Mediator structure and rearrangements required for holoenzyme formation

Nature

Volumn 544, Issue 7649, 2017, Pages 196-201

  Tsai, Kuang Lei ^a   Yu, Xiaodi ^a   Gopalan, Sneha ^b   Chao, Ti Chun ^c   Zhang, Ying ^b   Florens, Laurence ^b   Washburn, Michael P ^b,d   Murakami, Kenji ^e,f   Conaway, Ronald C ^b,d   Conaway, Joan W ^b,d   Asturias, Francisco J ^a,g  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOLOENZYME; MEDIATOR COMPLEX; RNA POLYMERASE II; MED14 PROTEIN, S POMBE; PROTEIN BINDING; PROTEIN SUBUNIT; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ELECTRON MICROSCOPY; ENZYME; ENZYME ACTIVITY; EUKARYOTE; YEAST;

ARTICLE; BINDING SITE; ELECTRON MICROSCOPY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION INITIATION; CHEMISTRY; CRYOELECTRON MICROSCOPY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN SUBUNIT; SCHIZOSACCHAROMYCES; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE;

BINDING SITES; CRYOELECTRON MICROSCOPY; HOLOENZYMES; MEDIATOR COMPLEX; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RNA POLYMERASE II; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85027930061     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature21393     Document Type: Article

References (60)

