Solution structure of the two RNA recognition motifs of hnRNP A1 using segmental isotope labeling: How the relative orientation between RRMs influences the nucleic acid binding topology

Journal of Biomolecular NMR

Volumn 55, Issue 1, 2013, Pages 119-138

  Barraud, Pierre ^a   Allain, Frédéric H T ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

13C edited half filter NOESY; Domain orientation; Expressed protein ligation; HnRNP A1; Intein; Inter domain interaction; NMR; RNA recognition modes; RRM; Segmental isotope labeling; Structural biology; UP1

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; ISOTOPE LABELING; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN RNA BINDING; RNA ANALYSIS; RNA CONFORMATION; RNA STRUCTURE;

AMINO ACID MOTIFS; BINDING SITES; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; ISOTOPE LABELING; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA, MESSENGER;

EID: 84873059804     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-012-9696-4     Document Type: Article

References (83)

1. Allain FH, Bouvet P, Dieckmann T, Feigon J (2000a) Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin. EMBO J 19(24):6870-6881
2. Allain FH, Gilbert DE, Bouvet P, Feigon J (2000b) Solution structure of the two N-terminal RNA-binding domains of nucleolin and NMR study of the interaction with its RNA target. J Mol Biol 303(2):227-241
3. Anderson LL, Marshall GR, Crocker E, Smith SO, Baranski TJ (2005) Motion of carboxyl terminus of Galpha is restricted upon G protein activation. A solution NMR study using semisynthetic Galpha subunits. J Biol Chem 280(35):31019-31026
4. Arumugam S, Miller MC, Maliekal J, Bates PJ, Trent JO, Lane AN (2010) Solution structure of the RBD1,2 domains from human nucleolin. J Biomol NMR 47(1):79-83
5. Bae E, Reiter NJ, Bingman CA, Kwan SS, Lee D, Phillips GN Jr, Butcher SE, Brow DA (2007) Structure and interactions of the first three RNA recognition motifs of splicing factor prp24. J Mol Biol 367(5):1447-1458
6. Barraud P, Emmerth S, Shimada Y, Hotz HR, Allain FH, Buhler M (2011) An extended dsRBD with a novel zinc-binding motif mediates nuclear retention of fission yeast Dicer. EMBO J 30(20):4223-4235
7. Bax A, Kontaxis G, Tjandra N (2001) Dipolar couplings in macromolecular structure determination. Methods Enzymol 339:127-174
8. Brunger AT (2007) Version 1.2 of the crystallography and NMR system. Nat Protoc 2(11):2728-2733
9. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54(Pt 5):905-921
10. Cáceres JF, Stamm S, Helfman DM, Krainer AR (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265(5179):1706-1709
11. Camarero JA, Shekhtman A, Campbell EA, Chlenov M, Gruber TM, Bryant DA, Darst SA, Cowburn D, Muir TW (2002) Autoregulation of a bacterial sigma factor explored by using segmental isotopic labeling and NMR. Proc Natl Acad Sci U S A 99(13):8536-8541
12. Casas-Finet JR, Karpel RL, Maki AH, Kumar A, Wilson SH (1991) Physical studies of tyrosine and tryptophan residues in mammalian A1 heterogeneous nuclear ribonucleoprotein. support for a segmented structure. J Mol Biol 221(2):693-709
13. Chen J, Wang J (2011) A segmental labeling strategy for unambiguous determination of domain-domain interactions of large multi-domain proteins. J Biomol NMR 50(4):403-410
14. Chen J, Li Q, Wang J (2011) Topology of human apolipoprotein E3 uniquely regulates its diverse biological functions. Proc Natl Acad Sci U S A 108(36):14813-14818
15. Cordier F, Dingley AJ, Grzesiek S (1999) A doublet-separated sensitivity-enhanced HSQC for the determination of scalar and dipolar one-bond J-couplings. J Biomol NMR 13(2):175-180
16. Crichlow GV, Zhou H, Hsiao HH, Frederick KB, Debrosse M, Yang Y, Folta-Stogniew EJ, Chung HJ, Fan C, De la Cruz EM, Levens D, Lolis E, Braddock D (2008) Dimerization of FIR upon FUSE DNA binding suggests a mechanism of c-myc inhibition. EMBO J 27(1):277-289
