What contributions to protein side-chain dynamics are probed by NMR experiments? A molecular dynamics simulation analysis

Journal of Molecular Biology

Volumn 349, Issue 1, 2005, Pages 185-203

  Best, Robert B ^a,d   Clarke, Jane ^a   Karplus, Martin ^b,c  

^a MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

^b UNIVERSITÉ LOUIS PASTEUR   (France)

^c HARVARD UNIVERSITY   (United States)

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

Author keywords

Fibronectin type III; Normal mode analysis; Order parameter; Replica exchange; Side chain dynamics

Indexed keywords

FIBRONECTIN; FIBRONECTIN TYPE 3; SOLVENT; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; DELETION MUTANT; DENSITY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULAR PROBE; MOTION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION; SIMULATION; STATISTICAL ANALYSIS;

EID: 18144378006     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.03.001     Document Type: Article

References (87)

1. F.M. Richards The interpretation of protein structures: total volume, group volume distributions and packing density J. Mol. Biol. 82 1974 1 14
2. Y. Harpaz, M. Gerstein, and C. Chothia Volume changes on protein folding Structure 2 1994 641 649
3. J. Tsai, R. Taylor, C. Chothia, and M. Gerstein The packing density in proteins: standard radii and volumes J. Mol. Biol. 290 1999 253 266
4. B.R. Gelin, and M. Karplus Sidechain torsional potentials and motion of amino acids in proteins: bovine pancreatic trypsin inhibitor Proc. Natl Acad. Sci. USA 72 1975 2002 2006
5. I.D. Campbell, C.M. Dobson, and R.J. Williams Proton magnetic resonance studies of the tyrosine residues of hen lysozyme-assignment and detection of conformational mobility Proc. Roy. Soc. ser. B. 189 1975 503 509
6. K. Wüthrich, and G. Wagner NMR investigations of the dynamics of the aromatic amino acid residues in the basic pancreatic trypsin inhibitor FEBS Letters 50 1975 265 268
7. W.E. Hull, and B.D. Sykes Fluorotyrosine alkaline phosphatase: internal mobility of individual tyrosines and the role of chemical shift anisotropy as a 19F nuclear spin relaxation mechanism in proteins J. Mol. Biol. 98 1976 121 153
8. 13C in the methionine methyl groups J. Biol. Chem. 251 1976 7452 7460
9. R. Richarz, K. Nagayama, and K. Wüthrich Carbon-13 nuclear magnetic resonance relaxation studies of internal mobility of the polypeptide chain in basic pancreatic trypsic inhibitor and a selectively reduced analogue Biochemistry 19 1980 5189 5196
10. 13C NMR spectroscopy. Application to the leucine residues of staphylococcal nuclease Biochemistry 31 1992 5253 5263
11. J.C. Hoch, C.M. Dobson, and M. Karplus Vicinal coupling constants and protein dynamics Biochemistry 24 1985 3831 3841
12. C.M. Dobson, and M. Karplus Internal motion of proteins: nuclear magnetic resonance measurements and dynamic simulations Methods Enzymol. 131 1986 362 389
13. 2H-labelled proteins in solution J. Am. Chem. Soc. 117 1995 11536 11544
14. 2H-enriched proteins in solution J. Am. Chem. Soc. 124 2002 6439 6448
15. N.R. Skrynnikov, O. Millet, and L.E. Kay Deuterium spin probes of side-chain dynamics in proteins. 2. Spectral density mapping and identification of nanosecond time-scale side-chain motions J. Am. Chem. Soc. 124 2002 6449 6460
16. A. Mittermaier, and L.E. Kay The response of internal dynamics to hydrophobic core mutations in the SH3 domain from the Fyn tyrosine kinase Protein Sci. 13 2004 1088 1099
17. M.W. Clarkson, and A.L. Lee Long-range dynamic effects of point mutations propagate through side chains in the serine protease inhibitor eglin c Biochemistry 1 2004 1 11
