Structural Basis for Diversity of the EF-hand Calcium-binding Proteins

Journal of Molecular Biology

Volumn 359, Issue 3, 2006, Pages 509-525

  Grabarek, Zenon ^a  

^a BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

calcium binding proteins; calcium signaling; EF hand; structure and function

Indexed keywords

ASPARTIC ACID; CALBINDIN; CALCIUM BINDING PROTEIN; CALCIUM ION; CALCYCLIN; CALMODULIN; CALPAIN; EFBETA SCAFFOLD; GLUTAMIC ACID; LIGAND; MYOSIN LIGHT CHAIN KINASE; OSTEONECTIN; PARVALBUMIN; PROTEIN S 100; SCAFFOLD PROTEIN; TROPONIN C; TROPONIN I; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BINDING AFFINITY; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW;

EID: 33646761687     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.03.066     Document Type: Review

References (151)

1. Kretsinger R.H., and Nockolds C.E. Carp muscle calcium binding protein. II. Structure determination and general description. J. Biol. Chem. 248 (1973) 3313-3326
2. Collins J.H., Potter J.D., Horn M.J., Wilshire G., and Jackman N. The amino acid sequence of rabbit skeletal muscle troponin C: gene replication and homology with calcium-binding proteins from carp and hake muscle. FEBS Letters 36 (1973) 268-272
3. Collins J.H. Homology of myosin light chains, troponin-C and parvalbumins deduced from comparison of their amino acid sequences. Biochem. Biophys. Res. Commun. 58 (1974) 301-308
4. Stevens F.C., Walsh M., Ho H.C., Teo T.S., and Wang J.H. Comparison of calcium-binding proteins. Bovine heart and brain protein activators of cyclic nucleotide phosphodiesterase and rabbit skeletal muscle troponin C. J. Biol. Chem. 251 (1976) 4495-4500
5. 2+-dependent regulatory proteins of 3′:5′-cyclic nucleotide phosphodiesterase and actomyosin ATPase. J. Biol. Chem. 251 (1976) 4501-4513
6. Kawasaki H., and Kretsinger R.H. Calcium-binding proteins. 1: EF-hands. Protein Profile 1 (1994) 343-517
7. Kawasaki H., and Kretsinger R.H. Calcium-binding proteins 1: EF-hands. Protein Profile 2 (1995) 297-490
8. Berridge M.J., Bootman M.D., and Lipp P. Calcium-a life and death signal. Nature 395 (1998) 645-648
9. Berridge M.J., Lipp P., and Bootman M.D. The versatility and universality of calcium signalling. Nature Rev. Mol. Cell. Biol. 1 (2000) 11-21
10. Carafoli E., Santella L., Branca D., and Brini M. Generation, control, and processing of cellular calcium signals. Crit. Rev. Biochem. Mol. Biol. 36 (2001) 107-260
11. Kahl C.R., and Means A.R. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr. Rev. 24 (2003) 719-736
12. 2+ binding. Biometals 11 (1998) 297-318
13. Lewit-Bentley A., and Rety S. EF-hand calcium-binding proteins. Curr. Opin. Struct. Biol. 10 (2000) 637-643
14. 2+-saturated state. Biochemistry 36 (1997) 3448-3457
15. 2+ binding and conformational changes in a calmodulin domain. Biochemistry 37 (1998) 13744-13754
16. Malmendal A., Evenas J., Forsen S., and Akke M. Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J. Mol. Biol. 293 (1999) 883-899
17. Evenas J., Forsen S., Malmendal A., and Akke M. Backbone dynamics and energetics of a calmodulin domain mutant exchanging between closed and open conformations. J. Mol. Biol. 289 (1999) 603-617
18. 2+-calmodulin reveals flexible hand-like properties of its domains. Nature Struct. Biol. 8 (2001) 990-997
19. Chazin W.J. Releasing the calcium trigger. Nature Struct. Biol. 2 (1995) 707-710
20. McPhalen C.A., Strynadka N.C.J., and James M.N.G. Calcium-binding sites in proteins: a structural perspective. Advan. Protein Chem. 42 (1991) 77-144
21. Strynadka N.C.J., and James M.N.G. Crystal structures of the helix-loop-helix calcium-binding proteins. Annu. Rev. Biochem. 58 (1989) 951-998
22. Ikura M., and Ames J.B. Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality. Proc. Natl Acad. Sci. USA 103 (2006) 1159-1164
