XPhosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains

Cell

Volumn 155, Issue 5, 2013, Pages 1049-

  Kwon, Ilmin ^a   Kato, Masato ^a   Xiang, Siheng ^a   Wu, Leeju ^a   Theodoropoulos, Pano ^a   Mirzaei, Hamid ^a   Han, Tina ^a,c   Xie, Shanhai ^a,d   Corden, Jeffry L ^b   McKnight, Steven L ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Peloton Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FUSED IN SARCOMA PROTEIN; HYBRID PROTEIN; POLYMER; RNA BINDING PROTEIN; RNA POLYMERASE II;

ARTICLE; C TERMINAL DOMAIN; ENZYME PHOSPHORYLATION; FIBER; HUMAN; HYDROGEL; LOW COMPLEXITY DOMAIN; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; TRANSCRIPTION INITIATION;

EID: 84888440451     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.10.033     Document Type: Article

References (42)

1. M.S. Akhtar, M. Heidemann, J.R. Tietjen, D.W. Zhang, R.D. Chapman, D. Eick, and A.Z. Ansari TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II Mol. Cell 34 2009 387 393
2. M.K. Andersson, A. Ståhlberg, Y. Arvidsson, A. Olofsson, H. Semb, G. Stenman, O. Nilsson, and P. Aman The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type-specific expression patterns and involvement in cell spreading and stress response BMC Cell Biol. 9 2008 37
3. A. Arvand, and C.T. Denny Biology of EWS/ETS fusions in Ewing's family tumors Oncogene 20 2001 5747 5754
4. A. Bertolotti, B. Bell, and L. Tora The N-terminal domain of human TAFII68 displays transactivation and oncogenic properties Oncogene 18 1999 8000 8010
5. S. Buratowski Progression through the RNA polymerase II CTD cycle Mol. Cell 36 2009 541 546
6. R.D. Chapman, M. Heidemann, T.K. Albert, R. Mailhammer, A. Flatley, M. Meisterernst, E. Kremmer, and D. Eick Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7 Science 318 2007 1780 1782
7. J.L. Corden, D.L. Cadena, J.M. Ahearn Jr., and M.E. Dahmus A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II Proc. Natl. Acad. Sci. USA 82 1985 7934 7938
8. A. Crozat, P. Aman, N. Mandahl, and D. Ron Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma Nature 363 1993 640 644
9. A. Cumberworth, G. Lamour, M.M. Babu, and J. Gsponer Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes Biochem. J. 454 2013 361 369
10. N. Czudnochowski, C.A. Bösken, and M. Geyer Serine-7 but not serine-5 phosphorylation primes RNA polymerase II CTD for P-TEFb recognition Nat Commun 3 2012 842
11. S. Egloff, and S. Murphy Cracking the RNA polymerase II CTD code Trends Genet. 24 2008 280 288
12. S. Egloff, M. Dienstbier, and S. Murphy Updating the RNA polymerase CTD code: adding gene-specific layers Trends Genet. 28 2012 333 341
13. K. Gangwal, S. Sankar, P.C. Hollenhorst, M. Kinsey, S.C. Haroldsen, A.A. Shah, K.M. Boucher, W.S. Watkins, L.B. Jorde, B.J. Graves, and S.L. Lessnick Microsatellites as EWS/FLI response elements in Ewing's sarcoma Proc. Natl. Acad. Sci. USA 105 2008 10149 10154
14. O. Guipaud, F. Guillonneau, V. Labas, D. Praseuth, J. Rossier, B. Lopez, and P. Bertrand An in vitro enzymatic assay coupled to proteomics analysis reveals a new DNA processing activity for Ewing sarcoma and TAF(II)68 proteins Proteomics 6 2006 5962 5972
15. T.W. Han, M. Kato, S. Xie, L.C. Wu, H. Mirzaei, J. Pei, M. Chen, Y. Xie, J. Allen, G. Xiao, and S.L. McKnight Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies Cell 149 2012 768 779
16. M.A. Huntley, and G.B. Golding Simple sequences are rare in the Protein Data Bank Proteins 48 2002 134 140
17. H. Ichikawa, K. Shimizu, R. Katsu, and M. Ohki Dual transforming activities of the FUS (TLS)-ERG leukemia fusion protein conferred by two N-terminal domains of FUS (TLS) Mol. Cell. Biol. 19 1999 7639 7650
18. J.C. Jones, H.P. Phatnani, T.A. Haystead, J.A. MacDonald, S.M. Alam, and A.L. Greenleaf C-terminal repeat domain kinase I phosphorylates Ser2 and Ser5 of RNA polymerase II C-terminal domain repeats J. Biol. Chem. 279 2004 24957 24964
19. M. Kato, T.W. Han, S. Xie, K. Shi, X. Du, L.C. Wu, H. Mirzaei, E.J. Goldsmith, J. Longgood, and J. Pei Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels Cell 149 2012 753 767
