Mediator binding to UASs is broadly uncoupled from transcription and cooperative with TFIID recruitment to promoters

EMBO Journal

Volumn 35, Issue 22, 2016, Pages 2435-2446

  Grünberg, Sebastian ^a   Henikoff, Steven ^a,b   Hahn, Steven ^a   Zentner, Gabriel E ^c  

^a USA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

ChEC seq; Mediator; TFIID

Indexed keywords

DNA; MEDIATOR COMPLEX; TRANSCRIPTION FACTOR IID; FUNGAL DNA; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; SPT15 PROTEIN, S CEREVISIAE; TATA BINDING PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CHROMATIN; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION; GENE INACTIVATION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; UPREGULATION; UPSTREAM ACTIVATING SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; GENETICS; METABOLISM; REGULATORY SEQUENCE; SACCHAROMYCES CEREVISIAE;

CHROMATIN IMMUNOPRECIPITATION; DNA, FUNGAL; MEDIATOR COMPLEX; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TATA-BOX BINDING PROTEIN; TRANSCRIPTION, GENETIC;

EID: 84991790974     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201695020     Document Type: Article

References (67)

1. Allen BL, Taatjes DJ (2015) The Mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol 16: 155–166
2. Andrau J-C, van de Pasch L, Lijnzaad P, Bijma T, Koerkamp MG, van de Peppel J, Werner M, Holstege FCP (2006) Genome-Wide Location of the Coactivator Mediator: Binding without Activation and Transient Cdk8 Interaction on DNA. Mol Cell 22: 179–192
3. Ansari SA, Ganapathi M, Benschop JJ, Holstege FCP, Wade JT, Morse RH (2012) Distinct role of Mediator tail module in regulation of SAGA-dependent, TATA-containing genes in yeast. EMBO J 31: 44–57
4. Ansari SA, He Q, Morse RH (2009) Mediator complex association with constitutively transcribed genes in yeast. Proc Natl Acad Sci USA 106: 16734–16739
5. Ansari SA, Morse RH (2012) Selective role of Mediator tail module in the transcription of highly regulated genes in yeast. Transcription 3: 110–114
6. Baek HJ, Malik S, Qin J, Roeder RG (2002) Requirement of TRAP/Mediator for both activator-independent and activator-dependent transcription in conjunction with TFIID-associated TAFIIs. Mol Cell Biol 22: 2842–2852
7. Basehoar AD, Zanton SJ, Pugh BF (2004) Identification and distinct regulation of yeast TATA Box-containing genes. Cell 116: 699–709
8. Bonnet J, Wang C-Y, Baptista T, Vincent SD, Hsiao W-C, Stierle M, Kao C-F, Tora L, Devys D (2014) The SAGA coactivator complex acts on the whole transcribed genome and is required for RNA polymerase II transcription. Genes Dev 28: 1999–2012
9. de Bruin D, Zaman Z, Liberatore RA, Ptashne M (2001) Telomere looping permits gene activation by a downstream UAS in yeast. Nature 409: 109–113
10. Cai G, Imasaki T, Takagi Y, Asturias FJ (2009) Mediator structural conservation and implications for the regulation mechanism. Structure 17: 559–567
11. Chambers A, Stanway C, Kingsman AJ, Kingsman SM (1988) The UAS of the yeast PGK gene is composed of multiple functional elements. Nucleic Acids Res 16: 8245–8260
12. Churchman LS, Weissman JS (2011) Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469: 368–373
13. Durant M, Pugh BF (2007) NuA4-directed chromatin transactions throughout the Saccharomyces cerevisiae genome. Mol Cell Biol 27: 5327–5335
14. Erb I, van Nimwegen E (2011) Transcription factor binding site positioning in yeast: proximal promoter motifs characterize TATA-less promoters. PLoS One 6: e24279
15. Eyboulet F, Cibot C, Eychenne T, Neil H, Alibert O, Werner M, Soutourina J (2013) Mediator links transcription and DNA repair by facilitating Rad2/XPG recruitment. Genes Dev 27: 2549–2562
16. Fan X, Chou DM, Struhl K (2006) Activator-specific recruitment of Mediator in vivo. Nat Struct Mol Biol 13: 117–120
17. Fan X, Struhl K (2009) Where does Mediator bind in vivo? PLoS One 4: e5029
18. Gavin A-C, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dumpelfeld B, Edelmann A, Heurtier M-A, Hoffman V, Hoefert C, Klein K, Hudak M, Michon A-M, Schelder M, Schirle M, Remor M et al (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631–636
19. Gavin A-C, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon A-M, Cruciat C-M, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T et al (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141–147
