Dynamic motion of helix A in the amino-terminal domain of calmodulin is stabilized upon calcium activation

Biochemistry

Volumn 44, Issue 3, 2005, Pages 905-914

  Chen, Baowei ^a   Mayer, M Uljana ^a   Markillie, Lye Meng ^a   Stenoien, David L ^a   Squier, Thomas C ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANISOTROPY; CALCIUM; CALCIUM COMPOUNDS; FLUORESCENCE; PROTEINS;

CALCIUM BINDING; GLOBULAR DOMAINS; INTERNAL DYNAMICS;

BIOCHEMISTRY;

4',5' BIS(1,3,2 DITHIOARSOLAN 2 YL)FLUORESCEIN; CALCIUM; CALMODULIN; FLUORESCEIN; HELIX A PROTEIN; PROTEIN; SOLVENT; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL DOMAIN; AMINO TERMINAL SEQUENCE; ANISOTROPY; ARTICLE; CALCIUM BINDING; DYNAMICS; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN IMMOBILIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; TETRACYSTEINE BINDING MOTIF;

BASE SEQUENCE; CALCIUM; CALMODULIN; DNA PRIMERS; FLUORESCEINS; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; MUTAGENESIS, SITE-DIRECTED; ORGANOMETALLIC COMPOUNDS; PROTEIN CONFORMATION;

EID: 12344296442     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048332u     Document Type: Article

References (65)

