Functional characterization and comparative analysis of gene repression-mediating domains interacting with yeast pleiotropic corepressors Sin3, Cyc8 and Tup1.
Saccharomyces cerevisiae
/ genetics
Co-Repressor Proteins
/ genetics
DNA-Binding Proteins
/ genetics
Saccharomyces cerevisiae Proteins
/ genetics
Repressor Proteins
/ metabolism
Transcription, Genetic
Gene Expression Regulation, Fungal
Nuclear Proteins
/ genetics
Glutathione Peroxidase
/ genetics
Prions
/ genetics
Phosphatidate Phosphatase
/ genetics
Corepressor
Cyc8
Gene repression
Interaction specificity
Saccharomyces cerevisiae
Sin3
Tup1
Journal
Current genetics
ISSN: 1432-0983
Titre abrégé: Curr Genet
Pays: United States
ID NLM: 8004904
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
received:
13
01
2023
accepted:
12
02
2023
revised:
09
02
2023
medline:
8
5
2023
pubmed:
2
3
2023
entrez:
1
3
2023
Statut:
ppublish
Résumé
Transcriptional corepressors Sin3, Cyc8 and Tup1 are important for downregulation of gene expression by recruiting various histone deacetylases once they gain access to defined genomic locations by interaction with pathway-specific repressor proteins. In this work we systematically investigated whether 17 yeast repressor proteins (Cti6, Dal80, Fkh1, Gal80, Mig1, Mot3, Nrg1, Opi1, Rdr1, Rox1, Sko1, Ume6, Ure2, Xbp1, Yhp1, Yox1 and Whi5) representing several unrelated regulatory pathways are able to bind to Sin3, Cyc8 and Tup1. Our results show that paired amphipathic helices 1 and 2 (PAH1 and PAH2) of Sin3 are functionally redundant for some regulatory pathways. WD40 domains of Tup1 proved to be sufficient for interaction with repressor proteins. Using length variants of selected repressors, we mapped corepressor interaction domains (CIDs) in vitro and assayed gene repression in vivo. Systematic comparison of CID minimal sequences allowed us to define several related positional patterns of hydrophobic amino acids some of which could be confirmed as functionally supported by site-directed mutagenesis. Although structural predictions indicated that certain CIDs may be α-helical, most repression domains appear to be randomly structured and must be considered as intrinsically disordered regions (IDR) adopting a defined conformation only by interaction with a corepressor.
Identifiants
pubmed: 36854981
doi: 10.1007/s00294-023-01262-6
pii: 10.1007/s00294-023-01262-6
pmc: PMC10163088
doi:
Substances chimiques
Co-Repressor Proteins
0
DNA-Binding Proteins
0
Saccharomyces cerevisiae Proteins
0
Repressor Proteins
0
CYC8 protein, S cerevisiae
0
TUP1 protein, S cerevisiae
0
Nuclear Proteins
0
URE2 protein, S cerevisiae
EC 1.11.1.9
Glutathione Peroxidase
EC 1.11.1.9
Prions
0
PAH1 protein, S cerevisiae
EC 3.1.3.4
Phosphatidate Phosphatase
EC 3.1.3.4
Fkh1 protein, S cerevisiae
0
UME6 protein, S cerevisiae
0
SKO1 protein, S cerevisiae
0
Cti6 protein, S cerevisiae
0
Whi5 protein, S cerevisiae
0
DAL80 protein, S cerevisiae
0
MOT3 protein, S cerevisiae
0
OPI1 protein, S cerevisiae
0
NRG1 protein, S cerevisiae
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
127-139Informations de copyright
© 2023. The Author(s).
