Molecular mechanisms of calmodulin's functional versatility

Biochemistry and Cell Biology

Volumn 76, Issue 2-3, 1998, Pages 313-323

  Zhang, Mingjie ^a,b   Yuan, Tao ^b  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Calmodulin; Ligand specificity; NMR; Peptide targets; Structure and dynamics

Indexed keywords

CALCIUM; CALMODULIN;

AMINO ACID SEQUENCE; BINDING AFFINITY; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; HYDROPHOBICITY; PROTEIN BINDING; PROTEIN CONFORMATION; REVIEW;

EUKARYOTA;

EID: 0032469789     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o98-027     Document Type: Review

References (74)

1. Ames, J.B., Ishima, R., Tanaka, T., Gordon, J.I., Stryer, L., and Ikura, M. 1997. Molecular mechanics of calcium-myristoyl switch. Nature (London), 389: 198-202.
2. Andersson, A., Forsen, S., Thulin, E., and Vogel, HJ. 1983. Cadmium-113 nuclear magnetic resonance studies of proteolytic fragments of calmodulin: assignment of strong and weak cation binding sites. Biochemistry, 22: 2309-2313.
3. Babu, Y.S., Bugg, C.E., and Cook, W.J. 1988. Structure of calmodulin refined at 2.2 Å resolution. J. Mol. Biol. 204: 191-204.
4. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry, 31: 5269-5278.
5. Bernstein, H.D., Poritz, M.A., Strub, K., Hoben, P.J., Brenner, S., and Walter, P. 1989. Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature (London), 340: 482-486.
6. Chattopadkyaya, R., Meador, W.E., Means, A.R., and Quiocho, F.A. 1992. Calmodulin structure refined at 1.7 Å resolution. J. Mol. Biol. 228: 1177-1192.
7. Crivici, A, and Ikura, M. 1995. Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol. Struct. 24: 85-116.
8. 1H NMR studies of calmodulin: resonance assignment by use of tryptic fragments. Eur. J. Biochem. 138: 281-289.
9. Dasgupta, M., Honeycutt, T., and Blumenthal, D.K. 1989. The γ-subunit of skeletal muscle phosphorylase kinase contains two noncontiguous domains that act in concert to bind calmodulin. J. Biol. Chem. 264: 17 156-17 163.
10. Edwards, R.A., Walsh, M.P., Sutherland, C., and Vogel, H.J. 1998. Activation of calcineurin and smooth muscle myosin light clinn kinase by Met to Leu mutants of calmodulin. Biochem. J. 331: 149-152.
11. Ehlers, M.D., Zhang, S., Bernhardt, J.P., and Huganir, R.L. 1996. Interaction of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell, 84: 745-755.
12. Ehrhardt, M.R., Urbauer, J.L, and Wand, A.J. 1995. The energetics and dynamics of molecular recognition by calmodulin. Biochemistry, 34: 2731-2738.
13. Fabian, H., Yuan, T., Vogel, H.J., and Mantsh, H.H. 1996. Comparative analysis of the amino-and carboxyl-terminal domains of calmodulin by Fourier transform infrared spectroscopy. Eur. Biophys. J. 24: 195-201.
14. Gagne, S.M., Tsuda, S., Li, M.X., Smillie, L.B., and Sykes, B.D. 1995. Structures of the apo and calcium troponin-C regulatory domains: the muscle contraction switch. Nat. Struct. Biol. 2: 784-789.
15. Gellman, S.H. 1991. On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry, 30: 6633-6636.
16. Graether, S.P., Heinonen, T.Y.K., Raharjo, W.H., Jin, J.-P., and Mak, A.S. 1997. Tryptophan residues in caldesmon are major determinants for calmodulin binding. Biochemistry, 36: 364-369.
17. Gulati, J., Babu, A., Su, H., and Zhang, Y.-F. 1993. Identification of the regions conferring calmodulin-like properties to troponin C. J. Biol. Chem. 268: 11 685-11 690.
18. Houdusse, A., and Cohen, C. 1995. Target sequence recognition by the calmodulin superfamily: implication from light chain binding to the regulatory domain of scallop myosin. Proc. Natl. Acad. Sci. U.S.A. 92: 10 644-10 647.
19. 2+-switch in the calmodulin superfamily. Structure (London), 5: 1695-1711.
20. 2+-calmodulin. Biochem. J. 316: 413-420.
21. Ikura, M. 1996. Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21: 14-17.
22. Ikura, M., Hiraoki, T., Hikichi, K., Mikuni, T., Yazawa, M., and Yagi, K. 1983. Nuclear magnetic resonance studies on calmodulin: calcium-induced conformational change. Biochemistry; 22: 2573-2579.
23. 13C resonance assignments of calmodulin in solution by heteronuclear multidimensional NMR spectroscopy. Biochemistry, 30: 9216-9228.
24. Ikura, M., Clore, G.M., Gronenborn, A.M., Zhu, G., Klee, C.B., and Bax, A. 1992. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science (Washington, D.C.), 256: 632-638.
