Novel aspects of calmodulin target recognition and activation

European Journal of Biochemistry

Volumn 270, Issue 3, 2003, Pages 404-414

  Vetter, Stefan W ^a,b   Leclerc, Estelle ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Department of Molecular Biology ^*  (United States)

Author keywords

Ca2+ signaling; Calmodulin; CaM binding domains; CaM target activation; Cellular signaling

Indexed keywords

ANTHRAX TOXIN; CALCIUM BINDING PROTEIN; CALCIUM CHANNEL; CALCIUM ION; CALMODULIN; EXOTOXIN; MYOSIN LIGHT CHAIN KINASE; POTASSIUM CHANNEL; PROTEIN KINASE (CALCIUM,CALMODULIN);

BACILLUS SUBTILIS; CALCIUM BINDING; CALCIUM TRANSPORT; CELL MEMBRANE; COMPLEX FORMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; REVIEW; TOXIN ANALYSIS; X RAY CRYSTALLOGRAPHY;

ANIMALS; BINDING SITES; CALCIUM; CALMODULIN; HUMANS; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

ANTHRAX; BACILLUS SUBTILIS; INSERTION SEQUENCES;

EID: 0037318056     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03414.x     Document Type: Review

References (116)

1. Evenas, J., Malmendal, A. & Forsen, S. (1998) Calcium. Curr. Opin. Chem. Biol. 2, 293-302.
2. Carafoli, E. & Klee, C. (1999) Calcium as a Cellular Regulator. Oxford University Press, Oxford, UK.
3. Brini, M. & Carafoli, E. (2000) Calcium signaling: a historical account, recent developments and future perspectives. Cell. Mol. Life Sci. 57, 354-370.
4. Carafoli, E. (2002) Calcium signaling: a tale for all seasons. Proc. Natl Acad. Sci. USA 99, 1115-1122.
5. Endo, M., Tanaka, M. & Ogawa, Y. (1970) Calcium induced calcium release of calcium from the carcoplasmatic reticulum of skinned skeletal fibres. Nature 228, 34-36.
6. Berridge, M.J. (1993) Inositol and calcium signalling. Nature 361, 315-325.
7. Galione, A. (1994) Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and calcium signalling. Mol. Cell. Endocrinol. 98, 125-131.
8. Pozzan, T., Rizzuto, R., Volpe, P. & Meldolesi, J. (1994) Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev. 74, 595-636.
9. 2+ network. J. Cell. Biol. 136, 833-844.
10. Horne, J.H. & Meyer, T. (1997) Elementary calcium-release units induced by inositol trisphosphate. Science 276, 1690-1693.
11. Carafoli, E., Santella, L., Branca, D. & Brini, M. (2001) Generation, control, and processing of cellular calcium signals. Crit. Rev. Biochem. Mol. Biol. 36, 107-260.
12. Meyer, T., Wensel, T. & Stryer, L. (1990) Kinetics of calcium channel opening by inositol 1,4,5-trisphosphate. Biochemistry 29, 32-37.
13. Finch, E.A., Turner, T.J. & Goldin, S.M. (1991) Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252, 443-446.
14. 3- and calcium-gated channels from endoplasmatic reticulum of cerebellum. Nature 351, 751-754.
15. 2+ safeguards against spontanous activity. Curr. Biol. 7, 510-518.
16. 3) receptor. J. Membr. Biol. 145, 205-216.
17. Rebecchi, M.J. & Pentyala, S.N. (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol. Rev. 80, 1291-1335.
18. 2+. Nature 316, 541-542.
19. Woods, N.M., Cuthbertson, K.S.R. & Cobbold, P.H. (1986) Repetitive transient rises in cytoplasmatic free calcium in hormone-stimulated hepatocytes. Nature 319, 600-602.
20. Berridge, M.J. (1990) Calcium oscillations. J. Biol. Chem. 265, 9583-9586.
21. Meyer, T. & Stryer, L. (1991) Calcium spiking. Ann. Rev. Biophys. Chem. 20, 153-174.
22. 2+ oscillations. Cell Calcium 22, 321-331.
