Chinnadurai G. Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10467–10471. doi: 10.1073/pnas.92.23.10467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schaeper U., Subramanian T., Lim L., Boyd J. M., Chinnadurai G. Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J Biol Chem. 1998 Apr 10;273(15):8549–8552. doi: 10.1074/jbc.273.15.8549. [DOI] [PubMed] [Google Scholar]
  63. Sharrocks A. D., Brown A. L., Ling Y., Yates P. R. The ETS-domain transcription factor family. Int J Biochem Cell Biol. 1997 Dec;29(12):1371–1387. doi: 10.1016/s1357-2725(97)00086-1. [DOI] [PubMed] [Google Scholar]
  64. Sollerbrant K., Chinnadurai G., Svensson C. The CtBP binding domain in the adenovirus E1A protein controls CR1-dependent transactivation. Nucleic Acids Res. 1996 Jul 1;24(13):2578–2584. doi: 10.1093/nar/24.13.2578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sundqvist A., Sollerbrant K., Svensson C. The carboxy-terminal region of adenovirus E1A activates transcription through targeting of a C-terminal binding protein-histone deacetylase complex. FEBS Lett. 1998 Jun 12;429(2):183–188. doi: 10.1016/s0014-5793(98)00588-2. [DOI] [PubMed] [Google Scholar]
  66. Tolkunova E. N., Fujioka M., Kobayashi M., Deka D., Jaynes J. B. Two distinct types of repression domain in engrailed: one interacts with the groucho corepressor and is preferentially active on integrated target genes. Mol Cell Biol. 1998 May;18(5):2804–2814. doi: 10.1128/mcb.18.5.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Torchia J., Glass C., Rosenfeld M. G. Co-activators and co-repressors in the integration of transcriptional responses. Curr Opin Cell Biol. 1998 Jun;10(3):373–383. doi: 10.1016/s0955-0674(98)80014-8. [DOI] [PubMed] [Google Scholar]
  68. Treisman R. Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol. 1996 Apr;8(2):205–215. doi: 10.1016/s0955-0674(96)80067-6. [DOI] [PubMed] [Google Scholar]
  69. Versteege I., Sévenet N., Lange J., Rousseau-Merck M. F., Ambros P., Handgretinger R., Aurias A., Delattre O. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature. 1998 Jul 9;394(6689):203–206. doi: 10.1038/28212. [DOI] [PubMed] [Google Scholar]
  70. Wang J., Hoshino T., Redner R. L., Kajigaya S., Liu J. M. ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10860–10865. doi: 10.1073/pnas.95.18.10860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Wasylyk B., Hagman J., Gutierrez-Hartmann A. Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem Sci. 1998 Jun;23(6):213–216. doi: 10.1016/s0968-0004(98)01211-0. [DOI] [PubMed] [Google Scholar]
  72. Webster N., Jin J. R., Green S., Hollis M., Chambon P. The yeast UASG is a transcriptional enhancer in human HeLa cells in the presence of the GAL4 trans-activator. Cell. 1988 Jan 29;52(2):169–178. doi: 10.1016/0092-8674(88)90505-3. [DOI] [PubMed] [Google Scholar]
  73. Yu X., Wu L. C., Bowcock A. M., Aronheim A., Baer R. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J Biol Chem. 1998 Sep 25;273(39):25388–25392. doi: 10.1074/jbc.273.39.25388. [DOI] [PubMed] [Google Scholar]
  74. Zhang H., Levine M. Groucho and dCtBP mediate separate pathways of transcriptional repression in the Drosophila embryo. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):535–540. doi: 10.1073/pnas.96.2.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Zhang W., Bieker J. J. Acetylation and modulation of erythroid Krüppel-like factor (EKLF) activity by interaction with histone acetyltransferases. Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9855–9860. doi: 10.1073/pnas.95.17.9855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Zhang Y., Iratni R., Erdjument-Bromage H., Tempst P., Reinberg D. Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell. 1997 May 2;89(3):357–364. doi: 10.1016/s0092-8674(00)80216-0. [DOI] [PubMed] [Google Scholar]
  77. Zhang Y., Sun Z. W., Iratni R., Erdjument-Bromage H., Tempst P., Hampsey M., Reinberg D. SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex. Mol Cell. 1998 Jun;1(7):1021–1031. doi: 10.1016/s1097-2765(00)80102-1. [DOI] [PubMed] [Google Scholar]
  78. vom Baur E., Zechel C., Heery D., Heine M. J., Garnier J. M., Vivat V., Le Douarin B., Gronemeyer H., Chambon P., Losson R. Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1. EMBO J. 1996 Jan 2;15(1):110–124. [PMC free article] [PubMed] [Google Scholar]

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