Deuterium isotope shifts for backbone 1H, 15N and 13C nuclei in intrinsically disordered protein α-synuclein

Journal of Biomolecular NMR

Volumn 54, Issue 2, 2012, Pages 181-191

  Maltsev, Alexander S ^a   Ying, Jinfa ^a   Bax, Ad ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

2H; Chemical shift; IDP; IUP; Protein NMR; Random coil; Triple resonance NMR

Indexed keywords

ALPHA SYNUCLEIN; CARBON 13; DEUTERIUM; HYDROGEN; NITROGEN 15;

ANALYSIS; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DECOMPOSITION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE;

ALPHA-SYNUCLEIN; AMINO ACIDS; BINDING SITES; CARBON ISOTOPES; DEUTERIUM; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84868200793     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-012-9666-x     Document Type: Article

References (49)

1. Abildgaard J, Hansen PE, Manalo MN, LiWang A (2009) Deuterium isotope effects on N-15 backbone chemical shifts in proteins. J Biomol NMR 44:119-126
2. Bertoncini CW, Jung YS, Fernandez CO, Hoyer W, Griesinger C, Jovin TM, Zweckstetter M (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proc Natl Acad Sci USA 102:1430-1435 (Pubitemid 40209187)
3. Bodner CR, Dobson CM, Bax A (2009) Multiple tight phospholipidbinding modes of alpha-synuclein revealed by solution NMR spectroscopy. J Mol Biol 390:775-790
4. Camilloni C, De Simone A, Vranken WF, Vendruscolo M (2012) Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts. Biochemistry 51:2224-2231
5. Cavalli A, Salvatella X, Dobson CM, Vendruscolo M (2007) Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci USA 104:9615-9620 (Pubitemid 47175315)
6. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289-302 (Pubitemid 29143535)
7. De Simone A, Cavalli A, Hsu STD, Vranken W, Vendruscolo M (2009) Accurate random coil chemical shifts from an analysis of loop regions in native states of proteins. J Am Chem Soc 131:16332-16333
8. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRpipe-a multidimensional spectral processing system based on Unix pipes. J Biomol NMR 6:277-293
9. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:197-208 (Pubitemid 40314921)
10. Eghbalnia HR, Wang LY, Bahrami A, Assadi A, Markley JL (2005) Protein energetic conformational analysis from NMR chemical shifts (PECAN) and its use in determining secondary structural elements. J Biomol NMR 32:71-81 (Pubitemid 41086469)
11. Eliezer D, Kutluay E, Bussell R, Browne G (2001) Conformational properties of alpha-synuclein in its free and lipid-associated states. J Mol Biol 307:1061-1073 (Pubitemid 33029953)
12. Gardner KH, Rosen MK, Kay LE (1997) Global folds of highly deuterated, methyl-protonated proteins by multidimensional NMR. Biochemistry 36:1389-1401 (Pubitemid 27074963)
13. Garrett DS, Seok YJ, Liao DI, Peterkofsky A, Gronenborn AM, Clore GM (1997) Solution structure of the 30 kDa N-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system by multidimensional NMR. Biochemistry 36:2517-2530 (Pubitemid 27106644)
14. Goddard TD, Kneller DG (2008) Sparky 3. University of California, San Francisco
15. Griesinger C, Sørensen OW, Ernst RR (1986) Correlation of connected transitions by two-dimensional NMR spectroscopy. J Chem Phys 85:6837-6852
16. Gronenborn AM, Clore GM (1994) Identification of N-terminal helix capping boxes by means of 13C chemical shifts. J Biomol NMR 4:455-458
17. Hyberts SG, Milbradt AG, Wagner AB, Arthanari H, Wagner G (2012) Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional poisson gap scheduling. J Biomol NMR 52:315-327
18. Jameson CJ (1996) Isotope effects on chemical shifts and coupling constants. In: Grant DM, Harris RK (eds) Encyclopedia of nuclear magnetic resonance, vol 4. Wiley, New York, pp 2638-2655
19. Kazimierczuk K, Stanek J, Zawadzka-Kazimierczuk A, Kozminski W (2010) Random sampling in multidimensional NMR spectroscopy. Prog Nucl Magn Reson Spectrosc 57:420-434
20. Kjaergaard M, Brander S, Poulsen FM (2011) Random coil chemical shift for intrinsically disordered proteins: Effects of temperature and pH. J Biomol NMR 49:139-149
21. Lemaster DM (1994) Isotope labeling in solution protein assignment and structural analysis. Prog Nucl Magn Reson Spectrosc 26:371-419
22. Lemaster DM, Laiuppa JC, Kushlan DM (1994) Differential deuterium isotope shifts and one-bond 1H-13C scalar couplings in the conformational analysis of protein glycine residues. J Biomol NMR 4:863-870
23. Maltsev AS, Grishaev A, Bax A (2012a) Monomeric alpha-synuclein binds congo red micelles in a disordered manner. Biochemistry 51:631-642
24. Maltsev AS, Ying JF, Bax A (2012b) Impact of N-terminal acetylation of a-synuclein on its random coil and lipid binding properties. Biochemistry 51:5004-5013
