Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs

Biochemical Journal

Volumn 405, Issue 2, 2007, Pages 199-221

  Gifford, Jessica L ^a   Walsh, Michael P ^a   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Calbindin D9K; Calcium ions (Ca2+); Calmodulin; Co operativity; EF hand; Magnesium ions (Mg2+)

Indexed keywords

CALBINDIN; CALCIUM IONS; CALMODULIN; CYTOPLASMIC CONCENTRATION; MAGNESIUM IONS;

BINDING SITES; CONCENTRATION (PROCESS); MAGNESIUM COMPOUNDS; PROTEINS; SURFACE STRUCTURE;

CALCIUM COMPOUNDS;

CALCIUM ION; HELIX LOOP HELIX PROTEIN; MAGNESIUM ION; CALBINDIN; CALCIUM; CALMODULIN; MAGNESIUM;

CALCIUM BINDING; CALCIUM SIGNALING; CHEMICAL STRUCTURE; ENTHALPY; ENTROPY; EUKARYOTIC CELL; METAL BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; THERMODYNAMICS;

EUKARYOTA;

AMINO ACID SEQUENCE; CALCIUM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CALMODULIN; EF HAND MOTIFS; MAGNESIUM; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN INTERACTION MAPPING; THERMODYNAMICS;

EID: 34447130835     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070255     Document Type: Review

References (175)

1. Berridge, M. J., Lipp, P. and Bootman, M. D. (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21
2. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529
3. Grabarek, Z. (2006) Structural basis for diversity of the EF-hand calcium-binding proteins. J. Mol. Biol. 359, 509-525
4. Capozzi, F., Casadei, F. and Luchinat, C. (2006) EF-hand protein dynamics and evolution of calcium signal transduction: an NMR view. J. Biol. Inorg. Chem. 11, 949-962
5. Falke, J. J., Drake, S. K., Hazard, A. L. and Peersen, O. B. (1994) Molecular tuning of ion binding to calcium signalling proteins. Q. Rev. Biophys. 27, 219-290
6. Linse, S. and Forsen, S. (1995) Determinants that govern high-affinity calcium binding. Adv. Second Messenger Phosphoprotein Res. 30, 89-151
7. Kretsinger, R. H. and Nockolds, C. E. (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem. 248, 3313-3326
8. Pidcock, E. and Moore, G. R. (2001) Structural characteristics of protein binding sites for calcium and lanthanide ions. J. Biol. Inorg. Chem. 6, 479-489
9. McPhalen, C. A., Strynadka, N. C. and James, M. N. (1991) Calcium-binding sites in proteins: a structural perspective. Adv. Protein Chem. 42, 77-144
10. Strynadka, N. C. and James, M. N. (1989) Crystal structures of the helix-loop-helix calcium-binding proteins. Annu. Rev. Biochem. 58, 951-998
11. Godzik, A. and Sander, C. (1989) Conservation of residue interactions in a family of Ca-binding proteins. Protein Eng. 2, 589-596
12. 2+-saturated calmodulin D129N mutant studied by multiple molecular dynamics simulations. Protein Sci. 12, 2215-2229
13. Evenas, J., Malmendal, A. and Akke, M. (2001) Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant. Structure 9, 185-195
14. 2+ binding to calmodulin loop. Biophys. J. 90, 3043-3051
15. 9k in the apo and singly and doubly calcium-loaded states. Proteins 33, 265-284
16. Haiech, J., Moulhaye, S. B. and Kilhoffer, M. C. (2004) The EF-handome: combining comparative genomic study using FamDBtool, a new bioinformatics tool and the network of expertise of the European Calcium Society. Biochim. Biophys. Acta 1742, 179-183
