Evidence for Multiple Mediator Complexes in Yeast Independently Recruited by Activated Heat Shock Factor

REFERENCES

• Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA. 2013. Master transcription factors and Mediator establish super-enhancers at key cell identity genes. Cell 153:307–319. http://dx.doi.org/10.1016/j.cell.2013.03.035.
   PubMed Web of Science ®Google Scholar
• Haber JE. 2012. Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191:33–64. http://dx.doi.org/10.1534/genetics.111.134577.
   PubMed Web of Science ®Google Scholar
• Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-Andre V, Sigova AA, Hoke HA, Young RA. 2013. Super-enhancers in the control of cell identity and disease. Cell 155:934–947. http://dx.doi.org/10.1016/j.cell.2013.09.053.
   PubMed Web of Science ®Google Scholar
• Malik S, Roeder RG. 2010. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 11:761–772. http://dx.doi.org/10.1038/nrg2901.
   PubMed Web of Science ®Google Scholar
• Poss ZC, Ebmeier CC, Taatjes DJ. 2013. The Mediator complex and transcription regulation. Crit Rev Biochem Mol Biol 48:575–608. http://dx.doi.org/10.3109/10409238.2013.840259.
   PubMed Web of Science ®Google Scholar
• Ansari SA, Morse RH. 2013. Mechanisms of Mediator complex action in transcriptional activation. Cell Mol Life Sci 70:2743–2756. http://dx.doi.org/10.1007/s00018-013-1265-9.
   PubMed Web of Science ®Google Scholar
• Allen BL, Taatjes DJ. 2015. The Mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol 16:155–166. http://dx.doi.org/10.1038/nrm3951.
   PubMed Web of Science ®Google Scholar
• Bryant GO, Ptashne M. 2003. Independent recruitment in vivo by Gal4 of two complexes required for transcription. Mol Cell 11:1301–1309. http://dx.doi.org/10.1016/S1097-2765(03)00144-8.
   PubMed Web of Science ®Google Scholar
• Fishburn J, Mohibullah N, Hahn S. 2005. Function of a eukaryotic transcription activator during the transcription cycle. Mol Cell 18:369–378. http://dx.doi.org/10.1016/j.molcel.2005.03.029.
   PubMed Web of Science ®Google Scholar
• Reeves WM, Hahn S. 2005. Targets of the Gal4 transcription activator in functional transcription complexes. Mol Cell Biol 25:9092–9102. http://dx.doi.org/10.1128/MCB.25.20.9092-9102.2005.
   PubMed Web of Science ®Google Scholar
• Yang F, Vought BW, Satterlee JS, Walker AK, Jim Sun ZY, Watts JL, DeBeaumont R, Saito RM, Hyberts SG, Yang S, Macol C, Iyer L, Tjian R, van den Heuvel S, Hart AC, Wagner G, Naar AM. 2006. An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442:700–704. http://dx.doi.org/10.1038/nature04942.
   PubMed Web of Science ®Google Scholar
• Spaeth JM, Kim NH, Boyer TG. 2011. Mediator and human disease. Semin Cell Dev Biol 22:776–787. http://dx.doi.org/10.1016/j.semcdb.2011.07.024.
   PubMed Web of Science ®Google Scholar
• Lariviere L, Plaschka C, Seizl M, Wenzeck L, Kurth F, Cramer P. 2012. Structure of the Mediator head module. Nature 492:448–451. http://dx.doi.org/10.1038/nature11670.
   PubMed Web of Science ®Google Scholar
• Esnault C, Ghavi-Helm Y, Brun S, Soutourina J, Van Berkum N, Boschiero C, Holstege F, Werner M. 2008. Mediator-dependent recruitment of TFIIH modules in preinitiation complex. Mol Cell 31:337–346. http://dx.doi.org/10.1016/j.molcel.2008.06.021.
   PubMed Web of Science ®Google Scholar
• Soutourina J, Wydau S, Ambroise Y, Boschiero C, Werner M. 2011. Direct interaction of RNA polymerase II and Mediator required for transcription in vivo. Science 331:1451–1454. http://dx.doi.org/10.1126/science.1200188.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1038/nature14229.
