Detection of nanosecond time scale side-chain jumps in a protein dissolved in water/glycerol solvent

Journal of Biomolecular NMR

Volumn 45, Issue 1-2, 2009, Pages 57-72

  Xu, Jun ^a   Xue, Yi ^a   Skrynnikov, Nikolai R ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

ketoisovalerate labeling; Spectrin SH3 domain; Backbone 15N and methyl 13C relaxation; Extended Lipari Szabo model; Preferential hydration; Solvent slaving

Indexed keywords

FODRIN; GLYCEROL; LEUCINE; NITROGEN 15; PROTEIN SH3; VALINE; WATER;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISSOLUTION; HYDRATION; ISOTOPE LABELING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; SOLVATION; SOLVENT EFFECT; VISCOSITY;

ANIMALS; CARBON ISOTOPES; CHICKENS; GLYCEROL; LEUCINE; MODELS, CHEMICAL; MODELS, STATISTICAL; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS; REPRODUCIBILITY OF RESULTS; SPECTRIN; SRC HOMOLOGY DOMAINS; VALINE; WATER;

EID: 69249206528     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-009-9336-9     Document Type: Article

References (86)

1. Agarwal V, Reif B (2008) Residual methyl protonation in perdeuterated proteins for multi-dimensional correlation experiments in MAS solid-state NMR spectroscopy. J Magn Reson 194:16-24
2. 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
3. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest, 267-281
4. Albertyn J, Hohmann S, Thevelein JM, Prior BA (1994) Gpd1, which encodes gycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14:4135-4144
5. Allison SA, Tran VT (1995) Modeling the electrophoresis of rigid polyions - application to lysozyme. Biophys J 68:2261-2270
6. 2H NMR. Proc Natl Acad Sci USA 79:386-389
7. Baynes BM, Trout BL (2003) Proteins in mixed solvents: A molecular-level perspective. J Phys Chem B 107:14058-14067
8. Ben-Amotz A, Avron M (1973) The role of glycerol in osmotic regulation of the halophilic alga Dunaliella Parva. Plant Physiol 51:875-878
9. Best RB, Clarke J, Karplus M (2005) What contributions to protein side-chain dynamics are probed by NMR experiments? A molecular dynamics simulation analysis. J Mol Biol 349:185-203
10. Betting H, Häckel M, Hinz HJ, Stockhausen M (2001) Spectroscopic evidence for the preferential hydration of RNase a in glycerol-water mixtures: Dielectric relaxation studies. Phys Chem Chem Phys 3:1688-1692
11. Bizzarri AR, Cannistraro S (2002) Molecular dynamics of water at the protein-solvent interface. J Phys Chem B 106:6617-6633
12. 15N NMR assignment and solution structure of the SH3 domain of spectrin: comparison of unrefined and refined structure sets with the crystal structure. J Biomol NMR 9:347-357
13. Burnham KP, Anderson DR (2002) Model selection and multimodel interference: A practical information-theoretic approach. Springer, New York
14. Butler SL, Falke JJ (1996) Effects of protein stabilizing agents on thermal backbone motions: A disulfide trapping study. Biochemistry 35:10595-10600
15. Caliskan G, Mechtani D, Roh JH, Kisliuk A, Sokolov AP, Azzam S, Cicerone MT, Lin-Gibson S, Peral I (2004) Protein and solvent dynamics: How strongly are they coupled? J Chem Phys 121:1978-1983
16. Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420:98-102
17. Charron C, Kadri A, Robert MC, Giege R, Lorber B (2002) Crystallization in the presence of glycerol displaces water molecules in the structure of thaumatin. Acta Crystallogr D Biol Crystallogr 58:2060-2065
18. Chemical Rubber Company (1948) Handbook of chemistry and physics. Chemical Rubber Publishing, Cleveland
19. Chen JH, Brooks CL, Wright PE (2004) Model-free analysis of protein dynamics: Assessment of accuracy and model selection protocols based on molecular dynamics simulation. J Biomol NMR 29:243-257
20. Chevelkov V, Faelber K, Diehl A, Heinemann U, Oschkinat H, Reif B (2005) Detection of dynamic water molecules in a microcrystalline sample of the SH3 domain of α-spectrin by MAS solid-state NMR. J Biomol NMR 31:295-310
21. 15N relaxation data from solid- and solution-state NMR spectroscopy. J Am Chem Soc 129:12594-12595
22. Clarkson MW, Lee AL (2004) Long-range dynamic effects of point mutations propagate through side chains in the serine protease inhibitor eglin c. Biochemistry 43:12448-12458
23. Clore GM, Driscoll PC, Wingfield PT, Gronenborn AM (1990a) Analysis of the backbone dynamics of interleukin 1β using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy. Biochemistry 29:7387-7401
