NMR detection of multiple transitions to low-populated states in azurin

Protein Science

Volumn 12, Issue 1, 2003, Pages 56-65

  Korzhnev, Dmitry M ^a   Goran Karlsson B ^b   Orekhov, Vladislav Yu ^a   Billeter, Martin ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Blue copper proteins; Conformational exchange; CPMG; Dynamics; NMR relaxation

Indexed keywords

AZURIN; COPPER PROTEIN; HISTIDINE;

ARTICLE; ELECTRON TRANSPORT; ENERGY; ENTHALPY; ENTROPY; MAGNETIC FIELD; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; TEMPERATURE;

AZURIN; BINDING SITES; COPPER; HISTIDINE; KINETICS; MODELS, MOLECULAR; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTONS; PSEUDOMONAS AERUGINOSA; TEMPERATURE; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 12244298881     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0225403     Document Type: Article

References (47)

1. Adman, E.T. 1991. Copper protein structures. Adv. Protein Chem. 42: 145-197.
2. Akke, M. and Palmer, A.G. 1996. Monitoring macromolecular motions on microsecond to millisecond time scales by R1-Rho-R1 constant relaxation time NMR spectroscopy. J. Am. Chem. Soc. 118: 911-912.
3. Bertini, I., Bryant, D.A., Ciurli, S., Dikiy, A., Fernandez, C.O., Luchinat, C., Safarov, N., Vila, A.J., and Zhao, J.D. 2001. Backbone dynamics of plastocyanin in both oxidation states - Solution structure of the reduced form and comparison with the oxidized state. J. Biol. Chem. 276: 47217-47226.
4. Bloom, M., Reeves, L.W., and Wells, E.J. 1965. Spin echoes and chemical exchange. J. Chem. Phys. 42: 1615-1624.
5. Branden, C. and Tooze, A. 1999. Introduction to Protein Structure, Garland Publishing, New York.
6. Carver, J.P. and Richards, R.E. 1972. A general two-site solution for the chemical exchange produced dependence of T2 upon the Carr-Pursell pulse separation. J. Magn. Reson. 6: 89-105.
7. Davis, D.G., Perlman, M.E., and London, R.E. 1994. Direct measurements of the dissociation rate constant for inhibitor-enzyme complexes via the T1-Rho and T2 (CPMG) methods. J. Magn. Reson. Ser. B 104: 266-275.
8. Denisov, V.P., Peters, J., Horlein, H.D., and Halle, B. 1996. Using buried water molecules to explore the energy landscape of proteins. Nat. Struct. Biol. 3: 505-509.
9. DiBilio, A.J., Hill, M.G., Bonander, N., Karlsson, B.G., Villahermosa, R.M., Malmström, B.G., Winkler, J.R., and Gray, H.B. 1997. Reorganization energy of blue copper: Effects of temperature and driving force on the rates of electron transfer in ruthenium- and osmium-modified azurins. J. Am. Chem. Soc. 119: 9921-9922.
10. Farrow, N.A., Zhang, O.W., Forman-Kay, J.D., and Kay, L.E. 1994. A heteronuclear correlation experiment for simultaneous determination of N-15 longitudinal decay and chemical-exchange rates of systems in slow equilibrium. J. Biomol. NMR 4: 727-734.
11. Ferry, J.D., Grandine, L.D., and Fitzgerald, E.R. 1953. The relaxation distribution function of polyisobutylene in the transition from rubber-like to glass-like behavior. J. Appl. Phys. 24: 911-916.
12. Gray, H.B., Malmström, B.G., and Williams, R.J.P. 2000. Copper coordination in blue proteins. J. Biol. Inorg. Chem. 5: 551-559.
13. Henderson, R., Baldwin, J.M., Ceska, T.A., Zemlin, F., Beckmann, E., and Downing, K.H. 1990. Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy. J. Mol. Biol. 213: 899-929.
14. Ishima, R. and Torchia, D.A. 1999. Estimating the time scale of chemical exchange of proteins from measurements of transverse relaxation rates in solution. J. Biomol. NMR 14: 369-372.
15. Ishima, R., Louis, J.M., and Torchia, D.A. 1999. Transverse C-13 relaxation of CHD2 methyl isotopmers to detect slow conformational changes of protein side chains. J. Am. Chem. Soc. 121: 11589-11590.
16. Jeffrey, P.D., Ruso, A.A., Polyak, K., Gibbs, E., Hurwitz, J., Massague, J. and Pavletich, N.P. 1995. Mechanism of CDK activation revealed by the structure of a cyclina-CDK2 complex. Nature 376: 313-320.
17. Kalverda, A.P., Ubbink, M., Gilardi, G., Wijmenga, S.S., Crawford, A., Jeuken, L.J.C., and Canters, G.W. 1999. Backbone dynamics of azurin in solution: Slow conformational change associated with deprotonation of histidine 35. Biochemistry 38: 12690-12697.
18. Karlsson, B.G., Pascher, T., Nordling, M., Arvidsson, R.H.A., and Lundberg, L.G. 1989. Expression of the blue copper protein azurin from Pseudomonas aeruginosa in Escherichia coli. FEBS Lett. 246: 211-217.
19. Korzhnev, D.M., Tischenko, E.V., and Arseniev, A.S. 2000. Off-resonance effects in N-15 T-2 CPMG measurements. J. Biomol. NMR 17: 231-237.