20. T.K. Kim, M. Hemberg, J.M. Gray, A.M. Costa, D.M. Bear, J. Wu, D.A. Harmin, M. Laptewicz, K. Barbara-Haley, and S. Kuersten Widespread transcription at neuronal activity-regulated enhancers Nature 465 2010 182 187
21. M. Kim, H. Suh, E.J. Cho, and S. Buratowski Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7 J. Biol. Chem. 284 2009 26421 26426
22. M.T. Lam, H. Cho, H.P. Lesch, D. Gosselin, S. Heinz, Y. Tanaka-Oishi, C. Benner, M.U. Kaikkonen, A.S. Kim, and M. Kosaka Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription Nature 498 2013 511 515
23. C. Lemercier, A. Verdel, B. Galloo, S. Curtet, M.P. Brocard, and S. Khochbin mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity J. Biol. Chem. 275 2000 15594 15599
24. S.L. Lessnick, and M. Ladanyi Molecular pathogenesis of Ewing sarcoma: new therapeutic and transcriptional targets Annu. Rev. Pathol. 7 2012 145 159
25. W. Li, D. Notani, Q. Ma, B. Tanasa, E. Nunez, A.Y. Chen, D. Merkurjev, J. Zhang, K. Ohgi, and X. Song Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation Nature 498 2013 516 520
26. H.P. Phatnani, and A.L. Greenleaf Phosphorylation and functions of the RNA polymerase II CTD Genes Dev. 20 2006 2922 2936
27. T.H. Rabbitts, A. Forster, R. Larson, and P. Nathan Fusion of the dominant negative transcription regulator CHOP with a novel gene FUS by translocation t(12;16) in malignant liposarcoma Nat. Genet. 4 1993 175 180
28. Y. Ramanathan, S.M. Rajpara, S.M. Reza, E. Lees, S. Shuman, M.B. Mathews, and T. Pe'ery Three RNA polymerase II carboxyl-terminal domain kinases display distinct substrate preferences J. Biol. Chem. 276 2001 10913 10920
29. Rasband, W.S. (1997-2011). ImageJ (Bethesda: U. S. National Institute of Health).
30. P. Rickert, J.L. Corden, and E. Lees Cyclin C/CDK8 and cyclin H/CDK7/p36 are biochemically distinct CTD kinases Oncogene 18 1999 1093 1102
31. P.J. Robinson, D.A. Bushnell, M.J. Trnka, A.L. Burlingame, and R.D. Kornberg 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
32. R. Roy, J.P. Adamczewski, T. Seroz, W. Vermeulen, J.P. Tassan, L. Schaeffer, E.A. Nigg, J.H. Hoeijmakers, and J.M. Egly The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor Cell 79 1994 1093 1101
33. J.C. Schwartz, C.C. Ebmeier, E.R. Podell, J. Heimiller, D.J. Taatjes, and T.R. Cech FUS binds the CTD of RNA polymerase II and regulates its phosphorylation at Ser2 Genes Dev. 26 2012 2690 2695
34. J.C. Schwartz, X. Wang, E.R. Podell, and T.R. Cech RNA seeds higher-order assembly of FUS protein Cell Rep. 5 2013 10.1016/j.celrep.2013.11.017 Published online November 21, 2013
35. P. Sheffield, S. Garrard, and Z. Derewenda Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors Protein Expr. Purif. 15 1999 34 39
36. S. Trigon, H. Serizawa, J.W. Conaway, R.C. Conaway, S.P. Jackson, and M. Morange Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases J. Biol. Chem. 273 1998 6769 6775
37. K.L. Tsai, S. Sato, C. Tomomori-Sato, R.C. Conaway, J.W. Conaway, and F.J. Asturias A conserved Mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction Nat. Struct. Mol. Biol. 20 2013 611 619
38. V.N. Uversky Natively unfolded proteins: a point where biology waits for physics Protein Sci. 11 2002 739 756
39. D. Wang, I. Garcia-Bassets, C. Benner, W. Li, X. Su, Y. Zhou, J. Qiu, W. Liu, M.U. Kaikkonen, and K.A. Ohgi Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA Nature 474 2011 390 394
40. H. Zinszner, R. Albalat, and D. Ron A novel effector domain from the RNA-binding protein TLS or EWS is required for oncogenic transformation by CHOP Genes Dev. 8 1994 2513 2526
41. M. Patturajan, R.J. Schulte, B.M. Sefton, R. Berezney, M. Vincent, O. Bensaude, S.L. Warren, and J.L. Corden Growth-related changes in phosphorylation of yeast RNA polymerase II J. Biol. Chem. 273 1998 4689 4694
42. N.E. Thompson, D.B. Aronson, and R.R. Burgess Purification of eukaryotic RNA polymerase II by immunoaffinity chromatography. Elution of active enzyme with protein stabilizing agents from a polyol-responsive monoclonal antibody J. Biol. Chem. 265 1990 7069 7077