A 1.3-Å Structure of Zinc-bound N-terminal Domain of Calmodulin Elucidates Potential Early Ion-binding Step

Journal of Molecular Biology

Volumn 374, Issue 2, 2007, Pages 517-527

  Warren, Julia T ^a   Guo, Qing ^b   Tang, Wei Jen ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

calmodulin; EF hand motif; metal ion binding; metal ion induced conformational switch; X ray crystallography

Indexed keywords

CALCIUM BINDING PROTEIN; CALMODULIN; HELIX LOOP HELIX PROTEIN; SELENOMETHIONINE; ZINC; ADENYLATE CYCLASE; APOPROTEIN; CALCIUM; CROSS LINKING REAGENT; LIGAND;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; METAL BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN STRUCTURE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLIZATION; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ADENYLATE CYCLASE; APOPROTEINS; BINDING SITES; CALCIUM; CALMODULIN; CROSS-LINKING REAGENTS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; EF HAND MOTIFS; HUMANS; LIGANDS; MEMBRANE MICRODOMAINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; ZINC;

EID: 35548964668     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.09.048     Document Type: Article

References (47)

1. Means A.R. Molecular mechanisms of action of calmodulin. Recent Prog. Horm. Res. 44 (1988) 223-262
2. Mandell J.G., Roberts V.A., Pique M.E., Kotlovyi V., Mitchell J.C., Nelson E., et al. Protein docking using continuum electrostatics and geometric fit. Protein Eng. 14 (2001) 105-113
3. Klee C.B., Crouch T.H., and Richman P.G. Calmodulin. Annu. Rev. Biochem. 49 (1980) 489-515
4. Chin D., and Means A.R. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10 (2000) 322-328
5. Xia Z., and Storm D.R. The role of calmodulin as a signal integrator for synaptic plasticity. Nat. Rev. Neurosci. 6 (2005) 267-276
6. Van Eldik L.J., and Watterson D.M. Calmodulin and signal transduction (1998), Academic Press, San Diego
7. Ishida H., and Vogel H.J. Protein-peptide interaction studies demonstrate the versatility of calmodulin target protein binding. Protein Pept. Lett. 13 (2006) 455-465
8. Schumacher M.A., Crum M., and Miller M.C. Crystal structures of apocalmodulin and an apocalmodulin/SK potassium channel gating domain complex. Structure 12 (2004) 849-860
9. Kuboniwa H., Tjandra N., Grzesiek S., Ren H., Klee C.B., and Bax A. Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2 (1995) 768-776
10. Finn B.E., Evenas J., Drakenberg T., Waltho J.P., Thulin E., and Forsen S. Calcium-induced structural changes and domain autonomy in calmodulin. Nat. Struct. Biol. 2 (1995) 777-783
11. Babu Y.S., Bugg C.E., and Cook W.J. Structure of calmodulin refined at 2.2 A resolution. J. Mol. Biol. 204 (1988) 191-204
12. 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
13. Chou J.J., Li S., Klee C.B., and Bax A. Solution structure of Ca(2+)-calmodulin reveals flexible hand-like properties of its domains. Nat. Struct. Biol. 8 (2001) 990-997
14. 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
15. Akke M., and Chazin W.J. An open and shut case. Nat. Struct. Biol. 8 (2001) 910-912
16. Grabarek Z. Structural basis for diversity of the EF-hand calcium-binding proteins. J. Mol. Biol. 359 (2006) 509-525
17. Guo Q., Shen Y., Lee Y.S., Gibbs C.S., Mrksich M., and Tang W.J. Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin. EMBO J. 24 (2005) 3190-3201
18. Navaza J. AmoRe: an automated package for molecular replacement. Acta Crystallogr., Sect A: Found. Crystallogr. A50 (1994) 157-163
19. Rupp B., Marshak D.R., and Parkin S. Crystallization and preliminary X-ray analysis of two new crystal forms of calmodulin. Acta Crystallogr., Sect. D: Biol. Crystallogr. 52 (1996) 411-413
20. 2+-dependent conformational change and its functional implication. Biochemistry 39 (2000) 13660-13668
21. Brunger A.T., Adams P.D., Clore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
22. Chattopadhyaya R., Meador W.E., Means A.R., and Quiocho F.A. Calmodulin structure refined at 1.7 A resolution. J. Mol. Biol. 228 (1992) 1177-1192