25. James, P., Vorherr, T., and Carafoli, E. 1995. Calmodulin-binding domains: just two faced or multi faceted? Trends Biochem. Sci. 20: 38-42.
26. Juminaga, D., Albaugh, S.A., and Steiner, R.F. 1994. The interaction of calmodulin with regulatory peptides of phosphorylase kinase. J. Biol. Chem. 269: 1660-1667.
27. Kraulis, P.J. 1991. MOLSCRIPT: a program to produce detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
28. Krueger, J., Olah, G.A., Rokop, S.E., Zhi, G., Stull, J.T., and Trewhella, J. 1997. Structures of calmodulin and a functional myosin light chain kinase in the activated complex: a neutron scattering study. Biochemistry, 36: 6017-6023.
29. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C.B., and Bax, A. 1995. Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2: 768-776.
30. Lipari, G., and Szabo, A. 1982. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. J. Am. Chem. Soc. 104: 4546-4570.
31. 2+ on the secondary and tertiary structure of bovine testis calmodulin. Biochem. J. 238: 485-490.
32. Meador, W.E., Means, A.R., and Quiocho, F.A. 1992. Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulin-peptide complex. Science (Washington, D.C.), 257: 1251-1255.
33. Meador, W.E., Means, A.R., and Quiocho, F.A. 1993. Modulation of calmodulin plasticity in molecular recognition on the basis of X-ray structures. Science (Washington, D.C.), 262: 1718-1721.
34. Meador, W.E., George, S.E., Means, A.R., and Quiocho, F.A. 1995. X-ray analysis reveals conformational adaptation of the linker in functional calmodulin mutants. Nat. Struct. Biol. 2: 943-945.
35. Means, A.R., VanBerkum, M.F.A., Bagchi, I., Lu, K.P., and Rasmussen, C.D. 1991. Regulatory functions of calmodulin. Pharmacol. Ther. 50: 255-270.
36. Minakami, R., Jinnai, N., and Sugiyama, H. 1997. Phosphorylation and calmodulin binding of the metabotropic glutamate receptor subtypes (mGluR5) are antagonistic in vitro. J. Biol. Chem. 272: 20 291-20 298.
37. O'Neil, K.T., and DeGrado, W.F. 1990. How calmodulin binds its targets: sequence independent recognition of amphiphilic α-helices. Trends Biochem. Sci. 15: 59-64.
38. Osawa, M., Swindells, M.B., Tanikawa, J., Tanaka, T., Mase, T., Furuya, T., and Ikura, T. 1998. Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. J. Mol. Biol. 276: 165-176.
39. Persechini, A., Gansz, K., and Paresi, R. 1996. A role in enzyme activation of the N-terminal leader sequence in calmodulin. J. Biol. Chem. 271: 19 279-19 282.
40. Quiocho, F.A., Johnson, K.A., Meador, W.E., and Beckingham, K. 1997. X-ray structures of calmodulin bound to peptides. In Proceedings of the Tenth International Symposium on Calcium-binding Proteins and Calcium Function in Health and Disease, Lund, Sweden. p. 27. (Abstr.)
41. Rhoads, A.R., and Friedberg, F. 1997. Sequence motifs for calmodulin recognition. FASEB J. 11: 331-340.
42. 2+. J. Biol. Chem. 271: 22 679-22 686.
43. Siivari, K., Zhang, M., Palmer, A.G., III, and Vogel, H.J. 1995. NMR studies of the methionine methyl groups in calmodulin. FEBS Lett. 366: 104-108.
44. 2+-binding proteins. Nat. Struct. Biol. 1: 239-245.
45. Sonnenburg, W.K., Seger, D., Kwak, K.S., Huang, J., Charbonneau, H., and Beavo, J.A. 1995. Identification of inhibitory and calmodulin-binding domains of the PDE1A1 and PDE1A2 calmodulin-stimulated cyclic nucleotide phophodiesterase. J. Biol. Chem. 270: 30 989-31 000.
46. Strynadka, N.C.J., and James, M.N.G. 1991. Towards an understanding of the effects of calcium on protein structure and function. Curr. Opin. Struct. Biol. 1: 905-914.
47. Strynadka, N.C., Chervey, M., Sielecki, A.R., Li, M.X., Smillie, L.B., and James, M.N. 1997. 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: 238-255.
48. Swindells, M.B., and Ikura, M. 1996. Pre-formation of the semi-open conformation by the apo-calmodulin C-terminal domain and implications for binding IQ-motifs. Nat. Struct. Biol. 3: 501-504.
49. Tabernero, L., Taylor, D.A., Chandross, R., VanBerkum, M.F.A., Means, A.R., Quiocho, F.A., and Sack, J.S. 1997. The structure of a calmodulin mutant with a deletion in the central helix: implication for molecular recognition and protein binding. Structure (London), 5: 613-622.
50. Tanaka, T., Ames, J.B., Harvey, T.S., Stryer, L., and Ikura, M. 1995. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature (London), 376: 444-447.
