Structure and Ligand Binding of the Extended Tudor Domain of D. melanogaster Tudor-SN

Journal of Molecular Biology

Volumn 387, Issue 4, 2009, Pages 921-934

  Friberg, Anders ^a,b   Corsini, Lorenzo ^c   Mourão, André ^a,b,c   Sattler, Michael ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

crystallography; NMR; p100; sDMA; Tudor SN

Indexed keywords

ARGININE; CELL PROTEIN; INSECT PROTEIN; LIGAND; PEPTIDE; PROTEIN SM; SMALL NUCLEAR RIBONUCLEOPROTEIN; TUDOR SN PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL SURVIVAL; CONTROLLED STUDY; CRYSTAL STRUCTURE; DROSOPHILA MELANOGASTER; LIGAND BINDING; MOLECULAR RECOGNITION; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REGULATORY MECHANISM; SPLICEOSOME;

DROSOPHILA MELANOGASTER;

EID: 62649142373     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.02.018     Document Type: Article

References (61)

1. Tong X., Drapkin R., Yalamanchili R., Mosialos G., and Kieff E. The Epstein-Barr virus nuclear protein 2 acidic domain forms a complex with a novel cellular coactivator that can interact with TFIIE. Mol. Cell. Biol. 15 (1995) 4735-4744
2. Paukku K., Yang J., and Silvennoinen O. Tudor and nuclease-like domains containing protein p100 function as coactivators for signal transducer and activator of transcription 5. Mol. Endocrinol. 17 (2003) 1805-1814
3. Yang J., Aittomaki S., Pesu M., Carter K., Saarinen J., Kalkkinen N., et al. Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. EMBO J. 21 (2002) 4950-4958
4. Leverson J.D., Koskinen P.J., Orrico F.C., Rainio E.M., Jalkanen K.J., Dash A.B., et al. Pim-1 kinase and p100 cooperate to enhance c-Myb activity. Mol. Cell 2 (1998) 417-425
5. Yang J., Valineva T., Hong J., Bu T., Yao Z., Jensen O.N., et al. Transcriptional co-activator protein p100 interacts with snRNP proteins and facilitates the assembly of the spliceosome. Nucleic Acids Res. 35 (2007) 4485-4494
6. Listerman I., Sapra A.K., and Neugebauer K.M. Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells. Nat. Struct. Mol. Biol. 13 (2006) 815-822
7. Lin S., Coutinho-Mansfield G., Wang D., Pandit S., and Fu X.D. The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15 (2008) 819-826
8. Phatnani H.P., and Greenleaf A.L. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20 (2006) 2922-2936
9. Bass B.L. RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem. 71 (2002) 817-846
10. Scadden A.D., and O'Connell M.A. Cleavage of dsRNAs hyper-edited by ADARs occurs at preferred editing sites. Nucleic Acids Res. 33 (2005) 5954-5964
11. Ohlson J., Pedersen J.S., Haussler D., and Ohman M. Editing modifies the GABA(A) receptor subunit alpha3. RNA 13 (2007) 698-703
12. Schoft V.K., Schopoff S., and Jantsch M.F. Regulation of glutamate receptor B pre-mRNA splicing by RNA editing. Nucleic Acids Res. 35 (2007) 3723-3732
13. Chen L.L., DeCerbo J.N., and Carmichael G.G. Alu element-mediated gene silencing. EMBO J. 27 (2008) 1694-1705
14. Scadden A.D. The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nat. Struct. Mol. Biol. 12 (2005) 489-496
15. Li C.L., Yang W.Z., Chen Y.P., and Yuan H.S. Structural and functional insights into human Tudor-SN, a key component linking RNA interference and editing. Nucleic Acids Res. 36 (2008) 3579-3589
16. Yang W., Chendrimada T.P., Wang Q., Higuchi M., Seeburg P.H., Shiekhattar R., and Nishikura K. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat. Struct. Mol. Biol. 13 (2006) 13-21
17. Kawahara Y., Zinshteyn B., Sethupathy P., Iizasa H., Hatzigeorgiou A.G., and Nishikura K. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 315 (2007) 1137-1140
18. Caudy A.A., Ketting R.F., Hammond S.M., Denli A.M., Bathoorn A.M., Tops B.B., et al. A micrococcal nuclease homologue in RNAi effector complexes. Nature 425 (2003) 411-414
19. Paukku K., Kalkkinen N., Silvennoinen O., Kontula K.K., and Lehtonen J.Y. p100 increases AT1R expression through interaction with AT1R 3′-UTR. Nucleic Acids Res. 36 (2008) 4474-4487
20. Valineva T., Yang J., Palovuori R., and Silvennoinen O. The transcriptional co-activator protein p100 recruits histone acetyltransferase activity to STAT6 and mediates interaction between the CREB-binding protein and STAT6. J. Biol. Chem. 280 (2005) 14989-14996
21. Callebaut I., and Mornon J.P. The human EBNA-2 coactivator p100: multidomain organization and relationship to the staphylococcal nuclease fold and to the tudor protein involved in Drosophila melanogaster development. Biochem. J. 321 (1997) 125-132
22. Ponting C.P. P100, a transcriptional coactivator, is a human homologue of staphylococcal nuclease. Protein Sci. 6 (1997) 459-463
23. Shaw N., Zhao M., Cheng C., Xu H., Saarikettu J., Li Y., et al. The multifunctional human p100 protein 'hooks' methylated ligands. Nat. Struct. Mol. Biol. 14 (2007) 779-784