23. 2+ binding to calmodulin: proteolytic susceptibility of E31 and E87 indicates interdomain interactions. Biochemistry 34 (1995) 1179-1196
24. Beckingham K. Use of site-directed mutations in the individual Ca2(+)-binding sites of calmodulin to examine Ca2(+)-induced conformational changes. J. Biol. Chem. 266 (1991) 6027-6030
25. 2+ binding and conformational change in two series of point mutations to the individual Ca(2+)-binding sites of calmodulin. J. Biol. Chem. 267 (1992) 5286-5295
26. Baudier J., Haglid K., Haiech J., and Gerard D. Zinc ion binding to human brain calcium binding proteins, calmodulin and S100b protein. Biochem. Biophys. Res. Commun. 114 (1983) 1138-1146
27. Rainteau D., Wolf C., and Lavialle F. Effects of calcium and calcium analogs on calmodulin: a Fourier transform infrared and electron spin resonance investigation. Biochim. Biophys. Acta 1011 (1989) 81-87
28. Shen Y., Lee Y.S., Soelaiman S., Bergson P., Lu D., Chen A., et al. Physiological calcium concentrations regulate calmodulin binding and catalysis of adenylyl cyclase exotoxins. EMBO J. 21 (2002) 6721-6732
29. Shen Y., Zhukovskaya N.L., Guo Q., Florian J., and Tang W.J. Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor. EMBO J. 24 (2005) 929-941
30. Nakashima K., Ishida H., Ohki S.Y., Hikichi K., and Yazawa M. Calcium binding induces interaction between the N- and C-terminal domains of yeast calmodulin and modulates its overall conformation. Biochemistry 38 (1999) 98-104
31. Malmendal A., Evenas J., Thulin E., Gippert G.P., Drakenberg T., and Forsen S. When size is important. Accommodation of magnesium in a calcium binding regulatory domain. J. Biol. Chem. 273 (1998) 28994-29001
32. 2+ on target recognition by calmodulin. Biochemistry 36 (1997) 4309-4316
33. Ohki S., Miura K., Saito M., Nakashima K., Maekawa H., Yazawa M., et al. Secondary structure and Ca(2+)-binding property of the N-terminal half domain of calmodulin from yeast Saccharomyces cerevisiae as studied by NMR. J. Biochem. (Tokyo) 119 (1996) 1045-1055
34. Drake S.K., and Falke J.J. Kinetic tuning of the EF-hand calcium binding motif: the gateway residue independently adjusts (i) barrier height and (ii) equilibrium. Biochemistry 35 (1996) 1753-1760
35. Drake S.K., Zimmer M.A., Kundrot C., and Falke J.J. Molecular tuning of an EF-hand-like calcium binding loop. Contributions of the coordinating side chain at loop position 3. J. Gen. Physiol. 110 (1997) 173-184
36. Dudev T., and Lim C. Principles governing Mg, Ca, and Zn binding and selectivity in proteins. Chem. Rev. 103 (2003) 773-788
37. Vogel H.J., Lindahl L., and Thulin E. Calcium-dependent hydrophobic interaction chromatography of calmodulin, troponin C and their proteolytic fragments. FEBS Lett. 157 (1983) 241-246
38. Doublie S. Preparation of selenomethionyl proteins for phase determination. Methods in Enzymology 276 (1997) 523-530
39. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
40. Terwilliger T.C., and Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 849-861
41. Bricogne E.d.L.F.a.G. Maximum likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength diffraction methods. Methods Enzymol. 276 (1997) 472-494
42. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
43. Wilson M.A., and Brunger A.T. The 1.0 A crystal structure of Ca(2+)-bound calmodulin: an analysis of disorder and implications for functionally relevant plasticity. J. Mol. Biol. 301 (2000) 1237-1256
44. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
45. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemistry quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
46. Soelaiman S., Wei B.Q., Bergson P., Lee Y.S., Shen Y., Mrksich M., et al. Structure-based inhibitor discovery against adenylyl cyclase toxins from pathogenic bacteria that cause anthrax and whooping cough. J. Biol. Chem. 278 (2003) 25990-25997
47. 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