Structural basis for recognition and remodeling of the TBP:DNA:NC2 complex by Mot1

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages 1-22

  Butryn, Agata ^a   Schuller, Jan M ^b   Stoehr, Gabriele ^a   Runge Wollmann, Petra ^a   Förster, Friedrich ^b   Auble, David T ^c   Hopfner, Karl Peter ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; MODIFIER OF TRANSCRIPTION 1; PEPTIDES AND PROTEINS; SELENOMETHIONINE; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR NC2; UNCLASSIFIED DRUG; DOWN-REGULATOR OF TRANSCRIPTION 1; FUNGAL DNA; PHOSPHOPROTEIN; TATA BINDING PROTEIN ASSOCIATED FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; COMPLEX FORMATION; CROSS LINKING; CRYSTALLIZATION; DNA CONFORMATION; DNA PROTEIN COMPLEX; ELECTRON MICROSCOPY; ENCEPHALITOZOON CUNICULI; GEL MOBILITY SHIFT ASSAY; GEOMETRY; MASS SPECTROMETRY; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DNA, FUNGAL; ENCEPHALITOZOON CUNICULI; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; PHOSPHOPROTEINS; PROTEIN CONFORMATION; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TATA-BOX BINDING PROTEIN; TRANSCRIPTION FACTORS;

EID: 84941356543     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07432     Document Type: Article

References (94)

1. Adamkewicz JI, Mueller CG, Hansen KE, Prud’homme WA, Thorner J. 2000. Purification and enzymic properties of Mot1 ATPase, a regulator of basal transcription in the yeast Saccharomyces cerevisiae. The Journal of Biological Chemistry 275:21158–21168. doi: 10.1074/jbc.M002639200.
2. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica. Section D, Biological Crystallography 66:213–221. doi: 10.1107/S0907444909052925.
3. Afonine PV, Moriarty NW, Mustyakimow M, Sobolec OV, Terwilliger TC, Turk D, Urzhumtsev A, Adams PD. 2015. FEM:feature-enhanced map. Acta Crystallographica. Section D, Biological Crystallography 71:646–666. doi: 10.1107/S1399004714028132.
4. Alcolea MP, Casado P, Rodriguez-Prados JC, Vanhaesebroeck B, Cutillas PR. 2012. Phosphoproteomic analysis of leukemia cells under basal and drug-treated conditions identifies markers of kinase pathway activation and mechanisms of resistance. Molecular & Cellular Proteomics 11:453–466. doi: 10.1074/mcp.M112.017483.
5. Andrau JC, Van Oevelen CJ, Van Teeffelen HA, Weil PA, Holstege FC, Timmers HT. 2002. Mot1p is essential for TBP recruitment to selected promoters during in vivo gene activation. The EMBO Journal 21:5173–5183. doi: 10.1093/emboj/cdf485.
6. Auble DT. 2009. The dynamic personality of TATA-binding protein. Trends in Biochemical Sciences 34:49–52. doi: 10.1016/j.tibs.2008.10.008.
7. Auble DT, Hahn S. 1993. An ATP-dependent inhibitor of TBP binding to DNA. Genes & Development 7:844–856. doi: 10.1101/gad.7.5.844.
8. Auble DT, Hansen KE, Mueller CG, Lane WS, Thorner J, Hahn S. 1994. Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. Genes & Development 8:1920–1934. doi: 10.1101/gad.8.16.1920.
9. Auble DT, Steggerda SM. 1999. Testing for DNA tracking by MOT1, a SWI2/SNF2 protein family member. Molecular and Cellular Biology 19:412–423.
10. Auble DT, Wang D, Post KW, Hahn S. 1997. Molecular analysis of the SWI2/SNF2 protein family member MOT1, an ATP-driven enzyme that dissociates TATA-binding protein from DNA. Molecular and Cellular Biology 17:4842–4851.
11. Bricogne G, Blanc E, Brandl M, Flensbueg C, Keller P, Paciorek W, Roversi P, Sharff A, Smart OS, Vonrhein C, Womack TO. 2011. BUSTER version 2.10.1. Cambridge: United Kingdom Glob Phasing Ltd.