17. Cook, W. J., Jeffrey, L. C., Cox, J. A. and Vijay-Kumar, S. (1993) Structure of a sarcoplasmic calcium-binding protein from amphioxus refined at 2.4 Å resolution. J. Mol. Biol. 229, 461-471
18. Vijay-Kumar, S. and Cook, W. J. (1992) Structure of a sarcoplasmic calcium-binding protein from Nereis diversicolor refined at 2.0 A resolution. J. Mol. Biol. 224, 413-426
19. Gentry, H. R., Singer, A. U., Betts, L., Yang, C., Ferrara, J. D., Sondek, J. and Parise, L. V. (2005) Structural and biochemical characterization of CIB1 delineates a new family of EF-hand-containing proteins. J. Biol. Chem. 280, 8407-8415
20. Nagae, M., Nozawa, A., Koizumi, N., Sano, H., Hashimoto, H., Sato, M. and Shimizu, T. (2003) The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana. J. Biol. Chem. 278, 42240-42246
21. 2+-binding module in BM-40. Nat. Struct. Biol. 3, 67-73
22. Houdusse, A. and Cohen, C. (1996) Structure of the regulatory domain of scallop myosin at 2 Å resolution: implications for regulation. Structure 4, 21-32
23. 2+-induced conformational changes. Nat. Struct. Biol. 4, 532-538
24. 2+ affinities and target recognition. J. Biol. Chem. 275, 10514-10518
25. 2+-induced changes in penta-EF-hand proteins. Structure 9, 267-275
26. 2+ to a canonical EF-hand of a conventional myosin. J. Biol. Chem. 280, 41458-41464
27. Biekofsky, R. R. and Feeney, J. (1998) Co-operative cyclic interactions involved in metal binding to pairs of sites in EF-hand proteins. FEBS Lett. 439, 101-106
28. 2+ binding and conformational changes in a calmodulin domain. Biochemistry 37, 13744-13754
29. Malmendal, A., Evenas, J., Forsen, S. and Akke, M. (1999) Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J. Mol. Biol. 293, 883-899
30. 15N NMR relaxation. Biochemistry 32, 9832-9844
31. 9k. Nat. Struct. Biol. 7, 245-250
32. Reid, R. E. (1990) Synthetic fragments of calmodulin calcium-binding site III. A test of the acid pair hypothesis. J. Biol. Chem. 265, 5971-5976
33. 1H NMR structural evidence. Science 249, 280-283
34. Shaw, G. S., Findlay, W. A., Semchuk, P. D., Hodges, R. S. and Sykes, B. D. (1992) Specific formation of a heterodimeric two-site calcium-binding domain from synthetic peptides. J. Am. Chem. Soc. 114, 6258-6259
35. 9k: stability, calcium binding and NMR studies. Protein Sci. 2, 985-1000
36. Durussel, I., Luan-Rilliet, Y., Petrova, T., Takagi, T. and Cox, J. A. (1993) Cation binding and conformation of tryptic fragments of Nereis sarcoplasmic calcium-binding protein: calcium-induced homo- and heterodimerization. Biochemistry 32, 2394-2400
37. Reid, R. E., Gariepy, J., Saund, A. K. and Hodges, R. S. (1981) Calcium-induced protein folding. Structure-affinity relationships in synthetic analogs of the helix-loop-helix calcium binding unit. J. Biol. Chem. 256, 2742-2751
38. Shaw, G. S., Golden, L. F., Hodges, R. S. and Sykes, B. D. (1991) Interactions between paired calcium-binding sites in proteins: NMR determination of the stoichiometry of calicum binding to a synthetic troponin-C peptide. J. Am. Chem. Soc. 113, 5557-5563
39. Lopez, M. M., Chin, D. H., Baldwin, R. L. and Makhatadze, G. I. (2002) The enthalpy of the alanine peptide helix measured by isothermal titration calorimetry using metal-binding to induce helix formation. Proc. Natl. Acad. Sci. U.S.A. 99, 1298-1302
40. Tsalkova, T. N. and Privalov, P. L. (1980) Stability of troponin C. Biochim. Biophys. Acta 624, 196-204