23. Evenas J., Malmendal A., and Forsen S. Calcium. Curr. Opin. Chem. Biol. 2 (1998) 293-302
24. 2+ binding in proteins of the calmodulin superfamily: cooperativity, electrostatic contributions and molecular mechanisms. CIBA Found. Symp. 161 (1991) 222-236
25. Forsen S., and Linse S. Cooperativity: over the Hill. Trends Biochem. Sci. 20 (1995) 495-497
26. Linse S., and Forsen S. Determinants that govern high-affinity calcium binding. In: Means A.R. (Ed). Advances in Second Messenger and Phosphoprotein Research vol. 30 (1995), Raven Press, Ltd, New York
27. Falke J.J., Drake S.K., Hazard A.L., and Peersen O.B. Molecular tuning of ion binding to calcium signaling proteins [Review]. Quart. Rev. Biophys. 27 (1994) 219-290
28. Haiech J., and Kilhoffer M.C. Deconvolution of calcium-binding curves. Facts and fantasies. Methods Mol. Biol. 173 (2002) 25-42
29. Crivici A., and Ikura M. Molecular and structural basis of target recognition by calmodulin. [Review]. Annu. Rev. Biophys. Biomol. Struct. 24 (1995) 85-116
30. Rhoads A.R., and Friedberg F. Sequence motifs for calmodulin recognition. FASEB J. 11 (1997) 331-340
31. Jurado L.A., Chockalingam P.S., and Jarrett H.W. Apocalmodulin. Physiol. Rev. 79 (1999) 661-682
32. Hoeflich K.P., and Ikura M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108 (2002) 739-742
33. Bahler M., and Rhoads A. Calmodulin signaling via the IQ motif. FEBS Letters 513 (2002) 107-113
34. Bhattacharya S., Bunick C.G., and Chazin W.J. Target selectivity in EF-hand calcium binding proteins. Biochim. Biophys. Acta 1742 (2004) 69-79
35. Yamniuk A.P., and Vogel H.J. Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol. Biotechnol. 27 (2004) 33-57
36. Carafoli E., and Klee C.B. Calcium as a Cellular Regulator (1999), Oxford University Press, New York, Oxford
37. Grabarek Z. Structure of a trapped intermediate of calmodulin: calcium regulation of EF-hand proteins from a new perspective. J. Mol. Biol. 346 (2005) 1351-1366
38. Szebenyi D.M.E., Obendorf S.K., and Moffat K. Structure of vitamin D-dependent calcium-binding protein from bovine intestine. Nature 294 (1981) 327-332
39. Szebenyi D.M.E., and Moffat K. The refined structure of vitamin D-dependent calcium-binding protein from bovine intestine. Molecular detail, ion binding, and implicaions for the structure of other calcium-binding proteins. J. Biol. Chem. 261 (1986) 8761-8777
40. 2+-induced conformational changes. Nature Struct. Biol. 4 (1997) 532-538
41. Lin G.D., Chattopadhyay D., Maki M., Wang K.K., Carson M., Jin L., et al. Crystal structure of calcium bound domain VI of calpain at 1.9 A resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nature Struct. Biol. 4 (1997) 539-547
42. Jia J., Han Q., Borregaard N., Lollike K., and Cygler M. Crystal structure of human grancalcin, a member of the penta-EF-hand protein family. J. Mol. Biol. 300 (2000) 1271-1281
43. 2+-induced changes in penta-EF-hand proteins. Structure (Camb) 9 (2001) 267-275
44. 2+-binding module in Bm-40. Nature Struct. Biol. 3 (1996) 67-73
45. Cates M.S., Berry M.B., Ho E.L., Li Q., Potter J.D., and Phillips Jr. G.N. Metal-ion affinity and specificity in EF-hand proteins: coordination geometry and domain plasticity in parvalbumin. Struct. Fold. Des. 7 (1999) 1269-1278
46. Gentry H.R., Singer A.U., Betts L., Yang C., Ferrara J.D., Sondek J., and Parise L.V. Structural and biochemical characterization of CIB1 delineates a new family of EF-hand-containing proteins. J. Biol. Chem. 280 (2005) 8407-8415
47. Scannevin R.H., Wang K., Jow F., Megules J., Kopsco D.C., Edris W., et al. Two N-terminal domains of Kv4 K(+) channels regulate binding to and modulation by KChIP1. Neuron 41 (2004) 587-598
48. 2+-specific site. J. Biol. Chem. 270 (1995) 6773-6778
