Unwinding the helical linker of calcium-loaded calmodulin: A molecular dynamics study

Proteins: Structure, Function and Genetics

Volumn 61, Issue 4, 2005, Pages 829-839

  Fiorin, G ^a   Biekofsky, R R ^b   Pastore, A ^b   Carloni, P ^a,b  

^a SISSA   (Italy)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Conformational flexibility; Covariance analysis; EF hands; Electrostatics; Large scale motions; NMR order parameters

Indexed keywords

CALCIUM; CALMODULIN; GLOBULAR PROTEIN;

AQUEOUS SOLUTION; ARTICLE; CALCULATION; ENTROPY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RADIATION SCATTERING; SIMULATION; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CALCIUM; CALMODULIN; COMPUTER SIMULATION; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY;

HOMO SAPIENS;

EID: 28644432411     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20597     Document Type: Article

References (77)

1. Kawasaki H, Kretsinger RH. Calcium-binding proteins 1: EF-hands. Protein Profile 1995;2:297-490.
2. Carafoli E. Calcium signaling: a tale for all seasons. Proc Natl Acad Sci USA 2002;99:1115-1122.
3. 2+-dependent regulator protein of cyclic nucleotide phosphodiesterase. J Biol Chem 1977;252:8415-8422.
4. Berridge MJ, Bootman MD, Lipp P. Calcium-a life and death signal. Nature 1998;395:645-648.
5. Kuboniwa HNT, Grzesiek S, Ren H, Klee CB, Bax A. Solution structure of calcium-free calmodulin. Nat Struct Biol 1995;2:768-776.
6. Chattopadhyaya R, Meador WE, Means AR, Quiocho FA. Calmodulin structure refined at 1.7 Å resolution. J Mol Biol 1992;228:1177-1192.
7. Ikura M. Calcium binding and conformational response in EF-hand proteins. Trends Biochem Sci 1996;21:14-21.
8. Blumenthal DK, Stull JT. Effects of pH, ionic strength, and temperature on activation by calmodulin and catalytic activity of myosin light chain kinase. Biochemistry 1982;21:2386-2391.
9. Babu YS, Bugg CE, Cook WJ. Structure of calmodulin refined at 2.2 Å resolution. J Mol Biol 1988;204:191-204.
10. Herzberg O, James MN. Refined crystal structure of troponin C from turkey skeletal muscle at 2.0 Å resolution. J Mol Biol 1988;203:761-779.
11. 13C resonance assignments of calmodulin in solution by heteronuclear multidimensional NMR spectroscopy. Biochemistry 1991;30:9216-9228.
12. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible? Biochemistry 1992;31:5269-5278.
13. Sun H, Yin D, Squier TC. Calcium-dependent structural coupling between opposing globular domains of calmodulin involves the central helix. Biochemistry 1999;38:12266-12279.
14. Seaton BA, Head JF, Engelman DM, Richards F. Calcium-induced increase in the radius of gyration and maximum dimension of calmodulin measured by small-angle X-ray scattering. Biochemistry 1985;24:6740-6743.
15. Heidorn DB, Trewhella J. Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry 1987;27:909-915.
16. 2+ and mastoparan to calmodulin induces a large change in the tertiary structure. J Biochem (Tokyo) 1989;105:883-887.
17. Kataoka M, Head JF, Seaton BA, Engelman DM. Melittin binding causes a large calcium-dependent conformational change in calmodulin. Proc Natl Acad Sci USA 1989;86:6944-6948.
18. Trewhella J, Krueger JK. Small-angle solution scattering reveals information on conformational dynamics in calcium-binding proteins and in their interactions with regulatory targets. Methods Mol Biol 2002;173:137-159.
19. O'Neil KT, DeGrado WF. How calmodulin binds its targets: sequence independent recognition of amphiphilic α-helices. Trends Biochem Sci 1990;15:59-64.
20. Zhang M, Tanaka T, Ikura M. Calcium-induced conformational transition revealed by the solution structure of apo-calmodulin. Nat Struct Biol 1995;2:758-767.
21. 2+-saturated calmodulin D129N mutant studied by multiple molecular dynamics simulations. Protein Sci 2003;12:2215-2229.