41. Herzberg, O. and James, M. N. (1988) Refined crystal structure of troponin C from turkey skeletal muscle at 2.0 Å resolution. J. Mol. Biol. 203, 761-779
42. Babu, Y. S., Sack, J. S., Greenhough, T. J., Bugg, C. E., Means, A. R. and Cook, W. J. (1985) Three-dimensional structure of calmodulin. Nature 315, 37-40
43. Ames, J. B., Hendricks, K. B., Strahl, T., Huttner, I. G., Hamasaki, N. and Thorner, J. (2000) Structure and calcium-binding properties of Frq1, a novel calcium sensor in the yeast Saccharomyces cerevisiae. Biochemistry 39, 12149-12161
44. Ames, J. B., Dizhoor, A. M., Ikura, M., Palczewski, K. and Stryer, L. (1999) Three-dimensional structure of guanylyl cyclase activating protein-2, a calcium-sensitive modulator of photoreceptor guanylyl cyclases. J. Biol. Chem. 274, 19329-19337
45. Rabah, G., Popescu, R., Cox, J. A., Engelborghs, Y. and Craescu, C. T. (2005) Solution structure and internal dynamics of NSCP, a compact calcium-binding protein. FEBS J. 272, 2022-2036
46. 28K. Nat. Struct. Mol. Biol. 13, 641-647
47. 2+ acting at an EF-hand motif in the COOH-terminal domain. J. Gen. Physiol. 126, 311-323
48. Babini, E., Bertini, I., Capozzi, F., Luchinat, C., Quattrone, A. and Turano, M. (2005) Principal component analysis of the conformational freedom within the EF-hand superfamily. J. Proteome Res. 4, 1961-1971
49. Cox, J. A., Durussel, I., Scott, D. J. and Berchtold, M. W. (1999) Remodeling of the AB site of rat paralbumin and oncomodulin into a canonical EF-hand. Eur. J. Biochem. 264, 790-799
50. 2+-dependent processes in the full-length protein. J. Mol. Biol. 317, 447-458
51. Jia, J., Han, Q., Borregaard, N., Lollike, K. and Cygler, M. (2000) Crystal structure of human grancalcin, a member of the penta-EF-hand protein family. J. Mol. Biol. 300, 1271-1281
52. Kitaura, Y., Satoh, H., Takahashi, H., Shibata, H. and Maki, M. (2002) Both ALG-2 and peflin, penta-EF-hand (PEF) proteins, are stabilized by dimerization through their fifth EF-hand regions. Arch. Biochem. Biophys. 399, 12-18
53. 2+-bound structures of a multidomain EF-hand protein, CBP40, from the lower eukaryote Physamm polycephalum. Structure 11, 75-85
54. Meng, W., Sawasdikosol, S., Burakoff, S. J. and Eck, M. J. (1999) Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase. Nature 398, 84-90
55. Christova, P., Cox, J. A. and Craescu, C. T. (2000) Ion-induced conformational and stability changes in Nereis sarcoplasmic calcium binding protein: evidence that the APO state is a molten globule. Proteins 40, 177-184
56. 2+ ion. FEBS Lett. 395, 89-94
57. Theret, I., Baladi, S., Cox, J. A., Sakamoto, H. and Craescu, C. T. (2000) Sequential calcium binding to the regulatory domain of calcium vector protein reveals functional asymmetry and a novel mode of structural rearrangement. Biochemistry 39, 7920-7926
58. 2+. Protein Sci. 10, 74-82
59. Li, M. X., Chandra, M., Pearlstone, J. R., Racher, K. I., Trigo-Gonzalez, G., Borgford, T., Kay, C. M. and Smillie, L. B. (1994) Properties of isolated recombinant N and C domains of chicken troponin C. Biochemistry 33, 917-925
60. 2+ domains of troponin C. Effect of pH. Eur. J. Biochem. 132, 85-88
61. Bairoch, A. and Cox, J. A. (1990) EF-hand motifs in inositol phospholipid-specific phospholipase C. FEBS Lett. 269, 454-456
