A maximum entropy approach to the study of residue-specific backbone angle distributions in α-synuclein, an intrinsically disordered protein

Protein Science

Volumn 23, Issue 9, 2014, Pages 1275-1290

  Mantsyzov, Alexey B ^a   Maltsev, Alexander S ^a   Ying, Jinfa ^a   Shen, Yang ^a   Hummer, Gerhard ^a,b   Bax, Ad ^a  

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

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Diffusion anisotropy; Intrinsically disordered proteins; Karplus curve; Random coil; Shortrange NOE

Indexed keywords

ALPHA SYNUCLEIN;

CHEMISTRY; ENTROPY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE;

ALPHA-SYNUCLEIN; ENTROPY; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84906850422     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2511     Document Type: Article

References (94)

1. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, Tantos A, Szabo B, Tompa P, Chen J, Uversky VN, Obradovic Z, Dunker AK (2007) DisProt: The database of disordered proteins. Nucleic Acid Res 35:D786- D793.
2. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41:6573-6582.
3. Csizmok V, Felli IC, Tompa P, Banci L, Bertini I (2008) Structural and dynamic characterization of intrinsically disordered human securin by NMR spectroscopy. J Am Chem Soc 130:16873-16879.
4. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208.
5. Shi ZS, Chen K, Liu ZG, Kallenbach NR (2006) Conformation of the backbone in unfolded proteins. Chem Rev 106:1877-1897.
6. Makowska J, Rodziewicz-Motowidlo S, Baginska K, Vila JA, Liwo A, Chmurzynski L, Scheraga HA (2006) Polyproline II conformation is one of many local conformational states and is not an overall conformation of unfolded peptides and proteins. Proc Natl Acad Sci U S A 103:1744-1749.
7. Dyson HJ, Wright PE (1991) Defining solution conformations of small linear peptides. Ann Rev Biophys Biophys Chem 20:519-538.
8. Baldwin RL, Rose GD (1999) Is protein folding hierarchic? I. Local structure and peptide folding. Trends Biochem Sci 24:26-33.
9. Smith LJ, Bolin KA, Schwalbe H, MacArthur MW, Thornton JM, Dobson CM (1996) Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J Mol Biol 255:494-506.
10. Graf J, Nguyen PH, Stock G, Schwalbe H (2007) Structure and dynamics of the homologous series of alanine peptides: A joint molecular dynamics/NMR study. J Am Chem Soc 129:1179-1189.
11. Hagarman A, Measey TJ, Mathieu D, Schwalbe H, Schweitzer-Stenner R (2010) Intrinsic propensities of amino acid residues in GxG peptides inferred from amide I ' band profiles and NMR scalar coupling constants. J Am Chem Soc 132:540-551.
12. Long HW, Tycko R (1998) Biopolymer conformational distributions from solid-state NMR: Alpha-helix and 3(10)-helix contents of a helical peptide. J Am Chem Soc 120:7039-7048.
13. Chiti F, Dobson CM (2006). Protein misfolding, functional amyloid, and human disease. Ann Rev Biochem 75:333-366.
14. Dyson HJ, Wright PE (2004) Unfolded proteins and protein folding studied by NMR. Chem Rev 104:3607- 3622.
15. 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.
16. Bodner CR, Dobson CM, Bax A (2009) Multiple tight phospholipid-binding modes of alpha-synuclein revealed by solution NMR spectroscopy. J Mol Biol 390: 775-790.
17. 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.
18. 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.
19. Maltsev AS, Ying JF, Bax A (2012) Impact of N-terminal acetylation of a-synuclein on its random coil and lipid binding properties. Biochemistry 51:5004-5013.
20. 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 U S A 102:1430-1435.
21. Bernado P, Bertoncini CW, Griesinger C, Zweckstetter M, Blackledge M (2005) Defining long-range order and local disorder in native alpha-synuclein using residual dipolar couplings. J Am Chem Soc 127:7968-17969.
22. Allison JR, Varnai P, Dobson CM, Vendruscolo M (2009) Determination of the free energy landscape of alpha-synuclein using spin label nuclear magnetic resonance measurements. J Am Chem Soc 131:18314- 18326.