25. Marsh JA, Singh VK, Jia ZC, Forman-Kay JD (2006) Sensitivity of secondary structure propensities to sequence differences between alpha-and gamma-synuclein: Implications for fibrillation. Protein Sci 15:2795-2804 (Pubitemid 44833760)
26. Neal S, Berjanskii M, Zhang HY, Wishart DS (2006) Accurate prediction of protein torsion angles using chemical shifts and sequence homology. Magn Reson Chem 44:S158-S167 (Pubitemid 44090402)
27. Nietlispach D, Clowes RT, Broadhurst RW, Ito Y, Keeler J, Kelly M, Ashurst J, Oschkinat H, Domaille PJ, Laue ED (1996) An approach to the structure determination of larger proteins using triple resonance NMR experiments in conjunction with random fractional deuteration. J Am Chem Soc 118:407-415 (Pubitemid 26050290)
28. Orekhov VY, Ibraghimov I, Billeter M (2003) Optimizing resolution in multidimensional NMR by three-way decomposition. J Biomol NMR 27:165-173 (Pubitemid 37045648)
29. Ottiger M, Bax A (1997) An empirical correlation between amide deuterium isotope effects on C-13(alpha) chemical shifts and protein backbone conformation. J Am Chem Soc 119:8070-8075 (Pubitemid 27380269)
30. Ozenne V, Bauer F, Salmon L, Huang J-r, Jensen MR, Segard S, Bernado P, Charavay C, Blackledge M (2012) Flexible-meccano: A tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 28:1463-1470
31. Peti W, Smith LJ, Redfield C, Schwalbe H (2001) Chemical shifts in denatured proteins: Resonance assignments for denatured ubiquitin and comparisons with other denatured proteins. J Biomol NMR 19:153-165 (Pubitemid 32184443)
32. Rezaei-Ghaleh N, Blackledge M, Zweckstetter M (2012) Intrinsically disordered proteins: From sequence and conformational properties toward drug discovery. Chem Bio Chem 13:930-950
33. RicharzR,WuthrichK(1978)13CNMRchemical shifts ofcommonamino acid residues measured in aqueous solutions of linear tetrapeptides H-GLY-GLY-X-L-ALA-OH. Biopolymers 17:2133-2141 (Pubitemid 9015225)
34. Romero P, Obradovic Z, Li XH, Garner EC, Brown CJ, Dunker AK (2001) Sequence complexity of disordered protein. Proteins Struct Funct Genet 42:38-48
35. Rovnyak D, Frueh DP, Sastry M, Sun ZYJ, Stern AS, Hoch JC, Wagner G (2004) Accelerated acquisition of high resolution triple-resonance spectra using non-uniform sampling and maximum entropy reconstruction. J Magn Reson 170:15-21
36. Schwarzinger S, Kroon GJA, Foss TR, Chung J, Wright PE, Dyson HJ (2001) Sequence-dependent correction of random coil NMR chemical shifts. J Am Chem Soc 123:2970-2978 (Pubitemid 32879567)
37. Shen Y, Bax A (2010) Prediction of Xaa-Pro peptide bond conformation from sequence and chemical shifts. J Biomol NMR 46:199-204
38. Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM, Liu GH, Eletsky A, Wu YB, Singarapu KK, Lemak A, Ignatchenko A, Arrowsmith CH, Szyperski T, Montelione GT, Baker D, Bax A (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci USA 105:4685-4690 (Pubitemid 351753807)
39. 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 44:213-223
40. Tamiola K, Acar B, Mulder FAA (2010) Sequence-specific random coil chemical shifts of intrinsically disordered proteins. J Am Chem Soc 132:18000-18003
41. Uversky VN, Dunker AK (2010) Understanding protein non-folding. BBA-Proteins. Proteomics 1804:1231-1264
42. Venters RA, Farmer BT, Fierke CA, Spicer LD (1996) Characterizing the use of perdeuteration in NMR studies of large proteins C-13, N-15 and H-1 assignments of human carbonic anhydrase II. J Mol Biol 264:1101-1116 (Pubitemid 27019495)
43. Wang YJ, Jardetzky O (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci 11:852-861 (Pubitemid 34241293)
44. Wang Y, Fisher JC, Mathew R, Ou L, Otieno S, Sublet J, Xiao L, Chen J, Roussel MF, Kriwacki RW (2011) Intrinsic disorder mediates the diverse regulatory functions of the Cdk inhibitor p21. Nat Chem Biol 7:214-221
45. Wishart DS, Sykes BD (1994) The C-13 chemical shift index-a simple method for the identification of protein secondary structure using C-13 chemical shift data. J Biomol NMR 4:171-180
46. Wishart DS, Sykes BD, Richards FM (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 222:311-333 (Pubitemid 121004009)
47. Wishart DS, Bigam CG, Holm A, Hodges RS, Sykes BD (1995) 1H, 13C and 15 N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J Biomol NMR 5:67-81
48. Wishart DS, Arndt D, Berjanskii M, Tang P, Zhou J, Lin G (2008) CS23D: A web server for rapid protein structure generation using NMR chemical shifts and sequence data. Nucleic Acids Res 36:496-502
49. Ying JF, Chill JH, Louis JM, Bax A (2007) Mixed-time parallel evolution in multiple quantum NMR experiments: Sensitivity and resolution enhancement in heteronuclear NMR. J Biomol NMR 37:195-204 (Pubitemid 46476997)