62. de Beer, T., Carter, R. E., Lobel-Rice, K. E., Sorkin, A. and Overduin, M. (1998) Structure and Asn-Pro-Phe binding pocket of the Eps15 homology domain. Science 281, 1357-1360
63. 2+ sensor proteins. Protein Sci. 7, 270-282
64. Yap, K. L., Ames, J. B., Swindells, M. B. and Ikura, M. (1999) Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins 37, 499-507
65. Zhang, M., Tanaka, T. and Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2, 758-767
66. 2+- saturated state. Biochemistry 36, 3448-3457
67. 9k: NMR studies of the N56A mutant. Protein Sci. 4, 1045-1055
68. Smith, S. P. and Shaw, G. S. (1998) A change-in-hand mechanism for S100 signalling. Biochem. Cell Biol. 76, 324-333
69. 2+-dependent interaction with annexin VII and the cardiac ryanodine receptor. Biochemistry 45, 12519-12529
70. Mella, M., Colotti, G., Zamparelli, C., Verzili, D., Ilari, A. and Chiancone, E. (2003) Information transfer in the penta-EF-hand protein sorcin does not operate via the canonical structural/functional pairing. A study with site-specific mutants. J. Biol. Chem. 278, 24921-24928
71. 2+-bound calmodulin: an analysis of disorder and implications for functionally relevant plasticity. J. Mol. Biol. 301, 1237-1256
72. 2+-calmodulin reveals flexible hand-like properties of its domains. Nat. Struct. Biol. 8, 990-997
73. 15N-NMR relaxation measurements. Eur. J. Biochem. 230, 1014-1024
74. Lundstrom, P., Mulder, F. A. and Akke, M. (2005) Correlated dynamics of consecutive residues reveal transient and co-operative unfolding of secondary structure in proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 16984-16989
75. Drake, S. K. and Falke, J. J. (1996) Kinetic tuning of the EF-hand calcium binding motif: the gateway residue independently adjusts (i) barrier height and (ii) equilibrium. Biochemistry 35, 1753-1760
76. Lee, Y. H., Tanner, J. J., Larson, J. D. and Henzl, M. T. (2004) Crystal structure of a high-affinity variant of rat α-parvalbumin. Biochemistry 43, 10008-10017
77. Yamniuk, A. P., Nguyen, L. T., Hoang, T. T. and Vogel, H. J. (2004) Metal ion binding properties and conformational states of calcium- and integrin-binding protein. Biochemistry 43, 2558-2568
78. Li, M. X., Gagne, S. M., Tsuda, S., Kay, C. M., Smillie, L. B. and Sykes, B. D. (1995) Calcium binding to the regulatory N-domain of skeletal muscle troponin C occurs in a stepwise manner. Biochemistry 34, 8330-8340
79. Strynadka, N. C., Cherney, M., Sielecki, A. R., Li, M. X., Smillie, L. B. and James, M. N. (1997) Structural details of a calcium-induced molecular switch: X-ray crystallographic analysis of the calcium-saturated N-terminal domain of troponin C at 1.75 Å resolution. J. Mol. Biol. 273, 238-255
80. Gagne, S. M., Li, M. X. and Sykes, B. D. (1997) Mechanism of direct coupling between binding and induced structural change in regulatory calcium binding proteins. Biochemistry 36, 4386-4392
81. 9k. J. Mol. Biol. 220, 173-189
82. Gagne, S. M., Tsuda, S., Spyracopoulos, L., Kay, L. E. and Sykes, B. D. (1998) Backbone and methyl dynamics of the regulatory domain of troponin C: anisotropic rotational diffusion and contribution of conformational entropy to calcium affinity. J. Mol. Biol. 278, 667-686
