Accessing ns-μs side chain dynamics in ubiquitin with methyl RDCs

Journal of Biomolecular NMR

Volumn 45, Issue 1-2, 2009, Pages 23-44

  Farès, Christophe ^a,b   Lakomek, Nils Alexander ^a,c   Walter, Korvin F A ^a   Frank, Benedikt T C ^a   Meiler, Jens ^d   Becker, Stefan ^a   Griesinger, Christian ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY HEALTH NETWORK   (Canada)

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

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Concerted motions; Dynamics; Methyl group; RDCs; Side chains; Ubiquitin

Indexed keywords

METHYL GROUP; SOLVENT; UBIQUITIN; BRANCHED CHAIN AMINO ACID; CARBON; NITROGEN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COUPLING FACTOR; HUMAN; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; ALGORITHM; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE; PHYSICAL CHEMISTRY; PROTEIN CONFORMATION; REPRODUCIBILITY;

ALGORITHMS; AMINO ACIDS, BRANCHED-CHAIN; CARBON ISOTOPES; HUMANS; MODELS, CHEMICAL; MODELS, MOLECULAR; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHYSICOCHEMICAL PHENOMENA; PROTEIN CONFORMATION; REPRODUCIBILITY OF RESULTS; SOLVENTS; UBIQUITIN;

EID: 69249213867     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-009-9354-7     Document Type: Article

References (79)