20. Korzhnev, D.M., Billeter, M., Arseniev, A.S., and Orekhov, V.Y. 2001a. NMR studies of Brownian tumbling and Internal motions in proteins. Prog. Nucl. Magn. Reson. Spectrosc. 38: 197-266.
21. Korzhnev, D.M., Ibraghimov, I.V., Billeter, M., and Orekhov, V.Y. 2001b. MUNIN: Application of three-way decomposition to the analysis of heteronuclear NMR relaxation data. J. Biomol. NMR 21: 263-268.
22. Leckner, J., Wittung, P., Bonander, N., Karlsson, B.G., and Malmström, B.G. 1997. The effect of redox state on the folding free energy of azurin. J. Biol. Inorg. Chem. 2: 368-371.
23. Lipari, G. and 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.
24. Loria, J.P., Rance, M., and Palmer, A.G. 1999. A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 121: 2331-2332.
25. Luz, Z. and Meiboom, S. 1963. Nuclear magnetic resonance study of the protolysis of trimethylammonium ion in aqueous solution - Order of the reaction with respect to solvent. J. Chem. Phys. 39: 366-370.
26. Malmström, B.G. 1964. In Oxidized and Related Redox Systems (eds. T.E. King et al.), pp. 207-216. Wiley, New York.
27. -, 1994. Rack-induced bonding in blue-copper proteins. Eur. J. Biochem. 223: 711-718.
28. Millet, O., Loria, J.P., Kroenke, C.D., Pons, M., and Palmer, A.G. 2000. The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122: 2867-2877.
29. Montelione, G.T. and Wagner, G. 1989. 2D chemical-exchange NMR spectroscopy by proton-detected heteronuclear correlation. J. Am. Chem. Soc. 111: 3096-3098.
30. Mulder, F.A.A., Mittermaier, A., Hon, B., Dahlquist, F.W., and Kay, L.E. 2001a. Studying excited states of proteins by NMR spectroscopy. Nat. Struct. Biol. 8: 932-935.
31. Mulder, F.A.A., Skrynnikov, N.R., Hon, B., Dahlquist, F.W., and Kay, L.E. 2001b. Measurement of slow (ms-ms) time scale dynamics in protein side chains by N-15 relaxation dispersion NMR spectroscopy: Application to Asn and Gln residues in a cavity mutant of T4 lysozyme. J. Am. Chem. Soc. 123: 967-975.
32. Nar, H., Messerschmidt, A., Huber, R., Vandekamp, M., and Canters, G.W. 1991. Crystal-structure analysis of oxidized Pseudomonas aeruginosa azurin at pH 5.5 and pH 9.0 - A pH-induced conformational transition involves a peptide-bond flip. J. Mol. Biol. 221: 765-772.
33. -. 1992. Crystal-structure of Pseudomonas aeruginosa apo-azurin at 1.85 angstrom resolution. FEBS Lett. 306: 119-124.
34. Orekhov, V.Y., Pervushin, K.V., and Arseniev, A.S. 1994. Backbone dynamics of (1-71)-bacterioopsin studied by two-dimensional H1-N15 NMR spectroscopy. Eur. J. Biochem. 219: 887-896.
35. Orekhov, V.Y., Korzhnev, D.M., Diercks, T., Kessler, H., and Arseniev, A.S. 1999. H-1-N-15 NMR dynamic study of an isolated α-helical peptide (1-36)-bacteriorhodopsin reveals the equilibrium helix-coil transitions. J. Biomol. NMR 14: 345-356.
36. Orekhov, V.Y., Ibraghimov, I.V., and Billeter, M. 2001. MUNIN: A new approach to multi-dimensional NMR spectra interpretation. J. Biomol. NMR 20: 49-60.
37. Palmer, A.G., Williams, J., and McDermott, A. 1996. Nuclear magnetic resonance studies of biopolymer dynamics. J. Phys. Chem. 100: 13293-13310.
38. 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.
39. Press, W.H. 1997. Numerical Recipes in C: The Art of Scientific Computing, 2nd Rev. Edition, Cambridge University Press, Cambridge, UK.
40. Ryde, U., Olsson, M.H.M., Pierloot, K., and Roos, B.O. 1996. The cupric geometry of blue copper proteins is not strained. J. Mol. Biol. 261: 586-596.
41. Schirmer, T. and Evans, P.R. 1990. Structural basis of the allosteric behavior of phosphofructokinase. Nature 343: 140-145.
42. Shepard, W.E.B., Anderson, B.F., Lewandoski, D.A., Norris, G.E., and Baker, E.N. 1990. Copper coordination geometry in azurin undergoes minimal change on reduction of copper(II) to copper(I). J. Am. Chem. Soc. 112: 7817-7819.
43. Skrynnikov, N.R., Mulder, F.A.A., Hon, B., Dahlquist, F.W., and Kay, L.E. 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.
44. Szyperski, T., Luginbühl, P., Otting, G., Güntert, P., and Wüthrich, K. 1993. Protein dynamics studied by rotating frame N15 spin relaxation times. J. Biomol. NMR 3: 151-164.
45. 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.
46. Wang, C.Y., Grey, M.J., and Palmer, A.G. 2001. CPMG sequences with enhanced sensitivity to chemical exchange. J. Biomol. NMR 21: 361-366.
47. Wider, G., Neri, D., and Wüthrich, K. 1991. Studies of slow conformational equilibria in macromolecules by exchange of heteronuclear longitudinal 2-spin-order in a 2D difference correlation experiment. J. Biomol. NMR 1: 93-98.