83. Foguel, D., Suarez, M. C., Barbosa, C., Rodrigues, Jr, J. J., Sorenson, M. M., Smillie, L. B. and Silva, J. L. (1996) Mimicry of the calcium-induced conformational state of troponin C by low temperature under pressure. Proc. Natl. Acad. Sci. U.S.A. 93, 10642-10646
84. 2+-binding constants by global least-squares analysis of isothermal titration calorimetry data. Anal. Biochem. 319, 216-233
85. Gilli, R., Lafitte, D., Lopez, C., Kilhoffer, M., Makarov, A., Briand, C. and Haiech, J. (1998) Thermodynamic analysis of calcium and magnesium binding to calmodulin. Biochemistry 37, 5450-5456
86. 2+ differentially regulate DNA binding and dimerization of DREAM. J. Biol. Chem. 280, 18008-18014
87. 2+ binding to CaBP1, a neuron-specific regulator of calcium channels. J. Biol. Chem. 280, 37461-37470
88. Reid, R. E. and Hodges, R. S. (1980) Co-operativity and calcium/magnesium binding to troponin C and muscle calcium binding paralbumin: an hypothesis. J. Theor. Biol. 84, 401-444
89. 1H-NMR studies of synthetic peptide analogues of calcium-binding site III of rabbit skeletal troponin C: effect on the lanthanum affinity of the interchange of aspartic acid and asparagine residues at the metal ion coordinating positions. Biochemistry 27, 4198-4206
90. 2+ association. Biochemistry 39, 13831-13837
91. 2+. Biochemistry 35, 5856-5869
92. Ye, Y., Lee, H. W., Yang, W., Shealy, S. and Yang, J. J. (2005) Probing site-specific calmodulin calcium and lanthanide affinity by grafting. J. Am. Chem. Soc. 127, 3743-3750
93. 1H NMR studies of calcium binding to synthetic and variant site III helix-loop-helix peptides. Biochemistry 30, 8339-8347
94. 2+ coordination, by genetic engineering. J. Biol. Chem. 267, 15469-15474
95. Linse, S., Brodin, P., Johansson, C., Thulin, E., Grundstrom, T. and Forsen, S. (1988) The role of protein surface charges in ion binding. Nature 335, 651-652
96. 9k: stopped-flow studies. Biochemistry 29, 4188-4193
97. 1H NMR spectroscopic studies of calcium-binding proteins. 1. Stepwise proteolysis of the C-terminal α-helix of a helix-loop-helix metal-binding domain. Biochemistry 25, 1817-1826
98. Marsden, B. J., Shaw, G. S. and Sykes, B. D. (1990) Calcium binding proteins. Elucidating the contributions to calcium affinity from an analysis of species variants and peptide fragments. Biochem. Cell Biol. 68, 587-601
99. Sekharudu, Y. C. and Sundaralingam, M. (1988) A structure-function relationship for the calcium affinities of regulatory proteins containing 'EF-hand' pairs. Protein Eng. 2, 139-146
100. 2+ exchange and affinity in the C terminal of cardiac troponin C. Biochemistry 37, 14539-14544
101. 2+ binding and dissociation. Biochemistry 37, 8926-8937
102. Nicholson, H., Becktel, W. J. and Matthews, B. W. (1988) Enhanced protein thermostability from designed mutations that interact with alpha-helix dipoles. Nature 336, 651-656
103. Trigo-Gonzalez, G., Awang, G., Racher, K., Neden, K. and Borgford, T. (1993) Helix variants of troponin C with tailored calcium affinities. Biochemistry 32, 9826-9831
104. Linse, S., Helmersson, A. and Forsen, S. (1991) Calcium binding to calmodulin and its globular domains. J. Biol. Chem. 266, 8050-8054
105. Masino, L., Martin, S. R. and Bayley, P. M. (2000) Ligand binding and thermodynamic stability of a multidomain protein, calmodulin. Protein Sci. 9, 1519-1529
