Multiple loop conformations of peptides predicted by molecular dynamics simulations are compatible with nuclear magnetic resonance

Biochemistry

Volumn 44, Issue 12, 2005, Pages 4829-4840

  Carstens, Heiko ^a   Renner, Christian ^b   Milbradt, Alexander G ^b   Moroder, Luis ^b   Tavan, Paul ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; AZO DYES; CONFORMATIONS; FREE ENERGY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PROTEINS;

OCTAPEPTIDES; PEPTIDES; PROTEIN-PROTEIN INTERACTIONS; SURFACE LOOPS;

POLYPEPTIDES;

AZOBENZENE; DISULFIDE; DYE; OCTAPEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION; STRUCTURE ANALYSIS; SURFACE PROPERTY;

AMINOBENZOIC ACIDS; AZO COMPOUNDS; COLORING AGENTS; COMPUTER SIMULATION; DISULFIDES; ISOMERISM; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES, CYCLIC; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS;

EID: 15444367895     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047453r     Document Type: Article

References (66)

1. Ulloa-Aguirre, A., Stanislaus, D., Janovick, J. A., and Conn, P. M. (1999) Structure-activity relationships of G protein-coupled receptors, Arch. Med. Res. 30, 420-435.
2. Pfaff, M. (1997) in Integrin-Ligand Interaction (Eble, J. A., and Kühn, K., Eds.) pp 101-113, Springer-Verlag, Heidelberg, Germany.
3. Yu, H., Rosen, M. K., Shin, T. B., Seidel-Dugan, C., Brugge, J. S., and Schreiber, S. L. (1992) Solution structure of the SH3 domain of Src and identification of its ligand binding site, Science 258, 1665-1668.
4. Tang, K. E. S., and Dill, K. A. (1999) How experiments see fluctuations of native proteins: Perspective from an exact model, Int. J. Quantum Chem. 75, 147-164.
5. Feher, V. A., and Cavanagh, J. (1999) Millisecond-time-scale motions contribute to the function of the bacterial response regulator protein Spo0F, Nature 400, 289-293.
6. Colson, A. O., Perlman, J. H., Smolyar, A., Gershengorn, M. C., and Osman, R. (1998) Static and dynamic roles of extracellular loops in G-protein-coupled receptors: A mechanism for sequential binding of thyrotropin-releasing hormone to its receptor, Biophys. J. 74, 1087-1100.
7. Hynes, R. O. (2002) Integrins: Bidirectional, allosteric signaling machines, Cell 110, 673-687.
8. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley and Sons, New York.
9. Olejniczak, E. T., Dobson, C. M., Karplus, M., and Levy, R. M. (1984) Motional averaging of proton nuclear Overhauser effects in proteins - Predictions from a molecular dynamics simulation of lysozyme, J. Am. Chem. Soc. 106, 1923-1930.
10. Kessler, H., Griesinger, C., Lautz, J., Muller, A., van Gunsteren, W. F., and Berendsen, H. J. C. (1988) Conformational dynamics detected by nuclear magnetic resonance NOE values and J-coupling constants, J. Am. Chem. Soc. 110, 3393-3396.
11. Abseher, R., Lüdemann, S., Schreiber, H., and Steinhauser, O. (1994) Influence of molecular motion on the accuracy of NMR-derived distances - A molecular dynamics study of 2 solvated model peptides, J. Am. Chem. Soc. 116, 4006-4018.
12. Brüschweiler, R., and Case, D. A. (1994) Characterization of biomolecular structure and dynamics by NMR cross-relaxation, Prog. NMR Spectrosc. 26, 27-58.
13. Constantine, K. L., Mueller, L., Andersen, N. H., Tong, H., Wandler, C. F., Friedrichs, M. S., and Bruccoleri, R. E. (1995) Structural and dynamic properties of a β-hairpin-forming linear peptide. 1. Modeling using ensemble-averaged constraints, J. Am. Chem. Soc. 117, 10841-10854.
14. Cuniasse, P., Raynal, I., Yiotakis, A., and Dive, V. (1997) Accounting for conformational variability in NMR structure of cyclopeptides: Ensemble averaging of interproton distance and coupling constant restraints, J. Am. Chem. Soc. 119, 5239-5248.
15. Melacini, G., Zhu, Q., and Goodman, M. (1997) Multiconformational NMR analysis of sandostatin (octreotide): Equilibrium between β-sheet and partially helical structures, Biochemistry 36, 1233-1241.
16. Baysal, C., and Meirovitch, H. (1998) Determination of the stable microstates of a peptide from NOE distance constraints and optimization of atomic solvation parameters, J. Am. Chem. Soc. 120, 800-812.
17. Schneider, T. R., Brunger, A. T., and Nilges, M. (1999) Influence of internal dynamics on accuracy of protein NMR structures: Derivation of realistic model distance data from a long molecular dynamics trajectory, J. Mol. Biol. 285, 727-740.