1. James, P., Vorherr, T., and Carafoli, E. (1995) Calmodulin-binding domains: Just two faced or multi-faceted? Trends Biochem. Sci. 20, 38-42.
2. Yap, K. L., Kim, J., Truong, K., Sherman, M., Yuan, T., and Ikura, M. (2000) Calmodulin target database, J. Struct. Funct. Genomics 1, 8-14.
3. Squier, T. C., and Bigelow, D. J. (2000) Protein oxidation and age-dependent alterations in calcium homeostasis, Front. Biosci. 5, 1-23.
4. Wang, H., and Storm, D. R. (2003) Calcium-regulated adenylyl cyclases: Cross-talk and plasticity in central nervous system, Mol. Pharmacol. 63, 463-468.
5. Fournier, V., Leclerc, P., Cormier, N., and Bailey, J. L. (2003) Implication of calmodulin-dependent phosphodiesterase type 1 during bovine sperm capacitation, J. Androl. 24, 104-112.
6. LaPorte, D. C., Wierman, B. M., and Storm, D. R. (1980) Calcium-induced exposure of a hydrophobic surface on calmodulin, Biochemistry 19, 3814-3819.
7. 2+-calmodulin reveals flexible hand-like properties of its domains, Nat. Struct. Biol. 8, 990-997.
8. 2+ binding sites in calmodulin and troponin C alter interhelical angle movements, FEBS Lett. 561, 51-57.
9. Yang, C., Jas, G. S., and Kuczera, K. (2004) Structure, dynamics and interaction with kinase targets: Computer simulations of calmodulin, Biochim. Biophys. Acta 1697, 289-300.
10. Persechini, A., McMillan, K., and Leaky, P. (1994) Activation of myosin light chain kinase and nitric oxide synthase activities by calmodulin fragments, J. Biol. Chem. 23, 16148-16154.
11. Crivici, A., and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin, Annu. Rev. Biophys. Biomol. Struct. 24, 85-116.
12. Ehrhardt, M. R., Urbauer, J. L., and Wand, A. J. (1995) The energetics and dynamics of molecular recognition by calmodulin, Biochemistry 34, 2731-2738.
13. Sun, H., and Squier, T. C. (2000) Ordered and cooperative binding of opposing globular domains of calmodulin to the plasma membrane Ca-ATPase, J. Biol. Chem. 275, 1731-1738.
14. Kranz, J. K., Flynn, P. F., Fuentes, E. J., and Wand, A. J. (2002) Dissection of the pathway of molecular recognition by calmodulin, Biochemistry 41, 2599-2608.
15. Shifman, J. M., and Mayo, S. L. (2003) Exploring the origins of binding specificity through the computational redesign of calmodulin, Proc. Natl. Acad. Sci. U.S.A. 100, 13274-13279.
16. Yamniuk, A. P., and Vogel, H. J. (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides, Mol. Biotechnol. 27, 33-57.
17. 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.
18. Chattopadhyaya, R., Mendor, W. E., Means, A. R., and Quiocho, F. A. (1992) Calmodulin structure refined at 1.7 Å resolution, J. Mol. Biol. 228, 1177-1192.
19. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C. B., and Bax, A. (1995) Solution structure of calcium-free calmodulin, Nat. Struct. Biol. 2, 768-776.
20. 2+-bound calmodulin: An analysis of disorder and implications for functionally relevant plasticity, J. Mol. Biol. 301, 1237-1256.
21. Jaren, O. R., Krantz, J. K., Sorensen, B. R., Wand, A. J., and Shea, M. A. (2002) Calcium-induced conformational switching of Paramecium calmodulin provides evidence for domain coupling, Biochemistry 41, 14158-14166.
22. 2+-calmodulin, Structure 11, 1303-1307.
23. Wriggers, W., Mehler, E., Pitici, F., Weinstein, H., and Schulten, K. (1998) Structure and dynamics of calmodulin in solution, Biophys. J. 74, 1622-1639.
24. Griffin, B. A., Adams, S. R., and Tsien, R. Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells, Science 281, 269-272.
25. Adams, S. R., Campbell, R. E., Gross, L. A., Martin, B. R., Walkup, G. K., Yao, Y., Liopis, J., and Tsien, R. Y. (2002) New biarsenical ligands are tetracysteine motifs for protein labeling in vitro and vivo: Synthesis and biological application, J. Am. Chem. Soc. 124, 6063-6075.
26. Strasburg, G. M., Hogan, M., Birmachu, W., Thomas, D. D., and Louis, C. F. (1988) Site-specific derivatives of wheat germ calmodulin. Interactions with troponin and sarcoplasmic reticulum, J. Biol. Chem. 263, 542-548.
27. 138 disrupts the structural coupling between the opposing domains in vertebrate calmodulin, Biochemistry 40, 9605-9617.
28. Klee, C. B., Crouch, T. H., and Krinks, M. H. (1979) Calcineurin: A calcium- and calmodulin-binding protein of the nervous system, Proc. Natl. Acad. Sci. U.S.A. 76, 6270-6273.
29. Schiefer, S. (1986) Calmodulin, in Methods of enzymatic analysis (Bergmeyer, H. U., Bergmeyer, J., and Grable, M., Eds.) Vol. 9, pp 317-331, VCH Publishers, Deerfield Beach, FL.
30. Lakowicz. J. R. (1999) in Principles of Fluorescence Spectroscopy, 2nd ed., Kluwer Academic/Plenum Publishers, New York.
31. Gratton, E., and Limkeman, M. (1983) A continuously variable frequency cross-correlation phase fluorometer with picosecond resolution, Biophys. J. 44, 315-324.
32. Lakowicz, J. R., and Maliwal, B. (1985) Construction and performance of a variable-frequency phase-modulation fluorometer, Biophys. Chem. 21, 61-78.
33. Bevington, P. R. (1969) in Data Reduction and Error Analysis for the Physical Sciences, McGraw-Hill, New York.
34. Hunter, G. W., and Squier, T. C. (1998) Phospholipid acyl chain rotational dynamics are independent of headgroup structure in unilamellar vesicles containing binary mixtures of dioleoyl-phosphatidylcholine and dioleoyl-phosphatidylethanolamine, Biochim. Biophys. Acta 1415, 63-76.
35. Weber, G. (1981) Resolution of the fluorescence lifetimes in a heterogeneous system by phase and modulation measurements, J. Phys. Chem. 85, 949-953.
36. Faga, L. A., Sorensen, B. R., VanScyoc, W. S., and Shea, M. A. (2003) Basic interdomain boundary residues in calmodulin decrease calcium affinity of sites 1 and 11 by stabilizing helix-helix interactions, Proteins 50, 381-391.