24. 15N nuclear magnetic relaxation of proteins. J Am Chem Soc 112:4989-4991
25. Cole R, Loria JP (2003) FAST-modelfree: A program for rapid automated analysis of solution NMR spin-relaxation data. J Biomol NMR 26:203-213
26. Cornilescu G, Bax A (2000) Measurement of proton, nitrogen, and carbonyl chemical shielding anisotropies in a protein dissolved in a dilute liquid crystalline phase. J Am Chem Soc 122:10143-10154
27. Courtenay ES, Capp MW, Anderson CF, Record MT (2000) Vapor pressure osmometry studies of osmolyte-protein interactions: Implications for the action of osmoprotectants in vivo and for the interpretation of "osmotic stress" experiments in vitro. Biochemistry 39:4455-4471
28. Dastidar SG, Mukhopadhyay C (2003) Structure, dynamics, and energetics of water at the surface of a small globular protein: A molecular dynamics simulation. Phys Rev E 68
29. de la Torre JG, Huertas ML, Carrasco B (2000a) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J 78:719-730
30. de la Torre JG, Huertas ML, Carrasco B (2000b) HYDRONMR: Prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J Magn Reson B 147:138-146
31. 15N NMR relaxation. Biochemistry 33:5984-6003
32. Feder ME, Burggren WW (eds) (1992) Environmental physiology of the amphibians. University of Chicago Press, Chicago
33. Fenimore PW, Frauenfelder H, McMahon BH, Parak FG (2002) Slaving: solvent fluctuations dominate protein dynamics and functions. Proc Natl Acad Sci USA 99:16047-16051
34. Finerty PJ, Muhandiram R, Forman-Kay JD (2002) Side-chain dynamics of the SAP SH2 domain correlate with a binding hot spot and a region with conformational plasticity. J Mol Biol 322:605-620
35. Foord RL, Leatherbarrow RJ (1998) Effect of osmolytes on the exchange rates of backbone amide protons in proteins. Biochemistry 37:2969-2978
36. Frederick KK, Marlow MS, Valentine KG, Wand AJ (2007) Conformational entropy in molecular recognition by proteins. Nature 448:325-329
37. Garman EF, Doublie S (2003) Cryocooling of macromolecular crystals: optimization methods. Methods Enzymol 368:188-216
38. Gekko K, Timasheff SN (1981a) Mechanism of protein stabilization by glycerol - preferential hydration in glycerol-water mixtures. Biochemistry 20:4667-4676
39. Gekko K, Timasheff SN (1981b) Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20:4677-4686
40. 2H-labeled proteins. J Biomol NMR 13:369-374
41. Hansen DF, Kay LE (2007) Improved magnetization alignment schemes for spin-lock relaxation experiments. J Biomol NMR 37:245-255
42. Hologne M, Faelber K, Diehl A, Reif B (2005) Characterization of dynamics of perdeuterated proteins by MAS solid-state NMR. J Am Chem Soc 127:11208-11209
43. Hu H, Clarkson MW, Hermans J, Lee AL (2003) Increased rigidity of eglin c at acidic pH: Evidence from NMR spin relaxation and MD simulations. Biochemistry 42:13856-13868
44. Hu H, Hermans J, Lee AL (2005) Relating side-chain mobility in proteins to rotameric transitions: Insights from molecular dynamics simulations and NMR. J Biomol NMR 32:151-162
45. Hurvich CM, Tsai CL (1989) Regression and time-series model selection in small samples. Biometrika 76:297-307
46. Igumenova TI, Lee AL, Wand AJ (2005) Backbone and side chain dynamics of mutant calmodulin-peptide complexes. Biochemistry 44:12627-12639
47. 13C longitudinal and transverse relaxation rates measured in the same protein sample. J Am Chem Soc 123:6164-6171
48. 2H NMR relaxation study. J Mol Biol 357:1237-1252
49. Kay LE, Muhandiram DR, Farrow NA, Aubin Y, Forman-Kay JD (1996) Correlation between dynamics and high affinity binding in an SH2 domain interaction. Biochemistry 35:361-368
50. Kempkes R, Stofko E, Lam K, Snell EH (2008) Glycerol concentrations required for the successful vitrification of cocktail conditions in a high-throughput crystallization screen. Acta Crystallogr D Biol Crystallogr 64:287-301
51. Knubovets T, Osterhout JJ, Connolly PJ, Klibanov AM (1999) Structure, thermostability, and conformational flexibility of hen egg-white lysozyme dissolved in glycerol. Proc Natl Acad Sci USA 96:1262-1267
52. Korchuganov DS, Gagnidze IE, Tkach EN, Schulga AA, Kirpichnikov MP, Arseniev AS (2004) Determination of protein rotational correlation time from NMR relaxation data at various solvent viscosities. J Biomol NMR 30:431-442
53. Korzhnev DM, Skrynnikov NR, Millet O, Torchia DA, Kay LE (2002) An NMR experiment for the accurate measurement of heteronuclear spin-lock relaxation rates. J Am Chem Soc 124:10743-10753