Références
Adams GE, Chandru A, Cowley SM (2018) Co-repressor, co-activator and general transcription factor: the many faces of the Sin3 histone deacetylase (HDAC) complex. Biochem J 475:3921–3932. https://doi.org/10.1042/BCJ20170314
doi: 10.1042/BCJ20170314
pubmed: 30552170
Aref R, Schüller HJ (2020) Functional analysis of Cti6 core domain responsible for recruitment of epigenetic regulators Sin3, Cyc8 and Tup1. Curr Genet 66:1191–1203. https://doi.org/10.1007/s00294-020-01109-4
doi: 10.1007/s00294-020-01109-4
pubmed: 32980916
pmcid: 7599196
Aref R, Sanad MNME, Schüller HJ (2021) Forkhead transcription factor Fkh1: insights into functional regulatory domains crucial for recruitment of Sin3 histone deacetylase complex. Curr Genet 67:487–499. https://doi.org/10.1007/s00294-021-01158-3
doi: 10.1007/s00294-021-01158-3
pubmed: 33635403
pmcid: 8139909
Baxa U, Speransky V, Steven AC, Wickner RB (2002) Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc Natl Acad Sci USA 99:5253–5260. https://doi.org/10.1073/pnas.082097899
doi: 10.1073/pnas.082097899
pubmed: 11959975
pmcid: 122756
Brubaker K, Cowley SM, Huang K, Loo L, Yochum GS, Ayer DE, Eisenman RN, Radhakrishnan I (2000) Solution structure of the interacting domains of the Mad-Sin3 complex: implications for recruitment of a chromatin-modifying complex. Cell 103:655–665. https://doi.org/10.1016/s0092-8674(00)00168-9
doi: 10.1016/s0092-8674(00)00168-9
pubmed: 11106735
Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581–592. https://doi.org/10.1016/j.cell.2005.10.023
doi: 10.1016/j.cell.2005.10.023
pubmed: 16286007
Conlan RS, Gounalaki N, Hatzis P, Tzamarias D (1999) The Tup1-Cyc8 protein complex can shift from a transcriptional co-repressor to a transcriptional co-activator. J Biol Chem 274:205–210. https://doi.org/10.1074/jbc.274.1.205
doi: 10.1074/jbc.274.1.205
pubmed: 9867831
Cooper TG (2002) Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol Rev 26:223–238. https://doi.org/10.1111/j.1574-6976.2002.tb00612.x
doi: 10.1111/j.1574-6976.2002.tb00612.x
pubmed: 12165425
Cortajarena AL, Wang J, Regan L (2010) Crystal structure of a designed tetratricopeptide repeat module in complex with its peptide ligand. FEBS J 277:1058–1066. https://doi.org/10.1111/j.1742-4658.2009.07549.x
doi: 10.1111/j.1742-4658.2009.07549.x
pubmed: 20089039
Cumberworth A, Lamour G, Babu MM, Gsponer J (2013) Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes. Biochem J 454:361–369. https://doi.org/10.1042/BJ20130545
doi: 10.1042/BJ20130545
pubmed: 23988124
Cunningham TS, Cooper TG (1993) The Saccharomyces cerevisiae DAL80 repressor protein binds to multiple copies of GATAA-containing sequences (URS
doi: 10.1128/jb.175.18.5851-5861.1993
pubmed: 8376332
pmcid: 206664
D’Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28:655–662. https://doi.org/10.1016/j.tibs.2003.10.007
doi: 10.1016/j.tibs.2003.10.007
pubmed: 14659697
Davie JK, Edmondson DG, Coco CB, Dent SY (2003) Tup1-Ssn6 interacts with multiple class I histone deacetylases in vivo. J Biol Chem 278:50158–50162. https://doi.org/10.1074/jbc.M309753200