   PubMed Web of Science ®Google Scholar
• Robinson PJ, Bushnell DA, Trnka MJ, Burlingame AL, Kornberg RD. 2012. Structure of the Mediator head module bound to the carboxy-terminal domain of RNA polymerase II. Proc Natl Acad Sci U S A 109:17931–17935. http://dx.doi.org/10.1073/pnas.1215241109.
   PubMed Web of Science ®Google Scholar
• Cai G, Imasaki T, Yamada K, Cardelli F, Takagi Y, Asturias FJ. 2010. Mediator head module structure and functional interactions. Nat Struct Mol Biol 17:273–279. http://dx.doi.org/10.1038/nsmb.1757.
   PubMed Web of Science ®Google Scholar
• Cevher MA, Shi Y, Li D, Chait BT, Malik S, Roeder RG. 2014. Reconstitution of active human core Mediator complex reveals a critical role of the MED14 subunit. Nat Struct Mol Biol 21:1028–1034. http://dx.doi.org/10.1038/nsmb.2914.
   PubMed Web of Science ®Google Scholar
• Tsai KL, Tomomori-Sato C, Sato S, Conaway RC, Conaway JW, Asturias FJ. 2014. Subunit architecture and functional modular rearrangements of the transcriptional Mediator complex. Cell 157:1430–1444. http://dx.doi.org/10.1016/j.cell.2014.05.015.
   PubMed Web of Science ®Google Scholar
• Robinson PJ, Trnka MJ, Pellarin R, Greenberg CH, Bushnell DA, Davis R, Burlingame AL, Sali A, Kornberg RD. 2015. Molecular architecture of the yeast Mediator complex. eLife 4:e08719. http://dx.doi.org/10.7554/eLife.08719.
   PubMedGoogle Scholar
• Baumli S, Hoeppner S, Cramer P. 2005. A conserved mediator hinge revealed in the structure of the MED7.MED21 (Med7.Srb7) heterodimer. J Biol Chem 280:18171–18178. http://dx.doi.org/10.1074/jbc.M413466200.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1128/MCB.01046-09.
   PubMed Web of Science ®Google Scholar
• Thakur JK, Arthanari H, Yang F, Pan SJ, Fan X, Breger J, Frueh DP, Gulshan K, Li DK, Mylonakis E, Struhl K, Moye-Rowley WS, Cormack BP, Wagner G, Naar AM. 2008. A nuclear receptor-like pathway regulating multidrug resistance in fungi. Nature 452:604–609. http://dx.doi.org/10.1038/nature06836.
   PubMed Web of Science ®Google Scholar
• Thakur JK, Arthanari H, Yang F, Chau KH, Wagner G, Naar AM. 2009. Mediator subunit Gal11p/MED15 is required for fatty acid-dependent gene activation by yeast transcription factor Oaf1p. J Biol Chem 284:4422–4428. http://dx.doi.org/10.1074/jbc.M808263200.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1074/jbc.M109.071589.
   PubMed Web of Science ®Google Scholar
• Kim S, Gross DS. 2013. Mediator recruitment to heat shock genes requires dual Hsf1 activation domains and Mediator Tail subunits Med15 and Med16. J Biol Chem 288:12197–12213. http://dx.doi.org/10.1074/jbc.M112.449553.
   PubMed Web of Science ®Google Scholar
• Taatjes DJ, Naar AM, Andel F, Nogales E, Tjian R. 2002. Structure, function, and activator-induced conformations of the CRSP coactivator. Science 295:1058–1062. http://dx.doi.org/10.1126/science.1065249.
   PubMed Web of Science ®Google Scholar
• Cai G, Imasaki T, Takagi Y, Asturias F. 2009. Mediator structural conservation and implications for the regulation mechanism. Structure 17:559–567. http://dx.doi.org/10.1016/j.str.2009.01.016.