23. Berridge, M., Bootman, M.D. & Lipp, P. (1998) Calcium - a life and death signal. Nature 395, 645-648.
24. Schuster, S., Marhl, M. & Hofer, T. (2002) Modelling of simple and complex calcium oscillations. Eur. J. Biochem. 269, 1333-1355.
25. 3-dependent calcium-induced calcium release mediates bidirectional calcium waves in neurons: functional implications for synaptic plasticity. Biochim. Biophys. Acta 1600, 12-18.
26. 2+/calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61, 559-601.
27. 2+ oscillations. Science 279, 227-230.
28. Schulman, H. & Braun, A. (1999) Calcium/calmodulin dependent kinases. In Calcium as a Cellular Regulator (Carafoli, E. & Klee, C., eds), pp. 311-343. Oxford Univerisity Press, Oxford, UK.
29. 2+ oscillations. EMBO J. 21, 3590-3597.
30. Nakayama, S. & Kretsinger, R.H. (1994) Evolution of the EF-hand family of proteins. Annu. Rev. Biophys. Biolmol. Struct. 23, 4673-4507.
31. Ikura, M. (1996) Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21, 14-17.
32. 2+-binding. Biometals 11, 297-318.
33. Lewit-Bentley, A. & Rety, S. (2000) EF-hand calcium-binding proteins. Curr. Opin. Struct. Biol. 10, 637-643.
34. Kretsinger, R.H. (1996) EF-hands reach out. Nat. Struct. Biol. 3, 12-15.
35. Chazin, W.J. (1995) Releasing the calcium trigger. Nat. Struct. Biol. 2, 707-710.
36. Dibois, T., Oudinet, J.P., Mira, J.P. & Russo-Marie, F. (1996) Annexins and protein kinases C. Biochim. Biophys. Acta 1313, 290-294.
37. Nelsestuen, G.L. & Gaul Ostrowski, B. (1999) Membrane association with multiple calcium ions: vitamin-K-dependent proteins, annexins and pentaxins. Curr. Opin. Struct. Biol. 9, 433-437.
38. 2+-binding domain. J. Biol. Chem. 273, 15879-15882.
39. Nalepski, E.A. & Falke, J.J. (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 5, 2375-2390.
40. Essen, L.O., Perisic, O., Cheung, R., Katan, M. & Williams, R.L. (1996) Crystal structure of a mammalian phosphoinositide-specific phospholipase Cδ. Nature 380, 595-602.
41. 2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273, 248-251.
42. Trahey, M., Wong, G., Halenbeck, R., Rubinfeld, B., Martin, G.A., Ladner, M., Long, C.M., Crosier, W.J., Watt, K., Koths, K. & McCormick, F. (1988) Molecular cloning of two types of GAP complementary DNA from human placenta. Science 242, 1697-1700.
43. Nishizuka, Y. (1988) The molecular heterogeneity of protein kinase C and its implication for cellular regulation. Nature 334, 661-665.
44. 2+-dependent translocation domain with homology tp PKC and GAP. Cell 65, 1043-1051.
45. Rhee, S.G., Suh, P.-G., Ryu, S.-H. & Lee, S.Y. (1989) Studies of inositol phospholipid-specific phospholipase C. Science 244, 546-550.
46. Hiles, I.D, Otsu, M., Volinia, S., Fry, M.J., Gout, I., Dhand, R., Panayotou, G., Ruiz-Larrea, F., Thompson, A., Totty, N.F., Hsuan, J.J., Courtneidge, S.A., Parker, P.J. & Waterfield, M.D. (1992) Phosphatidylinositol 3-kinase: structure and expression of the 110kD catalytic subunit. Cell 70, 419-429.
47. Coussens, L., Parker, P.J., Rhee, L., Yang-Feng, T.L., Chen, E., Waterfield, M.D., Francke, U. & Ulrich, A. (1986) Multiple, distinct forms of bovine and human protein kinase C suggest diversity in celular signaling pathways. Science 233, 859-866.
48. Knopf, J.L., Lee, M.H., Sultzman, L.A., Kriz, R.W., Loomis, C.R., Hewick, R.M. & Bell, R.M. (1986) Cloning and expression of multiple protein kinase C cDNAs. Cell 46, 491-502.