106. 2+-calmodulin: evidence of interdomain coupling and structural collapse on the nanosecond timescale. Biophys. J. 87, 780-791
107. 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
108. Fredricksen, R. S. and Swenson, C. A. (1996) Relationship between stability and function for isolated domains of troponin C. Biochemistry 35, 14012-14026
109. Ababou, A. and Desjarlais, J. R. (2001) Solvation energetics and conformational change in EF-hand proteins. Protein Sci. 10, 301-312
110. 2+-discharged photoprotein: implications for mechanisms of the calcium trigger and bioluminescence. J. Biol. Chem. 279, 33647-33652
111. 2+ binding. Biochemistry 30, 8690-8697
112. Ouyang, H. and Vogel, H. J. (1998) Metal ion binding to calmodulin: NMR and fluorescence studies. Biometals 11, 213-222
113. Ebel, H. and Gunther, T. (1980) Magnesium metabolism: a review. J. Clin. Chem. Clin. Biochem. 18, 257-270
114. Martin, R. B. (1990) Bioinorganic Chemistry of Magnesium. In Metal Ions in Biological Systems (Sigel, H., ed.), pp. 1-13, Marcel Dekker Inc., New York
115. 2+ on target recognition by calmodulin. Biochemistry 36, 4309-4316
116. Malmendal, A., Evenas, J., Thulin, E., Gippert, G. P., Drakenberg, T. and Forsen, S. (1998) When size is important. Accommodation of magnesium in a calcium binding regulatory domain. J. Biol. Chem. 273, 28994-29001
117. 9k. Protein Sci. 6, 1139-1147
118. Declercq, J. P., Tinant, B., Parello, J. and Rambaud, J. (1991) Ionic interactions with parvalbumins. Crystal structure determination of pike 4.10 parvalbumin in four different ionic environments. J. Mol. Biol. 220, 1017-1039
119. 2+ exchange in parvalbumin and other EF-hand proteins. A theoretical study. J. Mol. Biol. 285, 857-873
120. Blumenschein, T. M. and Reinach, F. C. (2000) Analysis of affinity and specificity in an EF-hand site using double mutant cycles. Biochemistry 39, 3603-3610
121. 2+-specific site. J. Biol. Chem. 270, 6773-6778
122. Cates, M. S., Berry, M. B., Ho, E. L., Li, Q., Potter, J. D. and Phillips, Jr, G. N. (1999) Metal-ion affinity and specificity in EF-hand proteins: coordination geometry and domain plasticity in parvalbumin. Structure 7, 1269-1278
123. Procyshyn, R. M. and Reid, R. E. (1994) A structure/activity study of calcium affinity ant selectivity using a synthetic peptide model of the helix-loop-helix calcium-binding motif. J. Biol. Chem. 269, 1641-1647
124. 2+ binding and exchange with the N-terminal of calmodulin. Biochemistry 40, 3348-3353
125. Potter, J. D. and Gergely, J. (1975) The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J. Biol. Chem. 250, 4628-4633
126. 2+ sites on troponin C in the regulation of muscle contraction. Preparation and properties of troponin C depleted myofibrils. J. Biol. Chem. 257, 7678-7683
127. 2+-bound form is the physiological activator of photorecepto guanylyl cyclase. J. Biol. Chem. 281, 23830-23841
128. Malmendal, A., Linse, S., Evenas, J., Forsen, S. and Drakenberg, T. (1999) Battle for the EF-hands: magnesium-calcium interference in calmodulin. Biochemistry 38, 11844-11850
129. 2+ exchange with troponin C. J. Biol. Chem. 254, 3497-3502
130. Trigo-Gonzalez, G., Racher, K., Burtnick, L. and Borgford, T. (1992) A comparative spectroscopic study of tryptophan probes engineered into high- and low-affinity domains of recombinant chicken troponin C. Biochemistry 31, 7009-7015