   PubMed Web of Science ®Google Scholar
• Ebmeier CC, Taatjes DJ. 2010. Activator-Mediator binding regulates Mediator-cofactor interactions. Proc Natl Acad Sci U S A 107:11283–11288. http://dx.doi.org/10.1073/pnas.0914215107.
   PubMed Web of Science ®Google Scholar
• Kremer SB, Kim S, Jeong JO, Moustafa YM, Chen A, Zhao J, Gross DS. 2012. Role of Mediator in regulating Pol II elongation and nucleosome displacement in Saccharomyces cerevisiae. Genetics 191:95–106. http://dx.doi.org/10.1534/genetics.111.135806.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Parmely TJ, Sato S, Tomomori-Sato C, Banks CA, Kong SE, Szutorisz H, Swanson SK, Martin-Brown S, Washburn MP, Florens L, Seidel CW, Lin C, Smith ER, Shilatifard A, Conaway RC, Conaway JW. 2011. Human Mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146:92–104. http://dx.doi.org/10.1016/j.cell.2011.06.005.
   PubMed Web of Science ®Google Scholar
• Donner AJ, Ebmeier CC, Taatjes DJ, Espinosa JM. 2010. CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat Struct Mol Biol 17:194–201. http://dx.doi.org/10.1038/nsmb.1752.
   PubMed Web of Science ®Google Scholar
• Dai C, Whitesell L, Rogers AB, Lindquist S. 2007. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130:1005–1018. http://dx.doi.org/10.1016/j.cell.2007.07.020.
   PubMed Web of Science ®Google Scholar
• Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM, Fraenkel E, Ince TA, Whitesell L, Lindquist S. 2012. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150:549–562. http://dx.doi.org/10.1016/j.cell.2012.06.031.
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Santagata S, Mendillo ML, Sholl LM, Ben-Aharon I, Beck AH, Dias-Santagata D, Koeva M, Stemmer SM, Whitesell L, Lindquist S. 2014. The reprogramming of tumor stroma by HSF1 is a potent enabler of malignancy. Cell 158:564–578. http://dx.doi.org/10.1016/j.cell.2014.05.045.
   PubMed Web of Science ®Google Scholar
• Liu XD, Liu PC, Santoro N, Thiele DJ. 1997. Conservation of a stress response: human heat shock transcription factors functionally substitute for yeast HSF. EMBO J 16:6466–6477. http://dx.doi.org/10.1093/emboj/16.21.6466.
   PubMedGoogle Scholar
• Singh H, Erkine AM, Kremer SB, Duttweiler HM, Davis DA, Iqbal J, Gross RR, Gross DS. 2006. A functional module of yeast Mediator that governs the dynamic range of heat-shock gene expression. Genetics 172:2169–2184.
   PubMedGoogle Scholar
• McDaniel D, Caplan AJ, Lee MS, Adams CC, Fishel BR, Gross DS, Garrard WT. 1989. Basal-level expression of the yeast HSP82 gene requires a heat shock regulatory element. Mol Cell Biol 9:4789–4798. http://dx.doi.org/10.1128/MCB.9.11.4789.
   PubMedGoogle Scholar
• Gross DS, English KE, Collins KW, Lee S. 1990. Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements. J Mol Biol 216:611–631. http://dx.doi.org/10.1016/0022-2836(90)90387-2.
   PubMedGoogle Scholar
• Giardina C, Lis JT. 1995. Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol Cell Biol 15:2737–2744. http://dx.doi.org/10.1128/MCB.15.5.2737.
   PubMedGoogle Scholar
• Hahn JS, Hu Z, Thiele DJ, Iyer VR. 2004. Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24:5249–5256. http://dx.doi.org/10.1128/MCB.24.12.5249-5256.2004.
   PubMed Web of Science ®Google Scholar
• Erkine AM, Magrogan SF, Sekinger EA, Gross DS. 1999. Cooperative binding of heat shock factor to the yeast HSP82 promoter in vivo and in vitro. Mol Cell Biol 19:1627–1639. http://dx.doi.org/10.1128/MCB.19.3.1627.