24. Selenko P., Sprangers R., Stier G., Buhler D., Fischer U., and Sattler M. SMN tudor domain structure and its interaction with the Sm proteins. Nat. Struct. Biol. 8 (2001) 27-31
25. Sprangers R., Groves M.R., Sinning I., and Sattler M. High-resolution X-ray and NMR structures of the SMN Tudor domain: conformational variation in the binding site for symmetrically dimethylated arginine residues. J. Mol. Biol. 327 (2003) 507-520
26. Cote J., and Richard S. Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280 (2005) 28476-28483
27. Botuyan M.V., Lee J., Ward I.M., Kim J.E., Thompson J.R., Chen J., and Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127 (2006) 1361-1373
28. Huang Y., Fang J., Bedford M.T., Zhang Y., and Xu R.M. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312 (2006) 748-751
29. Buhler D., Raker V., Luhrmann R., and Fischer U. Essential role for the tudor domain of SMN in spliceosomal U snRNP assembly: implications for spinal muscular atrophy. Hum. Mol. Genet. 8 (1999) 2351-2357
30. Sanders S.L., Portoso M., Mata J., Bahler J., Allshire R.C., and Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119 (2004) 603-614
31. Mouaikel J., Verheggen C., Bertrand E., Tazi J., and Bordonne R. Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus. Mol. Cell 9 (2002) 891-901
32. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26 (1993) 795-800
33. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
34. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007) W375-W383
35. Libson A.M., Gittis A.G., and Lattman E.E. Crystal structures of the binary Ca2+ and pdTp complexes and the ternary complex of the Asp21→Glu mutant of staphylococcal nuclease. Implications for catalysis and ligand binding. Biochemistry 33 (1994) 8007-8016
36. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
37. 13C chemical-shift data. J. Biomol. NMR 4 (1994) 171-180
38. Clore G.M., and Garrett D.S. R-factor, free R, and complete cross-validation for dipolar coupling refinement of NMR structures. J. Am. Chem. Soc. 121 (1999) 9008-9012
39. Eyal E., Gerzon S., Potapov V., Edelman M., and Sobolev V. The limit of accuracy of protein modeling: influence of crystal packing on protein structure. J. Mol. Biol. 351 (2005) 431-442
40. 15N-NMR relaxation measurements. Eur. J. Biochem. 230 (1995) 1014-1024
41. Garcia de la Torre J., Huertas M.L., and Carrasco B. HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J. Magn. Reson. 147 (2000) 138-146
42. Kelly R.C., Jensen D.E., and von Hippel P.H. DNA "melting" proteins. IV. Fluorescence measurements of binding parameters for bacteriophage T4 gene 32-protein to mono-, oligo-, and polynucleotides. J. Biol. Chem. 251 (1976) 7240-7250
43. Brahms H., Raymackers J., Union A., de Keyser F., Meheus L., and Luhrmann R. The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies. J. Biol. Chem. 275 (2000) 17122-17129
44. Barth S., Liss M., Voss M.D., Dobner T., Fischer U., Meister G., and Grasser F.A. Epstein-Barr virus nuclear antigen 2 binds via its methylated arginine-glycine repeat to the survival motor neuron protein. J. Virol. 77 (2003) 5008-5013
45. Corsini L., and Sattler M. Tudor hooks up with DNA repair. Nat. Struct. Mol. Biol. 14 (2007) 98-99
46. Lee J., Thompson J.R., Botuyan M.V., and Mer G. Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor. Nat. Struct. Mol. Biol. 15 (2008) 109-111
47. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 40 (2007) 658-674
48. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
49. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr., Sect. D: Biol. Crystallogr. 57 (2001) 122-133
50. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 (2002) 1948-1954
51. Perrakis A., Morris R., and Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 (1999) 458-463
52. Koradi, R., Billeter, M. & Wuthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55, 29-32.
53. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA
54. Rocchia W., Alexov E., and Honig B. Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions. J. Phys. Chem. B 105 (2001) 6507-6514
55. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
56. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
57. Sattler M., Schleucher J., and Griesinger C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed. Prog. Nucl. Magn. Reson. Spectrosc. 34 (1999) 93-158
58. 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
59. Cordier F., Dingley A.J., and Grzesiek S. A doublet-separated sensitivity-enhanced HSQC for the determination of scalar and dipolar one-bond J-couplings. J. Biomol. NMR 13 (1999) 175-180
60. Ruckert M., and Otting G. Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J. Am. Chem. Soc. 122 (2000) 7793-7797
61. Kontaxis G., Delaglio F., and Bax A. Molecular fragment replacement approach to protein structure determination by chemical shift and dipolar homology database mining. Methods Enzymol. 394 (2005) 42-78