Calcium binding decreases the stokes radius of calmodulin and mutants R74A, R90A, and R90G

Biophysical Journal

Volumn 71, Issue 6, 1996, Pages 3407-3420

  Sorensen, Brenda R ^a   Shea, Madeline A ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; CALCIUM; CALCIUM BINDING PROTEIN; CALMODULIN; GLYCINE; PROTEIN;

ARTICLE; CALCIUM BINDING; CONFORMATIONAL TRANSITION; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR DYNAMICS; MUTANT; MUTATION; RADIATION SCATTERING;

EID: 0029753786     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79535-8     Document Type: Article

References (103)

1. Abola, E. E., F. C. Bernstein, S. H. Bryant, T. F. Koetzleand, and J. Weng. 1987. Protein Data Bank. In Crystallographic Databases - Information Content, Software Systems, Scientific Applications. F. H. Allen, G. Bergerhoff and R. Sievers, editors. Data Commission of the International Union of Crystallography, Bonn/Cambridge/Chester. 107-132.
2. Ackers, G. K. 1964. Molecular exclusion and restricted diffusion processes in molecular-sieve chromatography. Biochemistry. 3:723-730.
3. Ackers, G. K. 1967. A new calibration procedure for gel filtration columns. J. Biol. Chem. 242:3237-3238.
4. Ackers, G. K. 1970. Analytical gel chromatography of proteins. Adv. Protein Chem. 24:343-446.
5. Ackers, G. K., and T. E. Thompson. 1965. Determination of stoichiometry and equilibrium constants for reversibly associating systems by molecular sieve chromatography. Proc. Natl. Acad. Sci. USA. 53:342-349.
6. Andrews, P. 1964. Estimation of the molecular weights of proteins by Sephadex gel-filtration. Biochem. J. 91:222-233.
7. Andrews, P. 1965. The gel-filtration behaviour of proteins related to their molecular weights over a wide range. Biochem. J. 96:595-606.
8. Andrews, P. 1970. Estimation of molecular size and molecular weights of biological compounds by gel filtration. In Methods of Biochemical Analysis. D. Glick, editor. John Wiley and Sons, New York. 1-53.
9. Aulabaugh, A., W. P. Niemczura, and W. A. Gibbons. 1984. High field proton NMR studies of tryptic fragments of calmodulin: a comparison with the native protein. Biochem. Biophys. Res. Commun. 118:225-232.
10. Babu. Y. S., C. E. Bugg, and W. J. Cook. 1988. Structure of calmodulin refined at 2.2 A resolution. J. Mol. Biol. 204:191-204.
11. Babu, Y. S., J. S. Sack, T. J. Greenhough, C. E. Bugg, A. R. Means, and W. J. Cook. 1985. Three-dimensional structure of calmodulin. Nature. 315:37-41.
12. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry. 31:5269-5278.
13. Bayley, P. M., and S. R. Martin. 1992. The α-helical content of calmodulin is increased by solution conditions favouring protein crystallisation. Biochim. Biophys. Acta. 1160:16-21.
14. Bayley, P., S. Martin, and G. Jones. 1988. The conformation of calmodulin: a substantial environmentally sensitive helical transition in Ca4-calmodulin with potential mechanistic function. FEBS Lett. 238: 61-66.
15. Bernstein, F. C., T. F. Koetzle, G. J. B. Williams, E. F. Meyer, Jr., M. D. Brice, J. R. Rodgers, O. Kennard, T. Shimanouchi, and M. Tasumi. 1977. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:535-542.
16. Burz, D. S., D. Beckett, N. Benson, and G. K. Ackers. 1994. Self-assembly of bacteriophage λ cl represser: effects of single-site mutations on the monomer-dimer equilibrium. Biochemistry. 33:8399-8405.
17. Chattopadhyaya, R., W. E. Meador, A. R. Means, and F. A. Quiocho. 1992. Calmodulin structure refined at 1.7 Å resolution. J. Mol. Biol. 228: 1177-1192.
18. Clore, G. M., and A. M. Gronenborn. 1994. Structures of larger proteins, protein-ligand and protein-DNA complexes by multidimensional heteronuclear NMR. Protein Sci. 3:372-390.
19. Cook, W. J., and J. S. Sack. 1983. Preparation of calmodulin crystals. Methods Enzymol. 102:143-147.
20. Cook, W. J., L. J. Walter, and M. R. Walter. 1994. Drug binding by calmodulin: crystal structure of a calmodulin-trifluoperazine complex. Biochemistry. 33:15259-15265.
21. Cox, J. A. 1988. Interactive properties of calmodulin. Biochem. J. 249: 621-629.