18. Bürgi, R., Daura, X., Mark, A., Bellanda, M., Mammi, S., Peggion, E., and van Gunsteren, W. (2001) Folding study of an Aib-rich peptide in DMSO by molecular dynamics simulations, J. Pept. Res. 57, 107-118.
19. Ponder, J. W., and Case, D. A. (2003) Force fields for protein simulation, Adv. Protein Chem. 66, 27-85.
20. Tavan, P., Carstens, H., and Mathias, G. (2005) in Protein Folding Handbook (Buchner, J., and Kiefhaber, T., Eds.) Vol. 1, pp 1166-1191, Wiley-VCH, Weinheim, Germany.
21. van Gunsteren, W. F., and Berendsen, H. J. C. (1990) computer simulation of molecular dynamics - Methodology, applications, and perspectives in chemistry, Angew. Chem., Int. Ed. 29, 992-1023.
22. Brooks, C. L. (2002) Protein and peptide folding explored with molecular simulations, Acc. Chem. Res. 35, 447-454.
23. Karplus, M., and McCammon, J. A. (2002) Molecular dynamics simulations of biomolecules, Nat. Struct. Biol. 9, 646-652.
24. Daura, X., van Gunsteren, W. F., and Mark, A. E. (1999) Folding-unfolding thermodynamics of a β-heptapeptide from equilibrium simulations, Proteins 34, 269-280.
25. Daura, X., Gademann, K., Schafer, H., Jaun, B., Seebach, D., and van Gunsteren, W. F. (2001) The β-peptide hairpin in solution: Conformational study of a β-hexapeptide in methanol by NMR spectroscopy and MD simulation, J. Am. Chem. Soc. 123, 2393-2404.
26. Stocker, U., and van Gunsteren, W. F. (2000) Molecular dynamics simulation of hen egg white lysozyme: A test of the GROMOS96 force field against nuclear magnetic resonance data, Proteins 40, 145-153.
27. Arthanari, H., McConnell, K. J., Beger, R., Young, M. A., Beveridge, D. L., and Bolton, P. H. (2003) Assessment of the molecular dynamics structure of DNA in solution based on calculated and observed NMR NOESY volumes and dihedral angles from scalar coupling constants, Biopolymers 68, 3-15.
28. Li, A. J., and Daggett, V. (1995) Investigation of the solution structure of chymotrypsin inhibitor 2 using molecular dynamics: Comparison to X-ray crystallographic and NMR data, Protein Eng. 8, 1117-1128.
29. Lei, H. X., and Smith, P. E. (2003) The effects of internal water molecules on the structure and dynamics of chymotrypsin inhibitor 2, J. Phys. Chem. B 107, 1395-1402.
30. Colombo, G., Roccatano, D., and Mark, A. E. (2002) Folding and stability of the three-stranded β-sheet peptide betanova: Insights from molecular dynamics simulations, Proteins 46, 380-392.
31. Stole, R. H., Dejaegere, A. P., Lefevre, J. F., and Karplus, M. (2000) Multiple conformations of RGDW and DRGDW: A theoretical study and comparison with NMR results, J. Phys. Chem. B 104, 1624-1636.
32. Lee, M. R., and Kollman, P. A. (2001) Free-energy calculations highlight differences in accuracy between X-ray and NMR structures and add value to protein structure prediction, Structure 9, 905-916.
33. Philippopoulos, M., and Lim, C. (1999) Exploring the dynamic information content of a protein NMR structure: Comparison of a molecular dynamics simulation with the NMR and X-ray structures of Escherichia coli ribonuclease HI, Proteins 36, 87-110.
34. Prompers, J. J., and Brüschweiler, R. (2001) Reorientational eigenmode dynamics: A combined MD/NMR relaxation analysis method for flexible parts in globular proteins, J. Am. Chem. Soc. 123, 7305-7313.
35. Dvorsky, R., Hornak, V., Sevcik, J., Tyrrell, G. P., Caves, L. S. D., and Verma, C. S. (2002) Dynamics of Rnase Sa: A simulation perspective complementary to NMR/X-ray, J. Phys. Chem. B 106, 6038-6048.
36. Prabhu, N. V., Lee, A. L., Wand, A. J., and Sharp, K. A. (2003) Dynamics and entropy of a calmodulin-peptide complex studied by NMR and molecular dynamics, Biochemistry 42, 562-570.
37. Behrendt, R., Renner, C., Schenk, M., Wang, F. Q., Wachtveitl, J., Oesterhelt, D., and Moroder, L. (1999) Photomodulation of the conformation of cyclic peptides with azobenzene moieties in the peptide backbone, Angew. Chem., Int. Ed. 38, 2771-2774.
38. Renner, C., Behrendt, R., Spörlein, S., Wachtveitl, J., and Moroder, L. (2000) Photomodulation of conformational states. I. Mono- and bicyclic peptides with (4-amino)phenylazobenzoic acid as backbone constituent, Biopolymers 54, 489-500.
39. Renner, C., Cramer, J., Behrendt, R., and Moroder, L. (2000) Photomodulation of conformational states. II. Mono- and bicyclic peptides with (4-aminomethyl)phenylazobenzoic acid as backbone constituent, Biopolymers 54, 501-514.
40. Spörlein, S., Carstens, H., Satzger, H., Renner, C., Behrendt, R., Moroder, L., Tavan, P., Zinth, W., and Wachtveitl, J. (2002) Ultrafast spectroscopy reveals subnanosecond peptide conformational dynamics and validates molecular dynamics simulation, Proc. Natl. Acad. Sci. U.S.A. 99, 7998-8002.