12. Cang Y, Auble DT, Prelich G. 1999. A new regulatory domain on the TATA-binding protein. The EMBO Journal 18:6662–6671. doi: 10.1093/emboj/18.23.6662.
13. Chacón P, Wriggers W. 2002. Multi-resolution contour-based fitting of macromolecular structures. Journal of Molecular Biology 317:375–384. doi: 10.1006/jmbi.2001.5438.
14. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annual Review of Biochemistry 78:273–304. doi: 10.1146/annurev.biochem.77.062706.153223.
15. Clapier CR, Nightingale KP, Becker PB. 2002. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Research 30:649–655. doi: 10.1093/nar/30.3.649.
16. Cowtan K. 2010. Recent developments in classical density modification. Acta Crystallographica. Section D, Biological Crystallography 66:470–478. doi: 10.1107/S090744490903947X.
17. Dang W, Bartholomew B. 2007. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Molecular and Cellular Biology 27:8306–8317. doi: 10.1128/MCB.01351-07.
18. Darst RP, Dasgupta A, Zhu C, Hsu JY, Vroom A, Muldrow T, Auble DT. 2003. Mot1 regulates the DNA binding activity of free TATA-binding protein in an ATP-dependent manner. The Journal of Biological Chemistry 278:13216–13226. doi: 10.1074/jbc.M211445200.
19. Darst RP, Wang D, Auble DT. 2001. MOT1-catalyzed TBP-DNA disruption: uncoupling DNA conformational change and role of upstream DNA. The EMBO Journal 20:2028–2040. doi: 10.1093/emboj/20.8.2028.
20. Dasgupta A, Darst RP, Martin KJ, Afshari CA, Auble DT. 2002. Mot1 activates and represses transcription by direct, ATPase-dependent mechanisms. Proceedings of the National Academy of Sciences of USA 99:2666–2671. doi: 10.1073/pnas.052397899.
21. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB III, Snoeyink J, Richardson JS, Richardson DC. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Research 35:W375–W383. doi: 10.1093/nar/gkm216.
22. Dechassa ML, Hota SK, Sen P, Chatterjee N, Prasad P, Bartholomew B. 2012. Disparity in the DNA translocase domains of SWI/SNF and ISW2. Nucleic Acids Research 40:4412–4421. doi: 10.1093/nar/gks007.
23. Dephoure N, Zhou C, Villé n J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP. 2008. A quantitative atlas of mitotic phosphorylation. Proceedings of the National Academy of Sciences of USA 105:10762–10767. doi: 10.1073/pnas.0805139105.
24. Dü rr H, Körner C, Mü ller M, Hickmann V, Hopfner KP. 2005. X-Ray structures of the Sulfolobus solfataricus SWI2/ SNF2 ATPase core and its complex with DNA. Cell 121:363–373. doi: 10.1016/j.cell.2005.03.026.
25. Dutta A, Gogol M, Kim JH, Smolle M, Venkatesh S, Gilmore J, Florens L, Washburn MP, Workman JL. 2014. Swi/ Snf dynamics on stress-responsive genes is governed by competitive bromodomain interactions. Genes & Development 28:2314–2330. doi: 10.1101/gad.243584.114.
26. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica. Section D, Biological Crystallography 66:486–501. doi: 10.1107/S0907444910007493.
27. Ferreira H, Flaus A, Owen-Hughes T. 2007. Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. Journal of Molecular Biology 374:563–579. doi: 10.1016/j.jmb.2007.09.059.
28. Flaus A, Martin DM, Barton GJ, Owen-Hughes T. 2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Research 34:2887–2905. doi: 10.1093/nar/gkl295.
29. Gangaraju VK, Bartholomew B. 2007. Mechanisms of ATP dependent chromatin remodeling. Mutation Research 618:3–17. doi: 10.1016/j.mrfmmm.2006.08.015.