49. Houdusse A., and Cohen C. Structure of the regulatory domain of scallop myosin at 2 Angstrom resolution-implications for regulation. Structure 4 (1996) 21-32
50. Kuboniwa H., Tjandra N., Grzesiek S., Ren H., Klee C.B., and Bax A. Solution structure of calcium-free calmodulin. Nature Struct. Biol. 2 (1995) 768-776
51. Zhang M., Tanaka T., and Ikura M. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nature Struct. Biol. 2 (1995) 758-767
52. Herzberg O., and James M.N. Refined crystal structure of troponin C from turkey skeletal muscle at 2.0 Å resolution. J. Mol. Biol. 203 (1988) 761-779
53. 2+ sensor proteins. Protein Sci. 7 (1998) 270-282
54. Kawasaki H., Nakayama S., and Kretsinger R.H. Classification and evolution of EF-hand proteins. Biometals 11 (1998) 277-295
55. 1H NMR structural evidence. Science 249 (1990) 280-283
56. Shaw G.S., Hodges R.S., Kay C.M., and Sykes B.D. Relative stabilities of synthetic peptide homo- and heterodimeric troponin-C domains. Protein Sci. 3 (1994) 1010-1019
57. 2+-binding subdomains by a combination of mutagenesis and chemical cleavage. FEBS Letters 298 (1992) 211-214
58. Wojcik J., Goral J., Pawlowski K., and Bierzynski A. Isolated calcium-binding loops of EF-hand proteins can dimerize to form a native-like structure. Biochemistry 36 (1997) 680-687
59. Thepaut M., Strub M.P., Cave A., Baneres J.L., Berchtold M.W., Dumas C., and Padilla A. Structure of rat parvalbumin with deleted AB domain: implications for the evolution of EF hand calcium-binding proteins and possible physiological relevance. Proteins: Struct. Funct. Genet. 45 (2001) 117-128
60. Cox J.A., Durussel I., Scott D.J., and Berchtold M.W. Remodeling of the AB site of rat parvalbumin and oncomodulin into a canonical EF-hand. Eur. J. Biochem. 264 (1999) 790-799
61. Kretsinger R.H. Calcium coordination and the calmodulin fold: divergent versus convergent evolution. Cold Spring Harbor Symp. Quant. Biol. 52 (1987) 499-510
62. Drabikowski W., Grabarek Z., and Barylko B. Degradation of TN-C component of troponin by trypsin. Biochim. Biophys. Acta 490 (1977) 216-224
63. 2+-induced changes between troponic-C and protein activator of 3′:5′-cyclic nucleotide phosphodiesterase and their tryptic fragments. Biochim. Biophys. Acta 485 (1977) 124-133
64. Walsh M., Stevens F.C., Kuznicki J., and Drabikowski W. Characterization of tryptic fragments obtained from bovine brain protein modulator of cyclic nucleotide phosphodiesterase. J. Biol. Chem. 252 (1977) 7440-7443
65. Herzberg O., and James M.N. Structure of the calcium regulatory muscle protein troponin-C at 2.8 Å resolution. Nature 313 (1985) 653-659
66. Sundaralingam M., Bergstrom R., Strasburg G., Rao S.T., Roychowdhury P., Greaser M., and Wang B.C. Molecular structure of troponin C from chicken skeletal muscle at 3-angstrom resolution. Science 227 (1985) 945-948
67. Babu Y.S., Sack J.S., Greenhough T.J., Bugg C.E., Means A.R., and Cook W.J. Three-dimensional structure of calmodulin. Nature 315 (1985) 37-40
68. Zot A.S., and Potter J.D. Structural aspects of troponin-tropomyosin regulation of skeletal muscle contraction. Annu. Rev. Biophys. Biophys. Chem. 16 (1987) 535-559
69. Grabarek Z., Tao T., and Gergely J. Molecular mechanism of troponin-C function. J. Muscle Res. Cell Motil. 13 (1992) 383-393
70. 2+-saturated form. Nature 424 (2003) 35-41
71. 2+-regulated structural changes in troponin. Proc. Natl Acad. Sci. USA 102 (2005) 5038-5043
72. Meador W.E., Means A.R., and Quiocho F.A. Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulin-peptide complex. Science 257 (1992) 1251-1255
73. Ikura M., Clore G.M., Gronenborn A.M., Zhu G., Klee C.B., and Bax A. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256 (1992) 632-638
74. Clore G.M., Bax A., Ikura M., and Gronenborn A.M. Structure of calmodulin target peptide complexes. Curr. Opin. Struct. Biol. 3 (1993) 838-845