   PubMedGoogle Scholar
• Fan X, Chou DM, Struhl K. 2006. Activator-specific recruitment of Mediator in vivo. Nat Struct Mol Biol 13:117–120. http://dx.doi.org/10.1038/nsmb1049.
   PubMed Web of Science ®Google Scholar
• Zhao J, Herrera-Diaz J, Gross DS. 2005. Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol Cell Biol 25:8985–8999. http://dx.doi.org/10.1128/MCB.25.20.8985-8999.2005.
   PubMed Web of Science ®Google Scholar
• Erkina TY, Tschetter PA, Erkine AM. 2008. Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes. Mol Cell Biol 28:1207–1217. http://dx.doi.org/10.1128/MCB.01069-07.
   PubMedGoogle Scholar
• Kremer SB, Gross DS. 2009. SAGA and Rpd3 chromatin modification complexes dynamically regulate heat shock gene structure and expression. J Biol Chem 284:32914–32931. http://dx.doi.org/10.1074/jbc.M109.058610.
   PubMedGoogle Scholar
• Erkina TY, Zou Y, Freeling S, Vorobyev VI, Erkine AM. 2010. Functional interplay between chromatin remodeling complexes RSC, SWI/SNF and ISWI in regulation of yeast heat shock genes. Nucleic Acids Res 38:1441–1449. http://dx.doi.org/10.1093/nar/gkp1130.
   PubMedGoogle Scholar
• 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. http://dx.doi.org/10.1038/cr.2014.64.
   PubMed Web of Science ®Google Scholar
• Zhang F, Sumibcay L, Hinnebusch AG, Swanson MJ. 2004. A triad of subunits from the Gal11/tail domain of Srb mediator is an in vivo target of transcriptional activator Gcn4p. Mol Cell Biol 24:6871–6886. http://dx.doi.org/10.1128/MCB.24.15.6871-6886.2004.
   PubMed Web of Science ®Google Scholar
• Li Y, Bjorklund S, Jiang YW, Kim YJ, Lane WS, Stillman DJ, Kornberg RD. 1995. Yeast global transcriptional regulators Sin4 and Rgr1 are components of mediator complex/RNA polymerase II holoenzyme. Proc Natl Acad Sci U S A 92:10864–10868. http://dx.doi.org/10.1073/pnas.92.24.10864.
   PubMedGoogle Scholar
• Haruki H, Nishikawa J, Laemmli UK. 2008. The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol Cell 31:925–932. http://dx.doi.org/10.1016/j.molcel.2008.07.020.
   PubMed Web of Science ®Google Scholar
• Knop M, Siegers K, Pereira G, Zachariae W, Windsor B, Nasmyth K, Schiebel E. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15:963–972. http://dx.doi.org/10.1002/(SICI)1097-0061(199907)15:10B<963::AID-YEA399>3.0.CO;2-W.
   PubMed Web of Science ®Google Scholar
• Erkine AM, Adams CC, Diken T, Gross DS. 1996. Heat shock factor gains access to the yeast HSC82 promoter independently of other sequence-specific factors and antagonizes nucleosomal repression of basal and induced transcription. Mol Cell Biol 16:7004–7017. http://dx.doi.org/10.1128/MCB.16.12.7004.
   PubMedGoogle Scholar
• Balakrishnan SK, Gross DS. 2008. The tumor suppressor p53 associates with gene coding regions and co-traverses with elongating RNA polymerase II in an in vivo model. Oncogene 27:2661–2672. http://dx.doi.org/10.1038/sj.onc.1210935.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
   PubMed Web of Science ®Google Scholar
• Andrau JC, van de Pasch L, Lijnzaad P, Bijma T, Koerkamp MG, van de Peppel J, Werner M, Holstege FC. 2006. Genome-wide location of the coactivator Mediator: binding without activation and transient Cdk8 interaction on DNA. Mol Cell 22:179–192. http://dx.doi.org/10.1016/j.molcel.2006.03.023.
   PubMed Web of Science ®Google Scholar
• Fan X, Struhl K. 2009. Where does Mediator bind in vivo? PLoS One 4:e5029. http://dx.doi.org/10.1371/journal.pone.0005029.