1. Agarwal V, Xue Y, Reif B, Skrynnikov NR (2008) Protein side-chain dynamics as observed by solution- and solid-state NMR spectroscopy: A similarity revealed. J Am Chem Soc 130:16611-16621
2. Bax A, Grishaev A (2005) Weak alignment NMR: A hawk-eyed view of biomolecular structure. Curr Opin Struct Biol 15:563-570
3. Boehr DD, McElheny D, Dyson HJ, Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638-1642
4. Bouvignies G, Bernadó P, Meier S, Cho K, Grzesiek S, Brüschweiler R, Blackledge M (2005) Identification of slow correlated motions in proteins using residual dipolar and hydrogen-bond scalar couplings. Proc Natl Acad Sci USA 102:13885-13890
5. Brath U, Akke M (2009) Differential responses of the backbone and side-chain conformational dynamics in FKBP12 upon binding the transition-state analog FK506: Implications for transition-state stabilization and target protein recognition. J Mol Biol 387:233-244
6. Brath U, Akke M, Yang D, Kay LE, Mulder FAA (2006) Functional dynamics of human FKBP12 revealed by methyl 13C rotating frame relaxation dispersion NMR spectroscopy. J Am Chem Soc 128:5718-5727
7. Chou JJ, Bax A (2001) Protein side-chain rotamers from dipolar couplings in a liquid crystalline phase. J Am Chem Soc 123:3844-3845
8. Chou JJ, Case DA, Bax A (2003) Insights into the mobility of methyl-bearing side chains in proteins from (3)J(CC) and (3)J(CN) couplings. J Am Chem Soc 125:8959-8966
9. Cierpicki T, Bushweller JH (2004) Charged gels as orienting media for measurement of residual dipolar couplings in soluble and integral membrane proteins. J Am Chem Soc 126:16259-16266
10. Clore GM, Schwieters CD (2004) Amplitudes of protein backbone dynamics and correlated motions in a small alpha/beta protein: Correspondence of dipolar coupling and heteronuclear relaxation measurements. Biochemistry 43:10678-10691
11. Clore GM, Schwieters CD (2006) Concordance of residual dipolar couplings, backbone order parameters and crystallographic B-factors for a small alpha/beta protein: A unified picture of high probability, fast atomic motions in proteins. J Mol Biol 355:879-886
12. Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120:6836-6837
13. Davis IW, Arendall WB, Richardson DC, Richardson JS (2006) The backrub motion: How protein backbone shrugs when a sidechain dances. Structure 14:265-274
14. Dunbrack RL, Karplus M (1993) Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J Mol Biol 230:543-574
15. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121
16. Flynn PF, Bieber Urbauer RJ, Zhang H, Lee AL, Wand AJ (2001) Main chain and side chain dynamics of a heme protein: 15N and 2H NMR relaxation studies of R. capsulatus ferrocytochrome c2. Biochemistry 40:6559-6569
17. Frederick KK, Kranz JK, Wand AJ (2006) Characterization of the backbone and side chain dynamics of the CaM-CaMKIp complex reveals microscopic contributions to protein conformational entropy. Biochemistry 45:9841-9848
18. Friedland GD, Linares AJ, Smith CA, Kortemme T (2008) A simple model of backbone flexibility improves modeling of side-chain conformational variability. J Mol Biol 380:757-774
19. Friedland GD, Lakomek N, Griesinger C, Meiler J, Kortemme T (2009) A correspondence between solution-state dynamics of an individual protein and the sequence and conformational diversity of its family. PLoS Comput Biol 5:e1000393
20. Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450:913-916
21. Ho BK, Agard DA (2009) Probing the flexibility of large conformational changes in protein structures through local perturbations. PLoS Comput Biol 5:e1000343
22. Houben K, Boelens R (2004) Side chain dynamics monitored by 13C-13C cross-relaxation. J Biomol NMR 29:151-166
23. Hus J, Brüschweiler R (2002) Principal component method for assessing structural heterogeneity across multiple alignment media. J Biomol NMR 24:123-132
24. Hus J, Peti W, Griesinger C, Brüschweiler R (2003) Self-consistency analysis of dipolar couplings in multiple alignments of ubiquitin. J Am Chem Soc 125:5596-5597
25. Igumenova TI, Frederick KK, Wand AJ (2006) Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution. Chem Rev 106:1672-1699
26. Janin J, Wodak S, Levitt M, Maigret B (1978) Conformation of amino-acid side-chains in proteins. J Mol Biol 125:357-386