51. Thulin, E., Andersson, A., Drakenberg, T., Forsen, S., and Vogel, H.J. 1984. Metal ion and drug binding to proteolytic fragments of calmodulin: proteolytic, cadmium-113 and proton nuclear magnetic resonance studies. Biochemistry, 23: 1860-1870.
52. 15N NMR relaxation measurements. Eur. J. Biochem. 230: 1014-1024.
53. Trewhella, J., Blumenthal, D.K., Rokop, S.E., and Seeger, P.A. 1990. Small-angle scattering studies show distinct conformations of calmodulin in its complexes with two peptides based on the regulatory domain of the catalytic subunit of phosphorylase kinase. Biochemistry, 29: 9316-9324.
54. Tsalkova, T.N., and Privalov, P. 1985. Thermodynamic study of domain organization in troponin C and calmodulin. J. Mol. Biol. 181: 533-544.
55. Urbauer, J.L., Short, J.H., Dow, L.K., and Wand, A.J. 1995. Structural analysis of a novel interaction by calmodulin: high-affinity binding of a peptide in the absence of calcium. Biochemistry, 34: 8099-8109.
56. Urbauer, J.L., Ehrhardt, M.R., Bieber, R.J., Flynn, P.F., and Wand, A.J. 1996. High-resolution triple-resonance NMR spectroscopy of a novel calmodulin-peptide complex at kilobar pressures. J. Am. Chem. Soc. 118: 11 329-11 330.
57. VanBerkum, M.F.A., George, S.E., and Means, A.R. 1990. Calmodulin activation of target enzymes. Consequence of deletions in the central helix J. Biol. Chem. 265: 3750-3756.
58. Venema, R.C., Sayegh, H.S., Kent, J.D., and Harrison, D.G. 1996. Identification, characterization, and comparison of the calmodulin-binding domains of the endothelial and inducible nitric oxide synthases. J. Biol. Chem. 271: 6435-6440.
59. Vogel, H.J. 1994. Calmodulin: a versatile calcium mediator protein. Biochem. Cell Biol. 72: 357-376.
60. Vogel, H.J., and Zhang, M. 1995. Protein engineering and NMR studies of calmodulin. Mol. Cell. Biochem. 149-150: 3-15.
61. Wang, K.L., Khan, M.T., and Roufogalis, B.D. 1997a. Identification and characterization of a calmodulin-binding domain in Ral-A, a Ras-related GTP-binding protein purified from human erythrocyte membrane. J. Biol. Chem. 272: 16 002-16 009.
62. Wang, E., Zhung, S., Kordowska, J., Grabarek, Z., and Wang, C.-L.A. 1997b. Calmodulin binds to caldesmon in an antiparallel manner. Biochemistry, 36: 15 026-15 034.
63. Yuan, T., Mietzner, T.A., Montelaro, R.C., and Vogel, H.J. 1995. Characterization of the calmodulin binding domain of SIV transmembrane glycoprotein by NMR and CD spectroscopy. Biochemistry, 34: 10 690-10 696.
64. Yuan, T., Weljie, A.M., and Vogel, H.J. 1998. Tryptophan fluorescence quenching by methionine and selenomethionine residues of calmodulin: orientation of peptide and protein binding. Biochemistry. 37: 3187-3195.
65. Zhang, M., and Vogel, H.J. 1994a. The calmodulin-binding domain of caldesmon binds to calmodulin in an α-helical conformation. Biochemistry, 33: 1163-1171.
66. Zhang, M., and Vogel, H.J. 1994b. Two-dimensional NMR studies of selenomethionyl calmodulin. J. Mol. Biol. 239: 545-554.
67. Zhang, M., Yuan, T., and Vogel, H.J. 1993. A peptide analog of the calmodulin-binding of myosin light chain kinase adopts an α-helical structure in aqueous trifluoroethanol. Protein Sci. 2: 1931-1937.
68. Zhang, M., Fabian, H., Mantsch, H.H., and Vogel, H.J. 1994a. Isotope-edited Fourier transform infrared spectroscopy studies of calmodulin's interaction with its target peptides. Biochemistry, 33: 10 883-10 888.
69. Zhang, M., Vogel, H.J., and Zwiers, H. 1994b. Nuclear magnetic resonance studies of the structure of B50/neuromodulin and its interaction with calmodulin. Biochem. Cell Biol. 72: 109-116.
70. Zhang, M., Li, M., Wang, J.H., and Vogel, H.J. 1994c. The effect of Met→Leu mutations on calmodulin's ability to activate cyclic nucleotide phosphodiesterase. J. Biol. Chem. 269: 15 546-15 552.
71. Zhang, M., Tanaka, T., and Ikura, M. 1995a. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2: 758-767.
72. Zhang, M., Yuan, T., Aramini, J.M., and Vogel, H.J. 1995b. Interaction of calmodulin with its binding domain of rat cerebellar nitric oxide synthase: a multinuclear NMR study. J. Biol. Chem. 270: 20 901-20 907.
73. Zhou, N., Yuan, T., Mak, A.S., and Vogel, H.J. 1997. NMR studies of caldesmon-calmodulin interactions. Biochemistry, 36: 2817-2825.
74. Zhu, T., and Ikebe, M.A. 1994. A novel myosin I from bovine adrenal gland. FEBS Lett. 339: 31-36.