22. Crivici, A., and M. Ikura. 1995. Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol Struct. 24: 85-116.
23. Crouch, T. H., and C. B. Klee. 1980. Positive cooperative binding of calcium to bovine brain calmodulin. Biochemistry. 19:3692-3698.
24. Davis, T. N., M. S. Urdea, F. R. Masiarz, and J. Thorner. 1986. Isolation of the yeast calmodulin gene: calmodulin is an essential protein. Cell. 47:423-431.
25. 2+-binding, conformational changes, and phosphodiesterase activity. J. Biol. Chem. 252:8415-8422.
26. Finn, B. E., J. Evenäs, T. Drakenberg, J. P. Waltho, E. Thulin, and S. Forsén. 1995. Calcium-induced structural changes and domain autonomy in calmodulin. Nature Struct. Biol. 2:777-783.
27. Garcia de la Torre, J., and V. A. Bloomfield. 1981. Hydrodynamic properties of complex, rigid, biological macromolecules: theory and applications. Q. Rev. Biophys. 14:81-139.
28. Garcia de la Torre, J., S. Navarro, M. C. Lopez Martinez, F. G. Diaz, and J. J. Lopez Cascales. 1994. HYDRO: a computer program for the prediction of hydrodynamic properties of macromolecules. Biophys. J. 67:530-531.
29. George, S. E., Z. Su, D. Fan, and A. R. Means. 1993. Calmodulin-cardiac troponin C chimeras: effects of domain exchange on calcium binding and enzyme activation. J. Biol. Chem. 265:2513-25220.
30. Harmon, S. D., and M. A. Shea. 1995. Allosteric disruption of paramecium calmodulin. Biophys. J. 68:A140.
31. Heidorn, D. B., and J. Trewhella. 1988. Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry. 27: 909-915.
32. Heidorn, D. B., and J. Trewhella. 1990. Low resolution studies of proteins in solution: calmodulin. Comments Mol. Cell Biophys. 6:329-359.
33. Henn, S. W., and G. K. Ackers. 1969. Molecular sieve studies of interacting protein systems. V. Association of subunits of D-amino acid oxidase apoenzyme. Biochemistry. 8:3829-3838.
34. 1H-homonuclear 2D-NMR. In Techniques in Protein Chemistry II. J. Villafranca, editor. Academic Press, San Diego. 383-391.
35. Horiike, K., H. Tojo, T. Yamano, and M. Nozaki. 1983. Interpretation of the stokes radius of macromolecules determined by gel filtration chromatography. J. Biochem. (Tokyo). 93:99-106.
36. Ikura, M., T. Hiraoki, K. Hikichi, T. Mikuni, M. Yazawa, and K. Yagi. 1983. Nuclear magnetic resonance studies on calmodulin: calcium-induced conformational change. Biochemistry. 22:2573-2579.
37. 2+-dependent spectral change of proteolytic fragments. Biochemistry. 23:3124-3128.
38. Ikura, M., O. Minowa, and K. Hikichi. 1985. Hydrogen bonding in the carboxyl-terminal half-fragment 78-148 of calmodulin as studied by two-dimensional nuclear magnetic resonance. Biochemistry. 24: 4264-4269.
39. 13C resonance assignments of calmodulin in solution by heteronuclear multidimensional NMR spectroscopy. Biochemistry. 30:9216-9228.
40. Johnson, M. L., and S. G. Frasier. 1985. Nonlinear least-squares analysis. Methods Enzymol. 117:301-342.
41. Kataoka, M., J. F. Head, A. Persechini, R. H. Kretsinger, and D. M. Engelman. 1991a. Small-angle X-ray scattering studies of calmodulin mutants with deletions in the linker region of the central helix indicate that the linker region retains a predominantly α-helical conformation. Biochemistry. 30:1188-1192.
42. Kataoka, M., J. F. Head, B. A. Seaton, and D. M. Engelman. 1989. Melittin binding causes a large calcium-dependent conformational change in calmodulin. Proc. Natl. Acad. Sci. USA. 86:6944-6948.
43. 2+ pump. Biochemistry. 30:6247-6251.
44. Kita, Y., T. Arakawa, T. Lin, and S. N. Timasheff. 1994. Contribution of the surface free energy perturbation to protein-solvent interactions. Biochemistry. 33:15178-15189.
45. Klee, C. B., and P. Cohen. 1988. The calmodulin-regutated protein phosphatase. In Calmodulin. P. Cohen and C. B. Klee, editors. Elsevier, New York. 225-248.
46. Klee. C. B., and T. C. Vanaman. 1982. Calmodulin. Adv. Protein Chem. 35:213-321.
47. 2+-dependent conformational change. Eur. J. Biochem. 139:109-114.
48. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
49. Kretsinger, R. H. 1992. The linker of calmodulin: to helix or not to helix. Cell Calcium. 13:363-376.