27. Johnson EC, Lazar GA, Desjarlais JR, Handel TM (1999) Solution structure and dynamics of a designed hydrophobic core variant of ubiquitin. Structure 7:967-976
28. Kay LE (1998) Protein dynamics from NMR. Nat Struct Biol 5(Suppl):513-517
29. Kay LE, Torchia DA, Bax A (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28:8972-8979
30. Kontaxis G, Bax A (2001) Multiplet component separation for measurement of methyl C-13-H-1 dipolar couplings in weakly aligned proteins. J Biomol NMR 20:77-82
31. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graph 14(51-55):29-32
32. Korzhnev DM, Kloiber K, Kanelis V, Tugarinov V, Kay LE (2004) Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: Application to a 723-residue enzyme. J Am Chem Soc 126:3964-3973
33. Lakomek NA, Farès C, Becker S, Carlomagno T, Meiler J, Griesinger C (2005) Side-chain orientation and hydrogen-bonding imprint supra-Tau(c) motion on the protein backbone of ubiquitin. Angew Chem Int Ed Engl 44:7776-7778
34. Lakomek NA, Carlomagno T, Becker S, Griesinger C, Meiler J (2006) A thorough dynamic interpretation of residual dipolar couplings in ubiquitin. J Biomol NMR 34:101-115
35. Lakomek NA, Walter KF, Fares C, Lange OF, de Groot BL, Grubmuller H, Bruschweiler R, Munk A, Becker S, Meiler J, Griesinger C (2008a) Self-consistent residual dipolar coupling based model-free analysis for the robust determination of nanosecond to microsecond protein dynamics. J Biomol NMR 41:139-155
36. Lakomek NA, Lange OF, Walter KF, Farès C, Egger D, Lunkenheimer P, Meiler J, Grubmuller H, Becker S, de Groot BL, Griesinger C (2008b) Residual dipolar couplings as a tool to study molecular recognition of ubiquitin. Biochem Soc Trans 36:1433-1437
37. Lange OF, Lakomek NA, Farès C, Schroder GF, Walter KF, Becker S, Meiler J, Grubmuller H, Griesinger C, de Groot BL (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320:1471-1475
38. Lee AL, Flynn PF, Wand AJ (1999) Comparison of 2H and 13C NMR relaxation techniques for the study of protein methyl group dynamics in solution. J Am Chem Soc 121:2891-2902
39. Lee AL, Kinnear SA, Wand AJ (2000) Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex. Nat Struct Biol 7:72-77
40. LeMaster DM (1999) NMR relaxation order parameter analysis of the dynamics of protein side chains. J Am Chem Soc 121:1726-1742
41. LeMaster DM, Kushlan DM (1996) Dynamical mapping of E. coli thioredoxin via 13C NMR relaxation analysis. J Am Chem Soc 118:9255-9264
42. Li D, Brüschweiler R (2009) A dictionary for protein side-chain entropies from NMR order parameters. J Am Chem Soc 131:7226-7227
43. Lindorff-Larsen K, Best RB, Depristo MA, Dobson CM, Vendruscolo M (2005) Simultaneous determination of protein structure and dynamics. Nature 433:128-132
44. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104:4546-4559
45. Lorieau JL, McDermott AE (2006) Conformational flexibility of a microcrystalline globular protein: Order parameters by solid-state NMR spectroscopy. J Am Chem Soc 128:11505-11512
46. Lorieau JL, Day LA, McDermott AE (2008) Conformational dynamics of an intact virus: Order parameters for the coat protein of Pf1 bacteriophage. Proc Natl Acad Sci USA 105:10366-10371
47. Mandel AM, Akke M, Palmer AG (1996) Dynamics of ribonuclease H: temperature dependence of motions on multiple time scales. Biochemistry 35:16009-16023
48. Markwick PRL, Bouvignies G, Blackledge M (2007) Exploring multiple timescale motions in protein GB3 using accelerated molecular dynamics and NMR spectroscopy. J Am Chem Soc 129:4724-4730
49. Meiler J, Blomberg N, Nilges M, Griesinger C (2000) A new approach for applying residual dipolar couplings as restraints in structure elucidation. J Biomol NMR 16:245-252
50. Meiler J, Prompers JJ, Peti W, Griesinger C, Bruschweiler R (2001) Model-free approach to the dynamic interpretation of residual dipolar couplings in globular proteins. J Am Chem Soc 123:6098-6107
51. Meirovitch E, Polimeno A, Freed JH (2006) Methyl dynamics in proteins from NMR slowly relaxing local structure spin relaxation analysis: A new perspective. J Phys Chem B 110:20615-20628
52. Millet O, Mittermaier A, Baker D, Kay LE (2003) The effects of mutations on motions of side-chains in protein L studied by 2H NMR dynamics and scalar couplings. J Mol Biol 329:551-563
53. Ming D, Brüschweiler R (2004) Prediction of methyl-side chain dynamics in proteins. J Biomol NMR 29:363-368