18. V.A. Goehlert, E. Krupinska, L. Regan, and M.J. Stone Analysis of side-chain mobility among protein G B1 domain mutants with widely varying stabilities Protein Sci. 13 2004 3322 3330
19. L.E. Kay, D.R. Muhandiram, G. Wolf, S.E. Shoelson, and J.D. Forman-Kay Correlation between binding and dynamics at SH2 domain interfaces Nature Struct. Biol. 5 1998 156 163
20. M.M. Chaykovski, L.C. Bae, M.-C. Cheng, J.H. Murray, K.E. Tortolani, and R. Zhang Methyl side-chain dynamics in proteins using selective enrichment with a single isotopomer J. Am. Chem. Soc. 125 2003 15767 15771
21. W.Y. Choy, D. Shortle, and L.E. Kay Side-chain dynamics in unfolded protein states: an NMR based H-2 spin relaxation study of Δ131Δ J. Am. Chem. Soc. 287 2003 1748 1758
22. R.B. Best, T.J. Rutherford, S.M.V. Freund, and J. Clarke Hydrophobic core fluidity of homologous protein domains: relation of side-chain dynamics to core composition and packing Biochemistry 45 2004 1145 1155
23. D. Yang, and L.E. Kay Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding J. Mol. Biol. 263 1996 369 382
24. E.R. Henry, and A. Szabo Influence of vibrational motion on solid state line shapes and NMR relaxation J. Chem. Phys. 82 1985 4753 4761
25. S. Sunada, N. Go, and P. Koehl Calculation of nuclear magnetic resonance order parameters in proteins by normal mode analysis J. Chem. Phys. 104 1996 4768 4775
26. F. Zhang, and R. Brüschweiler Contact model for the prediction of NMR N-H order parameters in globular proteins J. Am. Chem. Soc. 124 2002 12654 12655
27. B. Halle Flexibility and packing in proteins Proc. Natl Acad. Sci. USA. 99 2002 1274 1279
28. A. Mittermaier, L.E. Kay, and J.D. Forman-Kay Analysis of deuterium relaxation-derived methyl axis order parameters and correlation with local structure J. Biomol. NMR 13 1999 181 185
29. D. Ming, and R. Brüschweiler Prediction of methyl-side chain dynamics in proteins J. Biomol. NMR 29 2004 363 368
30. CN couplings J. Am. Chem. Soc. 125 2003 8959 8966
31. R.B. Best, J. Clarke, and M. Karplus The origin of protein side chain order parameter distributions J. Am. Chem. Soc. 126 2004 7734 7735
32. D.A. Case Molecular dynamics and NMR spin relaxation in proteins Accts Chem. Res. 35 2002 325 331
33. 13C NMR relaxation data J. Am. Chem. Soc. 120 1998 5301 5311
34. 2 methyl isotopomers to detect slow conformational changes of protein side chains J. Am. Chem. Soc. 121 1999 11589 11590
35. K.-B. Wong, and V. Daggett Barstar has a highly dynamic hydrophobic core: evidence from molecular dynamics simulations and nuclear magnetic resonance data Biochemistry 37 1998 11182 11192
36. R. Ishima, and D.A. Torchia Protein dynamics from NMR Nature Struct. Biol. 7 2000 740 743
37. N.V. Prabhu, A.L. Lee, A.J. Wand, and K.A. Sharp Dynamics and entropy of a calmodulin-peptide complex studied by NMR and molecular dynamics Biochemistry 42 2003 562 570
38. D.J. Leahy, I. Aukhils, and H.P. Erickson 2.0 Å Crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region Cell 84 1996 155 164
39. C.D. Dickinson, B. Veerapandian, X.-P. Dai, R.C. Hamlin, N.H. Xuong, and E. Ruoslahti Crystal structure of the tenth type III cell adhesion molecule of human fibronectin J. Mol. Biol. 236 1994 1079 1092
40. M. Karplus, T. Ichiye, and B.M. Pettitt Configurational entropy of native proteins Biophys. J. 52 1987 1083 1085
41. A.J. Wand Dynamic activation of protein function: a view emerging from NMR spectroscopy Nature Struct. Biol. 8 2001 926 931