49. Perin, M.S., Fried, V.A., Mignery, G.A., Jahn, R. & Sudhof, T.C. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345, 260-263.
50. Perin, M.S., Brose, N., Jahn, R. & Sudhof, T.C. (1991) Domain structure of synaptotagmin (p65). J. Biol. Chem. 266, 623-629.
51. Brose, N., Petrenko, A.G., Sudhof, T.C. & Jahn, R. (1992) Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256, 1021-1025.
52. 2+ sensor for transmitter release at a central synase. Cell 79, 717-727.
53. Cohen, P. & Klee, C.B. (1988) Calmodulin. Elsevier, Amsterdam, the Netherlands.
54. Eldik, L.V. & Watterson, D.M. (1998) Calmodulin and signal transduction (Van Eldrick, L.J. & Watterson, D.M., eds). Academic Press, New York, USA.
55. Babu, Y.S., Sack, J.S., Greenhough, T.J., Bugg, C.E., Means, A.R. & Cook, W.J. (1985) Three-dimensional structure of calmodulin. Nature 315, 37-40.
56. Babu, Y.S., Bugg, C.E. & Cook, W.J. (1988) Structure of calmodulin refined at 2.2 Å resolution. J. Mol. Biol. 204, 191-204.
57. Reference withdrawn.
58. 2+ binding to Calmodulin. Methods Enzymol. 102, 135-143.
59. 2+, pH and temperature. J. Biochem. 95, 19-28.
60. Haiech, J., Klee, C.B. & Demaille, J.G. (1981) Effects of cations on affinity of calmodulin for calcium: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes. Biochemistry 20, 3890-3897.
61. 2+ binding and implications for kinase activation. Protein Sci. 6, 794-807.
62. Brown, S.E., Martin, S.R. & Bayley, P.M. (1997) Kinetic control of the dissociation pathway of calmodulin-peptide complexes. J. Biol. Chem. 272, 3389-3397.
63. Mirzoeva, S., Weigand, S., Lukas, T.J., Shuvalova, L., Anderson, W.F. & Watterson, D.M. (1999) Analysis of the functional coupling between calmodulin's calcium binding and peptide recognition properties. Biochemistry 38, 3936-3947.
64. Small, E.W. & Anderson, S.R. (1988) Fluorescence anisotropy decay demonstrates calcium-dependent shape changes in photocross-linked calmodulin. Biochemistry 27, 419-428.
65. Chapman, E.R., Alexander, K., Vorherr, T., Carafoli, E. & Storm, D.R. (1992) Fluorescence energy transfer analysis of calmodulin-peptide complexes. Biochemistry 31, 12819-12825.
66. Seaton, B.A., Head, J.F. & Richards, F.M. (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.
67. Kataoka, M., Head, J.F., Vorherr, T., Krebs, J. & Carafoli, E. (1991) Small-angle x-ray scattering study of calmodulin bound to two peptides corresponding to parts of the calmodulin-binding domain of the plasma membrane Ca-pump. Biochemistry 30, 6247-6251.
68. Meador, W.E., George, S.E., Means, A.R. & Quicho, F.A. (1995) X-ray analysis reveals conformational adaptation of the linker in functional calmodulin mutants. Nat. Struct. Biol. 2, 943-945.
69. Trewhella, J., Blumenthal, D.K., Rokop, S.E. & 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.
70. Putkey, J.A., Ono, T., VanBerkum, M.F.A. & Means, A.R. (1988) Functional significance of the central helix in calmodulin. J. Biol. Chem. 262, 11242-11249.
71. Persechini, A. & Kretsinger, R.H. (1988) The central helix of calmodulin functions as a flexible tether. J. Biol. Chem. 263, 12175-12178.
72. Persechini, A., Blumenthal, D.K., Jarrett, H.W., Klee, C.B., Hardy, D.O. & Kretsinger, R.H. (1989) The effects of deletions in the central helix of calmodulin on enzyme activation and peptide bindng. J. Biol. Chem. 264, 8052-8058.
73. Persechini, A., Kretsinger, R.H. & Davis, T.N. (1991) Calmodulin with deletions in the central helix functionally replace the native protein in yeast cells. Proc. Natl Acad. Sci. USA 88, 449-452.
