Two-dimensional measurement of proton T1ρ relaxation in unlabeled proteins: Mobility changes in α-bungarotoxin upon binding of an acetylcholine receptor peptide

Biochemistry

Volumn 44, Issue 32, 2005, Pages 10926-10934

  Samson, Abraham O ^a   Chill, Jordan H ^a,b   Anglister, Jacob ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

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

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CHEMICAL RELAXATION; COMPLEXATION; MATHEMATICAL MODELS; NUCLEAR MAGNETIC RESONANCE; PROTEINS; TOXICITY;

ACETYLCHOLINE RECEPTORS (ACHR); PEPTIDES; PROTON RELAXATION; RELAXATION TIME;

PROTONS;

ALPHA BUNGAROTOXIN; CHOLINERGIC RECEPTOR; PROTEIN;

ARTICLE; COMPLEX FORMATION; CORRELATION ANALYSIS; MATHEMATICAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TRANSPORT; PROTON TRANSPORT; PULSE RATE; RECEPTOR BINDING;

ANIMALS; BUNGAROTOXINS; MOTION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTONS; RECEPTORS, CHOLINERGIC;

EID: 23844472634     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050645h     Document Type: Article

References (61)

1. 13C magnetic resonance, Biochemistry; 14, 887-900.
2. Jardetzky, O., and Roberts, G. C. K. (1981) NMR in molecular biology. Academic Press, New York.
3. 1H NMR with application to phage λ repressor, Proc. Natl. Acad. Sci. U.S.A. 81, 6019-23.
4. 15N transverse relaxation to detect millisecond time-scale motions in perdeuterated proteins: Application to HIV-1 protease, J. Am. Chem. Soc. 120, 10534-42.
5. Boulat, B., and Bodenhausen, G. (1993) Measurement of proton relaxation rates in proteins, J. Biomol. NMR 3, 335-48.
6. α backbone protons in proteins with tailored initial conditions, J. Magn. Reson. 139, 434-8.
7. Boulat, B., Konrat, R., Burghardt, I., and Bodenhausen, G. (1992) Measurement of relaxation rates in crowded NMR spectra by selective coherence transfer, J. Magn. Reson. 114, 5412-4.
8. Arseniev, A. S., Sobol, A. G., and Bystrov, V. F. (1986) T, relaxation measurement by two-dimensional NMR spectroscopy, J. Mol. Graphics 70, 427-35.
9. Kay, L. E., and Prestegard, J. H. (1988) Spin-lattice relaxation rates of coupled spins from 2D accordion spectroscopy, J. Magn. Reson. 77, 599-605.
10. Bodenhausen, G., and Ernst, R. R. (1981) The accordion experiment, a simple approach to three-dimensional NMR spectroscopy, J. Magn. Reson. 45, 367.
11. Bodenhausen, G., and Ernst, R. R. (1982) Direct determination of rate constants of slow dynamic processes by two-dimensional "accordion" spectroscopy in nuclear magnetic resonance, J. Am. Chem. Soc. 104, 1304.
12. Frederick, A. F., Kay, L. E., and Prestegard, J. H. (1988) Location of divalent ion sites in acyl carrier protein using relaxation perturbed 2D NMR, FEBS Lett. 238, 43-8.
13. Ulmer, T. S., Campbell, I. D., and Boyd, J. (2004) Amide proton relaxation measurements employing a highly deuterated protein, J. Magn. Reson. 166, 190-201.
14. Wang, Y. S., and Ikuta, S. (1989) Proton on-resonance rotating frame spin-lattice relaxation measurements of B and Z double-helical oligodeoxyribonucleotides in solution. J. Am. Chem. Soc. 111, 1243-8.
15. Schmitz, U., Sethson, I., Egan, W. M., and James, T. L. (1992) Solution structure of a DNA octamer containing the Pribnow box via restrained molecular dynamics simulation with distance and torsion angle constraints derived from two-dimensional nuclear magnetic resonance spectral fitting, J. Mol. Biol. 227, 510-31.
16. Kennedy, M. A., Nuutero, S. T., Davis, J. T., Drobny, G. P., and Reid, B. R. (1993) Mobility at the TpA cleavage site in the T3A3-containing AhaIII and PmeI restriction sequences, Biochemistry 32, 8022-35.
17. Bleich, H. E., and Glasel, J. A. (1978) Rotating frame spin-lattice relaxation experiments and the problem of intramolecular motions of peptides in solution, Biopolymers 17, 2445-57.
18. Bleich, H. E., Day, A. R., Freer, R. J., and Glasel, J. A. (1979) NMR rotating frame relaxation studies of intramolecular motion in peptides. Tyrosine ring motion in methionine-enkephalin. Biochem. Biophys. Res. Commun. 87, 1146-53.
