Solution structure of the N-terminal dsRBD of Drosophila ADAR and interaction studies with RNA

Biochimie

Volumn 94, Issue 7, 2012, Pages 1499-1509

  Barraud, Pierre ^a   Heale, Bret S E ^b,c   O'Connell, Mary A ^b   Allain, Frédéric H T ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

ADAR; Drosophila; dsRBD; dsRBM; GluR 2 R G site; NMR; RNA editing

Indexed keywords

ADENOSINE DEAMINASE; DOUBLE STRANDED RNA; INOSINE; MESSENGER RNA; PHOSPHATE; SUGAR;

ARTICLE; CATALYSIS; DIMERIZATION; DROSOPHILA; MAMMAL; NONHUMAN; PROTEIN DOMAIN; PROTEIN INTERACTION; RNA BINDING; RNA SEQUENCE; RNA STRUCTURE;

ADENOSINE DEAMINASE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHOSPHATES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUTAMATE; RNA, DOUBLE-STRANDED; SOLUTIONS; SUBSTRATE SPECIFICITY;

MAMMALIA; VERTEBRATA;

EID: 84861599510     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2011.12.017     Document Type: Article

References (56)

1. B.L. Bass RNA editing by adenosine deaminases that act on RNA Annu. Rev. Biochem. 71 2002 817 846
2. L. Valente, and K. Nishikura ADAR gene family and A-to-I RNA editing: diverse roles in posttranscriptional gene regulation Prog. Nucleic Acid Res. Mol. Biol. 79 2005 299 338
3. K. Nishikura Functions and regulation of RNA editing by ADAR deaminases Annu. Rev. Biochem. 79 2010 321 349
4. P. Barraud, and F.H. Allain ADAR proteins: double-stranded RNA and Z-DNA binding domains Curr. Top. Microbiol. Immunol. 353 2012 35 60
5. K.A. Lehmann, and B.L. Bass The importance of internal loops within RNA substrates of ADAR1 J. Mol. Biol. 291 1999 1 13
6. O.M. Stephens, B.L. Haudenschild, and P.A. Beal The binding selectivity of ADAR2's dsRBMs contributes to RNA-editing selectivity Chem. Biol. 11 2004 1239 1250
7. R. Stefl, F.C. Oberstrass, J.L. Hood, M. Jourdan, M. Zimmermann, L. Skrisovska, C. Maris, L. Peng, C. Hofr, R.B. Emeson, and F.H.-T. Allain The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove Cell 143 2010 225 237
8. J.M. Eggington, T. Greene, and B.L. Bass Predicting sites of ADAR editing in double-stranded RNA Nat. Commun. 2 2011 319
9. B. Sommer, M. Köhler, R. Sprengel, and P.H. Seeburg RNA editing in brain controls a determinant of ion flow in glutamate-gated channels Cell 67 1991 11 19
10. C.M. Burns, H. Chu, S.M. Rueter, L.K. Hutchinson, H. Canton, E. Sanders-Bush, and R.B. Emeson Regulation of serotonin-2C receptor G-protein coupling by RNA editing Nature 387 1997 303 308
11. B. Hoopengardner, T. Bhalla, C. Staber, and R. Reenan Nervous system targets of RNA editing identified by comparative genomics Science 301 2003 832 836
12. T. Bhalla, J.J.C. Rosenthal, M. Holmgren, and R. Reenan Control of human potassium channel inactivation by editing of a small mRNA hairpin Nat. Struct. Mol. Biol. 11 2004 950 956
13. M.J. Palladino, L.P. Keegan, M.A. O'Connell, and R.A. Reenan A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity Cell 102 2000 437 449
14. L.P. Keegan, J. Brindle, A. Gallo, A. Leroy, R.A. Reenan, and M.A. O'Connell Tuning of RNA editing by ADAR is required in Drosophila EMBO J. 24 2005 2183 2193
15. S. Paro, X. Li, M.A. O'Connell, and L.P. Keegan Regulation and functions of ADAR in Drosophila Curr. Top. Microbiol. Immunol. 353 2012 221 236