20. Grokhovsky SL, Il'icheva IA, Nechipurenko DY, Golovkin MV, Panchenko LA, Polozov RV, Nechipurenko YD (2011) Sequence-specific ultrasonic cleavage of DNA. Biophys J 100: 117–125
21. Haruki H, Nishikawa J, Laemmli UK (2008) The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol Cell 31: 925–932
22. He Y, Swaminathan A, Lopes JM (2012) Transcription regulation of the Saccharomyces cerevisiae PHO5 gene by the Ino2p and Ino4p basic helix–loop–helix proteins. Mol Microbiol 83: 395–407
23. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576–589
24. Henikoff JG, Belsky JA, Krassovsky K, MacAlpine DM, Henikoff S (2011) Epigenome characterization at single base-pair resolution. Proc Natl Acad Sci USA 108: 18318–18323
25. Herbig E, Warfield L, Fish L, Fishburn J, Knutson BA, Moorefield B, Pacheco D, Hahn S (2010) Mechanism of mediator recruitment by tandem Gcn4 activation domains and three Gal11 activator-binding domains. Mol Cell Biol 30: 2376–2390
26. Hinnebusch AG (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59: 407–450
27. Holstege FCP, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717–728
28. Hsieh TH, Weiner A, Lajoie B, Dekker J, Friedman N, Rando OJ (2015) Mapping nucleosome resolution chromosome folding in yeast by micro-C. Cell 162: 108–119
29. Imasaki T, Calero G, Cai G, Tsai K-L, Yamada K, Cardelli F, Erdjument-Bromage H, Tempst P, Berger I, Kornberg GL, Asturias FJ, Kornberg RD, Takagi Y (2011) Architecture of the Mediator head module. Nature 475: 240–243
30. Jedidi I, Zhang F, Qiu H, Stahl SJ, Palmer I, Kaufman JD, Nadaud PS, Mukherjee S, Wingfield PT, Jaroniec CP, Hinnebusch AG (2010) Activator Gcn4 employs multiple segments of Med15/Gal11, including the KIX domain, to recruit mediator to target genes in vivo. J Biol Chem 285: 2438–2455
31. Jeronimo C, Robert F (2014) Kin28 regulates the transient association of Mediator with core promoters. Nat Struct Mol Biol 21: 449–455
32. Jia M, Larossa R, Lee J, Rafalski A, Derose E, Gonye G, Xue Z (2000) Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron methyl. Physiol Genomics 3: 83–92
33. Johnson KM, Carey M (2003) Assembly of a Mediator/TFIID/TFIIA complex bypasses the need for an activator. Curr Biol 13: 772–777
34. Johnson KM, Wang J, Smallwood A, Arayata C, Carey M (2002) TFIID and human mediator coactivator complexes assemble cooperatively on promoter DNA. Genes Dev 16: 1852–1863
35. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430–435
36. Knutson BA, Hahn S (2011) Domains of Tra1 important for activator recruitment and transcription coactivator functions of SAGA and NuA4 complexes. Mol Cell Biol 31: 818–831
37. Komarnitsky PB, Michel B, Buratowski S (1999) TFIID-specific yeast TAF40 is essential for the majority of RNA polymerase II-mediated transcription in vivo. Genes Dev 13: 2484–2489
38. Larivière L, Plaschka C, Seizl M, Petrotchenko EV, Wenzeck L, Borchers CH, Cramer P (2013) Model of the Mediator middle module based on protein cross-linking. Nucleic Acids Res 41: 9266–9273
39. Lariviere L, Plaschka C, Seizl M, Wenzeck L, Kurth F, Cramer P (2012) Structure of the Mediator head module. Nature 492: 448–451
40. Li X-Y, Bhaumik SR, Zhu X, Li L, Shen W-C, Dixit BL, Green MR (2002) Selective recruitment of TAFs by yeast upstream activating sequences: implications for eukaryotic promoter structure. Curr Biol 12: 1240–1244
41. Liu Y, Kung C, Fishburn J, Ansari AZ, Shokat KM, Hahn S (2004) Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol Cell Biol 24: 1721–1735
42. Louder RK, He Y, López-Blanco JR, Fang J, Chacón P, Nogales E (2016) Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature 531: 604–609
43. Lubliner S, Keren L, Segal E (2013) Sequence features of yeast and human core promoters that are predictive of maximal promoter activity. Nucleic Acids Res 41: 5569–5581
44. MacIsaac K, Wang T, Gordon DB, Gifford D, Stormo G, Fraenkel E (2006) An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7: 113
45. Matangkasombut O, Buratowski RM, Swilling NW, Buratowski S (2000) Bromodomain factor 1 corresponds to a missing piece of yeast TFIID. Genes Dev 14: 951–962
