Structure of a Complete Mediator-RNA Polymerase II Pre-Initiation Complex

Cell

Volumn 166, Issue 6, 2016, Pages 1411-1422.e16

  Robinson, Philip J ^a   Trnka, Michael J ^b   Bushnell, David A ^a   Davis, Ralph E ^a   Mattei, Pierre Jean ^a   Burlingame, Alma L ^b   Kornberg, Roger D ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cross linking; cryo EM; mass spectrometry; Mediator complex; Pre initiation complex; RNA polymerase II carboxy terminal domain; TFIIH; TFIIK; Transcription

Indexed keywords

MEDIATOR COMPLEX; RNA POLYMERASE II; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CROSS LINKING; CRYOELECTRON MICROSCOPY; ENZYME STRUCTURE; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

CRYOELECTRON MICROSCOPY; GENE EXPRESSION REGULATION; MASS SPECTROMETRY; MEDIATOR COMPLEX; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84986277745     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.08.050     Document Type: Article

References (57)

1. Allison, L.A., Ingles, C.J., Mutations in RNA polymerase II enhance or suppress mutations in GAL4. Proc. Natl. Acad. Sci. USA 86 (1989), 2794–2798.
2. Asturias, F.J., Jiang, Y.W., Myers, L.C., Gustafsson, C.M., Kornberg, R.D., Conserved structures of mediator and RNA polymerase II holoenzyme. Science 283 (1999), 985–987.
3. Baumli, S., Hoeppner, S., Cramer, P., A conserved mediator hinge revealed in the structure of the MED7.MED21 (Med7.Srb7) heterodimer. J. Biol. Chem. 280 (2005), 18171–18178.
4. Béve, J., Hu, G.Z., Myers, L.C., Balciunas, D., Werngren, O., Hultenby, K., Wibom, R., Ronne, H., Gustafsson, C.M., The structural and functional role of Med5 in the yeast Mediator tail module. J. Biol. Chem. 280 (2005), 41366–41372.
5. Bich, C., Maedler, S., Chiesa, K., DeGiacomo, F., Bogliotti, N., Zenobi, R., Reactivity and applications of new amine reactive cross-linkers for mass spectrometric detection of protein-protein complexes. Anal. Chem. 82 (2010), 172–179.
6. Brenner, C., Fuller, R.S., Structural and enzymatic characterization of a purified prohormone-processing enzyme: secreted, soluble Kex2 protease. Proc. Natl. Acad. Sci. USA 89 (1992), 922–926.
7. Brzovic, P.S., Heikaus, C.C., Kisselev, L., Vernon, R., Herbig, E., Pacheco, D., Warfield, L., Littlefield, P., Baker, D., Klevit, R.E., Hahn, S., The acidic transcription activator Gcn4 binds the mediator subunit Gal11/Med15 using a simple protein interface forming a fuzzy complex. Mol. Cell 44 (2011), 942–953.
8. Bushnell, D.A., Bamdad, C., Kornberg, R.D., A minimal set of RNA polymerase II transcription protein interactions. J. Biol. Chem. 271 (1996), 20170–20174.
9. Cai, G., Chaban, Y.L., Imasaki, T., Kovacs, J.A., Calero, G., Penczek, P.A., Takagi, Y., Asturias, F.J., Interaction of the mediator head module with RNA polymerase II. Structure 20 (2012), 899–910.
10. Carlson, M., Genetics of transcriptional regulation in yeast: connections to the RNA polymerase II CTD. Annu. Rev. Cell Dev. Biol. 13 (1997), 1–23.
11. Chen, Z.A., Jawhari, A., Fischer, L., Buchen, C., Tahir, S., Kamenski, T., Rasmussen, M., Lariviere, L., Bukowski-Wills, J.C., Nilges, M., et al. Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J. 29 (2010), 717–726.
12. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
13. Feaver, W.J., Gileadi, O., Li, Y., Kornberg, R.D., CTD kinase associated with yeast RNA polymerase II initiation factor b. Cell 67 (1991), 1223–1230.
14. Feaver, W.J., Svejstrup, J.Q., Henry, N.L., Kornberg, R.D., Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell 79 (1994), 1103–1109.
15. Flanagan, P.M., Kelleher, R.J. 3rd, Sayre, M.H., Tschochner, H., Kornberg, R.D., A mediator required for activation of RNA polymerase II transcription in vitro. Nature 350 (1991), 436–438.