19. 2. Conformations in crystals and a Tip examination of internal mobility in solution, J. Am. Chem. Soc. 108, 4637-42.
20. Kopple, K., Wang, S. Y., Cheng, A. G., and Bhandary, K. K. (1988) Conformations of cyclic octapeptides. 5. Crystal structure of cyclo(Cys-Gly-Pro-Phe)2 and rotating frame relaxation (Tip) NMR studies of internal mobility in cyclic octapeptides. J. Am. Chem. Soc. 110, 4168-76.
21. Scheucher, J., and Wijmenga, S. S. (2002) How to detect internal motion by homonuclear NMR, J. Am. Chem. Soc. 124, 5881-9.
22. Karlin, A. (1993) Structure of nicotinic acetylcholine receptors. Curr. Opin. Neurobiol. 3, 299-309.
23. Corringer, P. J., Le Novere, N., and Changeux, J. P. (2000) Nicotinic receptors at the amino acid level, Annu. Rev. Pharmacol. Toxicol. 40,431-58.
24. Blount, P., and Merlie, J. P. (1989) Molecular basis of the two nonequivalent ligand binding sites of the muscle nicotinic acetylcholine receptor, Neuron 3, 349-57.
25. 125I-α-bungarotoxin binding activity to the α subunit of Torpedo acetylcholine receptor isolated by gel electrophoresis in sodium dodecyl sulfate, J. Biol. Chem. 256, 8294-7.
26. Wilson, P. T., Hawrot, E., and Lentz, T. L. (1988) Distribution of α-bungarotoxin binding sites over residues 173-204 of the α subunit of the acetylcholine receptor, Mol. Pharmacol. 34, 643-50.
27. Wilson, P. T., Lentz, T. L., and Hawrot, E. (1985) Determination of the primary amino acid sequence specifying the α-bungarotoxin binding site on the α subunit of the acetylcholine receptor from Torpedo californica, Proc. Natl. Acad. Sci. U.S.A. 82, 8790-4.
28. Wilson, P. T., and Lentz, T. L. (1988) Binding of α-bungarotoxin to synthetic peptides corresponding to residues 173-204 of the α subunit of Torpedo, calf, and human acetylcholine receptor and restoration of high-affinity binding by sodium dodecyl sulfate, Biochemistry 27, 6667-74.
29. Ralston, S., Sarin, V., Thanh, H. L., Rivier, J., Fox, J. L., and Lindstrom, J. (1987) Synthetic peptides used to locate the α-bungarotoxin binding site and immunogenic regions on α subunits of the nicotinic acetylcholine receptor, Biochemistry 26, 3261-6.
30. Conti-Tronconi, B. M., Tang, F., Diethelm, B. M., Spencer, S. R., Reinhardt-Maelicke, S., and Maelicke, A. (1990) Mapping of a cholinergic binding site by means of synthetic peptides, monoclonal antibodies, and α-bungarotoxin, Biochemistry 29, 6221-30.
31. Neumann, D., Barchan, D., Safran, A., Gershoni, J. M., and Fuchs, S. (1986) Mapping of the α-bungarotoxin binding site within the α subunit of the acetylcholine receptor, Proc. Natl. Acad. Sci. U.S.A. 83, 3008-11.
32. Samson, A. O., Chill, J. H., Rodriguez, E., Scherf, T., and Anglister, J. (2001) NMR mapping and secondary structure determination of the major acetylcholine receptor α-subunit determinant interacting with α-bungarotoxin, Biochemistry 40, 5464-73.
33. Samson, A., Scherf, T., Eisenstein, M., Chill, J., and Anglister, J. (2002) The mechanism for acetylcholine receptor inhibition by α-neurotoxins and species-specific resistance to α-bungarotoxin revealed by NMR, Neuron 35, 319-32.
34. Aronheim, A., Eshel, Y., Mosckovitz, R., and Gershoni, J. M. (1988) Characterization of the binding of α-bungarotoxin to bacterially expressed cholinergic binding sites, J. Biol. Chem. 263, 9933-7.
35. 1ρ-filtered two-dimensional transferred NOE spectrum for studying antibody interactions with peptide antigens, Biophys. J. 64, 754-61.
36. Zvi, A., Kustanovich, I., Feigelson, D., Levy, R., Eisenstein, M., Matsushita, S., Richalet-Secordel, P., Regenmortel, M. H., and Anglister, J. (1995) NMR mapping of the antigenic determinant recognized by an anti-gp120, human immunodeficiency virus neutralizing antibody, Eur. J. Biochem. 229, 178-87.
37. Braunschweiler, L., and Ernst, R. R. (1983) Coherence transfer by isotropic mixing: Application to proton correlation spectroscopy, J. Magn. Reson. 53, 521-8.
38. Bax, A., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 335.