23. Paleologou KE, Schmid AW, Rospigliosi CC, Kim HY, Lamberto GR, Fredenburg RA, Lansbury PT, Fernandez CO, Eliezer D, Zweckstetter M, Lashuel HA (2008) Phosphorylation at Ser-129 but not the phosphomimics S129E/D inhibits the fibrillation of alpha-synuclein. J Biol Chem 283:16895-16905.
24. Wu KP, Weinstock DS, Narayanan C, Levy RM, Baum J (2009) Structural reorganization of alpha-synuclein at low pH observed by NMR and REMD simulations. J Mol Biol 391:784-796.
25. Pashley CL, Morgan GJ, Kalverda AP, Thompson GS, Kleanthous C, Radford SE (2012) Conformational properties of the unfolded state of Im7 in nondenaturing conditions. J Mol Biol 416:300-318.
26. 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.
27. Salmon L, Nodet G, Ozenne V, Yin GW, Jensen MR, Zweckstetter M, Blackledge M (2010) NMR characterization of long-range order in intrinsically disordered proteins. J Am Chem Soc 132:8407-8418.
28. Tamiola K, Mulder FAA (2012) Using NMR chemical shifts to calculate the propensity for structural order and disorder in proteins. Biochem Soc Trans 40:1014- 1020.
29. 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.
30. Nodet G, Salmon L, Ozenne V, Meier S, Jensen MR, Blackledge M (2009) Quantitative description of backbone conformational sampling of unfolded proteins at amino acid resolution from NMR residual dipolar couplings. J Am Chem Soc 131:17908-17918.
31. Sziegat F, Silvers R, Haehnke M, Jensen MR, Blackledge M, Wirmer-Bartoschek J, Schwalbe H (2012) Disentangling the coil: modulation of conformational and dynamic properties by site-directed mutation in the non-native state of hen egg white lysozyme. Biochemistry 51:3361-3372.
32. Choy WY, Forman-Kay JD (2001) Calculation of ensembles of structures representing the unfolded state of an SH3 domain. J Mol Biol 308:1011-1032.
33. Krzeminski M, Marsh JA, Neale C, Choy W-Y, Forman-Kay JD (2013) Characterization of disordered proteins with ENSEMBLE. Bioinformatics 29:398-399.
34. Marsh JA, Forman-Kay JD (2012) Ensemble modeling of protein disordered states: experimental restraint contributions and validation. Proteins 80:556-572.
35. Marsh JA, Teichmann SA, Forman-Kay JD (2012) Probing the diverse landscape of protein flexibility and binding. Curr Opin Struct Biol 22:643-650.
36. Feldman HJ, Hogue CWV (2000) A fast method to sample real protein conformational space. Proteins 39:112- 131.
37. Varadi M, Kosol S, Lebrun P, Valentini E, Blackledge M, Dunker AK, Felli IC, Forman-Kay JD, Kriwacki RW, Pierattelli R, Sussman J, Svergun DI, Uversky VN, Vendruscolo M, Wishart D, Wright PE, Tompa P (2014) pE-DB: A database of structural ensembles of intrinsically disordered and of unfolded proteins. Nucleic Acids Res 42:D326-D335.
38. Louhivuori M, Paakkonen K, Fredriksson K, Permi P, Lounila J, Annila A (2003) On the origin of residual dipolar couplings from denatured proteins. J Am Chem Soc 125:15647-15650.
39. Dames SA, Aregger R, Vajpai N, Bernado P, Blackledge M, Grzesiek S (2006) Residual dipolar couplings in short peptides reveal systematic conformational preferences of individual amino acids. J Am Chem Soc 128: 13508-13514.
40. Meier S, Blackledge M, Grzesiek S (2008) Conformational distributions of unfolded polypeptides from novel NMR techniques. J Chem Phys 128:052204.
41. Obolensky OI, Schlepckow K, Schwalbe H, Solov'yov AV (2007) Theoretical framework for NMR residual dipolar couplings in unfolded proteins. J Biomol NMR 39:1-16.
42. Fawzi NL, Phillips AH, Ruscio JZ, Doucleff M, Wemmer DE, Head-Gordon T (2008) Structure and dynamics of the A ss(21-30) peptide from the interplay of NMR experiments and molecular simulations. J Am Chem Soc 130:6145-6158.
43. Ball KA, Phillips AH, Nerenberg PS, Fawzi NL, Wemmer DE, Head-Gordon T (2011) Homogeneous and heterogeneous tertiary structure ensembles of amyloidbeta peptides. Biochemistry 50:7612-7628.
44. Bruun SW, Iesmantavicius V, Danielsson J, Poulsen FM (2010) Cooperative formation of native-like tertiary contacts in the ensemble of unfolded states of a four-helix protein. Proc Natl Acad Sci U S A 107:13306-13311.