16. Gerber, H.P., Hagmann, M., Seipel, K., Georgiev, O., West, M.A., Litingtung, Y., Schaffner, W., Corden, J.L., RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature 374 (1995), 660–662.
17. Guglielmi, B., van Berkum, N.L., Klapholz, B., Bijma, T., Boube, M., Boschiero, C., Bourbon, H.M., Holstege, F.C., Werner, M., A high resolution protein interaction map of the yeast Mediator complex. Nucleic Acids Res. 32 (2004), 5379–5391.
18. Heymann, J.B., Cardone, G., Winkler, D.C., Steven, A.C., Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol. 161 (2008), 232–242.
19. Imasaki, T., Calero, G., Cai, G., Tsai, K.L., Yamada, K., Cardelli, F., Erdjument-Bromage, H., Tempst, P., Berger, I., Kornberg, G.L., et al. Architecture of the Mediator head module. Nature 475 (2011), 240–243.
20. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M., Sakaki, Y., A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98 (2001), 4569–4574.
21. Jedidi, I., Zhang, F., Qiu, H., Stahl, S.J., Palmer, I., Kaufman, J.D., Nadaud, P.S., Mukherjee, S., Wingfield, P.T., Jaroniec, C.P., Hinnebusch, A.G., Activator Gcn4 employs multiple segments of Med15/Gal11, including the KIX domain, to recruit mediator to target genes in vivo. J. Biol. Chem. 285 (2010), 2438–2455.
22. Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N., Sternberg, M.J., The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10 (2015), 845–858.
23. Kim, Y.J., Björklund, S., Li, Y., Sayre, M.H., Kornberg, R.D., A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell 77 (1994), 599–608.
24. Kornberg, R.D., Mediator and the mechanism of transcriptional activation. Trends Biochem. Sci. 30 (2005), 235–239.
25. Koschubs, T., Seizl, M., Larivière, L., Kurth, F., Baumli, S., Martin, D.E., Cramer, P., Identification, structure, and functional requirement of the Mediator submodule Med7N/31. EMBO J. 28 (2009), 69–80.
26. Kremer, J.R., Mastronarde, D.N., McIntosh, J.R., Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116 (1996), 71–76.
27. Larivière, L., Plaschka, C., Seizl, M., Wenzeck, L., Kurth, F., Cramer, P., Structure of the Mediator head module. Nature 492 (2012), 448–451.
28. Larivière, L., Plaschka, C., Seizl, M., Petrotchenko, E.V., Wenzeck, L., Borchers, C.H., Cramer, P., Model of the Mediator middle module based on protein cross-linking. Nucleic Acids Res. 41 (2013), 9266–9273.
29. Laybourn, P.J., Dahmus, M.E., Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before the initiation of transcription. J. Biol. Chem. 265 (1990), 13165–13173.
30. Liu, X., Bushnell, D.A., Wang, D., Calero, G., Kornberg, R.D., Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science 327 (2010), 206–209.
31. Luo, J., Cimermancic, P., Viswanath, S., Ebmeier, C.C., Kim, B., Dehecq, M., Raman, V., Greenberg, C.H., Pellarin, R., Sali, A., et al. Architecture of the Human and Yeast General Transcription and DNA Repair Factor TFIIH. Mol. Cell 59 (2015), 794–806.
32. Max, T., Søgaard, T.M., Svejstrup, J.Q., Hyperphosphorylation of the C-terminal repeat domain of RNA polymerase II facilitates dissociation of its complex with mediator. J. Biol. Chem. 282 (2007), 14113–14120.
33. Mühlbacher, W., Sainsbury, S., Hemann, M., Hantsche, M., Neyer, S., Herzog, F., Cramer, P., Conserved architecture of the core RNA polymerase II initiation complex. Nat. Commun., 5, 2014, 4310.
34. Murakami, K., Gibbons, B.J., Davis, R.E., Nagai, S., Liu, X., Robinson, P.J., Wu, T., Kaplan, C.D., Kornberg, R.D., Tfb6, a previously unidentified subunit of the general transcription factor TFIIH, facilitates dissociation of Ssl2 helicase after transcription initiation. Proc. Natl. Acad. Sci. USA 109 (2012), 4816–4821.
35. Murakami, K., Elmlund, H., Kalisman, N., Bushnell, D.A., Adams, C.M., Azubel, M., Elmlund, D., Levi-Kalisman, Y., Liu, X., Gibbons, B.J., et al. Architecture of an RNA polymerase II transcription pre-initiation complex. Science, 342, 2013, 1238724.