22. 2+-calmodulin. Structure 2003;11:1303-1307.
23. Ikura M, Clore GM, Gronenborn AM, Zhu G, Klee CB, Bax A. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 1992;256:632-638.
24. Meador WE, Means AR, Quiocho FA. Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulin-peptide complex. Science 1992;257:1251-1255.
25. Heller W, Krueger J, Trewhella J. Further insights into calmodulin-myosin light chain kinase interaction from solution scattering and shape restoration. Biochemistry 2003;42:10579-10588.
26. Pascual-Ahuir JL, Mehler E, Weinstein H. Calmodulin structure and function: implication of arginine residues in the compaction related to ligand binding. Mol Eng 1991;1:231-247.
27. Mehler EL, Pascual-Ahuir JL, Weinstein H. Structural dynamics of calmodulin and troponin C. Protein Eng 1991;4:625-637.
28. 2+-binding and structural dynamics in the functions of calmodulin. Annu Rev Physiol 1994;56:213-236.
29. Wriggers W, Mehler E, Pitici F, Weinstein H, Schulten K. Structure and dynamics of calmodulin in solution. Biophys J 1998;74:1622-1639.
30. Van Gunsteren WF, Berendsen HJC. Gromos-87 manual. Groeningen, the Netherlands: Biornos B.V.; 1987.
31. 2+-calmodulin: evidence of interdomain coupling and structural collapse on the nanosecond timescale. Biophys J 2004;87:780-791.
32. Rao ST, Wu S, Satyshur KA, Ling KY, Kung C, Sundaralingam M. Structure of Paramecium tetraurelia calmodulin at 1.8 Å resolution. Protein Sci 1993;2:436-447.
33. Cornell WD, Cieplak P, Bayly CI, Gould IR, Caldwell JW, Kollman PA. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J Am Chem Soc 1995;117:5179-5197.
34. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001;98:10037-10041.
35. Honig B, Nicholls A. Classical electrostatics in biology and chemistry. Science 1995;268:1144-1149.
36. Berendsen HJC, van der Spoel D, van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comp Phys Comm 1995;91:43-56.
37. Lindahl E, Hess B, Van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Mod 2001;7:306-317.
38. Cheatham TE, Cieplak III P, Kollman PA. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J Biomol Struct Dyn 1999;1:845-862.
39. Åqvist J. Ion-water interaction potentials derived from free energy perturbation simulations. J Phys Chem 1990;94:8021-8024.
40. 2+-ATPase: insights from molecular modeling. Proteins 2003;50:104-113.
41. Essman U, Perela L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Phys 1995;103:8577-8592.
42. Nosé S. A molecular dynamics method for simulations in the canonical ensemble. Mol Phys 1984;52:255-268.
43. Hoover WG. Canonical dynamics: equilibrium phase-space distributions. Phys Rev A 1985;31:1695-1697.
44. Parrinello M, Rahman A. Polymorphic transition in single crystals: a new molecular dynamics method. J Appl Phys 1981;52:7182-7190.
45. Berendsen HJC, Postma JPM, Di Nola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
46. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. LINCS: a linear constraint solver for molecular simulations. J Comp Chem 1997;18:1463-1472.
47. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comp Phys 1977;23:327-341.
48. Yao Y, Schöneich C, Squier TC. Resolution of structural changes associated with calcium activation of calmodulin using frequency domain fluorescence spectroscopy. Biochemistry 1994;33:7797-7810.
49. Yang C, Jas GS, Kuczera K. Structure and dynamics of calcium-activated calmodulin in solution. J Biomol Struct Dyn 2001;18:247-271.
50. Yang C, Kuczera K. Molecular dynamics simulations of calcium-free calmodulin in solution. J Biomol Struct Dyn 2002;19:801-819.
51. 2+-dependent conformational change of calmodulin. FEBS Lett 2002;521:133-139.
52. Walther D, Eisenhaber F, Argos P. Principles of helix-helix packing in proteins: the helical lattice superposition model. J Mol Biol 1996;255:536-553.