37. Zhang, M., Li, M., Wang, J. H., and Vogel, H. J. (1994) The effect of Met → Leu mutations on calmodulin's ability to activate cyclic nucleotide phosphodiesterase, J. Biol. Chem. 269, 15546-15552.
38. Nakanishi, J., Maeda, M., and Umezawa, Y. (2004) A new protein conformation indicator based on biarsenical fluorescent with an extended benzoic acid moiety, Anal. Sci. 20, 273-278.
39. Chen, B., Jones, T. E., and Bigelow, D. J. (1999) The nucleotide-binding site of the sarcoplasmic reticulum Ca-ATPase is conformationally altered in aged skeletal muscle, Biochemistry 38, 14887-14896.
40. Chen, B., and Bigelow, D. J. (2002) Phosphorylation induces a conformational transition near the lipid-water interface of phospholamban reconstituted with the Ca-ATPase, Biochemistry 41, 13965-13972.
41. Steiner, R. E. (1991) in Fluorescence Spectroscopy (Lakowicz, J. R., Ed.) Vol. 2, pp 1-52, Plenum Press, New York.
42. Cantor, C. R., and Schimmel, P. R. (1980) Biophysical Chemistry, Part II: Techniques for the study of biological structure and function, p 461, W. H. Freeman and Co., San Francisco.
43. Garcia de la Torre, J., Huertas, M. L., and Carrasco, B. (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure, Biophys. J. 78. 719-730.
44. Small, E. W., and Anderson, S. R. (1988) Fluorescence anisotropy decay demonstrates calcium-dependent shape changes in photo-cross-linked calmodulin, Biochemistry 27, 419-428.
45. Yao, Y., Schöneich, C., and Squier, T. C. (1994) Resolution of structural changes associated with calcium activation of calmodulin using frequency domain fluorescence spectroscopy, Biochemistry 33, 7797-7810.
46. Sun, H., Yin, D., and Squier, T. C. (1999) Calcium-dependent structural coupling between opposing globular domains of calmodulin involves the central helix, Biochemistry 38, 12266-12279.
47. Chang, S.-L., Szabo, A., and Tjandra, N. (2003) Temperature dependence of domain motions of calmodulin probes by NMR relaxation at multiple fields, J. Am. Chem. Soc. 125, 11379-11384.
48. Beechem, J. M., Gratton, E., Ameloot, M., Knutson, J. R., and Brand, L. (1991) The global analysis of fluorescence intensity and anisotropy decay data: Second generation theory and programs, in Topics in Fluorescence Spectroscopy (Lakowicz, J. R., Ed.) pp 241-305, Plenum Press, New York.
49. Kinosita, K., Jr., Ishiwata, S., Yoshimura, H., Asai, H., and Ikegami, A. (1984) Submicrosecond and microsecond rotational motions of myosin head in solution and in myosin synthetic filaments as revealed by time-resolved optical anisotropy decay measurements, Biochemistry 23, 5963-5975.
50. Prochniewicz, E., Zhang, Q., Howard, E. C., and Thomas, D. D. (1996) Microsecond rotational dynamics of actin: Spectroscopic detection and theoretical simulation, J. Mol. Biol. 255, 446-457.
51. Sabbert, D., Engelbrecht, S., and Junge, W. (1997) Functional and idling rotatory motion within F1-ATPase, Proc. Natl. Acad. Sci. U.S.A. 94, 4401-4405.
52. Shea, M. A., Verhoeven, A. S., and Pedigo, S. (1996) Calcium-induced interactions of calmodulin domains revealed by quantitative thrombin footprinting of Arg37 and Arg106, Biochemistry 35, 2943-2957.
53. Yao, Y., Yin, D., Jas, G., Kuczera, K., Williams, T. D., Schöneich, Ch., and Squier, T. C. (1996) Oxidative modification of a carboxyl-terminal vicinal methionine in calmodulin by hydrogen peroxide inhibits calmodulin-dependent activation of the plasma membrane Ca-ATPase, Biochemistry 35, 2767-2789.
54. Gao, J., Yin, D., Yao, Y., Sun, H., Qin, Z., Schöneich, Ch., Williams, T. D., and Squier, T. C. (1998) Loss of conformational stability in calmodulin upon methionine oxidation, Biophys. J. 74, 1115-1134.
55. 2 modulates the ability to activate the plasma membrane Ca-ATPase, Chem. Res. Toxicol. 13, 103-110.
56. 148, Biochemistry 39, 10255-10268.
57. Qin, Z., and Squier, T. C. (2001) Calcium-dependent stabilization of the central sequence between Met76 and Ser81 in vertebrate calmodulin, Biophys. J. 81, 2908-2918.
58. VanScyoc, W. S., and Shea, M. A. (2001) Phenyalanine fluorescence studies of calcium binding to N-domain fragments of Paramecium calmodulin mutants show increased calcium affinity correlates with increased disorder, Protein Sci. 10, 1758-1768.
59. Sorensen, B. R., Faga, L. A., Hultman, R., and Shea, M. A. (2002) An interdomain linker increases the thermostability and decreases the calcium affinity of the calmodulin N-domain, Biochemistry 41, 15-20.
60. VanScyoc, W. S., Sorensen, B. R., Rusinova, E., Laws, W. R., Ross, J. B. A., and Shea, M. A. (2002) Calcium binding to calmodulin mutants monitored by domain-specific intrinsic phenyalanine and tyrosine fluorescence, Biophys. J. 83, 2767-2780.
61. Vigil, D., Gallagher, S. C., Trewhella, J., and Garcia, A. E. (2001) Functional dynamics of the hydrophobic cleft in the N-domain of calmodulin, Biophys. J. 80, 2082-2092.
62. Barbato, G., Ikura, M., Kay, L. E., Pastor, R. W., and Bax, A. (1992) Backbone dynamics of calmodulin studied by nitrogen-15 relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible, Biochemistry 31, 5269-5278.
63. Gao, J., Yao, Y., and Squier, T. C. (2001) Oxidatively modified calmodulin binds to the plasma membrane Ca-ATPase in a nonproductive and conformationally disordered complex, Biophys. J. 80, 1791-1801.
64. Ikura, M., Spera, S., Barbato, G., Kay, L. E., Krinks, M., and Bax, A. (1991) Secondary structure and side-chain proton and carbon-13 resonance assignments of calmodulin in solution by heteronuclear multidimensional NMR spectroscopy, Biochemistry 30, 9216-9228.
65. Jencks, W. P. (1969) Catalysis in Chemistry and Enzymology, pp 564-565, McGraw-Hill, New York.