131. Osawa, M., Tong, K. I., Lilliehook, C., Wasco, W., Buxbaum, J. D., Cheng, H. Y., Penninger, J. M., Ikura, M. and Ames, J. B. (2001) Calcium-regulated DNA binding and oligomerization of the neuronal calcium-sensing protein, calsenilin/DREAM/KChlP3. J. Biol. Chem. 276, 41005-41013
132. 2+ channels. Biophys. J. 78, 1906-1920
133. Headrick, J. P. and Willis, R. J. (1991) Cytosolic free magnesium in stimulated, hypoxic and underperfused rat heart. J. Mol. Cell Cardiol. 23, 991-999
134. 9k. Biochemistry 30, 154-162
135. 9K. J. Am. Chem. Soc. 115, 9832-9833
136. Evenas, J., Forsen, S., Malmendal, A. and Akke, M. (1999) Backbone dynamics and energetics of a calmodulin domain mutant exchanging between closed and open conformations. J. Mol. Biol. 289, 603-617
137. I,II2 binding pathway. J. Mol. Biol. 252, 102-121
138. Vogel, H. J., Drakenberg, T., Forsen, S., O'Neil, J. D. and Hofmann, T. (1985) Structural differences in the two calcium binding sites of the porcine intestinal calcium binding protein: a multinuclear NMR study. Biochemistry 24, 3870-3876
139. 2+ binding in proteins of the calmodulin superfamily: co-operativity, electrostatic contributions and molecular mechanisms. Ciba Found. Symp. 161, 222-236
140. 9k. The rates of amide proton exchange with solvent. J. Mol. Biol. 227, 1100-1117
141. Monod, J., Changeux, J. P. and Jacob, F. (1963) Allosteric proteins and cellular control systems. J. Mol. Biol. 6, 306-329
142. 9k EF-hands. Proteins 47, 323-333
143. 2+ ions bound to the protein: a microdielectric study. Protein Eng. 4, 121-124
144. George, S. E., Su, Z., Fan, D. and Means, A. R. (1993) Calmodulin-cardiac troponin C chimeras. Effects of domain exchange on calcium binding and enzyme activation. J. Biol. Chem. 268, 25213-25220
145. 2+ binding property. Biochemistry 41, 15536-15542
146. Luan-Rilliet, Y., Milos, M. and Cox, J. A. (1992) Thermodynamics of cation binding to Nereis sarcoplasmic calcium-binding protein. Direct binding studies, microcalorimetry and conformational changes. Eur. J. Biochem. 208, 133-138
147. Martin, S. R., Maune, J. F., Beckingham, K. and Bayley, P. M. (1992) Stopped-flow studies of calcium dissociation from calcium-binding-site mutants of Drosophila melanogaster calmodulin. Eur. J. Biochem. 205, 1107-1114
148. Baladi, S., Tsvetkov, P. O., Petrova, T. V., Takagi, T., Sakamoto, H., Lobachov, V. M., Makarov, A. A. and Cox, J. A. (2001) Folding units in calcium vector protein of amphioxus: Structural and functional properties of its amino- and carboxy-terminal halves. Protein Sci. 10, 771-778
149. Linse, S. and Chazin, W. J. (1995) Quantitative measurements of the co-operativity in an EF-hand protein with sequential calcium binding. Protein Sci. 4, 1038-1044
150. Reference deleted
151. 2+ binding to the regulatory domains of cardiac and E41A skeletal muscle troponin C reveal the importance of site I to energetics of the induced structural changes. Biochemistry 36, 12519-12525
152. Ames, J. B., Ishima, R., Tanaka, T., Gordon, J. I., Stryer, L. and Ikura, M. (1997) Molecular mechanics of calcium-myristoyl switches. Nature 389, 198-202
153. Ames, J. B., Hamasaki, N. and Molchanova, T. (2002) Structure and calcium-binding studies of a recoverin mutant (E85Q) in an allosteric intermediate state. Biochemistry 41, 5776-5787
