X-ray structures of magnesium and manganese complexes with the N-terminal domain of calmodulin: Insights into the mechanism and specificity of metal ion binding to an EF-hand

Biochemistry

Volumn 51, Issue 31, 2012, Pages 6182-6194

  Senguen, F Timur ^a   Grabarek, Zenon ^a  

^a BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTIONS; CONFORMATIONAL CHANGE; EF-HAND; HYDRATION WATER; MANGANESE COMPLEXES; METAL ION BINDING; MICROMOLAR CONCENTRATION; N-TERMINAL DOMAINS; OCTAHEDRALLY COORDINATED; PROTEIN SURFACE; RELATIVE POSITIONS; SIDE-CHAINS; STRUCTURAL BASIS; WATER MOLECULE; X-RAY STRUCTURE;

CALCIUM; CAMS; HYDRATION; LIGANDS; MAGNESIUM; MANGANESE; MANGANESE COMPOUNDS; METAL IONS; ZINC;

CALMODULIN;

CALCIUM ION; CALMODULIN; MAGNESIUM ION; MANGANESE; ZINC ION;

AMINO TERMINAL SEQUENCE; ARTICLE; CALCIUM BINDING; CONFORMATIONAL TRANSITION; HUMAN; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; METAL BINDING; PRIORITY JOURNAL; PROTEIN MOTIF; X RAY;

CALMODULIN; CRYSTALLOGRAPHY, X-RAY; EF HAND MOTIFS; HUMANS; MAGNESIUM; MANGANESE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; ZINC;

EID: 84864679389     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300698h     Document Type: Article

References (71)