17. Crowder SM, Kanaar R, Rio DC, Alber T (1999) Absence of inter domain contacts in the crystal structure of the RNA recognition motifs of sex-lethal. Proc Natl Acad Sci U S A 96(9):4892-4897
18. Cukier CD, Hollingworth D, Martin SR, Kelly G, Diaz-Moreno I, Ramos A (2010) Molecular basis of FIR-mediated c-myc transcriptional control. Nat Struct Mol Biol 17(9):1058-1064
19. David R, Richter MP, Beck-Sickinger AG (2004) Expressed protein ligation. Method and applications. Eur J Biochem 271(4):663-677
20. Dayie KT, Wagner G, Lefèvre JF (1996) Theory and practice of nuclear spin relaxation in proteins. Annu Rev Phys Chem 47:243-282
21. Deo RC, Bonanno JB, Sonenberg N, Burley SK (1999) Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98(6):835-845
22. Ding J, Hayashi MK, Zhang Y, Manche L, Krainer AR, Xu RM (1999) Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA. Genes Dev 13(9):1102-1115
23. Dominguez C, Allain FH-T (2006) NMR structure of the three quasi RNA recognition motifs (qRRMs) of human hnRNP F and interaction studies with Bcl-x G-tract RNA: a novel mode of RNA recognition. Nucleic Acids Res 34(13):3634-3645
24. Doreleijers JF, Sousa da Silva AW, Krieger E, Nabuurs SB, Spronk CAEM, Stevens TJ, Vranken WF, Vriend G, Vuister GW (2012) CING: an integrated residue-based structure validation program suite. J Biomol NMR 54(3):267-283
25. Dosset P, Hus JC, Marion D, Blackledge M (2001) A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings. J Biomol NMR 20(3):223-231
26. Dreyfuss G, Matunis MJ, Piñol-Roma S, Burd CG (1993) hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62:289-321
27. Flynn RL, Centore RC, O'Sullivan RJ, Rai R, Tse A, Songyang Z, Chang S, Karlseder J, Zou L (2011) TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471(7339):532-536
28. Fushman D, Weisemann R, Thüring H, Rüterjans H (1994) Backbone dynamics of ribonuclease T1 and its complex with 2′GMP studied by two-dimensional heteronuclear NMR spectroscopy. J Biomol NMR 4(1):61-78
29. Garrett DS, Lodi PJ, Shamoo Y, Williams KR, Clore GM, Gronenborn AM (1994) Determination of the secondary structure and folding topology of an RNA binding domain of mammalian hnRNP A1 protein using three-dimensional heteronuclear magnetic resonance spectroscopy. Biochemistry 33(10):2852-2858
30. Goddard T, Kneller D (2006) SPARKY 3. University of California, San Francisco
31. Guil S, Cáceres JF (2007) The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat Struct Mol Biol 14(7):591-596
32. Guntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278:353-378
33. Guntert P, Mumenthaler C, Wuthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273(1):283-298
34. Handa N, Nureki O, Kurimoto K, Kim I, Sakamoto H, Shimura Y, Muto Y, Yokoyama S (1999) Structural basis for recognition of the tra mRNA precursor by the sex-lethal protein. Nature 398(6728):579-585
35. Herrmann T, Guntert P, Wuthrich K (2002a) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319(1):209-227
36. Herrmann T, Guntert P, Wuthrich K (2002b) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J Biomol NMR 24(3):171-189
37. Johansson C, Finger LD, Trantirek L, Mueller TD, Kim S, Laird-Offringa IA, Feigon J (2004) Solution structure of the complex formed by the two N-terminal RNA-binding domains of nucleolin and a pre-rRNA target. J Mol Biol 337(4):799-816
38. Kay LE, Torchia DA, Bax A (1989) Backbone dynamics of proteins as studied by 15 N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28(23):8972-8979
39. LaBranche H, Dupuis S, Ben-David Y, Bani MR, Wellinger RJ, Chabot B (1998) Telomere elongation by hnRNP A1 and a derivative that interacts with telomeric repeats and telomerase. Nat Genet 19(2):199-202