154. Permyakov, S. E., Cherskaya, A. M., Senin, I. I., Zargarov, A. A., Shulga-Morskoy, S. V., Alekseev, A. M., Zinchenko, D. V., Lipkin, V. M., Philippov, P. P., Uversky, V. N. and Permyakov, E. A. (2000) Effects of mutations in the calcium-binding sites of recoverin on its calcium affinity: evidence for successive filling of the calcium binding sites. Protein Eng, 13, 783-790
155. Ames, J. B., Porumb, T., Tanaka, T., Ikura, M. and Stryer, L. (1995) Amino-terminal myristoylation induces co-operative calcium binding to recoverin. J. Biol. Chem. 270, 4526-4533
156. Xie, X., Harrison, D. H., Schlichting, I., Sweet, R. M., Kalabokis, V. N., Szent-Gyorgyi, A. G. and Cohen, C. (1994) Structure of the regulatory domain of scallop myosin at 2.8 Å resolution. Nature 368, 306-312
157. Hohenester, E., Maurer, P. and Timpl, R. (1997) Crystal structure of a pair of follistatin-like and EF-hand calcium-binding domains in BM-40. EMBO J. 16, 3778-3786
158. 2+ binding sites of calmodulin. J. Biol. Chem. 271, 761-767
159. 2+, calmodulin, skeletal muscle myosin light chain kinase and kinase substrates. J. Biol. Chem. 259, 10949-10955
160. Olwin, B. B. and Storm, D. R. (1985) Calcium binding to complexes of calmodulin and calmodulin binding proteins. Biochemistry 24, 8081-8086
161. 2+ dissociation from complexes of calmodulin with nitric oxide synthase or myosin light chain kinase. J. Biol. Chem. 271, 62-67
162. Yazawa, M., Vorherr, T., James, P., Carafoli, E. and Yagi, K. (1992) Binding of calcium by calmodulin: influence of the calmodulin binding domain of the plasma membrane calcium pump. Biochemistry 31, 3171-3176
163. Durussel, I., Mehul, B., Bernard, D., Schmidt, R. and Cox, J. A. (2002) Cation- and peptide-binding properties of human calmodulin-like skin protein. Biochemistry 41, 5439-5448
164. Stemmer, P. M. and Klee, C. B. (1994) Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 33, 6859-6866
165. 2+ binding and implications for kinase activation. Protein Sci. 6, 794-807
166. Haiech, J., Kilhoffer, M. C., Lukas, T. J., Craig, T. A., Roberts, D. M. and Watterson, D. M. (1991) Restoration of the calcium binding activity of mutant calmodulins toward normal by the presence of a calmodulin binding structure. J. Biol. Chem. 266, 3427-3431
167. O'Neil, K. T. and DeGrado, W. F. (1990) How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices. Trends Biochem. Sci. 15, 59-64
168. Petrova, T. V., Comte, M., Takagi, T. and Cox, J. A. (1995) Thermodynamic and molecular properties of the interaction between amphioxus calcium vector protein and its 26 kDa target. Biochemistry 34, 312-318
169. Calvert, P. D., Klenchin, V. A. and Bownds, M. D. (1995) Rhodopsin kinase inhibition by recoverin. Function of recoverin myristoylation. J. Biol. Chem. 270, 24127-24129
170. 1H NMR. J. Biol. Chem. 262, 10951-10954
171. Ikura, M., Clore, G. M., Gronenborn, A. M., Zhu, G., Klee, C. B. and Bax, A. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638
172. 2+/calmodulin. Nature 410, 1120-1124
173. + channels regulate binding to and modulation by KChlP1. Neuron 41, 587-598
174. Vogel, H. J. (1994) The Merck Frosst Award Lecture 1994: calmodulin: a versatile calcium mediator protein. Biochem. Cell Biol. 72, 357-376
175. Koradi, R., Billeter, M. and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55