39. Shaka, A. J., Keeler, J., and Freeman, R. (1983) Evaluation of a new broadband decoupling sequence: WALTZ-16, J. Magn. Reson. 53, 313-40.
40. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-5.
41. 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, 277-93.
42. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
43. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-5, 29-32.
44. Werbelow, L. G., and Grant, D. M. (1977) Intramolecular dipolar relaxation in multispin systems, Adv. Magn. Reson. 9, 189-299.
45. Vold, R. L., and Void, R. R. (1978) Nuclear magnetic relaxation in coupled spin systems, Prog. NMR Spectrosc. 12, 79-113.
46. 13C NMR and molecular dynamics study, J. Biomol. NMR 14, 47-66.
47. Gilquin, B., Bourgoin, M., Menez, R., Le Du, M. H., Servent, D., Zinn-Justin, S., and Menez, A. (2003) Motions and structural variability within toxins: Implication for their use as scaffolds for protein engineering, Protein Sci. 12, 266-77.
48. Basus, V. J., Song, G., and Hawrot, E. (1993) NMR solution structure of an α-bungarotoxin/nicotinic receptor peptide complex, Biochemistry 32, 12290-8.
49. Finerty, P. J., Jr., Mittermaier, A. K., Muhandiram, R., Kay, L. E., and Forman-Kay, J. D. (2005) NMR dynamics-derived insights into the binding properties of a peptide interacting with an SH2 domain. Biochemistry 44, 694-703.
50. Valeur, B., Jarry, J., Geny, F., and Monnerie, L. (1975) Dynamics of macromolecular chains. II. Orientation relaxation generated by elementary three-bond motions and notion of an independent kinetic segment, J. Polym. Sci., Part B: Polym. Phys. 13, 675-82.
51. Deverell, C., Morgan, R. E., and Strange, J. H. (1970) Studies of chemical exchange by nuclear magnetic relaxation in the rotating frame, Mol. Phys. 18, 553-9.
52. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., and Skelton, N. J. (1996) Protein NMR Spectroscopy: Principles and Practice, Academic Press, San Diego.
53. Connolly, P. J., Stern, A. S., Turner, C. J., and Hoch, J. C. (2003) Molecular dynamics of the long neurotoxin LSIII, Biochemistry 42, 14443-51.
54. Guenneugues, M., Drevet, P., Pinkasfeld, S., Gilquin, B., Menez, A., and Zinn-Justin, S. (1997) Picosecond to hour time scale dynamics of a "three finger" toxin: Correlation with its toxic and antigenic properties, Biochemistry 36, 16097-108.
55. Scarselli, M., Spiga, O., Ciutti, A., Bernini, A., Bracci, L., Lelli, B., Lozzi, L., Calamandrei, D., Di Maro, D., Klein, S., and Niccolai, N. (2002) NMR structure of α-bungarotoxin free and bound to a mimotope of the nicotinic acetylcholine receptor, Biochemistry 41, 1457-63.
56. Harel, M., Kasher, R., Nicolas, A., Guss, J. M., Balass, M., Fridkin, M., Smit, A. B., Brejc, K., Sixma, T. K., Katchalski-Katzir, E., Sussman, J. L., and Fuchs, S. (2001) The binding site of acetylcholine receptor as visualized in the X-ray structure of a complex between α-bungarotoxin and a mimotope peptide, Neuron 32, 265-75.
57. Scherf, T., Balass, M., Fuchs, S., Katchalski-Katzir, E., and Anglister, J. (1997) Three-dimensional solution structure of the complex of α-bungarotoxin with a library-derived peptide, Proc. Natl. Acad. Sci. U.S.A. 94, 6059-64.
58. Scherf, T., Kasher, R., Balass, M., Fridkin, M., Fuchs, S., and Katchalski-Katzir, E. (2001) A β-hairpin structure in a 13-mer peptide that binds α-bungarotoxin with high affinity and neutralizes its toxicity, Proc. Natl. Acad. Sci. U.S.A. 98, 6629-34.
59. Karlsson, E. (1979) in Handbook of experimental pharmacology (Lee, C. Y., Ed.) pp 159-212, Springer-Verlag, Berlin.
60. Rosenthal, J. A., Levandoski, M. M., Chang, B., Potts, J. F., Shi, Q. L., and Hawrot, E. (1999) The functional role of positively charged amino acid side chains in α-bungarotoxin revealed by site-directed mutagenesis of a His-tagged recombinant α-bungarotoxin, Biochemistry 38, 7847-55.
61. Zeng, H., Moise, L., Grant, M. A., and Hawrot, E. (2001) The solution structure of the complex formed between α-bungarotoxin and an 18mer cognate peptide derived from the α1 subunit of the nicotinic acetylcholine receptor from Torpedo californica, J. Biol. Chem. 18, 18.