doi: 10.1074/jbc.M309753200
pubmed: 14525981
Deckert J, Khalaf RA, Hwang SM, Zitomer RS (1999) Characterization of the DNA binding and bending HMG domain of the yeast hypoxic repressor Rox1. Nucleic Acids Res 27:3518–3526. https://doi.org/10.1093/nar/27.17.3518
doi: 10.1093/nar/27.17.3518
pubmed: 10446242
pmcid: 148596
Grzenda A, Lomberk G, Zhang JS, Urrutia R (2009) Sin3: master scaffold and transcriptional corepressor. Biochim Biophys Acta 1789:443–450. https://doi.org/10.1016/j.bbagrm.2009.05.007
doi: 10.1016/j.bbagrm.2009.05.007
pubmed: 19505602
pmcid: 3686104
He X, Nie Y, Zhou H, Hu R, Li Y, He T, Zhu J, Yang Y, Liu M (2021) Structural insight into the binding of TGIF1 to SIN3A PAH2 domain through a C-terminal amphipathic helix. Int J Mol Sci 22:12631. https://doi.org/10.3390/ijms222312631
doi: 10.3390/ijms222312631
pubmed: 34884456
pmcid: 8657803
Hellauer K, Akache B, MacPherson S, Sirard E, Turcotte B (2002) Zinc cluster protein Rdr1p is a transcriptional repressor of the PDR5 gene encoding a multidrug transporter. J Biol Chem 277:17671–17676. https://doi.org/10.1074/jbc.M201637200
doi: 10.1074/jbc.M201637200
pubmed: 11882665
Hildmann C, Riester D, Schwienhorst A (2007) Histone deacetylases–an important class of cellular regulators with a variety of functions. Appl Microbiol Biotechnol 75:487–497. https://doi.org/10.1007/s00253-007-0911-2
doi: 10.1007/s00253-007-0911-2
pubmed: 17377789
Hongay C, Jia N, Bard M, Winston F (2002) Mot3 is a transcriptional repressor of ergosterol biosynthetic genes and is required for normal vacuolar function in Saccharomyces cerevisiae. EMBO J 21:4114–4124. https://doi.org/10.1093/emboj/cdf415
doi: 10.1093/emboj/cdf415
pubmed: 12145211
pmcid: 126159
Jäschke Y, Schwarz J, Clausnitzer D, Müller C, Schüller HJ (2011) Pleiotropic corepressors Sin3 and Ssn6 interact with repressor Opi1 and negatively regulate transcription of genes required for phospholipid biosynthesis in the yeast Saccharomyces cerevisiae. Mol Genet Genom 285:91–100. https://doi.org/10.1007/s00438-010-0589-5
doi: 10.1007/s00438-010-0589-5
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589. https://doi.org/10.1038/s41586-021-03819-2
doi: 10.1038/s41586-021-03819-2
pubmed: 34265844
pmcid: 8371605
Kadosh D, Struhl K (1997) Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365–371. https://doi.org/10.1016/s0092-8674(00)80217-2
doi: 10.1016/s0092-8674(00)80217-2
pubmed: 9150136
Kliewe F, Engelhardt M, Aref R, Schüller HJ (2017) Promoter recruitment of corepressors Sin3 and Cyc8 by activator proteins of the yeast Saccharomyces cerevisiae. Curr Genet 63:739–750. https://doi.org/10.1007/s00294-017-0677-8
doi: 10.1007/s00294-017-0677-8
pubmed: 28175933
Komachi K, Redd MJ, Johnson AD (1994) The WD repeats of Tup1 interact with the homeo domain protein α2. Genes Dev 8:2857–2867. https://doi.org/10.1101/gad.8.23.2857
doi: 10.1101/gad.8.23.2857
pubmed: 7995523
