Characterization of the backbone and side chain dynamics of the CaM-CaMKIp complex reveals microscopic contributions to protein conformational entropy

Biochemistry

Volumn 45, Issue 32, 2006, Pages 9841-9848

  Frederick, Kendra King ^a   Kranz, James K ^a,c   Wand, A Joshua ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Johnson and Johnson PRD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; ENTROPY; INTERFACES (MATERIALS); THERMODYNAMICS;

CALMODULIN; HIGH-AFFINITY BINDING INTERACTIONS; MOLECULAR RECOGNITION; PROTEIN ENTROPY;

PROTEINS;

AMIDE; CALCIUM; CALMODULIN; CALMODULIN DEPENDENT PROTEIN KINASE I; CALMODULIN DERIVATIVE; METHYL GROUP; MYOSIN LIGHT CHAIN KINASE; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CALCIUM SIGNALING; ENTROPY; MICROSCOPY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALMODULIN; CHICKENS; ENTROPY; HYDROGEN BONDING; MODELS, MOLECULAR; MYOSIN-LIGHT-CHAIN KINASE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; TITRIMETRY;

EID: 33747508183     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060865a     Document Type: Article

References (42)

1. Chin, D., and Means, A. R. (2000) Calmodulin: A prototypical calcium sensor, Trends Cell Biol. 10, 322-328.
2. Crivici, A., and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin, Annu. Rev. Biophys. Biomol. Struct. 24, 85-116.
3. Babu, Y. S., Bugg, C. E., and Cook, W. J. (1988) Structure of calmodulin refined at 2.2 Å resolution, J. Mol. Biol. 204, 191-204.
4. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible, Biochemistry 31, 5269-5278.
5. Rhoads, A. R., and Friedberg, F. (1997) Sequence motifs for calmodulin recognition, FASEB J. 11, 331-340.
6. Kranz, J. K., Lee, E. K., Nairn, A. C., and Wand, A. J. (2002) A direct test of the reductionist approach to structural studies of calmodulin activity: Relevance of peptide models of target proteins, J. Biol. Chem. 277, 16351-16354.
7. Brokx, R. D., Lopez, M. M., Vogel, H. J., and Makhatadze, G. I. (2001) Energetics of target peptide binding by calmodulin reveals different modes of binding, J. Biol. Chem. 276, 14083-14091.
8. Lee, A. L., Kinnear, S. A., and Wand, A. J. (2000) Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex, Nat. Struct. Biol. 7, 72-77.
9. Li, Z., Raychaudhuri, S., and Wand, A. J. (1996) Insights into the local residual entropy of proteins provided by NMR relaxation, Protein Sci. 5, 2647-2650.
10. Urbauer, J. L., Short, J. H., Dow, L. K., and Wand, A. J. (1995) Structural analysis of a novel interaction by calmodulin: High-affinity binding of a peptide in the absence of calcium, Biochemistry 34, 8099-8109.
11. 2+-binding domains, Biochemistry 28, 4011-4020.
12. Muhandiram, D. R., and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity, J. Magn. Reson., Ser. B 103, 203-216.
13. Montelione, G. T., Lyons, B. A., Emerson, S. D., and Tashiro, M. (1992) An Efficient Triple Resonance Experiment Using C-13 Isotropic Mixing for Determining Sequence-Specific Resonance Assignments of Isotopically-Enriched Proteins, J. Am. Chem. Soc. 114, 10974-10975.
14. Uhrin, D., Uhrinova, S., Leadbeater, C., Nairn, J., Price, N. C., and Barlow, P. N. (2000) 3D HCCH3-TOCSY for resonance assignment of methyl-containing side chains in C-13-labeled proteins, J. Magn. Reson. 142, 288-293.
15. 13C labeling, Biochemistry 28, 7510-7516.
16. 3 Angular Information from Long-Range Proton-Carbon and Carbon-Carbon J-Correlation in a Calmodulin Peptide Complex, J. Biomol. NMR 4, 787-797.