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. Carafoli, E., Santella, L., Branca, D., and Brini, M. (2001) Generation, control, and processing of cellular calcium signals Crit. Rev. Biochem. Mol. Biol. 36, 107-260
3. Clapham, D. E. (2007) Calcium signaling Cell 131, 1047-1058
4. Romani, A. and Scarpa, A. (1992) Regulation of cell magnesium Arch. Biochem. Biophys. 298, 1-12
5. 2+ transport in the heart Nature 346, 841-844
6. Romani, A., Marfella, C., and Scarpa, A. (1993) Regulation of magnesium uptake and release in the heart and in isolated ventricular myocytes Circ. Res. 72, 1139-1148
7. 2+ during metabolic stimulation of rat cardiac myocytes and perfused hearts Arch. Biochem. Biophys. 374, 395-401
8. 2+ homeostasis by insulin in perfused rat livers and isolated hepatocytes FEBS Lett. 395, 241-244
9. 2+ transport and homeostasis in eukaryotic cells BioMetals 15, 271-283
10. Seelig, M. S. (1980) Magnesium deficiency in the pathogenesis of disease. Early roots of cardiovascular, skeletal and renal abnormalities, Goldwater Memorial Hospital, New York University Medical Center, New York.
11. Harkema, J. M. and Chaudry, I. H. (1992) Magnesium-adenosine triphosphate in the treatment of shock, ischemia, and sepsis Crit. Care Med. 20, 263-275
12. Grabarek, Z. (2011) Insights into modulation of calcium signaling by magnesium in calmodulin, troponin C and related EF-hand proteins Biochim. Biophys. Acta 1813, 913-921
13. Crivici, A. and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin Annu. Rev. Biophys. Biomol. Struct. 24, 85-116
14. Grabarek, Z. (2006) Structural basis for diversity of the EF-hand calcium-binding proteins J. Mol. Biol. 359, 509-525
15. 2+-binding helix-loop-helix EF-hand motifs Biochem. J. 405, 199-221
16. 2+ on target recognition by calmodulin Biochemistry 36, 4309-4316
17. 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
18. 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
19. 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
20. 2+-induced conformational transitions in calmodulin with disulfide bonds J. Biol. Chem. 271, 7479-7483
21. Chao, S. H., Suzuki, Y., Zysk, J. R., and Cheung, W. Y. (1984) Activation of calmodulin by various metal cations as a function of ionic radius Mol. Pharmacol. 26, 75-82
22. 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
23. Strynadka, N. C. J. and James, M. N. G. (1989) Crystal structures of the helix-loop-helix calcium-binding proteins Annu. Rev. Biochem. 58, 951-998
24. Grabarek, Z. (2005) Structure of a trapped intermediate of calmodulin: Calcium regulation of EF-hand proteins from a new perspective J. Mol. Biol. 346, 1351-1366
25. 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
26. 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
27. 2+-receptor calbindin D9k Protein Sci. 6, 1139-1147
28. Follenius, A. and Gerard, D. (1984) Fluorescence investigations of calmodulin hydrophobic sites Biochem. Biophys. Res. Commun. 119, 1154-1160
29. Doering, D. S. and Matsudaira, P. (1996) Cysteine scanning mutagenesis at 40 of 76 positions in villin headpiece maps the F-actin binding site and structural features of the domain Biochemistry 35, 12677-12685
30. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179, 131-137
31. 2+-induced conformational transition in the C-terminal domain of calmodulin J. Biol. Chem. 271, 11284-11290
32. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
33. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
34. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: Building new software for automated crystallographic structure determination Acta Crystallogr. D58, 1948-1954
35. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Adams, P. D., Read, R. J., Zwart, P. H., and Hung, L.-W. (2008) Iterative-build OMIT maps: Map improvement by iterative model building and refinement without model bias Acta Crystallogr. D64, 515-524
36. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
37. Tsai, M. D., Drakenberg, T., Thulin, E., and Forsen, S. (1987) Is the binding of magnesium(II) to calmodulin significant? An investigation by magnesium-25 nuclear magnetic resonance Biochemistry 26, 3635-3643
38. 2+-dependent interactions of calmodulin with target sequences Protein Sci. 9, 2477-2488
39. Warren, J. T., Guo, Q., and Tang, W. J. (2007) A 1.3-Å structure of zinc-bound N-terminal domain of calmodulin elucidates potential early ion-binding step J. Mol. Biol. 374, 517-527
40. Shannon, R. D. (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides Acta Crystallogr. A32, 751-767
41. Carrell, C. J., Carrell, H. L., Erlebacher, J., and Glusker, J. P. (1988) Structural aspects of metal-ion carboxylate interactions J. Am. Chem. Soc. 110, 8651-8656
42. Harding, M. M. (2006) Small revisions to predicted distances around metal sites in proteins Acta Crystallogr. D62, 678-682
43. Delville, A., Grandjean, J., Laszlo, P., Gerday, C., Brzeska, H., and Drabikowski, W. (1980) Sodium-23 nuclear magnetic resonance as an indicator of sodium binding to calmodulin and tryptic fragments, in relation to calcium content Eur. J. Biochem. 109, 515-522
44. Moroz, O. V., Blagova, E. V., Wilkinson, A. J., Wilson, K. S., and Bronstein, I. B. (2009) The crystal structures of human S100A12 in apo form and in complex with zinc: New insights into S100A12 oligomerisation J. Mol. Biol. 391, 536-551
45. Irving, H. and Williams, R. J. P. (1953) The stability of transition-metal complexes J. Chem. Soc., 3192-3210
46. Brzeska, H., Venyaminov, S. V., Grabarek, Z., and Drabikowski, W. (1983) Comparative studies on thermostability of calmodulin, skeletal muscle troponin C and their tryptic fragments FEBS Lett. 153, 169-173
47. Cates, M. S., Berry, M. B., Ho, E. L., Li, Q., Potter, J. D., and Phillips, G. N., Jr. (1999) Metal-ion affinity and specificity in EF-hand proteins: Coordination geometry and domain plasticity in parvalbumin Structure in Folding and Design 7, 1269-1278
48. Cates, M. S., Teodoro, M. L., and Phillips, G. N., Jr. (2002) Molecular mechanisms of calcium and magnesium binding to parvalbumin Biophys. J. 82, 1133-1146
49. Deerfield, D. W., II, Fox, D. J., Head-Gordon, M., Hiskey, R. G., and Pedersen, L. G. (1995) The first solvation shell of magnesium ion in a model protein environment with formate, water, and X-NH3, H2S, imidazole, formaldehyde, and chloride as ligands: An ab initio study Proteins 21, 244-255
50. 2+ coordination Biochemistry 37, 7617-7629
51. Maguire, M. E. and Cowan, J. A. (2002) Magnesium chemistry and biochemistry BioMetals 15, 203-210
52. 2O Acta Crystallogr. 18, 1004-1018
53. Diebler, H., Eigen, M., Ilgenfritz, G., Maass, G., and Winkler, R. (1969) Kinetics and mechanism of reactions of main group metal ions with biological carriers Pure Appl. Chem. 20, 93-115
54. 2+ binding and conformational changes in a calmodulin domain Biochemistry 37, 13744-13754
55. 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
56. 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
57. Dupuis, L. and Mousseau, N. (2012) Understanding the EF-hand closing pathway using non-biased interatomic potentials J. Chem. Phys. 136, 035101
58. Jurado, L. A., Chockalingam, P. S., and Jarrett, H. W. (1999) Apocalmodulin Physiol. Rev. 79, 661-682
59. Berridge, M. J., Bootman, M. D., and Lipp, P. (1998) Calcium: A life and death signal Nature 395, 645-648
60. Romani, A. M. and Scarpa, A. (2000) Regulation of cellular magnesium Front. Biosci. 5, D720-D734
61. Romani, A. M. (2011) Cellular magnesium homeostasis Arch. Biochem. Biophys. 512, 1-23
62. 2+ in cultured cortical neurons Neuron 11, 751-757
63. v2.1 channels Proc. Natl. Acad. Sci. U.S.A. 100, 16059-16064
64. 2+ acting at an EF-hand motif in the COOH-terminal domain J. Gen. Physiol. 126, 311-323
65. Rayssiguier, Y., Mbega, J. D., Durlach, V., Gueux, E., Durlach, J., Giry, J., Dalle, M., Mazur, A., Laurant, P., and Berthelot, A. (1992) Magnesium and blood pressure. I. Animal studies Magnesium Res. 5, 139-146
66. Touyz, R. M. (2003) Role of magnesium in the pathogenesis of hypertension Mol. Aspects Med. 24, 107-136
67. Touyz, R. M. (2004) Magnesium in clinical medicine Front. Biosci. 9, 1278-1293
68. Weglicki, W., Quamme, G., Tucker, K., Haigney, M., and Resnick, L. (2005) Potassium, magnesium, and electrolyte imbalance and complications in disease management Clin. Exp. Hypertens. 27, 95-112
69. Mazur, A., Maier, J. A., Rock, E., Gueux, E., Nowacki, W., and Rayssiguier, Y. (2007) Magnesium and the inflammatory response: Potential physiopathological implications Arch. Biochem. Biophys. 458, 48-56
70. Hsin, K., Sheng, Y., Harding, M. M., Taylor, P., and Walkinshaw, M. D. (2008) MESPEUS: A database of the geometry of metal sites in proteins J. Appl. Crystallogr. 41, 963-968
71. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, Palo Alto, CA.