Kuchin S, Carlson M (1998) Functional relationships of Srb10-Srb11 kinase, carboxy-terminal domain kinase CTDK-I, and transcriptional corepressor Ssn6-Tup1. Mol Cell Biol 18:1163–1171. https://doi.org/10.1128/MCB.18.3.1163
doi: 10.1128/MCB.18.3.1163
pubmed: 9488431
pmcid: 108829
Kumar GS, Xie T, Zhang Y, Radhakrishnan I (2011) Solution structure of the mSin3A PAH2-Pf1 SID1 complex: a Mad1/Mxd1-like interaction disrupted by MRG15 in the Rpd3S/Sin3S complex. J Mol Biol 408:987–1000. https://doi.org/10.1016/j.jmb.2011.03.043
doi: 10.1016/j.jmb.2011.03.043
pubmed: 21440557
pmcid: 3096069
Laherty CD, Yang WM, Sun JM, Davie JR, Seto E, Eisenman RN (1997) Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89:349–356. https://doi.org/10.1016/s0092-8674(00)80215-9
doi: 10.1016/s0092-8674(00)80215-9
pubmed: 9150134
Lettow J, Aref R, Schüller HJ (2022) Transcriptional repressor Gal80 recruits corepressor complex Cyc8-Tup1 to structural genes of the Saccharomyces cerevisiae GAL regulon. Curr Genet 68:115–124. https://doi.org/10.1007/s00294-021-01215-x
doi: 10.1007/s00294-021-01215-x
pubmed: 34622331
Mai B, Breeden L (2000) CLN1 and its repression by Xbp1 are important for efficient sporulation in budding yeast. Mol Cell Biol 20:478–487. https://doi.org/10.1128/MCB.20.2.478-487.2000
doi: 10.1128/MCB.20.2.478-487.2000
pubmed: 10611226
pmcid: 85107
Malavé TM, Dent SY (2006) Transcriptional repression by Tup1-Ssn6. Biochem Cell Biol 84:437–443. https://doi.org/10.1139/o06-073
doi: 10.1139/o06-073
pubmed: 16936817
Marcum RD, Radhakrishnan I (2020) The neuronal transcription factor Myt1L interacts via a conserved motif with the PAH1 domain of Sin3 to recruit the Sin3L/Rpd3L histone deacetylase complex. FEBS Lett 594:2322–2330. https://doi.org/10.1002/1873-3468.13811
doi: 10.1002/1873-3468.13811
pubmed: 32391601
pmcid: 8224932
Mumberg D, Müller R, Funk M (1994) Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res 22:5767–5768. https://doi.org/10.1093/nar/22.25.5767
doi: 10.1093/nar/22.25.5767
pubmed: 7838736
pmcid: 310147
Nehlin JO, Carlberg M, Ronne H (1992) Yeast SKO1 gene encodes a bZIP protein that binds to the CRE motif and acts as a repressor of transcription. Nucleic Acids Res 20:5271–5278. https://doi.org/10.1093/nar/20.20.5271
doi: 10.1093/nar/20.20.5271
pubmed: 1437546
pmcid: 334331
Nomura M, Uda-Tochio H, Murai K, Mori N, Nishimura Y (2005) The neural repressor NRSF/REST binds the PAH1 domain of the Sin3 corepressor by using its distinct short hydrophobic helix. J Mol Biol 354:903–915. https://doi.org/10.1016/j.jmb.2005.10.008
doi: 10.1016/j.jmb.2005.10.008
pubmed: 16288918
Östling J, Carlberg M, Ronne H (1996) Functional domains in the Mig1 repressor. Mol Cell Biol 16:753–761. https://doi.org/10.1128/MCB.16.3.753
doi: 10.1128/MCB.16.3.753
pubmed: 8622676
pmcid: 231055
Papamichos-Chronakis M, Petrakis T, Ktistaki E, Topalidou I, Tzamarias D (2002) Cti6, a PHD domain protein, bridges the Cyc8-Tup1 corepressor and the SAGA coactivator to overcome repression at GAL1. Mol Cell 9:1297–1305. https://doi.org/10.1016/s1097-2765(02)00545-2