74. Tabernero, L., Taylor, D.A., Chandross, R.J., VanBerkum, M.F., Means, A.R., Quiocho, F.A. & Sacks, J.S. (1997) The structure of a calmodulin mutant with a deletion in the central helix: implications for molecular recognition and protein binding. Structure 5, 613-622.
75. 15 relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 31, 5269-5278.
76. Wall, M.E., Clarage, J.B. & Phillips, G.N. (1997) Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering. Structure 5, 1599-1612.
77. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C.B. & Bax, A. (1995) Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2, 768-776.
78. Finn, B.E., Evenas, J., Drakenberg, T., Waltho, J.P., Thulin, E. & Forsen, S. (1995) Calcium-induced structural changes and domain autonomy in calmodulin. Nat. Struct. Biol. 2, 777-783.
79. Zhang, M., Tanaka, T. & Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2, 758-767.
80. 2+-calmodulin reveals flexible hand-like properties of its domains. Nat. Struct. Biol. 8, 990-997.
81. 2+calmodulin. Nat. Struct. Biol. 1, 795-801.
82. Malencik, D.A. & Anderson, S.R. (1993) Binding of hormones and neuropeptides by calmodulin. Biochemistry 22, 1995-2001.
83. Malencik, D.A. & Anderson, S.R. (1982) Binding of simple peptides, hormones and neurotransmitters by calmodulin. Biochemistry 21, 3480-3486.
84. Osawa, M., Swindells, M.B., Tanikawa, J., Tanaka, T., Mase, T., Furuya, T. & Ikura, M. (1998) Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. J. Mol. Biol. 276, 165-176.
85. DeGrado, W.F., Prendergast, F.G., Wolfe, H.R.J. & Cox, J.A. (1985) The design, synthesis, and characterization of tight-binding inhibitors of calmodulin. J. Cell. Biochem. 29, 83-93.
86. Cox, J.A., Comte, M., Fitton, J.E. & DeGrado, W.F. (1985) The interaction of calmodulin with amphiphilic peptides. J. Biol. Chem. 260, 2527-2534.
87. Erickson-Viitanen, S. & DeGrado, W.F. (1987) Recognition and characterization of calmodulin-binding sequences in peptides and proteins. Methods Enzymol. 139, 455-478.
88. DeGrado, W.F. (1988) Design of peptides and proteins. Adv. Protein Chem. 39, 51-125.
89. O'Neil, K.T. & DeGrado, W.F. (1990) How calmodulin binds its targets: sequence independent recognition of amphiphilic alphahelices. Trends Biochem. Sci. 15, 59-64.
90. Rhoads, A.R. & Friedberg, F. (1997) Sequence motifs for calmodulin recognition. FASEB J. 11, 331-340.
91. Heidorn, D.B., Seeger, P.A., Rokop, S.E., Blumenthal, D.K., Means, A.R., Crespi, H. & Trewhella, J. (1989) Change in the structure of calmodulin induced by a peptide based on the calmodulin-binding domain of myosin light chain kinase. Biochemistry 28, 6757-6764.
92. 2+ pump. Biochemistry 35, 8245-8251.
93. Vorherr, T., James, P., Krebs, J., Enyedi, A., McCormick, D.J., Penniston, J.T. & Carafoli, E. (1990) Interaction of calmodulin with the calmodulin binding domain of the plasma membrane calcium pump. Biochemistry 29, 355-365.
94. O'Neil, K.T. & DeGrado, W.F. (1989) The interaction of calmodulin with fluorescent and photoreactive model peptides: evidence for a short interdomain separation. Proteins 6, 284-293.
95. Vorherr, T., Kessler, O., Mark, A. & Carafoli, E. (1992) Construction and molecular dynamics simulation of calmodulin in the extended and in a bent conformation. Eur. J. Biochem. 204, 931-937.