50. Kretsinger, R. H., and C. E. Nockold. 1973. Carp muscle calcium-binding protein. J Biol. Chem. 215:3313-3326.
51. Kuboniwa, H., N. Tjandra, S. Grzesiek, H. Ren, C. B. Klee, and A. Bax. 1995. Solution structure of calcium-free calmodulin. Nature Struct. Biol. 2:768-776.
52. Kung, C., R. R. Preston, M. E. Maley, K.-Y. Ling, J. A. Kanabrocki, B. R. Seavey, and Y. Saimi. 1992. In vivo Paramecium mutants show that calmodulin orchestrates membrane responses to stimuli. Cell Calcium. 13:413-425.
53. Kuntz, I. D., and W. Kauzmann. 1974. Hydration of proteins and polypeptides. Adv. Protein Chem. 28:239-338.
54. Kupke, D. W. 1986. Sequential volume changes on a small sample by density. Anal. Biochem. 158:463-468.
55. Kupke, D. W., and B. S. Shank. 1989. Volume change for calcium(II) to tetracarboxylate sequestrants: relevance to calcium binding proteins. J. Phys. Chem. 93:2101-2106.
56. LaPorte, D. C., B. M. Wierman, and D. R. Storm. 1980. Calcium-induced exposure of a hydrophobic surface on calmodulin. Biochemistry. 19: 3814-3819.
57. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
58. Laurent, T. C., and J. Killander. 1964. A theory of gel filtration and its experimental verification. J. Chromatogr. 14:317-330.
59. Le Maire, M., A. Viel, and J. V. Mθller. 1989. Size exclusion chromatography and universal calibration of gel columns. Anal. Biochem. 177: 50-56.
60. Lu, K. P., and A. R. Means. 1993. Regulation of the cell cycle by calcium and calmodulin. Endocr. Rev. 14:40-58.
61. 2/M progression in Aspergillus nidulans. J. Cell Biol. 115:426 (Abstr.).
62. 2+ and mastoparan to calmodulin induces a large change in the tertiary structure. J. Biochem. (Tokyo). 105:883-887.
63. 2+-binding and calcineurin activation. J. Cell Biol. 107:287a. (Abstr.)
64. 2+-binding sites of calmodulin. J. Biol Chem. 267:5286-5295.
65. Mehler, E. L., J.-L. Pascual-Ahuir, and H. Weinstein. 1991. Structural dynamics of calmodulin and tryponin C. Protein Eng. 4:625-637.
66. Ogston, A. G. 1958. The spaces in a uniform random suspension of fibres. Trans. Faraday Soc. 54:1754-1757.
67. Oncley, J. L. 1941. Evidence from physical chemistry regarding the size and shape of protein molecules from ultra-centrifugation, diffusion, viscosity, dielectric dispersion, and double refraction of flow. Ann. N.Y. Acad. Sci. 41:121-150.
68. Pascual-Ahuir, J.-L., E. L. Mehler, and H. Weinstein. 1991. Calmodulin structure and function: implication of arginine in the compaction related to ligand binding. Mol Eng. 1:231-247.
69. 2+ binding to calmodulin: proteolytic susceptibility of E31 and E87 indicates interdomain interactions. Biochemistry. 34:1179-1196.
70. Perrin, F. 1936. Mouvement Brownien d'un ellipsoide (II). Rotation libre et depolarization des fluorescences. Translation et diffusion de molécules ellipsoidales. J. Phys. Radium. 7:1-11.
71. Persechini, A., and R. H. Kretsinger. 1988. The central helix of calmodulin functions as a flexible tether. J. Biol. Chem. 263:12175-12178.
72. Pharmacia Biotech. 1996. Gel Filtration Calibration Kit Instruction Manual for Protein Molecular Weight Determinations by Gel Filtration. Catalog no. 17-0441-01. Pharmacia Biotech, Piscataway, NJ.
73. Pharmacia LKB Biotechnology. 1991. Gel Filtration Principles and Methods. Pharmacia LKB Biotechnology, Uppsala, Sweden.
74. Porath, J. 1963. Some recently developed fractionation procedures and their application to peptide and protein hormones. J. Pure Appl. Chem. 6:233-244.
75. Potschka, M. 1987. Universal calibration of gel permeation chromatography and determination of molecular shape in solution. Anal. Biochem. 162:47-64.
76. Putkey, J. A., G. R. Slaughter, and A. R. Means. 1985. Bacterial expression and characterization of proteins derived from the chicken calmodulin cDNA and a calmodulin processed gene. J. Biol. Chem. 260: 4704-4712.
77. 1 and mitosis. EMBO J. 8:73-82.
78. Rasmussen, C. D., R. L. Means, K. P. Lu, G. S. May, and A. R. Means. 1990. Characterization and expression of the unique calmodulin gene of Aspergillus nidulans. J. Biol. Chem. 265:13767-13775.
