Solution and crystal structures of a C-terminal fragment of the neuronal isoform of the polypyrimidine tract binding protein (nPTB)

PeerJ

Volumn 2014, Issue 1, 2014, Pages

  Joshi, Amar ^a   Esteve, Vicent ^b   Buckroyd, Adrian N ^a   Blatter, Markus ^b   Allain, Frédéric H T ^b   Curry, Stephen ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

Nuclear magnetic resonance spectroscopy; Polypyrimidine tract binding protein; Pre mRNA splicing; Protein crystallography; Protein structure; RNA binding proteins

Indexed keywords

POLYPYRIMIDINE TRACT BINDING PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; GEL PERMEATION CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA SPLICING; STEREOCHEMISTRY; X RAY DIFFRACTION;

EID: 84897939104     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.305     Document Type: Article

References (51)

1. Adams PD, Afonine PV, Bunkoczi 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 66:213-221
2. Bashford D, Case DA. 2000. Generalized born models of macromolecular solvation effects. Annual Review of Physical Chemistry 51:129-152
3. Boutz PL, Stoilov P, Li Q, Lin C-H, Chawla G, Ostrow K, Shiue L, Ares M, Black DL. 2007. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes and Development 21:1636-1652
4. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W. 2003. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallographica 59:2023-2030.
5. 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 & NMR system: a new software suite for macromolecular structure determination. Acta Crystallographica 54:905-921
6. Clerte C, Hall KB. 2006. Characterization of multimeric complexes formed by the human PTB1 protein on RNA. RNA 12:457-475
7. Collaborative Computer Project No. 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallographica 50:760-763.
8. Conte MR, Grüne T, Ghuman J, Kelly G, Ladas A,Matthews S, Curry S. 2000. Structure of tandem RNA recognition motifs from polypyrimidine tract binding protein reveals novel features of the RRM fold. EMBO Journal 19:3132-3141
9. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallographica 62:1002-1011
10. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallographica 60:2126-2132.
11. Garći{dotless}a-Blanco MA, Jamison SF, Sharp PA. 1989. Identification and purification of a 62,000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes and Development 3:1874-1886
12. Gil A, Sharp PA, Jamison SF, Garcia-Blanco MA. 1991. Characterization of cDNAs encoding the polypyrimidine tract-binding protein. Genes and Development 5:1224-1236
13. Goddard TD, Kneller DG. 2007. SPARKY 3.114. San Francisco: University of California.
14. Gooding C, Kemp P, Smith CWJ. 2003. A novel polypyrimidine tract-binding protein paralog expressed in smooth muscle cells. Journal of Biological Chemistry 278:15201-15207
15. Guntert P. 2004. Automated NMR structure calculation with CYANA. Methods in Molecular Biology 278:353-378.
16. 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. Journal of Molecular Biology 319:209-227
17. Herrmann T, Guntert P,Wuthrich K. 2002b. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. Journal of Biomolecular NMR 24:171-189
18. Joshi A, Coelho MB, Kotik-Kogan O, Simpson PJ,Matthews SJ, Smith CW, Curry S. 2011. Crystallographic analysis of polypyrimidine tract-binding protein-raver1 interactions involved in regulation of alternative splicing. Structure 19:1816-1825
19. Joshi A, Esteve V, Buckroyd AN, Blatter M, Allain FH, Curry S. 2014. Solution and crystal structures of a C-terminal fragment of the neuronal isoform of the polypyrimidine tract binding protein (nPTB). PeerJ Preprints 2:e211v1
20. 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. Proceedings of the National Academy of Sciences of the United States of America 107:4105-4110
21. 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. Journal of Biomolecular NMR 8:477-486
22. Lindorff-Larsen K, Piana S, Palmo K,Maragakis P, Klepeis JL, Dror RO, Shaw DE. 2010. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78:1950-1958.
23. Llorian M, Schwartz S, Clark TA, Hollander D, Tan L-Y, Spellman R, Gordon A, Schweitzer AC, De La Grange P, Ast G, Smith CWJ. 2010. Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nature Structural Molecular Biology 17:1114-1123
24. Markovtsov V, Nikolic JM, Goldman JA, Turck CW, Chou MY, Black DL. 2000. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Molecular and Cellular Biology 20:7463-7479
