Ring flips revisited: 13C relaxation dispersion measurements of aromatic side chain dynamics and activation barriers in basic pancreatic trypsin inhibitor

Biochemistry

Volumn 53, Issue 28, 2014, Pages 4519-4525

  Weininger, Ulrich ^a   Modig, Kristofer ^a   Akke, Mikael ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIZATION; CHAINS; CHEMICAL ACTIVATION; DISPERSIONS; EXPERIMENTS; MOLECULAR DYNAMICS; PROTEINS;

ACTIVATION ENTROPIES; ACTIVATION PARAMETER; CONFORMATIONAL EXCHANGE; INTRAMOLECULAR MOTION; MOLECULAR DYNAMICS TRAJECTORIES; RELAXATION DISPERSION; STRUCTURAL FLUCTUATIONS; TRANSVERSE RELAXATION;

AROMATIC COMPOUNDS;

APROTININ; BASIC PANCREATIC TRYPSIN INHIBITOR; CARBON 13; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; DISPERSION; ENTROPY; ENVIRONMENTAL TEMPERATURE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIMULATION;

APROTININ; MOLECULAR DYNAMICS SIMULATION;

EID: 84904599245     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500462k     Document Type: Article

References (44)

1. Wagner, G., Demarco, A., and Wüthrich, K. (1976) Dynamics of Aromatic Amino-Acid Residues in Globular Conformation of Basic Pancreatic Trypsin-Inhibitor (BPTI). 1. H-1 NMR Studies Biophys. Struct. Mech. 2, 139-158
2. Wagner, G. and Wüthrich, K. (1978) Dynamic Model of Globular Protein Conformations Based on NMR Studies in Solution Nature 275, 247-248
3. Wagner, G. (1980) Activation Volumes ΔV Not Equal for the Rotational Flips of Internal Aromatic Rings in Globular-Proteins, Determined by High-Resolution 360-MHz H-1 NMR at Variable Pressure Experientia 36, 735-735
4. Wagner, G., Brühwiler, D., and Wüthrich, K. (1987) Reinvestigation of the Aromatic Side-Chains in the Basic Pancreatic Trypsin-Inhibitor by Heteronuclear Two-Dimensional Nuclear-Magnetic-Resonance J. Mol. Biol. 196, 227-231
5. Li, H., Yamada, H., and Akasaka, K. (1999) Effect of pressure on the tertiary structure and dynamics of folded basic pancreatic trypsin inhibitor Biophys. J. 77, 2801-2812
6. Skalicky, J. J., Mills, J. L., Sharma, S., and Szyperski, T. (2001) Aromatic ring-flipping in supercooled water: Implications for NMR-based structural biology of proteins J. Am. Chem. Soc. 123, 388-397
7. Dobson, C. M., Moore, G. R., and Williams, R. J. P. (1975) Assignment of Aromatic Amino-Acid PMR Resonances of Horse Ferricytochrome c FEBS Lett. 51, 60-65
8. Campbell, I. D., Dobson, C. M., Moore, G. R., Perkins, S. J., and Williams, R. J. P. (1976) Temperature-Dependent Molecular-Motion of a Tyrosine Residue of Ferrocytochrome c FEBS Lett. 70, 96-100
9. Rao, D. K. and Bhuyan, A. K. (2007) Complexity of aromatic ring-flip motions in proteins: Y97 ring dynamics in cytochrome c observed by cross-relaxation suppressed exchange NMR spectroscopy J. Biomol. NMR 39, 187-196
10. Nall, B. T. and Zuniga, E. H. (1990) Rates and Energetics of Tyrosine Ring Flips in Yeast Iso-2-Cytochrome c Biochemistry 29, 7576-7584
11. Campbell, I. D., Dobson, C. M., and Williams, R. J. P. (1975) Proton magnetic resonance studies of the tyrosine residues of hen lysozyme: Assignment and detection of conformational mobility Proc. R. Soc. B 189, 503-509
12. Hattori, M., Li, H., Yamada, H., Akasaka, K., Hengstenberg, W., Gronwald, W., and Kalbitzer, H. R. (2004) Infrequent cavity-forming fluctuations in HPr from Staphylococcus carnosus revealed by pressure- and temperature-dependent tyrosine ring flips Protein Sci. 13, 3104-3114
13. Baturin, S. J., Okon, M., and McIntosh, L. P. (2011) Structure, dynamics, and ionization equilibria of the tyrosine residues in Bacillus circulans xylanase J. Biomol. NMR 51, 379-394
14. Ulrich, E. L., Akutsu, H., Doreleijers, J. F., Harano, Y., Ioannidis, Y. E., Lin, J., Livny, M., Mading, S., Maziuk, D., Miller, Z., Nakatani, E., Schulte, C. F., Tolmie, D. E., Wenger, R. K., Yao, H. Y., and Markley, J. L. (2008) BioMagResBank Nucleic Acids Res. 36, D402-D408
15. Weininger, U., Respondek, M., Löw, C., and Akke, M. (2013) Slow Aromatic Ring Flips Detected Despite Near-Degenerate NMR Frequencies of the Exchanging Nuclei J. Phys. Chem. B 117, 9241-9247