40. Lamichhane R, Daubner GM, Thomas-Crusells J, Auweter SD, Manatschal C, Austin KS, Valniuk O, Allain FH-T, Rueda D (2010) RNA looping by PTB: evidence using FRET and NMR spectroscopy for a role in splicing repression. Proc Natl Acad Sci U S A 107(9):4105-4110
41. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8(4):477-486
42. Leeper TC, Qu X, Lu C, Moore C, Varani G (2010) Novel protein-protein contacts facilitate mRNA 3′-processing signal recognition by Rna15 and Hrp1. J Mol Biol 401(3):334-349
43. Mackereth CD, Sattler M (2012) Dynamics in multi-domain protein recognition of RNA. Curr Opin Struct Biol 22(3):287-296
44. Mackereth CD, Madl T, Bonnal S, Simon B, Zanier K, Gasch A, Rybin V, Valcarcel J, Sattler M (2011) Multi-domain conformational selection underlies pre-mRNA splicing regulation by U2AF. Nature 475(7356):408-411
45. Maris C, Dominguez C, Allain FH-T (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272(9):2118-2131
46. Martin-Tumasz S, Reiter NJ, Brow DA, Butcher SE (2010) Structure and functional implications of a complex containing a segment of U6 RNA bound by a domain of Prp24. RNA 16(4):792-804
47. Mayeda A, Krainer AR (1992) Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68(2):365-375
48. Mayeda A, Munroe SH, Xu RM, Krainer AR (1998) Distinct functions of the closely related tandem RNA-recognition motifs of hnRNP A1. RNA 4(9):1111-1123
49. Michel E, Skrisovska L, Wüthrich K, Allain FH (2013) Amino acid-selective segmental isotope labeling of multi-domain proteins for structural biology. Chembiochem (in press)
50. Michlewski G, Cáceres JF (2010) Antagonistic role of hnRNP A1 and KSRP in the regulation of let-7a biogenesis. Nat Struct Mol Biol 17(8):1011-1018
51. Michlewski G, Guil S, Semple CA, Cáceres JF (2008) Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 32(3):383-393
52. Minato Y, Ueda T, Machiyama A, Shimada I, Iwai H (2012) Segmental isotopic labeling of a 140 kDa dimeric multi-domain protein CheA from Escherichia coli by expressed protein ligation and protein trans-splicing. J Biomol NMR 53(3):191-207
53. Muralidharan V, Muir TW (2006) Protein ligation: an enabling technology for the biophysical analysis of proteins. Nat Methods 3(6):429-438
54. Myers JC, Shamoo Y (2004) Human UP1 as a model for understanding purine recognition in the family of proteins containing the RNA recognition motif (RRM). J Mol Biol 342(3):743-756
55. Myers JC, Moore SA, Shamoo Y (2003) Structure-based incorporation of 6-methyl-8-(2-deoxy-beta-ribofuranosyl) isoxanthopteridine into the human telomeric repeat DNA as a probe for UP1 binding and destabilization of G-tetrad structures. J Biol Chem 278(43):42300-42306
56. Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463(7280):457-463
57. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, Wenter P, Reymond L, Amir-Ahmady B, Pitsch S, Black DL, Allain FH-T (2005) Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 309(5743):2054-2057
58. Pelton JG, Torchia DA, Meadow ND, Roseman S (1993) Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci 2(4):543-558
59. Perez-Canadillas JM (2006) Grabbing the message: structural basis of mRNA 3′UTR recognition by Hrp1. EMBO J 25(13):3167-3178
60. Piñol-Roma S, Dreyfuss G (1992) Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355(6362):730-732
61. Pontius BW, Berg P (1990) Renaturation of complementary DNA strands mediated by purified mammalian heterogeneous nuclear ribonucleoprotein A1 protein: implications for a mechanism for rapid molecular assembly. Proc Natl Acad Sci U S A 87(21):8403-8407
62. Rückert M, Otting G (2000) Alignment of biological macromolecules in novel non ionic liquid crystalline media for NMR experiments. J Am Chem Soc 122(32):7793-7797