17. Yuan, T., Gomes, A. V., Barnes, J. A., Hunter, H. N., and Vogel, H. J. (2004) Spectroscopic characterization of the calmodulin-binding and autoinhibitory domains of calcium/calmodulin-dependent protein kinase I, Arch. Biochem. Biophys. 421, 192-206.
18. Goddard, T., and Kneller, D. (2004) SPARKY 3, University of California, San Francisco.
19. 15N NMR relaxation, Biochemistry 33, 5984-6003.
20. 2H-Labeled Proteins in Solution, J. Am. Chem. Soc. 117, 11536-11544.
21. 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.
22. Dellwo, M. J., and Wand, A. J. (1989) Model-Independent and Model-Dependent Analysis of the Global and Internal Dynamics of Cyclosporine-A, J. Am. Chem. Soc. 111, 4571-4578.
23. Kneller, J. M., Lu, M., and Bracken, C. (2002) An effective method for the discrimination of motional anisotropy and chemical exchange, J. Am. Chem. Soc. 124, 1852-1853.
24. Lee, A. L., and Wand, A. J. (1999) Assessing potential bias in the determination of rotational correlation times of proteins by NMR relaxation, J. Biomol. NMR 13, 101-112.
25. Ottiger, M., and Bax, A. (1998) Determination of relative N-H-N, N-C′, Cα-C′, and Cα-Hα effective bond lengths in a protein by NMR in a dilute liquid crystalline phase, J. Am. Chem. Soc. 120, 12334-12341.
26. Mittermaier, A., and Kay, L. E. (1999) Measurement of methyl H-2 quadrupolar couplings in oriented proteins. How uniform is the quadrupolar coupling constant? J. Am. Chem. Soc. 121, 10608-10613.
27. Edgington, E. (1995) Randomization Tests, 3rd ed., Marcel Dekker, New York.
28. Nicholls, A., Sharp, K. A., and Honig, B. (1991) Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins 11, 281-296.
29. Liu, W., Flynn, P. F., Fuentes, E. J., Kranz, J. K., McCormick, M., and Wand, A. J. (2001) Main chain and side chain dynamics of oxidized flavodoxin from Cyanobacterium anabaena, Biochemistry 40, 14744-14753.
30. Lee, A. L., and Wand, A. J. (2001) Microscopic origins of entropy, heat capacity and the glass transition in proteins, Nature 411, 501-504.
31. Igumenova, T. I., Frederick, K. K., and Wand, A. J. (2006) Characterization of the Fast Dynamics of Protein Amino Acid Side Chains Using NMR Relaxation in Solution, Chem. Rev. 106, 1672-1699.
32. Scott, D. (1979) On optimal and data-based histograms, Biometrika 10, 605-610.
33. Best, R. B., Clarke, J., and Karplus, M. (2004) The origin of protein sidechain order parameter distributions, J. Am. Chem. Soc. 126, 7734-7735.
34. Lee, A. L., Sharp, K. A., Kranz, J. K., Song, X. J., and Wand, A. J. (2002) Temperature dependence of the internal dynamics of a calmodulin-peptide complex, Biochemistry 41, 13814-13825.
35. CN couplings, J. Am. Chem. Soc. 125, 8959-8966.
36. Best, R. B., Clarke, J., and 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.
37. Hu, H., Hermans, J., and Lee, A. L. (2005) Relating side-chain mobility in proteins to rotameric transitions: Insights from molecular dynamics simulations and NMR, J. Biomol. NMR 32, 151-162.
38. Marlow, M. S., and Wand, A. J. (2006) Conformational dynamics of calmodulin in complex with the calmodulin dependent kinase kinase calmodulin-binding domain, Biochemistry 45, 8732-8741.
39. Yang, D. W., and Kay, L. E. (1996) Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: Application to protein folding, J. Mol. Biol. 263, 369-382.
40. 2+ Binding by Calbindin-D(9k), J. Am. Chem. Soc. 115, 9832-9833.
41. Clapperton, J. A., Martin, S. R., Smerdon, S. J., Gamblin, S. J., and Bayley, P. M. (2002) Structure of the complex of calmodulin with the target sequence of calmodulin-dependent protein kinase I: Studies of the kinase activation mechanism, Biochemistry 41, 14669-14679.
42. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.