96. Ikura, M., Clore, G.M., Gronenborn, A.M., Zhu, G., Klee, C.B. & Bax, A. (1992) Solution structure of a calmodulin target peptide complex by multidimensional NMR. Science 256, 632-638.
97. Meador, W.E., Means, A.R. & Quiocho, F.A. (1992) Target enzyme recognition by calmodulin: 2.4Å structure of calmodulinpeptide complex. Science 257, 1251-1255.
98. Meador, W.E., Means, A.R. & Quiocho, F.A. (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of X-ray structures. Science 262, 1718-1721.
99. 2+-ATPase of the erythrocyte membrane. A correlation between the structure and the function of the enzyme. J. Biol. Chem. 259, 618-664.
100. Edelman, A.M., Takio, A., Blumenthal, D.K., Hansen, R.S., Walsh, K.A., Titani, K. & Krebs, E.G. (1985) Characterization of the calmodulin-binding and catalytic domains in skeletal muscle myosin light chain kinase. J. Biol. Chem. 260, 1127-11285.
101. Olsen, N.J., Pearson, R.B., Needleman, D.S., Hurwitz, M.Y., Kemp, B.E. & Means, A.R. (1990) Regulatory and structural motifs of chicken myosin light chain kinase. Proc. Natl Acad. Sci. USA 87, 2284-2288.
102. Montgomery, H.J., Romanov, V. & Guillemette, J.G. (2000) Removal of a putative inhibitory element reduces the calcium-dependent calmodulin activation of neuronal nitric-oxide synthase. J. Biol. Chem 275, 5052-5058.
103. Hubbard, M.J. & Klee, C.B. (1989) Functional domain structure of calcineurin A: mapping by limited proteolysis. Biochemistry 28, 1868-1874.
104. 2+ pump. J. Membr. Biol. 120, 1-15.
105. Guerini, D., Krebs, J. & Carafoli, E. (1984) Stimulation of the purified erythrocyte Ca-ATPase by tryptic fragments of calmodulin. J. Biol. Chem. 259, 15172-15177.
106. 2+ pump. Biochemistry 38, 12320-12332.
107. 2+-calmodulin-dependent kinase kinase. Nat. Struct. Biol. 6, 819-824.
108. Soderling, T.R. (1999) The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem. Sci. 24, 232-236.
109. 2+/calmodulin. Nature 410, 1120-1124.
110. 2+-activated potassium channels. J. Neurosci. 19, 8830-8838.
111. Xia, X.-M., Fakler, B., Rivard, A., Wayman, G., Johnson-Pais, T., Keen, J.E., Ishii, T., Hirschberg, B., Bond, C.T., Lutsenko, S., Maylie, J. & Adelman, J.P. (1998) Mechanism of calcium gating in small-conductance calcium-ativated potassium channels. Nature 395, 503-507.
112. Drum, C.L., Yan, S.-Z., Bard, J., Shen, Y.-Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A. & Tang, W.-J. (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415, 396-402.
113. Drum, C.L., Shen, Y., Rice, P.A., Bohm, A. & Tang, W.J. (2001) Crystallization and preliminary X-ray study of the edema factor exotoxin adenylyl cyclase domain from Bacillus anthracis in the presence of its activator, calmodulin. Acta Crystallogr. D 57, 1881-1884.
114. Drum, C.L., Yan, S.Z., Sarac, R., Mabuchi, Y, Beckingham, K., Bohm, A., Grabarek, Z. & Tang, W.J. (2000) An extended conformation of calmodulin induces interaction between the structural domains of adenylyl cyclase from Bacillus anthracis to promote catalysis. J. Biol. Chem. 275, 36334-36340.
115. Leppla, S.H. (1982) Anthrax toxin edema factor, a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl Acad. Sci. USA 79, 3162-3166.
116. Munier, H., Blance, F.J., Precheur, B., Diesis, E., Nieto, J.L., Craescu, C.T. & Barzu, O. (1993) Characterization of a synthetic calmodulin-binding peptide derived from Bacillus anthraeis adenylate cyclase. J. Biol. Chem. 268, 1695-1701.