75. Drum C.L., Yan S.Z., Bard J., Shen Y.Q., Lu D., Soelaiman S., et al. Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415 (2002) 396-402
76. Terrak M., Rebowski G., Lu R.C., Grabarek Z., and Dominguez R. Structure of the light chain-binding domain of myosin V. Proc. Natl Acad. Sci. USA 102 (2005) 12718-12723
77. 2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I. Structure 8 (2000) 175-184
78. Sopkova-de Oliveira Santos J., Oling F.K., Rety S., Brisson A., Smith J.C., and Lewit-Bentley A. S100 protein-annexin interactions: a model of the (Anx2-p11)(2) heterotetramer complex. Biochim. Biophys. Acta 1498 (2000) 181-191
79. 2+-bound states. The calcium sensor mechanism of S100 proteins revealed at atomic resolution. Structure (Camb) 10 (2002) 557-567
80. Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim. Biophys. Acta 1450 (1999) 191-231
81. 2+-calcyclin. J. Mol. Biol. 317 (2002) 279-290
82. Cook W.J., Ealick S.E., Babu Y.S., Cox J.A., and Vijay-Kumar S. Three-dimensional structure of a sarcoplasmic calcium-binding protein from Nereis diversicolor. J. Biol. Chem. 266 (1991) 652-656
83. Vijay-Kumar S., and Cook W.J. Structure of a sarcoplasmic calcium-binding protein from Nereis diversicolor refined at 2.0 Å resolution. J. Mol. Biol. 224 (1992) 413-426
84. Flaherty K.M., Zozulya S., Stryer L., and Mckay D.B. Three-dimensional structure of recoverin, a calcium sensor in vision. Cell 75 (1993) 709-716
85. Tanaka T., Ames J.B., Harvey T.S., Stryer L., and Ikura M. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature 376 (1995) 444-447
86. Ames J.B., Ishima R., Tanaka T., Gordon J.I., Stryer L., and Ikura M. Molecular mechanics of calcium-myristoyl switches. Nature 389 (1997) 198-202
87. Ames J.B., Hendricks K.B., Strahl T., Huttner I.G., Hamasaki N., and Thorner J. Structure and calcium-binding properties of Frq1, a novel calcium sensor in the yeast Saccharomyces cerevisiae. Biochemistry 39 (2000) 12149-12161
88. Bourne Y., Dannenberg J., Pollmann V., Marchot P., and Pongs O. Immunocytochemical localization and crystal structure of human frequenin (neuronal calcium sensor 1). J. Biol. Chem. 276 (2001) 11949-11955
89. Griffith J.P., Kim J.L., Kim E.E., Sintchak M.D., Thomson J.A., Fitzgibbon M.J., et al. X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell 82 (1995) 507-522
90. 2+-induced conformational transition of troponin C. A trigger for muscle contraction. J. Biol. Chem. 261 (1986) 2638-2644
91. Grabarek Z., Tan R.Y., Wang J., Tao T., and Gergely J. Inhibition of mutant troponin C activity by an intra-domain disulphide bond. Nature 345 (1990) 132-135
92. Fujimori K., Sorenson M., Herzberg O., Moult J., and Reinach F.C. Probing the calcium-induced conformational transition of troponin C with site-directed mutants [see comments]. Nature 345 (1990) 182-184
93. 2+-triggered conformational transition in troponin C. Proc. Natl Acad. Sci. USA 89 (1992) 11814-11817
94. Gagne S.M., Tsuda S., Li M.X., Smillie L.B., and Sykes B.D. Structures of the troponin C regulatory domains in the apo and calcium-saturated states. Nature Struct. Biol. 2 (1995) 784-789
95. Slupsky C.M., and Sykes B.D. NMR solution structure of calcium-saturated skeletal muscle troponin C. Biochemistry 34 (1995) 15953-15964
96. 2+-switch in the calmodulin superfamily. Structure 5 (1997) 1695-1711
97. Strynadka N.C., Cherney M., Sielecki A.R., Li M.X., Smillie L.B., and James M.N. 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 (1997) 238-255
98. 1H NMR examination of the carboxy-terminal domain. FEBS Letters 336 (1993) 368-374
99. Finn B.E., Evanas J., Drakenberg T., Waltho J.P., Thulin E., and Forsen S. Calcium-induced structural changes and domain autonomy in calmodulin. Nature Struct. Biol. 2 (1995) 777-783