16. M. Stapleton, J.W. Carlson, and S.E. Celniker RNA editing in Drosophila melanogaster: new targets and functional consequences RNA 12 2006 1922 1932
17. B.R. Graveley, A.N. Brooks, J.W. Carlson, M.O. Duff, J.M. Landolin, L. Yang, C.G. Artieri, M.J. van Baren, N. Boley, and B.W. Booth The developmental transcriptome of Drosophila melanogaster Nature 471 2011 473 479
18. M. Higuchi, F.N. Single, M. Köhler, B. Sommer, R. Sprengel, and P.H. Seeburg RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency Cell 75 1993 1361 1370
19. H. Lomeli, J. Mosbacher, T. Melcher, T. Höger, J.R. Geiger, T. Kuner, H. Monyer, M. Higuchi, A. Bach, and P.H. Seeburg Control of kinetic properties of AMPA receptor channels by nuclear RNA editing Science 266 1994 1709 1713
20. S. Maas, Y. Kawahara, K.M. Tamburro, and K. Nishikura A-to-I RNA editing and human disease RNA Biol. 3 2006 1 9
21. J.L. Hood, and R.B. Emeson Editing of Neurotransmitter receptor and ion channel RNAs in the nervous system Curr. Top. Microbiol. Immunol. 353 2012 61 90
22. L.P. Keegan, L. McGurk, J.P. Palavicini, J. Brindle, S. Paro, X. Li, J.J.C. Rosenthal, and M.A. O'Connell Functional conservation in human and Drosophila of Metazoan ADAR2 involved in RNA editing: loss of ADAR1 in insects Nucleic Acids Res. 39 2011 7249 7262
23. M.J. Palladino, L.P. Keegan, M.A. O'Connell, and R.A. Reenan dADAR, a Drosophila double-stranded RNA-specific adenosine deaminase is highly developmentally regulated and is itself a target for RNA editing RNA 6 2000 1004 1018
24. M.R. Macbeth, H.L. Schubert, A.P. Vandemark, A.T. Lingam, C.P. Hill, and B.L. Bass Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing Science 309 2005 1534 1539
25. R. Stefl, M. Xu, L. Skrisovska, R.B. Emeson, and F.H.-T. Allain Structure and specific RNA binding of ADAR2 double-stranded RNA binding motifs Structure 14 2006 345 355
26. I. Fierro-Monti, and M.B. Mathews Proteins binding to duplexed RNA: one motif, multiple functions Trends Biochem. Sci. 25 2000 241 246
27. L.R. Saunders, and G.N. Barber The dsRNA binding protein family: critical roles, diverse cellular functions FASEB J. 17 2003 961 983
28. K.-Y. Chang, and A. Ramos The double-stranded RNA-binding motif, a versatile macromolecular docking platform FEBS J. 272 2005 2109 2117
29. R. Stefl, L. Skrisovska, and F.H.-T. Allain RNA sequence- and shape-dependent recognition by proteins in the ribonucleoprotein particle EMBO Rep. 6 2005 33 38
30. M. Bycroft, S. Grunert, A.G. Murzin, M. Proctor, and D. St Johnston NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5 EMBO J. 14 1995 3563 3571
31. A. Kharrat, M.J. Macias, T.J. Gibson, M. Nilges, and A. Pastore Structure of the dsRNA binding domain of E. coli RNase III EMBO J. 14 1995 3572 3584
32. J.M. Ryter, and S.C. Schultz Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA EMBO J. 17 1998 7505 7513
33. A. Ramos, S. Grünert, J. Adams, D.R. Micklem, M.R. Proctor, S. Freund, M. Bycroft, D. St Johnston, and G. Varani RNA recognition by a Staufen double-stranded RNA-binding domain EMBO J. 19 2000 997 1009
34. J. Blaszczyk, J. Gan, J.E. Tropea, D.L. Court, D.S. Waugh, and X. Ji Noncatalytic assembly of ribonuclease III with double-stranded RNA Structure 12 2004 457 466
35. H. Wu, A. Henras, G. Chanfreau, and J. Feigon Structural basis for recognition of the AGNN tetraloop RNA fold by the double-stranded RNA-binding domain of Rnt1p RNase III Proc. Natl. Acad. Sci. U S A 101 2004 8307 8312