45. Marsh JA, Neale C, Jack FE, Choy W-Y, Lee AY, Crowhurst KA, Forman-Kay JD (2007) Improved structural characterizations of the drkN SH3 domain unfolded state suggest a compact ensemble with native-like and non-native structure. J Mol Biol 367: 1494-1510.
46. Gillespie JR, Shortle D (1997) Characterization of longrange structure in the denatured state of staphylococcal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures. J Mol Biol 268:170-184.
47. Dedmon MM, Lindorff-Larsen K, Christodoulou J, Vendruscolo M, Dobson CM (2005) Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 127:476-477.
48. Francis CJ, Lindorff-Larsen K, Best RB, Vendruscolo M (2006) Characterization of the residual structure in the unfolded state of the Delta 131 Delta fragment of staphylococcal nuclease. Proteins 65:145-152.
49. Esteban-Martin S, Silvestre-Ryan J, Bertoncini CW, Salvatella X (YEAR) Identification of fibril-Like tertiary contacts in soluble monomeric alpha-synuclein. Biophys J 105:1192-1198.
50. Peter C, Daura X, van Gunsteren WF (2001) Calculation of NMR-relaxation parameters for flexible molecules from molecular dynamics simulations. J Biomol NMR 20:297-310.
51. Eker F, Griebenow K, Cao XL, Nafie LA, Schweitzer- Stenner R (2004) Preferred peptide backbone conformations in the unfolded state revealed by the structure analysis of alanine-based (AXA) tripeptides in aqueous solution. Proc Natl Acad Sci U S A 101:10054-10059.
52. Schweitzer-Stenner R (2009) Distribution of conformations sampled by the central amino acid residue in tripeptides inferred from amide I band profiles and NMR scalar coupling constants. J Phys Chem B 113:2922- 2932.
53. Zagrovic B, Lipfert J, Sorin EJ, Millett IS, van Gunsteren WF, Doniach S, Pande VS (2005) Unusual compactness of a polyproline type II structure. Proc Natl Acad Sci U S A 102:11698-11703.
54. Shi ZS, Chen K, Liu ZG, Ng A, Bracken WC, Kallenbach NR (2005) Polyproline II propensities from GGXGG peptides reveal an anticorrelation with betasheet scales. Proc Natl Acad Sci U S A 102:17964- 17968.
55. Fitzkee NC, Fleming PJ, Rose GD (2005) The protein coil library: A structural database of nonhelix, nonstrand fragments derived from the PDB. Proteins 58: 852-854.
56. Ozenne V, Schneider R, Yao M, Huang J-R, Salmon L, Zweckstetter M, Jensen MR, Blackledge M (2012) Mapping the potential energy landscape of intrinsically disordered proteins at amino acid resolution. J Am Chem Soc 134:15138-15148.
57. Kragelj J, Ozenne V, Blackledge M, Jensen MR (2013) Conformational propensities of intrinsically disordered proteins from NMR chemical shifts. ChemPhysChem 14:3034-3045.
58. Rozycki B, Kim YC, Hummer G (2011) SAXS ensemble refinement of ESCRT-III CHMP3 conformational transitions. Structure 19:109-116.
59. Vogeli B, Ying JF, Grishaev A, Bax A (2007) Limits on variations in protein backbone dynamics from precise measurements of scalar couplings. J Am Chem Soc 129:9377-9385.
60. Maltsev AS, Grishaev A, Roche J, Zasloff M, Bax A (2014) Improved cross validation of a static ubiquitin structure derived from high precision residual dipolar couplings measured in a drug-based liquid crystalline phase. J Am Chem Soc 136:3752-3755.
61. Vuister GW, Delaglio F, Bax A (1993) The use of 1JCaHa coupling constants as a probe for protein backbone conformation. J Biomol NMR 3:67-80.
62. Vuister GW, Delaglio F, Bax A (1992) An empirical correlation between 1J(CaHa) and protein backbone conformation. J Am Chem Soc 114:9674-9675.
63. Ding KY, Gronenborn AM (2004) Protein backbone H- 1(N)-C-13(alpha) and N-15-C-13(alpha) residual dipolar and J couplings: new constraints for NMR structure determination. J Am Chem Soc 126:6232-6233.
64. Delaglio F, Torchia DA, Bax A (1991) Measurement of 15N-13C J couplings in staphylococcal nuclease. J Biomol NMR 1:439-446.
65. Wirmer J, Schwalbe H (2002) Angular dependence of (1)J(N-i, C-alpha i) and (2)J(N-i, C alpha(i-1)) coupling constants measured in J-modulated HSQCs. J Biomol NMR 23:47-55.
66. Schmidt JM, Hua Y, Loehr F (2010) Correlation of (2)J couplings with protein secondary structure. Proteins 78:1544-1562.