42. D.C. Chatfield, A. Augsten, and C. D'Cunha Correlation times and adiabatic barriers for methyl rotation in Snase J. Biomol. NMR 29 2004 377 385
43. R. Levy, R. Sheridan, J. Keepers, G. Dubey, S. Swaminathan, and M. Karplus Molecular dynamics of myoglobin at 298 degrees K. Results from a 300-ps computer simulation Biophys. J. 48 1985 509 518
44. L. Roland, J. Dunbrack, and F.E. Cohen Bayesian statistical analysis of protein side-chain rotamer preferences Protein Sci. 6 1997 1661 1681
45. R.M. Levy, C.M. Dobson, and M. Karplus Dipolar NMR relaxation of non-protonated aromatic carbons in proteins, structural and dynamical effects Biophys. J. 39 1982 107 113
46. D. Vitkup, D. Ringe, G.A. Petsko, and M. Karplus Solvent mobility and the protein "glass" transition Nature Struct. Biol. 7 2000 34 38
47. B. Brooks, and M. Karplus Normal modes for specific motions of macromolecules: application to the hinge-bending mode of lysozyme Proc. Natl Acad. Sci. USA 82 1985 4995 4999
48. H.W.T. Van Vlijmen, and M. Karplus Analysis of calculated normal modes of a set of native and partially folded proteins J. Phys. Chem. B 103 1999 3009 3021
49. D. Janežiccaron;, R.M. Venable, and B.R. Brooks Harmonic analysis of large systems. III. Comparison with molecular dynamics J. Comput. Chem. 16 1995 1554 1566
50. Y. Zhou, D. Vitkup, and M. Karplus Native proteins are surface-molten solids: application of the Lindemann criterion for the solid versus liquid state J. Mol. Biol. 285 1999 1371 1375
51. G. Lipari, and A. Szabo Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity J. Am. Chem. Soc. 104 1982 4546 4559
52. I. Chadrasekhar, G.M. Clore, A. Szabo, A.M. Gronenborn, and B.R. Brooks A 500 ps molecular dynamics simulation study of interleukin-1β in water: correlation with nuclear magnetic resonance spectroscopy and crystallography J. Mol. Biol. 226 1992 239 250
53. P.A. Carr, H.P. Erickson, and A.G. Palmer III Backbone dynamics of homologous fibronectin type III cell adhesion domains from fibronectin and tenascin Structure 5 1997 949 959
54. J. Chen, C.L. Brooks III, and P.E. Wright Model-free analysis of protein dynamics: assessment of accuracy and model selection protocols based on molecular dynamics simulation J. Biomol. NMR 29 2004 243 257
55. B.R. Brooks, and M. Karplus Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor Proc. Natl Acad. Sci. USA 80 1983 6571 6575
56. D.C. Chatfield, and S.E. Wong Methyl motional parameters in crystalline l-alanine: molecular dynamics simulation and NMR J. Phys. Chem. B 104 1998 11342 11348
57. T. Lazaridis, and M. Karplus Effective energy function for proteins in solution Proteins: Struct. Funct. Genet. 35 1999 133 152
58. Y. Sugita, and Y. Okamoto Replica-exchange molecular dynamics methods for protein folding Chem. Phys. Letters 314 1999 141 151
59. A.L. Lee, K.A. Sharp, J.K. Kranz, X.-J. Song, and A.J. Wand Temperature dependence of the internal dynamics of a calmodulin-peptide complex Biochemistry 41 2002 13814 13825
60. T. Ichiye, and M. Karplus Collective motions in proteins-a covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations Proteins: Struct. Funct. Genet. 11 1991 205 217
61. M. Karplus, and T. Ichiye Fluctuations and cross correlation analysis of protein motions observed in nanosecond molecular dynamics simulations J. Mol. Biol. 263 1996 120 122
62. G.M. Clore, and C.D. Schwieters How much backbone motion in ubiquitin is required to account for dipolar coupling data measured in multiple alignment media as assessed by independent cross-validation? J. Am. Chem. Soc. 126 2004 2923 2938