25. Maynard CM, Hall KB. 2010. Interactions between PTB RRMs induce slow motions and increase RNA binding affinity. Journal of Molecular Biology 397:260-277
26. McCoy AJ, Grosse-Kunstleve RW, Adams PD,Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallography 40:658-674
27. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457-463
28. Nordlund HR, Hytönen VP, Laitinen OH, Uotila STH, Niskanen EA, Savolainen J, Porkka E, Kulomaa MS. 2003. Introduction of histidine residues into avidin subunit interfaces allows pH-dependent regulation of quaternary structure and biotin binding. FEBS Letters 555:449-454
29. 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 309:2054-2057
30. Pearlman DA, Case DA, Caldwell JW, RossWS, Cheatham Iii TE, DeBolt S, Ferguson D, Seibel G, Kollman P. 1995. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Computer Physics Communications 91:1-41
31. Pérez I, Lin CH,McAfee JG, Patton JG. 1997. Mutation of PTB binding sites causes misregulation of alternative 3′ splice site selection in vivo. RNA 3:764-778.
32. Petoukhov MV,Monie TP, Allain FH,Matthews S, Curry S, Svergun DI. 2006. Conformation of polypyrimidine tract binding protein in solution. Structure 14:1021-1027
33. Pilipenko EV, Viktorova EG, Guest ST, Agol VI, Roos RP. 2001. Cell-specific proteins regulate viral RNA translation and virus-induced disease. EMBO Journal 20:6899-6908
34. Polydorides AD, Okano HJ, Yang YY, Stefani G, Darnell RB. 2000. A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proceedings of the National Academy of Sciences of the United States of America 97:6350-6355
35. Rideau AP, Gooding C, Simpson PJ,Monie TP, Lorenz M, Hüttelmaier S, Singer RH, Matthews S, Curry S, Smith CWJ. 2006. A peptide motif in Raver1 mediates splicing repression by interaction with the PTB RRM2 domain. Nature Structural Molecular Biology 13:839-848
36. Robinson F, Smith CWJ. 2006. A splicing repressor domain in polypyrimidine tract-binding protein. Journal of Biological Chemistry 281:800-806
37. Sawicka K, Bushell M, Spriggs KA,Willis AE. 2008. Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochemical Society Transactions 36:641-647
38. Sharma S, Falick AM, Black DL. 2005. Polypyrimidine tract binding protein blocks the 5′ splice site-dependent assembly of U2AF and the prespliceosomal E complex. Molecular Cell 19:485-496
39. Sheldrick GM. 2008. A short history of SHELX. ACTA Crystallographica 64:112-122
40. Simpson PJ,Monie TP, Szendröi A, Davydova N, Tyzack JK, Conte MR, Read CM, Cary PD, Svergun DI, Konarev PV, Curry S,Matthews S. 2004. Structure and RNA interactions of the N-terminal RRM domains of PTB. Structure 12:1631-1643
41. Singh R, Valcárcel J, Green MR. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268:1173-1176
42. Spellman R, Llorian M, Smith CWJ. 2007. Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Molecular Cell 27:420-434
43. 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 Journal 25:150-162
44. Vonrhein C, Blanc E, Roversi P, Bricogne G. 2007. Automated structure solution with autoSHARP. Methods in Molecular Biology 364:215-230.
45. Winn MD,Murshudov GN, Papiz MZ. 2003. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods in Enzymology 374:300-321.
46. Witten JT, Ule J. 2011. Understanding splicing regulation through RNA splicing maps. Trends in Genetics 27:89-97
47. Xue Y, Zhou Y,Wu T, Zhu T, Ji X, Kwon Y-S, Zhang C, Yeo G, Black DL, Sun H, Fu X-D, Zhang Y. 2009. Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Molecular Cell 36:996-1006
48. Yamamoto H, Tsukahara K, Kanaoka Y, Jinno S, Okayama H. 1999. Isolation of a mammalian homologue of a fission yeast differentiation regulator. Molecular and Cellular Biology 19:3829-3841.
49. Yuan X, Davydova N, Conte MR, Curry S,Matthews S. 2002. Chemical shift mapping of RNA interactions with the polypyrimidine tract binding protein. Nucleic Acids Research 30:456-462
50. Zhang W, Zeng F, Liu Y, Zhao Y, Lv H, Niu L, Teng M, Li X. 2013. Crystal structures and RNA-binding properties of the RNA recognition motifs of heterogeneous nuclear ribonucleoprotein L: insights into its roles in alternative splicing regulation. Journal of Biological Chemistry 288:22636-22649
51. Zou P, Gautel M, Geerlof A,Wilmanns M, Koch MHJ, Svergun DI. 2003. Solution scattering suggests cross-linking function of telethonin in the complex with titin. Journal of Biological Chemistry 278:2636-2644