doi: 10.1016/s1097-2765(02)00545-2
pubmed: 12086626
Parnell EJ, Parnell TJ, Stillman DJ (2021) Genetic analysis argues for a coactivator function for the Saccharomyces cerevisiae Tup1 corepressor. Genetics 219:iyab120. https://doi.org/10.1093/genetics/iyab120
doi: 10.1093/genetics/iyab120
pubmed: 34849878
pmcid: 8633128
Pascual-Ahuir A, Posas F, Serrano R, Proft M (2001) Multiple levels of control regulate the yeast cAMP-response element-binding protein repressor Sko1p in response to stress. J Biol Chem 276:37373–37378. https://doi.org/10.1074/jbc.M105755200
doi: 10.1074/jbc.M105755200
pubmed: 11500510
Pramila T, Miles S, GuhaThakurta D, Jemiolo D, Breeden LL (2002) Conserved homeodomain proteins interact with MADS box protein Mcm1 to restrict ECB-dependent transcription to the M/G1 phase of the cell cycle. Genes Dev 16:3034–3045. https://doi.org/10.1101/gad.1034302
doi: 10.1101/gad.1034302
pubmed: 12464633
pmcid: 187489
Proft M, Struhl K (2002) Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress. Mol Cell 9:1307–1317. https://doi.org/10.1016/s1097-2765(02)00557-9
doi: 10.1016/s1097-2765(02)00557-9
pubmed: 12086627
Grigat M, Jäschke Y, Kliewe F, Pfeifer M, Walz S, Schüller HJ (2012) Multiple histone deacetylases are recruited by corepressor Sin3 and contribute to gene repression mediated by Opi1 regulator of phospholipid biosynthesis in the yeast Saccharomyces cerevisiae. Mol Genet Genomics 287:461–472. https://doi.org/10.1007/s00438-012-0692-x
doi: 10.1007/s00438-012-0692-x
Sahu SC, Swanson KA, Kang RS, Huang K, Brubaker K, Ratcliff K, Radhakrishnan I (2008) Conserved themes in target recognition by the PAH1 and PAH2 domains of the Sin3 transcriptional corepressor. J Mol Biol 375:1444–1456. https://doi.org/10.1016/j.jmb.2007.11.079
doi: 10.1016/j.jmb.2007.11.079
pubmed: 18089292
Schüller J, Lehming N (2003) The cyclin in the RNA polymerase holoenzyme is a target for the transcriptional repressor Tup1p in Saccharomyces cerevisiae. J Mol Microbiol Biotechnol 5:199–205. https://doi.org/10.1159/000071071
Schultz J, Marshall-Carlson L, Carlson M (1990) The N-terminal TPR region is the functional domain of SSN6, a nuclear phosphoprotein of Saccharomyces cerevisiae. Mol Cell Biol 10:4744–4756. https://doi.org/10.1128/mcb.10.9.4744-4756.1990
doi: 10.1128/mcb.10.9.4744-4756.1990
pubmed: 2201901
pmcid: 361075
Smith RL, Redd MJ, Johnson AD (1995) The tetratricopeptide repeats of Ssn6 interact with the homeo domain of α2. Genes Dev 9:2903–2910. https://doi.org/10.1101/gad.9.23.2903
doi: 10.1101/gad.9.23.2903
pubmed: 7498787
Sprague ER, Redd MJ, Johnson AD, Wolberger C (2000) Structure of the C-terminal domain of Tup1, a corepressor of transcription in yeast. EMBO J 19:3016–3027. https://doi.org/10.1093/emboj/19.12.3016
doi: 10.1093/emboj/19.12.3016
pubmed: 10856245
pmcid: 203344
Spronk CA, Tessari M, Kaan AM, Jansen JF, Vermeulen M, Stunnenberg HG, Vuister GW (2000) The Mad1-Sin3B interaction involves a novel helical fold. Nat Struct Biol 7:1100–1104. https://doi.org/10.1038/81944