79. Seamon, K. B. 1980. Calcium- and magnesium-dependent conformational states of calmodulin as determined by nuclear magnetic resonance. Biochemistry. 19:207-215.
80. Seaton, B. A., J. F. Head, D. M. Engelman, and F. M. Richards. 1985. Calcium-induced increase in the radius of gyration and maximum dimension of calmodulin measured by small-angle x-ray scattering. Biochemistry. 24:6740-6743.
81. Shea, M. A., A. S. Verhoeven, and S. Pedigo. 1996. Calcium-induced interactions of calmodulin domains revealed by quantitative thrombin footprinting of Arg37 and Arg106. Biochemistry. 35:2943-2957.
82. Siegel, L. M., and K. J. Monty. 1966. Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Application to crude preparations of sulfite and hydroxylamine reductases. Biochim. Biophys. Acta. 112: 346-362.
83. Small, E. W., and S. R. Anderson. 1988. Fluorescence anisotropy decay demonstrates calcium-dependent shape changes in photo-cross-linked calmodulin. Biochemistry. 27:419-428.
84. Sorensen, B. R., and M. A. Shea. 1995. Mutational perturbation of calmodulin structure. Biophys. J. 68:A403.
85. Squire, P. G. 1964. A relationship between the molecular weights of macromolecules and their elution volumes based on a model for Sephadex gel filtration. Arch. Biochem. Biophys. 107:471-478.
86. Squire, P. G., and M. E. Himmel. 1979. Hydrodynamics and protein hydration. Arch. Biochem. Biophys. 196:165-177.
87. Stafford, W. F., and T. M. Schuster. 1995. Hydrodynamic methods. In Introduction to Biophysical Methods for Protein and Nucleic Acid Research. Academic Press, San Diego. 111-145.
88. Strynadka, N. C. J., and M. N. G. James. 1989. Crystal structures of the helix-loop-helix calcium-binding proteins. Annu. Rev. Biochem. 58: 951-998.
89. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA. 82:1074-1078.
90. Tanford, C., Y. Nozaki, A. Reynolds, and S. Makino. 1974. Molecular characterization of proteins in detergent solutions. Biochemistry. 13: 2369-2376.
91. Taylor, D. A., J. S. Sack, J. F. Maune, K. Beckingham, and F. A. Quiocho. 1991. Structure of a recombinant calmodulin from Drosophila melanogaster refined at 2.2-Å resolution. J. Biol. Chem. 266:21375-21380.
92. 15N-NMR relaxation measurements. Eur. J. Biochem. 230:1014-1024. (Abstr.)
93. Török, K., A. N. Lane, S. R. Martin, J.-M. Janot, and P. M. Bayley. 1992. Effects of calcium binding on the internal dynamic properties of bovine brain calmodulin, studied by NMR and optical spectroscopy. Biochemistry. 31:3452-3462.
94. Urbauer, J. L., J. H. Short, L. K. Dow, and A. J. Wand. 1995. Structural analysis of a novel interaction by calmodulin: high affinity binding of a peptide in the absence of calcium. Biochemistry. 34:8099-8109.
95. Wang, C. A. 1989. pH-dependent conformational changes of wheat germ calmodulin. Biochemistry. 28:4816-4820.
96. 2+ binding to calmodulin. Biochem. Biophys. Res. Commun. 130:426-430.
97. Warshaw, H. S., and G. K. Ackers. 1971. Molecular sieve studies of interacting protein systems. VIII. Critical evaluation of the equilibrium sturation technique using stacked gel columns. Anal. Biochem. 42: 405-421.
98. 2+-binding and structural dynamics in the functions of calmodulin. Annu. Rev. Physiol. 56:213-236.
99. Yao, Y., C. Schöneich, and T. C. Squier. 1994. Resolution of structural changes associated with calcium activation of calmodulin using frequency domain fluorescence spectroscopy. Biochemistry. 33: 7797-7810.
100. Yazawa, M., F. Matsuzawa, and K. Yagi. 1990. Inter-domain interaction and the structural flexibility of calmodulin in the connecting region of the terminal two domains. J. Biochem. (Tokyo). 107:287-291.
101. Yoshino, H., O. Minari, N. Matsushima, T. Ueki, Y. Miyake, T. Matsuo, and Y. Izumi. 1989. Calcium-induced shape change of calmodulin with mastoparan studied by solution x-ray scattering. J. Biol. Chem. 264: 19706-19709.
102. Yoshino, H., M. Wakita, and Y. Izumi. 1993. Calcium-dependent changes in structure of calmodulin with substance P. J. Biol. Chem. 268: 12123-12128.
103. Zhang, M., T. Tanaka, and M. Ikura. 1995. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nature Struct. Biol. 2:758-767.