46. Mukundan B, Ansari A (2013) Srb5/Med18-mediated termination of transcription is dependent on gene looping. J Biol Chem 288: 11384–11394
47. Neph S, Kuehn MS, Reynolds AP, Haugen E, Thurman RE, Johnson AK, Rynes E, Maurano MT, Vierstra J, Thomas S, Sandstrom R, Humbert R, Stamatoyannopoulos JA (2012) BEDOPS: high-performance genomic feature operations. Bioinformatics 28: 1919–1920
48. Park D, Lee Y, Bhupindersingh G, Iyer VR (2013) Widespread misinterpretable ChIP-seq bias in yeast. PLoS One 8: e83506
49. Paul E, Zhu ZI, Landsman D, Morse RH (2015) Genome-wide association of mediator and RNA polymerase II in wild-type and mediator mutant yeast. Mol Cell Biol 35: 331–342
50. Plank JL, Dean A (2014) Enhancer function: mechanistic and genome-wide insights come together. Mol Cell 55: 5–14
51. Plaschka C, Lariviere L, Wenzeck L, Seizl M, Hemann M, Tegunov D, Petrotchenko EV, Borchers CH, Baumeister W, Herzog F, Villa E, Cramer P (2015) Architecture of the RNA polymerase II-Mediator core initiation complex. Nature 518: 376–380
52. Poptsova MS, Il'icheva IA, Nechipurenko DY, Panchenko LA, Khodikov MV, Oparina NY, Polozov RV, Nechipurenko YD, Grokhovsky SL (2014) Non-random DNA fragmentation in next-generation sequencing. Sci Rep 4: 4532
53. Reavey CT, Hickman MJ, Dobi KC, Botstein D, Winston F (2015) Analysis of polygenic mutants suggests a role for mediator in regulating transcriptional activation distance in Saccharomyces cerevisiae. Genetics 201: 599–612
54. Saint M, Sawhney S, Sinha I, Singh RP, Dahiya R, Thakur A, Siddharthan R, Natarajan K (2014) The TAF9 C-terminal conserved region domain is required for SAGA and TFIID promoter occupancy to promote transcriptional activation. Mol Cell Biol 34: 1547–1563
55. Takahashi H, Parmely Tari J, Sato S, Tomomori-Sato C, Banks Charles AS, Kong Stephanie E, Szutorisz H, Swanson Selene K, Martin-Brown S, Washburn Michael P, Florens L, Seidel Chris W, Lin C, Smith Edwin R, Shilatifard A, Conaway Ronald C, Conaway Joan W (2011) Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146: 92–104
56. Tatarakis A, Margaritis T, Martinez-Jimenez CP, Kouskouti A, Mohan Ii WS, Haroniti A, Kafetzopoulos D, Tora L, Talianidis I (2008) Dominant and redundant functions of TFIID involved in the regulation of hepatic genes. Mol Cell 31: 531–543
57. Teytelman L, Özaydın B, Zill O, Lefrançois P, Snyder M, Rine J, Eisen MB (2009) Impact of chromatin structures on DNA processing for genomic analyses. PLoS One 4: e6700
58. Teytelman L, Thurtle DM, Rine J, van Oudenaarden A (2013) Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc Natl Acad Sci USA 110: 18602–18607
59. Tsai K-L, Tomomori-Sato C, Sato S, Conaway Ronald C, Conaway Joan W, Asturias Francisco J (2014) Subunit architecture and functional modular rearrangements of the transcriptional mediator complex. Cell 157: 1430–1444
60. Van Slyke C, Grayhack EJ (2003) The essential transcription factor Reb1p interacts with the CLB2 UAS outside of the G2/M control region. Nucleic Acids Res 31: 4597–4607
61. Vega VB, Cheung E, Palanisamy N, Sung W-K (2009) Inherent signals in sequencing-based Chromatin-ImmunoPrecipitation control libraries. PLoS One 4: e5241
62. Wang X, Sun Q, Ding Z, Ji J, Wang J, Kong X, Yang J, Cai G (2014) Redefining the modular organization of the core Mediator complex. Cell Res 24: 796–808
63. Wong KH, Jin Y, Struhl K (2014) TFIIH phosphorylation of the Pol II CTD stimulates mediator dissociation from the preinitiation complex and promoter escape. Mol Cell 54: 601–612
64. Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Munster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM (2009) Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033–1037
65. Yan C, Zhang D, Raygoza Garay JA, Mwangi MM, Bai L (2015) Decoupling of divergent gene regulation by sequence-specific DNA binding factors. Nucleic Acids Res 43: 7292–7305
66. Zentner GE, Kasinathan S, Xin B, Rohs R, Henikoff S (2015) ChEC-seq kinetics discriminates transcription factor binding sites by DNA sequence and shape in vivo. Nat Commun 6: 8733
67. Zhu X, Zhang Y, Bjornsdottir G, Liu Z, Quan A, Costanzo M, Dávila López M, Westholm JO, Ronne H, Boone C, Gustafsson CM, Myers LC (2011) Histone modifications influence mediator interactions with chromatin. Nucleic Acids Res 39: 8342–8354