41. Bredenbeck, J., Helbing, J., Sieg, A., Schrader, T., Zinth, W., Renner, C., Behrendt, R., Moroder, L., Wachtveitl, J., and Hamm, P. (2003) Picosecond conformational transition and equilibration of a cyclic peptide, Proc. Natl. Acad. Sci. U.S.A. 100, 6452-6457.
42. Wachtveitl, J., Sporlein, S., Satzger, H., Fonrobert, B., Renner, C., Behrendt, R., Oesterhelt, D., Moroder, L., and Zinth, W. (2004) Ultrafast conformational dynamics in cyclic azobenzene peptides of increased flexibility, Biophys. J. 86, 2350-2362.
43. Carstens, H. (2004) Doktorarbeit, Fakultät für Physik, Ludwig-Maximilians-Universität München, Munich, Germany.
44. Bax, A., and Davis, D. G. (1985) MLEV-17 based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 355-360.
45. Bax, A., and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy, J. Magn. Reson. 63, 207-213.
46. 1H NMR spectra of proteins via double quantum filtering, Biochem. Biophys. Res. Commun. 117, 479-485.
47. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins, J. Phys. Chem. B 102, 3586-3616.
48. Bordat, P., Sacristan, J., Reith, D., Girard, S., Glattli, A., and Müller-Plathe, F. (2003) An improved dimethyl sulfoxide force field for molecular dynamics simulations, Chem. Phys. Lett. 374, 201-205.
49. Mathias, G., Egwolf, B., Nonella, M., and Tavan, P. (2003) A fast multipole method combined with a reaction field for long-range electrostatics in molecular dynamics simulations: The effects of truncation on the properties of water, J. Chem. Phys. 118, 10847-10860.
50. Niedermeier, C., and Tavan, P. (1994) A structure adapted multipole method for electrostatic interactions in protein dynamics, J. Chem. Phys. 101, 734-748.
51. Eichinger, M., Grubmüller, H., Heller, H., and Tavan, P. (1997) FAMUSAMM: An algorithm for rapid evaluation of electrostatic interactions in molecular dynamics simulations, J. Comput. Chem. 18, 1729-1749.
52. Krautler, V., van Gunsteren, W. F., and Hünenberger, P. H. (2001) A fast SHAKE: Algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations, J. Comput. Chem. 22, 501-508.
53. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
54. Kloppenburg, M., and Tavan, P. (1997) Deterministic annealing for density estimation by multivariate normal mixtures, Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. 55, R2089-R2092.
55. Albrecht, S., Busch, J., Kloppenburg, M., Metze, F., and Tavan, P. (2000) Generalized radial basis function networks for classification and novelty detection: Self-organization of optimal Bayesian decision, Neural Networks 13, 1075-1093.
56. Grubmüller, H., and Tavan, P. (1994) Molecular dynamics of conformational substates for a simplified protein model, J. Chem. Phys. 101, 5047-5057.
57. Hamprecht, F. A., Peter, C., Daura, X., Thiel, W., and van Gunsteren, W. F. (2001) A strategy for analysis of (molecular) equilibrium simulations: Configuration space density estimation, clustering, and visualization, J. Chem. Phys. 114, 2079-2089.
58. Jammalamadaka, S. R., and SenGupta, A. (2001) Topics in Circular Statistics, World Scientific Publishing, Singapore.
59. Bürgi, R., Pitera, J., and van Gunsteren, W. F. (2001) Assessing the effect of conformational averaging on the measured values of observables, J. Biomol. NMR 19, 305-320.
60. Abseher, R., Horstink, L., Hilbers, C. W., and Nilges, M. (1998) Essential spaces defined by NMR structure ensembles and molecular dynamics simulation show significant overlap, Proteins 31, 370-382.
61. Balsera, M. A., Wriggers, W., Oono, Y., and Schulten, K. (1996) Principal component analysis and long time protein dynamics, J. Phys. Chem. 100, 2567-2572.
62. Becker, O. M. (1998) Principal coordinate maps of molecular potential energy surfaces, J. Comput. Chem. 19, 1255-1267.
63. de Groot, B. L., Daura, X., Mark, A. E., and Grubmüller, H. (2001) Essential dynamics of reversible peptide folding: Memory-free conformational dynamics governed by internal hydrogen bonds, J. Mol. Biol. 309, 299-313.
64. Levy, Y., and Becker, O. M. (2001) Energy landscapes of conformationally constrained peptides, J. Chem. Phys. 114, 993-1009.
65. Rhee, Y. M., and Pande, V. S. (2003) Multiplexed-replica exchange molecular dynamics method for protein folding simulation, Biophys. J. 84, 775-786.
66. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD-Visual Molecular Dynamics, J. Mol. Graphics 14, 33-38.