67. Shen Y, Bax A (2013) Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J Biomol NMR 56:227-241.
68. Shen Y, Bax A (2007) Protein backbone chemical shifts predicted from searching a database for torsion angle and sequence homology. J Biomol NMR 38:289-302.
69. Bussell R, Eliezer D (2001) Residual structure and dynamics in Parkinson's disease-associated mutants of alpha-synuclein. J Biol Chem 276:45996-46003.
70. Wu K-P, Baum J (YEAR) Backbone assignment and dynamics of human alpha-synuclein in viscous 2 M glucose solution. Biomol NMR Assign 5:43-46.
71. Farrow NA, Zhang OW, Szabo A, Torchia DA, Kay LE (1995) Spectral density-function mapping using N-15 relaxation data exclusively. J Biomol NMR 6:153-162.
72. Ikura M, Bax A, Clore GM, Gronenborn AM (1990) Detection of nuclear Overhauser effects between degenerate amide proton resonances by heteronuclear threedimensional nuclear magnetic resonance spectroscopy. J Am Chem Soc 112:9020-9022.
73. Cavanagh J, Fairbrother WJ, Palmer AG, Rance M, Skelton N (2007) Protein NMR spectroscopy: principles and practice, 2nd ed. Burlington, MA: Elsevier Academic Press.
74. Lienin SF, Bremi T, Brutscher B, Bruschweiler R, Ernst RR (1998) Anisotropic intramolecular backbone dynamics of ubiquitin characterized by NMR relaxation and MD computer simulation. J Am Chem Soc 120: 9870-9879.
75. Gagne SM, Tsuda S, Li MX, Chandra M, Smillie LB, Sykes BD (1994) Quantification of the calcium-induced secondary structural changes in the regulatory domain of troponin-C. Protein Sci 3:1961-1974.
76. Ying J, Roche J, Bax A (2014) Homonuclear decoupling for enhancing resolution and sensitivity in NOE and RDC measurements of peptides and proteins. J Magn Reson 241:97-102.
77. Mukrasch MD, Markwick P, Biernat J, von Bergen M, Bernado P, Griesinger C, Mandelkow E, Zweckstetter M, Blackledge M (2007) Highly populated turn conformations in natively unfolded Tau protein identified from residual dipolar couplings and molecular simulation. J Am Chem Soc 129:5235-5243.
78. Wirmer J, Peti W, Schwalbe H (2006) Motional properties of unfolded ubiquitin: A model for a random coil protein. J Biomol NMR 35:175-186.
79. Kay LE, Keifer P, Saarinen T (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114:10663-10665.
80. Lakomek NA, Ying JF, Bax A (2012) Measurement of 15N relaxation rates in perdeuterated proteins by TROSY-based methods J Biomol NMR 53:209-221.
81. Favier A, Brutscher B (2011) Recovering lost magnetization: polarization enhancement in biomolecular NMR. J Biomol NMR 49:9-15.
82. 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.
83. 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.
84. Goddard TD, Kneller DG (2008) Sparky 3, University of California, San Francisco.
85. Yao L, Vogeli B, Torchia DA, Bax A (2008) Simultaneous NMR study of protein structure and dynamics using conservative mutagenesis. J Phys Chem B 112:6045-6056.
86. Shen Y, Bax A (2010) SPARTA plus: A modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network. J Biomol NMR 48:13-22.
87. Best RB, Hummer G (2009) Optimized molecular dynamics force fields applied to the helix-coil transition of polypeptides. J Phys Chem B 113:9004-9015.
88. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
89. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: Algorithms for highly efficient, loadbalanced, and scalable molecular simulation. J Chem Theory Comput 4:435-447.
90. Wang JM, Cieplak P, Kollman PA (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 21:1049- 1074.
91. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C (2006) Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins 65:712-725.
92. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE (2010) Improved sidechain torsion potentials for the Amber ff99SB protein force field. Proteins 78:1950-1958.
93. Parrinello M, Rahman A (1980) Crystal structure and pair potentials-a molecular dynamics study. Phys Rev Lett 45:1196-1199.
94. Darden T, York D, Pedersen L (1993) Particle Mesh Ewald-an N.log(N) method for Ewald sums in large systems. J Chem Phys 98:10089-10092.