doi: 10.1038/81944
pubmed: 11101889
Sternberg PW, Stern MJ, Clark I, Herskowitz I (1987) Activation of the yeast HO gene by release from multiple negative controls. Cell 48:567–577. https://doi.org/10.1016/0092-8674(87)90235-2
doi: 10.1016/0092-8674(87)90235-2
pubmed: 3545494
Stirnimann CU, Petsalaki E, Russell RB, Müller CW (2010) WD40 proteins propel cellular networks. Trends Biochem Sci 35:565–574. https://doi.org/10.1016/j.tibs.2010.04.003
doi: 10.1016/j.tibs.2010.04.003
pubmed: 20451393
Swanson KA, Knoepfler PS, Huang K, Kang RS, Cowley SM, Laherty CD, Eisenman RN, Radhakrishnan I (2004) HBP1 and Mad1 repressors bind the Sin3 corepressor PAH2 domain with opposite helical orientations. Nat Struct Mol Biol 11:738–746. https://doi.org/10.1038/nsmb798
doi: 10.1038/nsmb798
pubmed: 15235594
Tzamarias D, Struhl K (1994) Functional dissection of the yeast Cyc8-Tup1 transcriptional co-repressor complex. Nature 369:758–761. https://doi.org/10.1038/369758a0
doi: 10.1038/369758a0
pubmed: 8008070
Tzamarias D, Struhl K (1995) Distinct TPR motifs of Cyc8 are involved in recruiting the Cyc8-Tup1 corepressor complex to differentially regulated promoters. Genes Dev 9:821–831. https://doi.org/10.1101/gad.9.7.821
doi: 10.1101/gad.9.7.821
pubmed: 7705659
van Ingen H, Lasonder E, Jansen JF, Kaan AM, Spronk CA, Stunnenberg HG, Vuister GW (2004) Extension of the binding motif of the Sin3 interacting domain of the Mad family proteins. Biochemistry 43:46–54. https://doi.org/10.1021/bi0355645
doi: 10.1021/bi0355645
pubmed: 14705930
Varanasi US, Klis M, Mikesell PB, Trumbly RJ (1996) The Cyc8 (Ssn6)-Tup1 corepressor complex is composed of one Cyc8 and four Tup1 subunits. Mol Cell Biol 16:6707–6714. https://doi.org/10.1128/MCB.16.12.6707
doi: 10.1128/MCB.16.12.6707
pubmed: 8943325
pmcid: 231673
Vidal M, Strich R, Esposito RE, Gaber RF (1991) RPD1 (SIN3/UME4) is required for maximal activation and repression of diverse yeast genes. Mol Cell Biol 11:6306–6316. https://doi.org/10.1128/mcb.11.12.6306-6316.1991
doi: 10.1128/mcb.11.12.6306-6316.1991
pubmed: 1944290
pmcid: 361824
Wagner C, Dietz M, Wittmann J, Albrecht A, Schüller HJ (2001) The negative regulator Opi1 of phospholipid biosynthesis in yeast contacts the pleiotropic repressor Sin3 and the transcriptional activator Ino2. Mol Microbiol 41:155–166. https://doi.org/10.1046/j.1365-2958.2001.02495.x
doi: 10.1046/j.1365-2958.2001.02495.x
pubmed: 11454208
Wang H, Stillman DJ (1993) Transcriptional repression in Saccharomyces cerevisiae by a SIN3-LexA fusion protein. Mol Cell Biol 13:1805–1814. https://doi.org/10.1128/mcb.13.3.1805-1814,1993
doi: 10.1128/mcb.13.3.1805-1814,1993
pubmed: 8441414
pmcid: 359493
Wang H, Clark I, Nicholson PR, Herskowitz I, Stillman DJ (1990) The Saccharomyces cerevisiae SIN3 gene, a negative regulator of HO, contains four paired amphipathic helix motifs. Mol Cell Biol 10:5927–5936. https://doi.org/10.1128/mcb.10.11.5927-5936,1990