100. 2+-induced conformational transitions in calmodulin with disulfide bonds. J. Biol. Chem. 271 (1996) 7479-7483
101. 2+-signal transduction by S100 proteins. Structure 6 (1998) 223-231
102. Drohat A.C., Amburgey J.C., Abildgaard F., Starich M.R., Baldisseri D., and Weber D.J. Solution structure of rat apo-S100b(beta-beta) as determined by NMR spectroscopy. Biochemistry 35 (1996) 11577-11588
103. Kilby P.M., Van Eldik L.J., and Roberts G.C. The solution structure of the bovine S100B protein dimer in the calcium-free state. Structure 4 (1996) 1041-1052
104. Drohat A.C., Baldisseri D.M., Rustandi R.R., and Weber D.J. Solution structure of calcium-bound rat S100B(betabeta) as determined by nuclear magnetic resonance spectroscopy. Biochemistry 37 (1998) 2729-2740
105. Smith S.P., and Shaw G.S. A novel calcium-sensitive switch revealed by the structure of human S100B in the calcium-bound form. Structure 6 (1998) 211-222
106. Smith S.P., and Shaw G.S. A change-in-hand mechanism for S100 signalling. Biochem. Cell Biol. 76 (1998) 324-333
107. Drohat A.C., Tjandra N., Baldisseri D.M., and Weber D.J. The use of dipolar couplings for determining the solution structure of rat apo-S100B(betabeta). Protein Sci. 8 (1999) 800-809
108. Rustandi R.R., Baldisseri D.M., Inman K.G., Nizner P., Hamilton S.M., Landar A., et al. Three-dimensional solution structure of the calcium-signaling protein apo-S100A1 as determined by NMR. Biochemistry 41 (2002) 788-796
109. Fritz G., Mittl P.R., Vasak M., Grutter M.G., and Heizmann C.W. The crystal structure of metal-free human EF-hand protein S100A3 at 1.7-Å resolution. J. Biol. Chem. 277 (2002) 33092-33098
110. Crick F.H.C. The packing of alpha helices: simple coiled coils. Acta Crystallog. 6 (1953) 689-697
111. Chothia C., Levitt M., and Richardson D. Structure of proteins: packing of alpha-helices and pleated sheets. Proc. Natl Acad. Sci. USA 74 (1977) 4130-4134
112. Chothia C., Levitt M., and Richardson D. Helix to helix packing in proteins. J. Mol. Biol. 145 (1981) 215-250
113. 2+-binding proteins. Nature Struct. Biol. 1 (1994) 239-245
114. Ikura M. Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21 (1996) 14-17
115. Sia S.K., Li M.X., Spyracopoulos L., Gagne S.M., Liu W., Putkey J.A., and Sykes B.D. Structure of cardiac muscle troponin C unexpectedly reveals a closed regulatory domain. J. Biol. Chem. 272 (1997) 18216-18221
116. Spyracopoulos L., Li M.X., Sia S.K., Gagne S.M., Chandra M., Solaro R.J., and Sykes B.D. Calcium-induced structural transition in the regulatory domain of human cardiac troponin C. Biochemistry 36 (1997) 12138-12146
117. Li M.X., Spyracopoulos L., and Sykes B.D. Binding of cardiac troponin-I147-163 induces a structural opening in human cardiac troponin-C. Biochemistry 38 (1999) 8289-8298
118. Li Y., Love M.L., Putkey J.A., and Cohen C. Bepridil opens the regulatory N-terminal lobe of cardiac troponin C. Proc. Natl Acad. Sci. USA 97 (2000) 5140-5145
119. Gagne S.M., Li M.X., and Sykes B.D. Mechanism of direct coupling between binding and induced structural change in regulatory calcium binding proteins. Biochemistry 36 (1997) 4386-4392
120. 2+ and troponin I peptide binding to the E41A mutant of the N-domain of skeletal troponin C. Biochemistry 39 (2000) 12731-12738
121. Ababou A., and Desjarlais J.R. Solvation energetics and conformational change in EF-hand proteins. Protein Sci. 10 (2001) 301-312
122. Ababou A., Shenvi R.A., and Desjarlais J.R. Long-range effects on calcium binding and conformational change in the N-domain of calmodulin. Biochemistry 40 (2001) 12719-12726
123. Gellman S.H. On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry 30 (1991) 6633-6636
124. Zhang M., Li M., Wang J.H., and Vogel H.J. The effect of Met→Leu mutations on calmodulin's ability to activate cyclic nucleotide phosphodiesterase. J. Biol. Chem. 269 (1994) 15546-15552