16. Akke, M. (2002) NMR methods for characterizing microsecond-millisecond dynamics in recognition and catalysis Curr. Opin. Struct. Biol. 12, 642-647
17. Palmer, A. G. and Massi, F. (2006) Characterization of the dynamics of biomacromolecules using rotating-frame spin relaxation NMR spectroscopy Chem. Rev. 106, 1700-1719
18. Palmer, A. G., Kroenke, C. D., and Loria, J. P. (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339, 204-238
19. 13C labeling of aromatic side-chains in proteins for NMR relaxation measurements J. Am. Chem. Soc. 128, 2506-2507
20. 13C]-glucose facilitates the accurate measurement of dynamics at backbone Ca and side-chain methyl positions in proteins J. Biomol. NMR 38, 199-122
21. 13C labeling strategy reveals a range of aromatic side chain motion in calmodulin J. Am. Chem. Soc. 135, 9560-9563
22. 13C CPMG relaxation dispersion J. Biomol. NMR 54, 9-14
23. 13C in aromatic side chains using L-optimized TROSY-selection J. Biomol. NMR 59, 23-29
24. Hetzel, R., Wuthrich, K., Deisenhofer, J., and Huber, R. (1976) Dynamics of Aromatic Amino-Acid Residues in Globular Conformation of Basic Pancreatic Trypsin-Inhibitor (BPTI). 2. Semiempirical Energy Calculations Biophys. Struct. Mech. 2, 159-180
25. Gelin, B. R. and Karplus, M. (1975) Sidechain Torsional Potentials and Motion of Amino-Acids in Proteins: Bovine Pancreatic Trypsin-Inhibitor Proc. Natl. Acad. Sci. U.S.A. 72, 2002-2006
26. Shaw, D. E., Maragakis, P., Lindorff-Larsen, K., Piana, S., Dror, R. O., Eastwood, M. P., Bank, J. A., Jumper, J. M., Salmon, J. K., Shan, Y. B., and Wriggers, W. (2010) Atomic-Level Characterization of the Structural Dynamics of Proteins Science 330, 341-346
27. Persson, F. and Halle, B. (2013) Transient Access to the Protein Interior: Simulation versus NMR J. Am. Chem. Soc. 135, 8735-8748
28. Xue, Y., Ward, J. M., Yuwen, T. R., Podkorytov, I. S., and Skrynnikov, N. R. (2012) Microsecond Time-Scale Conformational Exchange in Proteins: Using Long Molecular Dynamics Trajectory To Simulate NMR Relaxation Dispersion Data J. Am. Chem. Soc. 134, 2555-2562
29. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
30. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278, 313-352
31. 2 upon the Carr-Purcell pulse separation J. Magn. Reson. 6, 89-105
32. 2 (CPMG) methods J. Magn. Reson., Ser. B 104, 266-275
33. Gutowsky, H. S., Vold, R. L., and Wells, E. J. (1965) Theory of chemical exchange effects in magnetic resonance J. Chem. Phys. 43, 4107-4125
34. Tollinger, M., Skrynnikov, N. R., Mulder, F. A. A., Forman-Kay, J. D., and Kay, L. E. (2001) Slow dynamics in folded and unfolded states of an SH3 domain J. Am. Chem. Soc. 123, 11341-11352
35. Press, W. H., Flannery, B. P., Teukolsky, S. A., and Vetterling, W. T. (1986) Numerical Recipes. The Art of Scientific Computing, Cambridge University Press, Cambridge, U.K.
36. 1p relaxation for two-site chemical exchange: General approximations and some exact solutions J. Magn. Reson. 177, 221-227
37. 15N spin relaxation times J. Biomol. NMR 3, 151-164
38. Grey, M. J., Wang, C., and Palmer, A. G. (2003) Disulfide bond isomerization in basic pancreatic trypsin inhibitor: Multisite chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling J. Am. Chem. Soc. 125, 14324-14335
39. Gottschalk, M., Venu, K., and Halle, B. (2003) Protein self-association in solution: The bovine pancreatic trypsin inhibitor decamer Biophys. J. 84, 3941-3958
40. 1H couplings ChemBioChem 14, 685-688
41. Wlodawer, A., Walter, J., Huber, R., and Sjolin, L. (1984) Structure of bovine pancreatic trypsin inhibitor. Results of joint neutron and X-ray refinement of crystal form II J. Mol. Biol. 180, 301-329
42. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures J. Mol. Graphics 14, 51-55
43. Makhatadze, G. I., Kim, K. S., Woodward, C., and Privalov, P. L. (1993) Thermodynamics of BPTI Folding Protein Sci. 2, 2028-2036
44. Karplus, M. (2000) Aspects of protein reaction dynamics: Deviations from simple behavior J. Phys. Chem. B 104, 11-27