30. Geisberg JV, Moqtaderi Z, Kuras L, Struhl K. 2002. Mot1 associates with transcriptionally active promoters and inhibits association of NC2 in Saccharomyces cerevisiae. Molecular and Cellular Biology 22:8122–8134. doi: 10.1128/MCB.22.23.8122-8134.2002.
31. de Graaf P, Mousson F, Geverts B, Scheer E, Tora L, Houtsmuller AB, Timmers HT. 2010. Chromatin interaction of TATA-binding protein is dynamically regulated in human cells. Journal of Cell Science 123:2663–2671. doi: 10.1242/jcs.064097.
32. Grü nwald M, Lazzaretti D, Bono F. 2013. Structural basis for the nuclear export activity of Importin13. The EMBO Journal 32:899–913. doi: 10.1038/emboj.2013.29.
33. Gumbs OH, Campbell AM, Weil PA. 2003. High-affinity DNA binding by a Mot1p-TBP complex: implications for TAF-independent transcription. The EMBO Journal 22:3131–3141. doi: 10.1093/emboj/cdg304.
34. Guo A, Gu H, Zhou J, Mulhern D, Wang Y, Lee KA, Yang V, Aguiar M, Kornhauser J, Jia X, Ren J, Beausoleil SA, Silva JC, Vemulapalli V, Bedford MT, Comb MJ. 2014. Immunoaffinity enrichment and mass spectrometry analysis of protein methylation. Molecular & Cellular Proteomics 13:372–387. doi: 10.1074/mcp.O113.027870.
35. Hauk G, Bowman GD. 2011. Structural insights into regulation and action of SWI2/SNF2 ATPases. Current Opinion in Structural Biology 21:719–727. doi: 10.1016/j.sbi.2011.09.003.
36. Hauk G, McKnight JN, Nodelman IM, Bowman GD. 2010. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Molecular Cell 39:711–723. doi: 10.1016/j.molcel.2010.08.012.
37. Hota SK, Bhardwaj SK, Deindl S, Lin YC, Zhuang X, Bartholomew B. 2013. Nucleosome mobilization by ISW2 requires the concerted action of the ATPase and SLIDE domains. Nature Structural & Molecular Biology 20:222–229. doi: 10.1038/nsmb.2486.
38. Hsu JY, Juven-Gershon T, Marr MT II, Wright KJ, Tjian R, Kadonaga JT. 2008. TBP, Mot1, and NC2 establish a regulatory circuit that controls DPE-dependent versus TATA-dependent transcription. Genes & Development 22:2353–2358. doi: 10.1101/gad.1681808.
39. Huber EM, Scharf DH, Hortschansky P, Groll M, Brakhage AA. 2012. DNA minor groove sensing and widening by the CCAAT-binding complex. Structure 20:1757–1768. doi: 10.1016/j.str.2012.07.012.
40. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, Villé n J, Haas W, Sowa ME, Gygi SP. 2010. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143:1174–1189. doi: 10.1016/j.cell.2010.12.001.
41. Inostroza JA, Mermelstein FH, Ha I, Lane WS, Reinberg D. 1992. Dr1, a TATA-binding phosphoprotein and inhibitor of class II gene transcription. Cell 70:477–489. doi: 10.1016/0092-8674(92)90172-9.
42. Kabsch W. 2010. XDS. Acta Crystallographica. Section D, Biological Crystallography 66:125–132. doi: 10.1107/S0907444909047337.
43. Kamada K, Shu F, Chen H, Malik S, Stelzer G, Roeder RG, Meisterernst M, Burley SK. 2001. Crystal structure of negative cofactor 2 recognizing the TBP-DNA transcription complex. Cell 106:71–81. doi: 10.1016/S0092-8674(01)00417-2.
44. Kessner D, Chambers M, Burke R, Agus D, Mallick P. 2008. ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 24:2534–2536. doi: 10.1093/bioinformatics/btn323.
45. Kim JL, Nikolov DB, Burley SK. 1993. Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature 365:520–527. doi: 10.1038/365520a0.
46. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, Sowa ME, Rad R, Rush J, Comb MJ, Harper JW, Gygi SP. 2011. Systematic and quantitative assessment of the ubiquitin-modified proteome. Molecular Cell 44:325–340. doi: 10.1016/j.molcel.2011.08.025.
47. Kim Y, Ebright YW, Goodman AR, Reinberg D, Ebright RH. 2008. Nonradioactive, ultrasensitive site-specific protein-protein photocrosslinking: interactions of alpha-helix 2 of TATA-binding protein with general transcription factor TFIIA and transcriptionalrepressor NC2. Nucleic Acids Research 36:6143–6154. doi: 10.1093/nar/gkn612.
48. Klejman MP, Pereira LA, van Zeeburg HJ, Gilfillan S, Meisterernst M, Timmers HT. 2004. NC2alpha interacts with BTAF1 and stimulates its ATP-dependent association with TATA-binding protein. Molecular and Cellular Biology 24:10072–10082. doi: 10.1128/MCB.24.22.10072-10082.2004.
49. Klejman MP, Zhao X, van Schaik FM, Herr W, Timmers HT. 2005. Mutational analysis of BTAF1-TBP interaction: BTAF1 can rescue DNA-binding defective TBP mutants. Nucleic Acids Research 33:5426–5436. doi: 10.1093/nar/gki850.
50. Koster MJ, Timmers HT. 2015. Regulation of anti-sense transcription by Mot1p and NC2 via removal of TATAbinding protein (TBP) from the 3′-end of genes. Nucleic Acids Research 43:143–152. doi: 10.1093/nar/gku1263.
51. Koster MJ, Yildirim AD, Weil PA, Holstege FC, Timmers HT. 2014. Suppression of intragenic transcription requires the MOT1 and NC2 regulators of TATA-binding protein. Nucleic Acids Research 42:4220–4229. doi: 10.1093/nar/gkt1398.
52. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. Journal of Molecular Biology 372:774–797. doi: 10.1016/j.jmb.2007.05.022.
53. Lewis R, Dü rr H, Hopfner KP, Michaelis J. 2008. Conformational changes of a Swi2/Snf2 ATPase during its mechano-chemical cycle. Nucleic Acids Research 36:1881–1890. doi: 10.1093/nar/gkn040.
54. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260. doi: 10.1038/38444.
55. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallography 40:658–674. doi: 10.1107/S0021889807021206.
56. Meisterernst M, Roeder RG. 1991. Family of proteins that interact with TFIID and regulate promoter activity. Cell 67:557–567. doi: 10.1016/0092-8674(91)90530-C.
57. Moyle-Heyrman G, Viswanathan R, Widom J, Auble DT. 2012. Two-step mechanism for modifier of transcription 1 (Mot1) enzyme-catalyzed displacement of TATA-binding protein (TBP) from DNA. The Journal of Biological Chemistry 287:9002–9012. doi: 10.1074/jbc.M111.333484.
58. Nardini M, Gnesutta N, Donati G, Gatta R, Forni C, Fossati A, Vonrhein C, Moras D, Romier C, Bolognesi M, Mantovani R. 2013. Sequence-specific transcription factor NF-Y displays histone-like DNA binding and H2B-like ubiquitination. Cell 152:132–143. doi: 10.1016/j.cell.2012.11.047.
59. Nguyen VQ, Ranjan A, Stengel F, Wei D, Aebersold R, Wu C, Leschziner AE. 2013. Molecular architecture of the ATP-dependent chromatin-remodeling complex SWR1. Cell 54:1220–1231. doi: 10.1016/j.cell.2013.08.018.
60. Nickell S, Förster F, Linaroudis A, Net DW, Beck F, Hegerl R, Baumeister W, Plitzko JM. 2005. TOM software toolbox: acquisition and analysis for electron tomography. Journal of Structural Biology 149:227–234. doi: 10.1016/j.jsb.2004.10.006.
61. Pereira LA, Klejman MP, Ruhlmann C, Kavelaars F, Oulad-Abdelghani M, Timmers HT, Schultz P. 2004. Molecular architecture of the basal transcription factor B-TFIID. The Journal of Biological Chemistry 279:21802–21807. doi: 10.1074/jbc.M313519200.
62. Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HD, Konarev PV, Svergun DI. 2012. New developments in the ATSAS program package for small-angle scattering data analysis. Journal of Applied Crystallography 45:342–350. doi: 10.1107/S0021889812007662.
63. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera–a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25:1605–1612. doi: 10.1002/jcc.20084.
64. Politis A, Stengel F, Hall Z, Herná ndez H, Leitner A, Walzthoeni T, Robinson CV, Aebersold R. 2014. A mass spectrometry-based hybrid method for structural modeling of protein complexes. Nature Methods 11:403–406. doi: 10.1038/nmeth.2841.
65. Ponomarev MA, Timofeev VP, Levitsky DI. 1995. The difference between ADP-beryllium fluoride and ADP-aluminium fluoride complexes of the spin-labeled myosin subfragment 1. FEBS Letters 371:261–263. doi: 10.1016/0014-5793(95)00898-J.
66. Saha A, Wittmeyer J, Cairns BR. 2002. Chromatin remodeling by RSC involves ATP-dependent DNA translocation. Genes & Development 16:2120–2134. doi: 10.1101/gad.995002.
67. Scheres SH, Núñez-Ramírez R, Sorzano CO, Carazo JM, Marabini R. 2008. Image processing for electron microscopy single-particle analysis using XMIPP. Nature Protocols 3:977–990. doi: 10.1038/nprot.2008.62.
68. Schluesche P, Stelzer G, Piaia E, Lamb DC, Meisterernst M. 2007. NC2 mobilizes TBP on core promoter TATA boxes. Nature Structural & Molecular Biology 14:1196–1201. doi: 10.1038/nsmb1328.
69. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S. 2006. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125:287–300. doi: 10.1016/j.cell.2006.01.054.
70. Sharma A, Jenkins KR, Hé roux A, Bowman GD. 2011. Crystal structure of the chromodomain helicase DNA-binding protein 1 (Chd1) DNA-binding domain in complex with DNA. The Journal of Biological Chemistry 286:42099–42104. doi: 10.1074/jbc.C111.294462.
71. Sharma K, D’Souza RC, Tyanova S, Schaab C, Wísniewski JR, Cox J, Mann M. 2014. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Reports 8:1583–1594. doi: 10.1016/j.celrep.2014.07.036.
72. Shaw G, Gan J, Zhou YN, Zhi H, Subburaman P, Zhang R, Joachimiak A, Jin DJ, Ji X. 2008. Structure of RapA, a Swi2/Snf2 protein that recycles RNA polymerase during transcription. Structure 16:1417–1427. doi: 10.1016/j.str.2008.06.012.
73. Spedale G, Meddens CA, Koster MJ, Ko CW, van Hooff SR, Holstege FC, Timmers HT, Pijnappel WW. 2012. Tight cooperation between Mot1p and NC2β in regulating genome-wide transcription, repression of transcription following heat shock induction and genetic interaction with SAGA. Nucleic Acids Research 40: 996–1008. doi: 10.1093/nar/gkr784.
74. Sprouse RO, Brenowitz M, Auble DT. 2006. Swi2/Snf2-related ATPase Mot1 drives displacement of TATA-binding protein by gripping DNA. The EMBO Journal 25:1492–1504. doi: 10.1038/sj.emboj.7601050.
75. Stein N. 2008. CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. Journal of Applied Crystallography 41:641–643. doi: 10.1107/S0021889808006985.
76. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for electron microscopy. Journal of Structural Biology 157:38–46. doi: 10.1016/j.jsb.2006.05.009.
77. Thomä NH, Czyzewski BK, Alexeev AA, Mazin AV, Kowalczykowski SC, Pavletich NP. 2005. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nature Structural & Molecular Biology 12:350–356. doi: 10.1038/nsmb919.
78. Tora L, Timmers HT. 2010. The TATA box regulates TATA-binding protein (TBP) dynamics in vivo. Trends in Biochemical Sciences 35:309–314. doi: 10.1016/j.tibs.2010.01.007.