   PubMed Web of Science ®Google Scholar
• Galdieri L, Desai P, Vancura A. 2012. Facilitated assembly of the preinitiation complex by separated tail and head/middle modules of the Mediator. J Mol Biol 415:464–474. http://dx.doi.org/10.1016/j.jmb.2011.11.020.
   PubMedGoogle Scholar
• Jeronimo C, Robert F. 2014. Kin28 regulates the transient association of Mediator with core promoters. Nat Struct Mol Biol 21:449–455. http://dx.doi.org/10.1038/nsmb.2810.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1128/MCB.00991-14.
   PubMed Web of Science ®Google Scholar
• Park D, Lee Y, Bhupindersingh G, Iyer VR. 2013. Widespread misinterpretable ChIP-seq bias in yeast. PLoS One 8:e83506. http://dx.doi.org/10.1371/journal.pone.0083506.
   PubMed Web of Science ®Google Scholar
• 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 U S A 110:18602–18607. http://dx.doi.org/10.1073/pnas.1316064110.
   PubMed Web of Science ®Google Scholar
• Tsai KL, Sato S, Tomomori-Sato C, Conaway RC, Conaway JW, Asturias FJ. 2013. A conserved Mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction. Nat Struct Mol Biol 20:611–619. http://dx.doi.org/10.1038/nsmb.2549.
   PubMed Web of Science ®Google Scholar
• Moustafa Y. 2015. Mediator is an intrinsically dynamic multisubunit complex that regulates heat shock gene transcription. Louisiana State University Health Sciences Center, Shreveport, LA.
   Google Scholar
• Bhaumik SR, Raha T, Aiello DP, Green MR. 2004. In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer. Genes Dev 18:333–343. http://dx.doi.org/10.1101/gad.1148404.
   PubMed Web of Science ®Google Scholar
• Bhoite LT, Yu Y, Stillman DJ. 2001. The Swi5 activator recruits the Mediator complex to the HO promoter without RNA polymerase II. Genes Dev 15:2457–2469. http://dx.doi.org/10.1101/gad.921601.
   PubMed Web of Science ®Google Scholar
• Leroy C, Cormier L, Kuras L. 2006. Independent recruitment of Mediator and SAGA by the activator Met4. Mol Cell Biol 26:3149–3163. http://dx.doi.org/10.1128/MCB.26.8.3149-3163.2006.
   PubMedGoogle Scholar
• Koschubs T, Lorenzen K, Baumli S, Sandstrom S, Heck AJ, Cramer P. 2010. Preparation and topology of the Mediator middle module. Nucleic Acids Res 38:3186–3195. http://dx.doi.org/10.1093/nar/gkq029.
   PubMed Web of Science ®Google Scholar
• Chong YT, Koh JL, Friesen H, Duffy K, Cox MJ, Moses A, Moffat J, Boone C, Andrews BJ. 2015. Yeast proteome dynamics from single cell imaging and automated analysis. Cell 161:1413–1424. http://dx.doi.org/10.1016/j.cell.2015.04.051.
   PubMed Web of Science ®Google Scholar
• Liu Y, Ranish JA, Aebersold R, Hahn S. 2001. Yeast nuclear extract contains two major forms of RNA polymerase II Mediator complexes. J Biol Chem 276:7169–7175.
   PubMed Web of Science ®Google Scholar
• Lariviere L, Geiger S, Hoeppner S, Rother S, Strasser K, Cramer P. 2006. Structure and TBP binding of the Mediator head subcomplex Med8-Med18-Med20. Nat Struct Mol Biol 13:895–901. http://dx.doi.org/10.1038/nsmb1143.
   PubMed Web of Science ®Google Scholar
• Koschubs T, Seizl M, Lariviere L, Kurth F, Baumli S, Martin DE, Cramer P. 2009. Identification, structure, and functional requirement of the Mediator submodule Med7N/31. EMBO J 28:69–80. http://dx.doi.org/10.1038/emboj.2008.254.
   PubMed Web of Science ®Google Scholar