54. Mittermaier A, Kay LE (2001) Chi1 torsion angle dynamics in proteins from dipolar couplings. J Am Chem Soc 123:6892-6903
55. Mittermaier A, Kay LE (2002) Effect of deuteration on some structural parameters of methyl groups in proteins as evaluated by residual dipolar couplings. J Biomol NMR 23:35-45
56. Mittermaier A, Kay LE, Forman-Kay JD (1999) Analysis of deuterium relaxation-derived methyl axis order parameters and correlation with local structure. J Biomol NMR 13:181-185
57. Mulder FA, Hon B, Mittermaier A, Dahlquist FW, Kay LE (2002) Slow internal dynamics in proteins: Application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme. J Am Chem Soc 124:1443-1451
58. Ottiger M, Bax A (1998) Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules. J Biomol NMR 12:361-372
59. Ottiger M, Bax A (1999) How tetrahedral are methyl groups in proteins? A liquid crystal NMR study. J Am Chem Soc 121:4690-4695
60. Palmer AG, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339:204-238
61. Reif B, Xue Y, Agarwal V, Pavlova MS, Hologne M, Diehl A, Ryabov YE, Skrynnikov NR (2006) Protein side-chain dynamics observed by solution- and solid-state NMR: Comparative analysis of methyl 2H relaxation data. J Am Chem Soc 128:12354-12355
62. Richter B, Gsponer J, Várnai P, Salvatella X, Vendruscolo M (2007) The MUMO (minimal under-restraining minimal over-restraining) method for the determination of native state ensembles of proteins. J Biomol NMR 37:117-135
63. Salmon L, Bouvignies G, Markwick P, Lakomek N, Showalter S, Li D, Walter K, Griesinger C, Brüschweiler R, Blackledge M (2009) Protein conformational flexibility from structure-free analysis of NMR dipolar couplings: Quantitative and absolute determination of backbone motion in ubiquitin. Angew Chem Int Ed Engl 48:4154-4157
64. Schindler H, Seelig J (1975) Deuterium order parameters in relation to thermodynamic properties of a phospholipid bilayer. A statistical mechanical interpretation. Biochemistry 14:2283-2287
65. Schneider DM, Dellwo MJ, Wand AJ (1992) Fast internal main-chain dynamics of human ubiquitin. Biochemistry 31:3645-3652
66. Seelig J (1977) Deuterium magnetic resonance: Theory and application to lipid membranes. Q Rev Biophys 10:353-418
67. Shajani Z, Varani G (2005) 13C NMR relaxation studies of RNA base and ribose nuclei reveal a complex pattern of motions in the RNA binding site for human U1A protein. J Am Chem Soc 349:699-715
68. Showalter SA, Johnson E, Rance M, Brüschweiler R (2007) Toward quantitative interpretation of methyl side-chain dynamics from NMR by molecular dynamics simulations. J Am Chem Soc 129:14146-14147
69. Skrynnikov NR, Mulder FA, Hon B, Dahlquist FW, Kay LE (2001) Probing slow time scale dynamics at methyl-containing side chains in proteins by relaxation dispersion NMR measurements: Application to methionine residues in a cavity mutant of T4 lysozyme. J Am Chem Soc 123:4556-4566
70. Tolman JR (2001) Dipolar couplings as a probe of molecular dynamics and structure in solution. Curr Opin Struct Biol 11:532-539
71. Tolman JR (2009) News and views: Protein dynamics from disorder. Nature 459:1063-1064
72. Tugarinov V, Kay LE (2005) Methyl groups as probes of structure and dynamics in NMR studies of high-molecular-weight proteins. Chembiochem 6:1567-1577
73. Tugarinov V, Kay LE (2006) A 2H NMR relaxation experiment for the measurement of the time scale of methyl side-chain dynamics in large proteins. J Am Chem Soc 128:12484-12489
74. Wang L, Pang Y, Holder T, Brender JR, Kurochkin AV, Zuiderweg ER (2001) Functional dynamics in the active site of the ribonuclease binase. Proc Natl Acad Sci USA 98:7684-7689
75. Xue Y, Pavlova MS, Ryabov YE, Reif B, Skrynnikov NR (2007) Methyl rotation barriers in proteins from 2H relaxation data. Implications for protein structure. J Am Chem Soc 129:6827-6838
76. Yao L, Vögeli B, Ying J, Bax A (2008) NMR determination of amide N-h equilibrium bond length from concerted dipolar coupling measurements. J Am Chem Soc 130:16518-16520
77. Zhang Q, Sun X, Watt ED, Al-Hashimi HM (2006) Resolving the motional modes that code for RNA adaptation. Science 311:653-656
78. Zhang Q, Stelzer AC, Fisher CK, Al-Hashimi HM (2007) Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 450:1263-1267
79. Zweckstetter M, Bax A (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J Am Chem Soc 122:3791-3792