79. Tosi A, Haas C, Herzog F, Gilmozzi A, Berninghausen O, Ungewickell C, Gerhold CB, Lakomek K, Aebersold R, Beckmann R, Hopfner KP. 2013. Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell 154:1207–1219. doi: 10.1016/j.cell.2013.08.016.
80. Van Hoof D, Muñoz J, Braam SR, Pinkse MW, Linding R, Heck AJ, Mummery CL, Krijgsveld J. 2009. Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5:214–226. doi: 10.1016/j.stem.2009.05.021.
81. Van Werven FJ, van Bakel H, van Teeffelen HA, Altelaar AF, Koerkamp MG, Heck AJ, Holstege FC, Timmers HT. 2008. Cooperative action of NC2 and Mot1p to regulate TATA-binding protein function across the genome. Genes & Development 22:2359–2369. doi: 10.1101/gad.1682308.
82. Wagner SA, Beli P, Weinert BT, Schölz C, Kelstrup CD, Young C, Nielsen ML, Olsen JV, Brakebusch C, Choudhary C. 2012. Proteomic analyses reveal divergent ubiquitylation site patterns in murinetissues. Molecular & Cellular Proteomics 12:1578–1585. doi: 10.1074/mcp.M112.017905.
83. Walzthoeni T, Claassen M, Leitner A, Herzog F, Bohn S, Förster F, Beck M, Aebersold R. 2012. False discovery rate estimation for cross-linked peptides identified by mass spectrometry. Nature Methods 9:901–903. doi: 10.1038/nmeth.2103.
84. Wang Z, Gucek M, Hart GW. 2008. Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proceedings of the National Academy of Sciences of USA 105:13793–13798. doi: 10.1073/pnas.0806216105.
85. Whitehouse I, Stockdale C, Flaus A, Szczelkun MD, Owen-Hughes T. 2003. Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Molecular and Cellular Biology 23:1935–1945. doi: 10.1128/MCB.23.6.1935-1945.2003.
86. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallographica. Section D, Biological Crystallography 67:235–242. doi: 10.1107/S0907444910045749.
87. Wollmann P, Cui S, Viswanathan R, Berninghausen O, Wells MN, Moldt M, Witte G, Butryn A, Wendler P, Beckmann R, Auble DT, Hopfner KP. 2011. Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP. Nature 475:403–407. doi: 10.1038/nature10215.
88. Wriggers W. 2010. Using Situs for the integration of multi-resolution structures. Biophysical Reviews 2:21–27. doi: 10.1007/s12551-009-0026-3.
89. Yamada K, Frouws TD, Angst B, Fitzgerald DJ, DeLuca C, Schimmele K, Sargent DF, Richmond TJ. 2011. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472:448–453. doi: 10.1038/nature09947.
90. Yeung K, Kim S, Reinberg D. 1997. Functional dissection of a human Dr1-DRAP1 repressor complex. Molecular and Cellular Biology 17:36–45.
91. Yeung KC, Inostroza JA, Mermelstein FH, Kannabiran C, Reinberg D. 1994. Structure-function analysis of the TBP-binding protein Dr1 reveals a mechanism for repression of class II gene transcription. Genes & Development 8:2097–2109. doi: 10.1101/gad.8.17.2097.
92. Zentner GE, Henikoff S. 2013. Mot1 redistributes TBP from TATA-containing to TATA-less promoters. Molecular and Cellular Biology 33:4996–5004. doi: 10.1128/MCB.01218-13.
93. Zhou H, Di Palma S, Preisinger C, Peng M, Polat AN, Heck AJ, Mohammed S. 2013. Toward a comprehensive characterization of a human cancer cell phosphoproteome. Journal of Proteome Research 12:260–271. doi: 10.1021/pr300630k.
94. Zofall M, Persinger J, Kassabov SR, Bartholomew B. 2006. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nature Structural & Molecular Biology 13:339–346. doi: 10.1038/nsmb1071.