1. Kornberg, R. D. Mediator and the mechanism of transcriptional activation. Trends Biochem. Sci. 30, 235-239 (2005).
2. Malik, S. & Roeder, R. G. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat. Rev. Genet. 11, 761-772 (2010).
3. Cai, G., Imasaki, T., Takagi, Y. & Asturias, F. J. Mediator structural conservation and implications for the regulation mechanism. Structure 17, 559-567 (2009).
4. Taatjes, D. J., Schneider-Poetsch, T. & Tjian, R. Distinct conformational states of nuclear receptor-bound CRSP-Med complexes. Nat. Struct. Mol. Biol. 11, 664-671 (2004).
5. 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, 985-987 (1999).
6. Meyer, K. D., Lin, S. C., Bernecky, C., Gao, Y. & Taatjes, D. J. p53 activates transcription by directing structural shifts in Mediator. Nat. Struct. Mol. Biol. 17, 753-760 (2010).
7. Näär, A. M., Taatjes, D. J., Zhai, W., Nogales, E. & Tjian, R. Human CRSP interacts with RNA polymerase II CTD and adopts a specific CTD-bound conformation. Genes Dev. 16, 1339-1344 (2002).
8. Tsai, K. L. et al. Subunit architecture and functional modular rearrangements of the transcriptional mediator complex. Cell 157, 1430-1444 (2014).
9. Tsai, K. L. et al. A conserved Mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction. Nat. Struct. Mol. Biol. 20, 611-619 (2013).
10. Wang, X. et al. Redefining the modular organization of the core Mediator complex. Cell Res. 24, 796-808 (2014).
11. Koschubs, T. et al. Identification, structure, and functional requirement of the Mediator submodule Med7N/31. EMBO J. 28, 69-80 (2009).
12. Imasaki, T. et al. Architecture of the Mediator head module. Nature 475, 240-243 (2011).
13. 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, 17931-17935 (2012).
14. Larivière, L. et al. Structure of the Mediator head module. Nature 492, 448-451 (2012).
15. 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, 18171-18178 (2005).
16. Plaschka, C. et al. Architecture of the RNA polymerase II-Mediator core initiation complex. Nature 518, 376-380 (2015).
17. He, Y. et al. Near-atomic resolution visualization of human transcription promoter opening. Nature 533, 359-365 (2016).
18. Cevher, M. A. et al. Reconstitution of active human core Mediator complex reveals a critical role of the MED14 subunit. Nat. Struct. Mol. Biol. 21, 1028-1034 (2014).
19. Robinson, P. J. et al. Molecular architecture of the yeast Mediator complex. eLife 4, e08719 (2015).
20. Boube, M., Joulia, L., Cribbs, D. L. & Bourbon, H. M. Evidence for a mediator of RNA polymerase II transcriptional regulation conserved from yeast to man. Cell 110, 143-151 (2002).
21. Larivière, L. et al. Model of the Mediator middle module based on protein cross-linking. Nucleic Acids Res. 41, 9266-9273 (2013).
22. Robinson, P. J. et al. Structure of a complete Mediator-RNA polymerase II pre-initiation complex. Cell 166, 1411-1422 (2016).
23. Takahashi, H., Kasahara, K. & Kokubo, T. Saccharomyces cerevisiae Med9 comprises two functionally distinct domains that play different roles in transcriptional regulation. Genes Cells 14, 53-67 (2009).
24. Fan, H. Y., Cheng, K. K. & Klein, H. L. Mutations in the RNA polymerase II transcription machinery suppress the hyperrecombination mutant hpr1 delta of Saccharomyces cerevisiae. Genetics 142, 749-759 (1996).
25. Gibbons, B. J. et al. Subunit architecture of general transcription factor TFIIH. Proc. Natl Acad. Sci. USA 109, 1949-1954 (2012).
26. Murakami, K. et al. Structure of an RNA polymerase II preinitiation complex. Proc. Natl Acad. Sci. USA 112, 13543-13548 (2015).
27. Murakami, K. et al. Architecture of an RNA polymerase II transcription pre-initiation complex. Science 342, 1238724 (2013).
28. Baidoobonso, S. M., Guidi, B. W. & Myers, L. C. Med19(Rox3) regulates Intermodule interactions in the Saccharomyces cerevisiae mediator complex. J. Biol. Chem. 282, 5551-5559 (2007).
29. Louder, R. K. et al. Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature 531, 604-609 (2016).
30. Plaschka, C. et al. Transcription initiation complex structures elucidate DNA opening. Nature 533, 353-358 (2016).
31. Myers, L. C. et al. The Med proteins of yeast and their function through the RNA polymerase II carboxy-terminal domain. Genes Dev. 12, 45-54 (1998).
32. Ranish, J. A., Yudkovsky, N. & Hahn, S. Intermediates in formation and activity of the RNA polymerase II preinitiation complex: holoenzyme recruitment and a postrecruitment role for the TATA box and TFIIB. Genes Dev. 13, 49-63 (1999).
33. Svejstrup, J. Q. et al. Evidence for a mediator cycle at the initiation of transcription. Proc. Natl Acad. Sci. USA 94, 6075-6078 (1997).
34. Esnault, C. et al. Mediator-dependent recruitment of TFIIH modules in preinitiation complex. Mol. Cell 31, 337-346 (2008).
35. Bähler, J. et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951 (1998).
36. Elmlund, H. et al. The cyclin-dependent kinase 8 module sterically blocks Mediator interactions with RNA polymerase II. Proc. Natl Acad. Sci. USA 103, 15788-15793 (2006).
37. Washburn, M. P., Wolters, D. & Yates, J. R. III. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247 (2001).
38. Florens, L. & Washburn, M. P. Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328, 159-175 (2006).
39. Eng, J. K., McCormack, A. L. & Yates, J. R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989 (1994).
40. Tabb, D. L., McDonald, W. H. & Yates, J. R., III. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26 (2002).
41. Florens, L. et al. Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods 40, 303-311 (2006).
42. Paoletti, A. C. et al. Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors. Proc. Natl Acad. Sci. USA 103, 18928-18933 (2006).
43. Zybailov, B. et al. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5, 2339-2347 (2006).
44. Zhang, Y., Wen, Z., Washburn, M. P. & Florens, L. Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal. Chem. 82, 2272-2281 (2010).
45. Takagi, Y., Chadick, J. Z., Davis, J. A. & Asturias, F. J. Preponderance of free mediator in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 280, 31200-31207 (2005).
46. Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41-60 (2005).
47. Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95-102 (2009).
48. Hohn, M. et al. SPARX, a new environment for Cryo-EM image processing. J. Struct. Biol. 157, 47-55 (2007).
49. Dubochet, J. et al. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129-228 (1988).
50. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10, 584-590 (2013).
51. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
52. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
53. Henderson, R. et al. Outcome of the first electron microscopy validation task force meeting. Structure 20, 205-214 (2012).
54. Koschubs, T. et al. Preparation and topology of the Mediator middle module. Nucleic Acids Res. 38, 3186-3195 (2010).
55. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
56. Sp?hr, H., Calero, G., Bushnell, D. A. & Kornberg, R. D. Schizosacharomyces pombe RNA polymerase II at 3.6-? resolution. Proc. Natl Acad. Sci. USA 106, 9185-9190 (2009).
57. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
58. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
59. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).
60. Kitazono, A. A., Tobe, B. T., Kalton, H., Diamant, N. & Kron, S. J. Marker-fusion PCR for one-step mutagenesis of essential genes in yeast. Yeast 19, 141-149 (2002).