63. Safaee N, Kozlov G, Noronha AM, Xie J, Wilds CJ, Gehring K (2012) Inter domain allostery promotes assembly of the poly(A) mRNA complex with PABP and eIF4G. Mol Cell 48(3):375-386
64. Shamoo Y, Abdul-Manan N, Patten AM, Crawford JK, Pellegrini MC, Williams KR (1994) Both RNA-binding domains in heterogenous nuclear ribonucleoprotein A1 contribute toward single-stranded-RNA binding. Biochemistry 33(27):8272-8281
65. Shamoo Y, Abdul-Manan N, Williams KR (1995) Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res 23(5):725-728
66. Shamoo Y, Krueger U, Rice LM, Williams KR, Steitz TA (1997) Crystal structure of the two RNA binding domains of human hnRNP A1 at 1.75 a resolution. Nat Struct Biol 4(3):215-222
67. Shen Y, Delaglio F, Cornilescu G, Bax A (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 44(4):213-223
68. Sickmier EA, Frato KE, Shen H, Paranawithana SR, Green MR, Kielkopf CL (2006) Structural basis for polypyrimidine tract recognition by the essential pre-mRNA splicing factor U2AF65. Mol Cell 23(1):49-59
69. Skelton N, Palmer A, Akke M, Kordel J, Rance M, Chazin W (1993) Practical aspects of two-dimensional proton-detected 15 N spin relaxation measurements. J Magn Reson B 102(3):253-264
70. Skrisovska L, Allain FH-T (2008) Improved segmental isotope labeling methods for the NMR study of multidomain or large proteins: application to the RRMs of Npl3p and hnRNP L. J Mol Biol 375(1):151-164
71. Skrisovska L, Schubert M, Allain FH (2010) Recent advances in segmental isotope labeling of proteins: NMR applications to large proteins and glycoproteins. J Biomol NMR 46(1):51-65
72. Southworth MW, Amaya K, Evans TC, Xu MQ, Perler FB (1999) Purification of proteins fused to either the amino or carboxy terminus of the Mycobacterium xenopi gyrase A intein. Biotechniques 27(1):110-114, 116, 118-120
73. Teplova M, Song J, Gaw HY, Teplov A, Patel DJ (2010) Structural insights into RNA recognition by the alternate-splicing regulator CUG-binding protein 1. Structure 18(10):1364-1377
74. Vitali J, Ding J, Jiang J, Zhang Y, Krainer AR, Xu R-M (2002) Correlated alternative side chain conformations in the RNA-recognition motif of heterogeneous nuclear ribonucleoprotein A1. Nucleic Acids Res 30(7):1531-1538
75. Vitali F, Henning A, Oberstrass FC, Hargous Y, Auweter SD, Erat M, Allain FH-T (2006) Structure of the two most C-terminal RNA recognition motifs of PTB using segmental isotope labeling. EMBO J 25(1):150-162
76. Wang X, Tanaka Hall TM (2001) Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat Struct Biol 8(2):141-145
77. 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 Crystallogr D Biol Crystallogr 67(Pt 4):235-242
78. Xu RM, Jokhan L, Cheng X, Mayeda A, Krainer AR (1997) Crystal structure of human UP1, the domain of hnRNP A1 that contains two RNA-recognition motifs. Structure 5(4):559-570
79. Yagi H, Tsujimoto T, Yamazaki T, Yoshida M, Akutsu H (2004) Conformational change of H+-ATPase beta monomer revealed on segmental isotope labeling NMR spectroscopy. J Am Chem Soc 126(50):16632-16638
80. Yang X, Bani MR, Lu SJ, Rowan S, Ben-David Y, Chabot B (1994) The A1 and A1B proteins of heterogeneous nuclear ribo nucleoparticles modulate 5′ splice site selection in vivo. Proc Natl Acad Sci U S A 91(15):6924-6928
81. Zhang Q-S, Manche L, Xu R-M, Krainer AR (2006) hnRNP A1 associates with telomere ends and stimulates telomerase activity. RNA 12(6):1116-1128
82. Zhang Y, Vasudevan S, Sojitrawala R, Zhao W, Cui C, Xu C, Fan D, Newhouse Y, Balestra R, Jerome WG, Weisgraber K, Li Q, Wang J (2007) A monomeric, biologically active, full-length human apolipoprotein E. Biochemistry 46(37):10722-10732
83. Zwahlen C, Legault P, Vincent SJF, Greenblatt J, Konrat R, Kay LE (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage λ N-peptide/boxB RNA complex. J Am Chem Soc 119(29):6711-6721