36. J. Gan, J.E. Tropea, B.P. Austin, D.L. Court, D.S. Waugh, and X. Ji Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III Cell 124 2006 355 366
37. S.W. Yang, H.Y. Chen, J. Yang, S. Machida, N.H. Chua, and Y.A. Yuan Structure of Arabidopsis HYPONASTIC LEAVES1 and its molecular implications for miRNA processing Structure 18 2010 594 605
38. Z. Wang, E. Hartman, K. Roy, G. Chanfreau, and J. Feigon Structure of a yeast RNase III dsRBD complex with a noncanonical RNA substrate provides new insights into binding specificity of dsRBDs Structure 19 2011 999 1010
39. T. Goddard, and D. Kneller SPARKY 3 2006 University of California San Francisco
40. T. Herrmann, P. Guntert, and K. Wuthrich Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA J. Mol. Biol. 319 2002 209 227
41. P. Guntert, C. Mumenthaler, and K. Wuthrich Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
42. P. Guntert Automated NMR structure calculation with CYANA Methods Mol. Biol. 278 2004 353 378
43. T. Herrmann, P. Guntert, and K. Wuthrich Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS J. Biomol. NMR 24 2002 171 189
44. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, and M. Nilges Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
45. A.T. Brunger Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2 2007 2728 2733
46. P. Barraud, S. Emmerth, Y. Shimada, H.-R. Hotz, F.H.-T. Allain, and M. Bühler An extended dsRBD with a novel zinc-binding motif mediates nuclear retention of fission yeast Dicer EMBO J. 30 2011 4223 4235
47. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486
48. W.L. DeLano The PyMOL Molecular Graphics System 2002
49. O. Duss, C. Maris, C. von Schroetter, and F.H.-T. Allain A fast, efficient and sequence-independent method for flexible multiple segmental isotope labeling of RNA using ribozyme and RNase H cleavage Nucleic Acids Res. 38 2010 e188
50. E. Bratt, and M. Ohman Coordination of editing and splicing of glutamate receptor pre-mRNA RNA 9 2003 309 318
51. N. Leulliot, S. Quevillon-Cheruel, M. Graille, H. van Tilbeurgh, T.C. Leeper, K.S. Godin, T.E. Edwards, S.T.L. Sigurdsson, N. Rozenkrants, R.J. Nagel, M. Ares, and G. Varani A new alpha-helical extension promotes RNA binding by the dsRBD of Rnt1p RNAse III EMBO J. 23 2004 2468 2477
52. D.-S.C. Cho, W. Yang, J.T. Lee, R. Shiekhattar, J.M. Murray, and K. Nishikura Requirement of dimerization for RNA editing activity of adenosine deaminases acting on RNA J. Biol. Chem. 278 2003 17093 17102
53. A. Gallo, L.P. Keegan, G.M. Ring, and M.A. O'Connell An ADAR that edits transcripts encoding ion channel subunits functions as a dimer EMBO J. 22 2003 3421 3430
54. C. Dominguez, M. Schubert, O. Duss, S. Ravindranathan, and F.H.-T. Allain Structure determination and dynamics of protein-RNA complexes by NMR spectroscopy Prog. Nucl. Magn. Reson. Spectrosc. 58 2011 1 61
55. P. Barraud, F. Dardel, and C. Tisné Optimizing HSQC experiment for the observation of exchange broadened signals in RNA-protein complexes Comptes Rendus Chim. 11 2008 474 479
56. B.C. Krovat, and M.F. Jantsch Comparative mutational analysis of the double-stranded RNA binding domains of Xenopus laevis RNA-binding protein A J. Biol. Chem. 271 1996 28112 28119