63. G.M. Clore, and C.D. Schwieters Amplitudes of protein backbone dynamics and correlated motions in a small α/β protein: correspondence of dipolar coupling and heteronuclear relaxation measurements Biochemistry 43 2004 10678 10691
64. D.C. Chatfield, A. Augsten, C. D'Cunha, and S.E. Wong Methyl dynamics in crystalline amino acids: MD and NMR J. Comp. Chem. 24 2003 1052 1058
65. 9k J. Am. Chem. Soc. 115 1993 9832 9833
66. Z. Li, S. Raychaudhuri, and A.J. Wand Insights into the local residual entropy of proteins provided by NMR relaxation Protein Sci. 5 1996 2647 2650
67. J.O. Wrabl, D. Shortle, and T.B. Woolf Correlation between changes in nuclear magnetic resonance order parameters and conformational entropy: molecular dynamics simulations of native and denatured staphyloccal nuclease Proteins: Struct. Funct. Genet. 38 2000 123 133
68. D. Yang, Y.-K. Mok, J.D. Forman-Kay, N.A. Farrow, and L.E. Kay Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation J. Mol. Biol. 272 1997 790 804
69. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
70. A.D. Mackerell Jr, D. Bashford, M. Bellot, R.L. Dunbrack Jr, J.D. Evanseck, and M.J. Field All-atom empirical potential for molecular modeling and dynamics studies of proteins, ff1 J. Phys. Chem. B 102 2000 3586 3616
71. W.L. Jorgensen Revised TIPS for simulations of liquid water and aqueous solutions J. Chem. Phys. 77 1982 4156 4163
72. S.E. Feller, Y. Zhang, R.W. Pastor, and B.R. Brooks Constant pressure molecular dynamics simulation: the Langevin piston method J. Chem. Phys. 103 1995 4613 4621
73. W.L. Jorgensen, and C. Jenson Temperature dependence of TIP3P, SPC, and TIP4P water from NPT Monte Carlo simulations: seeking temperatures of maximum density J. Comput. Chem. 19 1998 1179 1186
74. D.J. Leahy, W.A. Hendrickson, I. Aukhil, and H.P. Erickson Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein Science 258 1992 987 991
75. S.J. Hamill, A.E. Meekhof, and J. Clarke The effect of boundary selection on the stability and folding of the third fibronectin type III domain from human tenascin Biochemistry 37 1998 8071 8079
76. A.E. Meekhof, S.J. Hamill, V.L. Arcus, J. Clarke, and S.M.V. Freund The dependence of chemical exchange on boundary selection in a fibronectin type III domain from human tenascin J. Mol. Biol. 282 1998 181 194
77. A.T. Brünger, and M. Karplus Polar hydrogen positions in proteins; empirical energy placement and neutron diffraction comparison Proteins: Struct. Funct. Genet. 4 1988 148 156
78. H.C. Andersen Molecular dynamics simulations at constant pressure and/or temperature J. Chem. Phys. 72 1980 2384 2393
79. J.P. Ryckaert, G. Cicotti, and H.J.C. Berendsen Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
80. S. Nosé, and M.L. Klein Constant pressure molecular dynamics for molecular systems Mol. Phys. 50 1983 1055 1076
81. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
82. A.E. Garcia, and K.Y. Sanbonmatsu Exploring the energy landscape of a β hairpin in explicit solvent Proteins: Struct. Funct. Genet. 42 2001 345 354
83. B.R. Brooks, D. Janežič, and M. Karplus Harmonic analysis of large systems. I. Methodology J. Comput. Chem 16 1995 1522 1542
84. W. Kabsch A solution for the best rotation to relate two sets of vectors Acta Crystallog. sect. A 32 1997 922 923
85. W. Kabsch A discussion of the solution for the best rotation to relate two sets of vectors Acta Crystallog. sect. A 34 1978 922 923
86. M.P. Allen, and D.J. Tildesley Computer Simulation of Liquids 1st edit. 1989 Oxford Science Publications Oxford
87. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallog. 24 1991 946 950