125. Yuan T., and Vogel H.J. Substitution of the methionine residues of calmodulin with the unnatural amino acid analogs ethionine and norleucine: biochemical and spectroscopic studies. Protein Sci. 8 (1999) 113-121
126. Bunick C.G., Nelson M.R., Mangahas S., Hunter M.J., Sheehan J.H., Mizoue L.S., et al. Designing sequence to control protein function in an EF-hand protein. J. Am. Chem. Soc. 126 (2004) 5990-5998
127. Yap K.L., Ames J.B., Swindells M.B., and Ikura M. Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins: Struct. Funct. Genet. 37 (1999) 499-507
128. Babini E., Bertini I., Capozzi F., Luchinat C., Quattrone A., and Turano M. Principal component analysis of the conformational freedom within the EF-hand superfamily. J. Proteome Res. 4 (2005) 1961-1971
129. 2+-binding sites of calmodulin. J. Biol. Chem. 267 (1992) 5286-5295
130. Mukherjea P., and Beckingham K. Calcium binding site mutants of calmodulin adopt abnormal conformations in complexes with model target peptides. Biochem. Mol. Biol. Int. 29 (1993) 555-563
131. 2+ binding sites. J. Biol. Chem. 268 (1993) 20096-20104
132. 2+ coordination. Biochemistry 37 (1998) 7617-7629
133. Biekofsky R.R., and Feeney J. Cooperative cyclic interactions involved in metal binding to pairs of sites in EF-hand proteins. FEBS Letters 439 (1998) 101-106
134. 2+ binding to EF-hand proteins. Biochemistry 43 (2004) 6554-6564
135. 2+ to a canonical EF-hand of a conventional myosin. J. Biol. Chem. 280 (2005) 41458-41464
136. 2+-calmodulin. Structure 11 (2003) 1303-1307
137. Vigil D., Gallagher S.C., Trewhella J., and Garcia A.E. Functional dynamics of the hydrophobic cleft in the N-domain of calmodulin. Biophys. J. 80 (2001) 2082-2092
138. Evenas J., Malmendal A., and Akke M. Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant. Structure 9 (2001) 185-195
139. Skelton N.J., Kordel J., and Chazin W.J. Determination of the solution structure of Apo calbindin D9k by NMR spectroscopy. J. Mol. Biol. 249 (1995) 441-462
140. 2+-receptor calbindin D9k. Protein Sci. 6 (1997) 1139-1147
141. Svensson L.A., Thulin E., and Forsen S. Proline cis-trans isomers in calbindin D9k observed by X-ray crystallography. J. Mol. Biol. 223 (1992) 601-606
142. Kordel J., Skelton N.J., Akke M., and Chazin W.J. High-resolution solution structure of calcium-loaded calbindin-d(9k). J. Mol. Biol. 231 (1993) 711-734
143. Rety S., Sopkova J., Renouard M., Osterloh D., Gerke V., Tabaries S., et al. The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nature Struct. Biol. 6 (1999) 89-95
144. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
145. Schumacher M.A., Crum M., and Miller M.C. Crystal structures of apocalmodulin and an apocalmodulin/SK potassium channel gating domain complex. Structure (Camb) 12 (2004) 849-860
146. Chattopadhyaya R., Meador W.E., Means A.R., and Quiocho F.A. Calmodulin structure refined at 1.7 Å resolution. J. Mol. Biol. 228 (1992) 1177-1192
147. Rao S.T., Wu S., Satyshur K.A., Ling K.Y., Kung C., and Sundaralingam M. Structure of Paramecium tetraurelia calmodulin at 1.8 Å resolution. Protein Sci. 2 (1993) 436-447
148. Rupp B., Marshak D.R., and Parkin S. Crystallization and preliminary X-ray analysis of two new crystal forms of calmodulin. Acta Crystallog. sect. D 52 (1996) 411-413
149. Yun C.H., Bai J., Sun D.Y., Cui D.F., Chang W.R., and Liang D.C. Structure of potato calmodulin PCM6: the first report of the three-dimensional structure of a plant calmodulin. Acta Crystallog. sect. D 60 (2004) 1214-1219
150. Fenn, T. D., Ringe, D. & Petsko, G. A. (2003). POVScript+: a program for model data visualization using persistence of vision ray-tracing. J. Appl. Crystallog. 36, 944-947.
151. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.