doi: 10.1128/mcb.10.11.5927-5936,1990
pubmed: 2233725
pmcid: 361389
Washburn BK, Esposito RE (2001) Identification of the Sin3-binding site in Ume6 defines a two-step process for conversion of Ume6 from a transcriptional repressor to an activator in yeast. Mol Cell Biol 21:2057–2069. https://doi.org/10.1128/MCB.21.6.2057-2069.2001
doi: 10.1128/MCB.21.6.2057-2069.2001
pubmed: 11238941
pmcid: 86811
Watanabe K, Yamamoto S, Sakaguti S, Isayama K, Oka M, Nagano H, Mizukami Y (2018) A novel somatic mutation of SIN3A detected in breast cancer by whole-exome sequencing enhances cell proliferation through ER αexpression. Sci Rep 8:16000. https://doi.org/10.1038/s41598-018-34290-1
doi: 10.1038/s41598-018-34290-1
pubmed: 30375428
pmcid: 6207735
Watson AD, Edmondson DG, Bone JR, Mukai Y, Yu Y, Du W, Stillman DJ, Roth SY (2000) Ssn6-Tup1 interacts with class I histone deacetylases required for repression. Genes Dev 14:2737–2744. https://doi.org/10.1101/gad.829100
doi: 10.1101/gad.829100
pubmed: 11069890
pmcid: 317033
Williams FE, Trumbly RJ (1990) Characterization of TUP1, a mediator of glucose repression in Saccharomyces cerevisiae. Mol Cell Biol 10:6500–6511. https://doi.org/10.1128/mcb.10.12.6500-6511.1990
doi: 10.1128/mcb.10.12.6500-6511.1990
pubmed: 2247069
pmcid: 362927
Wong KH, Struhl K (2011) The Cyc8-Tup1 complex inhibits transcription primarily by masking the activation domain of the recruiting protein. Genes Dev 25:2525–2539. https://doi.org/10.1101/gad.179275.111
doi: 10.1101/gad.179275.111
pubmed: 22156212
pmcid: 3243062
Wu J, Suka N, Carlson M, Grunstein M (2001) TUP1 utilizes histone H3/H2B specific HDA1 deacetylase to repress gene activity in yeast. Mol Cell 7:117–126. https://doi.org/10.1016/s1097-2765(01)00160-5
doi: 10.1016/s1097-2765(01)00160-5
pubmed: 11172717
Xu C, Min J (2011) Structure and function of WD40 domain proteins. Protein Cell 2:202–214. https://doi.org/10.1007/s13238-011-1018-1
doi: 10.1007/s13238-011-1018-1
pubmed: 21468892
pmcid: 4875305
Zaman Z, Ansari AZ, Koh SS, Young R, Ptashne M (2001) Interaction of a transcriptional repressor with the RNA polymerase II holoenzyme plays a crucial role in repression. Proc Natl Acad Sci USA 98:2550–2554. https://doi.org/10.1073/pnas.041611198
doi: 10.1073/pnas.041611198
pubmed: 11226276
pmcid: 30175
Zeytuni N, Zarivach R (2012) Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure 20:397–405. https://doi.org/10.1016/j.str.2012.01.006
doi: 10.1016/j.str.2012.01.006
pubmed: 22404999
Zhang L, Guarente L (1994) Evidence that TUP1/SSN6 has a positive effect on the activity of the yeast activator HAP1. Genetics 136:813–817. https://doi.org/10.1093/genetics/136.3.813
doi: 10.1093/genetics/136.3.813
pubmed: 8005436
pmcid: 1205887
Zhang Z, Reese JC (2005) Molecular genetic analysis of the yeast repressor Rfx1/Crt1 reveals a novel two-step regulatory mechanism. Mol Cell Biol 25:7399–7411. https://doi.org/10.1128/MCB.25.17.7399-7411.2005
doi: 10.1128/MCB.25.17.7399-7411.2005
pubmed: 16107689
pmcid: 1190298