36. Murakami, K., Tsai, K.L., Kalisman, N., Bushnell, D.A., Asturias, F.J., Kornberg, R.D., Structure of an RNA polymerase II preinitiation complex. Proc. Natl. Acad. Sci. USA 112 (2015), 13543–13548.
37. Nonet, M., Sweetser, D., Young, R.A., Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell 50 (1987), 909–915.
38. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
39. Plaschka, C., Larivière, L., Wenzeck, L., Seizl, M., Hemann, M., Tegunov, D., Petrotchenko, E.V., Borchers, C.H., Baumeister, W., Herzog, F., et al. Architecture of the RNA polymerase II-Mediator core initiation complex. Nature 518 (2015), 376–380.
40. Robinson, P.J., Bushnell, D.A., Trnka, M.J., Burlingame, A.L., Kornberg, R.D., Structure of the mediator head module bound to the carboxy-terminal domain of RNA polymerase II. Proc. Natl. Acad. Sci. USA 109 (2012), 17931–17935.
41. Robinson, P.J., Trnka, M.J., Pellarin, R., Greenberg, C.H., Bushnell, D.A., Davis, R., Burlingame, A.L., Sali, A., Kornberg, R.D., Molecular architecture of the yeast Mediator complex. eLife, 4, 2015, 4.
42. Scafe, C., Chao, D., Lopes, J., Hirsch, J.P., Henry, S., Young, R.A., RNA polymerase II C-terminal repeat influences response to transcriptional enhancer signals. Nature 347 (1990), 491–494.
43. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180 (2012), 519–530.
44. Spåhr, H., Calero, G., Bushnell, D.A., Kornberg, R.D., Schizosacharomyces pombe RNA polymerase II at 3.6-A resolution. Proc. Natl. Acad. Sci. USA 106 (2009), 9185–9190.
45. Suh, H., Hazelbaker, D.Z., Soares, L.M., Buratowski, S., The C-terminal domain of Rpb1 functions on other RNA polymerase II subunits. Mol. Cell 51 (2013), 850–858.
46. Svejstrup, J.Q., Li, Y., Fellows, J., Gnatt, A., Bjorklund, S., Kornberg, R.D., Evidence for a mediator cycle at the initiation of transcription. Proc. Natl. Acad. Sci. USA 94 (1997), 6075–6078.
47. Takagi, Y., Kornberg, R.D., Mediator as a general transcription factor. J. Biol. Chem. 281 (2006), 80–89.
48. Tang, G., Peng, L., Baldwin, P.R., Mann, D.S., Jiang, W., Rees, I., Ludtke, S.J., EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157 (2007), 38–46.
49. Thompson, C.M., Young, R.A., General requirement for RNA polymerase II holoenzymes in vivo. Proc. Natl. Acad. Sci. USA 92 (1995), 4587–4590.
50. Trnka, M.J., Baker, P.R., Robinson, P.J., Burlingame, A.L., Chalkley, R.J., Matching cross-linked peptide spectra: only as good as the worse identification. Mol. Cell. Proteomics 13 (2014), 420–434.
51. Tsai, K.L., Tomomori-Sato, C., Sato, S., Conaway, R.C., Conaway, J.W., Asturias, F.J., Subunit architecture and functional modular rearrangements of the transcriptional mediator complex. Cell 157 (2014), 1430–1444.
52. Uetz, P., Giot, L., Cagney, G., Mansfield, T.A., Judson, R.S., Knight, J.R., Lockshon, D., Narayan, V., Srinivasan, M., Pochart, P., et al. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403 (2000), 623–627.
53. Wang, X., Sun, Q., Ding, Z., Ji, J., Wang, J., Kong, X., Yang, J., Cai, G., Redefining the modular organization of the core Mediator complex. Cell Res. 24 (2014), 796–808.
54. Winston, F., Dollard, C., Ricupero-Hovasse, S.L., Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11 (1995), 53–55.
55. Wong, K.H., Jin, Y., Struhl, K., TFIIH phosphorylation of the Pol II CTD stimulates mediator dissociation from the preinitiation complex and promoter escape. Mol. Cell 54 (2014), 601–612.
56. Zhang, F., Sumibcay, L., Hinnebusch, A.G., Swanson, M.J., 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 (2004), 6871–6886.
57. Zheng, S.Q., Keszthelyi, B., Branlund, E., Lyle, J.M., Braunfeld, M.B., Sedat, J.W., Agard, D.A., UCSF tomography: an integrated software suite for real-time electron microscopic tomographic data collection, alignment, and reconstruction. J. Struct. Biol. 157 (2007), 138–147.