54. Lee LK, Rance M, Chazin WJ, Palmer AG (1997) Rotational diffusion anisotropy of proteins from simultaneous analysis of N-15 and C-13(alpha) nuclear spin relaxation. J Biomol NMR 9:287-298
55. 15N relaxation measurements. Biochemistry 34:2408-2423
56. Lienin SF, Brüschweiler R, Ernst RR (1998) Rotational motion of a solute molecule in a highly viscous liquid studied by 13C NMR: 1, 3-dibromoadamantane in polymeric chlorotrifluoroethene. J Magn Reson 131:184-190
57. Lipari G, Szabo A (1982a) 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
58. Lipari G, Szabo A (1982b) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J Am Chem Soc 104:4559-4570
59. Lovell SC, Word JM, Richardson JS, Richardson DC (2000) The penultimate rotamer library. Proteins Struct Funct Genet 40:389-408
60. Mandel AM, Akke M, Palmer AG (1995) Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme. J Mol Biol 246:144-163
61. 2H-enriched proteins in solution. J Am Chem Soc 124:6439-6448
62. 2H NMR dynamics and scalar couplings. J Mol Biol 329:551-563
63. Mittermaier A, Kay LE (2004) The response of internal dynamics to hydrophobic core mutations in the SH3 domain from the fyn tyrosine kinase. Protein Sci 13:1088-1099
64. Modig K, Liepinsh E, Otting G, Halle B (2004) Dynamics of protein and peptide hydration. J Am Chem Soc 126:102-114
65. Musacchio A, Noble M, Pauptit R, Wierenga R, Saraste M (1992) Crystal structure of a src-homology 3 (SH3) domain. Nature 359:851-855
66. 13C NMR spectroscopy: Application to the leucine residues of staphylococcal nuclease. Biochemistry 31:5253-5263
67. Pal SK, Peon J, Zewail AH (2002) Biological water at the protein surface: Dynamical solvation probed directly with femtosecond resolution. Proc Natl Acad Sci USA 99:1763-1768
68. Pegg DE (2007) Principles of cryopreservation. Methods Mol Biol 368:39-57
69. Priev A, Almagor A, Yedgar S, Gavish B (1996) Glycerol decreases the volume and compressibility of protein interior. Biochemistry 35:2061-2066
70. Rariy RV, Klibanov AM (1997) Correct protein folding in glycerol. Proc Natl Acad Sci USA 94:13520-13523
71. 2H relaxation data. J Am Chem Soc 128:12354-12355
72. Roche CJ, Guo F, Friedman JM (2006) Molecular level probing of preferential hydration and its modulation by osmolytes through the use of pyranine complexed to hemoglobin. J Biol Chem 281:38757-38768
73. Sinibaldi R, Ortore MG, Spinozzi F, Carsughi F, Frielinghaus H, Cinelli S, Onori G, Mariani P (2007) Preferential hydration of lysozyme in water/ glycerol mixtures: A small-angle neutron scattering study. J Chem Phys 126
74. Skrynnikov NR (2007) Asymmetric doublets in MAS NMR: Coherent and incoherent mechanisms. Magn Reson Chem 45:S161-S173
75. Skrynnikov NR, Millet O, Kay LE (2002) 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 124:6449-6460
76. Sousa R (1995) Use of glycerol, polyols and other protein structure stabilizing agents in protein crystallization. Acta Crystallogr D Biol Crystallogr 51:271-277
77. Tarek M, Tobias DJ (2008) The role of protein-solvent hydrogen bond dynamics in the structural relaxation of a protein in glycerol versus water. Eur Biophys J Biophys Lett 37:701-709
78. Tjandra N, Feller SE, Pastor RW, Bax A (1995) Rotational diffusion anisotropy of human ubiquitin from N-15 NMR relaxation. J Am Chem Soc 117:12562-12566
79. Tjandra N, Wingfield P, Stahl S, Bax A (1996) Anisotropic rotational diffusion of perdeuterated HIV protease from N-15 NMR relaxation measurements at two magnetic fields. J Biomol NMR 8:273-284
80. Tollinger M, Skrynnikov NR, Mulder FAA, Forman-Kay JD, Kay LE (2001) Slow dynamics in folded and unfolded states of an SH3 domain. J Am Chem Soc 123:11341-11352
81. 2H NMR relaxation studies of the 723-residue enzyme malate synthase G reveal a dynamic binding interface. Biochemistry 44:15970-15977
82. Tugarinov V, Kanelis V, Kay LE (2006) Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat Protoc 1:749-754
83. Venable RM, Pastor RW (1988) Frictional models for stochastic simulations of proteins. Biopolymers 27:1001-1014
84. Woessner DE (1962) Nuclear spin relaxation in ellipsoids undergoing rotational brownian motion. J Chem Phys 37:647-654
85. 2H relaxation data. Implications for protein structure. J Am Chem Soc 129:6827-6838
86. 15N relaxation study of the cold shock protein CspB at various solvent viscosities. J Biomol NMR 27:221-234