53. Hess B. Similarities between principal components of protein dynamics and random diffusion. Phys Rev E 2000;62:8438-8448.
54. Hess B. Convergence of sampling in protein simulations. Phys Rev E 2002;65:031910.
55. Wriggers W, Schulten K. Protein domain movements: detection of rigid domains and visualization of hinges in comparisons of atomic coordinates. Proteins 1997;29:1-14.
56. Lipari G, Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules: 1. Theory and range of validity. J Am Chem Soc 1982;104:4546-4559.
57. Lipari G, Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules: 2. Analysis of experimental results. J Am Chem Soc 1982;104:4559-4510.
58. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 1989;28:8972-8979.
59. 2+-calmodulin reveals flexible hand-like properties of its domains. Nat Struct Biol 2001;8:990-997.
60. Bertini I, Del Bianco C, Gelis I, Katsaros N, Luchinat C, Parigi G, Peana M, Provenzani A, Zoroddu MA. Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc Natl Acad Sci USA 2004;101:6841-6846.
61. Humphrey W, Dalke A, Schulten K. VMD-visual molecular dynamics. J Mol Graphics 1996;14:33-38.
62. Marchand S, Roux B. Molecular dynamics study of calbindin D9k in the apo and singly and doubly calcium-loaded states. Proteins 1998;33:265-284.
63. Philippopoulos M, Mandel AM, Palmer AGI, Lim C. Accuracy and precision of NMR relaxation experiments and MD simulations for characterizing protein dynamics. Proteins 1997;28:481-493.
64. Qin Z, Squier TC. Calcium-dependent stabilization of the central sequence between Met76 and Ser81 in vertebrate calmodulin. Biophys J 2001;81:2908-2918.
65. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comp Chem 1983;4:187-217.
66. de Souza NO, Ornstein RL. Molecular dynamics simulations of a protein-protein dimer: particle-mesh Ewald electrostatic model yields far superior results to standard cutoff model. J Biomol Struct Dyn 1999;16:1205-1218.
67. MacKerell AD, Bashford D, Bellot M, Dunbrack RL Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, and Ha S. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102:3586-3616.
68. Van der Spoel D, De Groot BL, Hayward S, Berendsen HJC, Vogel HJ. Bending of the calmodulin central helix: a theoretical study. Protein Sci 1996;5:2044-2053.
69. Yoda T, Sugita Y, Okamoto Y. Comparisons of force fields for proteins by generalized-ensemble simulations. Chem Phys Lett 2004;386:460-467.
70. Deserno M, Holm C. A theoretical and numerical comparison of various particle mesh routines. J Chem Phys 1998;109:7678-7693.
71. Vigil D, Gallagher SC, Trewhella J, Garcia AE. Functional dynamics of the hydrophobic cleft in the N-domain of calmodulin. Biophys J 2001;80:2082-2092.
72. 2+-calmodulin- dependent protein kinase kinase. Nat Struct Biol 1999;6:819-824.
73. Persechini A, McMillan K, Leakey P. Activation of myosin light chain kinase and nitric oxide synthase activities by calmodulin fragments. J Biol Chem 1994;269:16148-16154.
74. Brokx RD, Lopez MM, Vogel HJ, Makhatadze GI. Energetics of target peptide binding by calmodulin reveals different modes of binding. J Biol Chem 2001;276:14083-14091.
75. Martin SR, Bayley PM, Brown SE, Porumb T, Zhang M, Ikura M. Spectroscopic characterization of a high-affinity calmodulin-target peptide hybrid molecule. Biochemistry, 1996;35:3508-3517.
76. Barbieri R, Bertini I, Cavallaro G, Lee YM, Luchinat C, Rosato A. Paramagnetically induced residual dipolar couplings for solution structure determination of lanthanide binding proteins. J Am Chem Soc 2002;124:5581-5587.
77. Bertini I, Longinetti M, Luchinat C, Parigi G, Sgheri L. Efficiency of paramagnetism-based constraints to determine the spatial arrangement of alpha-helical secondary structure elements. J Biomol NMR 2002;22:123-136.