11 Calmodulin
Annual Plant Reviews book series, Volume 7: Protein-Protein Interactions in Plant Biology
Teerapong Buaboocha,
Raymond E. Zielinski,
Teerapong Buaboocha
Department of Biochemistry, Chulalongkorn University, Bangkok, Thailand
Search for more papers by this authorRaymond E. Zielinski
Department of Plant Biology and the Physiological and Molecular Plant Biology Program, University of Illinois, Urbana, IL, 61801 USA
Search for more papers by this authorTeerapong Buaboocha,
Raymond E. Zielinski,
Teerapong Buaboocha
Department of Biochemistry, Chulalongkorn University, Bangkok, Thailand
Search for more papers by this authorRaymond E. Zielinski
Department of Plant Biology and the Physiological and Molecular Plant Biology Program, University of Illinois, Urbana, IL, 61801 USA
Search for more papers by this authorFirst published: 19 April 2018
This article was originally published in 2002 in Protein-Protein Interactions in Plant Biology, Volume 7 (ISBN 9781841272290) of the Annual Plant Reviews book series, this volume edited by Michael T. McManus and William A. Laing and Andrew C. Allan. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
The sections in this article are
- Introduction
- Calmodulin Sequences and Structures
- Structures of Ca2+ /CaM–Target Peptide Complexes
- Prospects for Monitoring Calmodulin Function in vivo
References
- Arazi, T., Baum, G., Snedden, W.A., Shelp, B.J. and Fromm, H. (1995) Molecular and biochemical analysis of calmodulin interactions with the calmodulin-binding domain of plant glutamate decarboxylase. Plant Physiol., 108, 551-561.
- 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.
- Baum, G., Chen, Y., Arazi, T., Takatsuji, H. and Fromm, H. (1993) A plant glutamate decarboxylase containing a calmodulin-binding domain: cloning, sequence and functional analysis. J. Biol. Chem., 268, 19,610-19,617.
- Baum, G., Lev-Yadun, S., Fridmann, Y. et al. (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J., 15, 2988-2996.
- 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 54 K subunit of signal recognition particle. Nature, 340, 482-486.
- Berridge, M.J., Lipp, P. and Bootman, M.D. (2000) The versatility and universality of calcium signaling. Nature Rev., 1, 11-21.
- Brokx, R.D., Lopez, M.M., Vogel, H.J. and Makhatadze, G.L. (2001) Energetics of target peptide binding by calmodulin reveals different modes of binding. J. Biol. Chem., 276, 14,083-14,091.
- Brown, S.E., Martin, S.R. and Bayley, P.M. (1997) Kinetic control of the dissociation pathway of calmodulin-peptide complexes. J. Biol. Chem., 272, 3389-3397.
- Cates, M.S., Berry, M.B., Ho, E.L., Li, Q., Potter, J.D. and Phillips Jr, G.N. (1999) Metal-ion affinity and specificity in EF-hand proteins: coordination geometry and domain plasticity in parvalbumin. Structure, 7, 1269-1278.
- Chattopadhyaya, R., Meador, W.E., Means, A.R. and Quiocho, F.A. (1992) Calmodulin structure refined at 1.7Å resolution. J. Mol. Biol., 228, 1177-1192.
- Chin, D. and Means, A.R. (1996) Methionine to glutamine substitutions in the C-terminal domain of calmodulin impair the activation of three protein kinases. J. Biol. Chem., 271, 30,465-30,471.
- Chin, D., Sloan, D.J., Quiocho, F.A. and Means, A.R. (1997) Functional consequences of truncating amino acid side chains located at a calmodulin-peptide interface. J. Biol. Chem., 272, 5510-5513.
- Cho, M.J., Vaghy, P.L., Kondo, R. et al. (1998) Reciprocal regulation of mammalian nitric oxide synthase and calcineurin by plant calmodulin isoforms. Biochemistry, 37, 15,593-15,597.
- Craig, T.A., Watterson, D.M., Prendergast, F.G., Haiech, J. and Roberts, D.M. (1987) Site-specific mutagenesis of the α-helices of calmodulin. Effects of altering a charge cluster in the helix that links the two halves of calmodulin. J. Biol. Chem., 262, 3278-3284.
- Crivici, A. and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin. Ann. Rev. Biophys. Biomol. Struct., 24, 85-116.
- Elshorst, B., Hennig, M., Forsterling, H. et al. (1999) NMR solution structure of a complex of calmodulin with a binding peptide of the Ca2+ pump. Biochemistry, 38, 12,320-12,332.
- Erickson-Viitanen, S. and DeGrado, W.F. (1987) Recognition and characterization of calmodulin-binding sequences in peptides and proteins. Methods Enzymol., 139, 455-478.
- Falke, J.J., Drake, S.K., Hazard, A.L. and Peersen, O.B. (1994) Molecular tuning of ion binding to calcium signaling proteins. Q. Rev. Biophys., 27, 219-290.
- Findlay, W.A., Martin, S.R., Beckingham, K. and Bayley, P.M. (1995) Recovery of native structure by calcium binding site mutants of calmodulin upon binding of sk-MLCK target peptides. Biochemistry, 34, 2087-2094.
- Finn, B.E., Evenas, J., Drakenberg, T., Waltho, J.P., Thulin, E. and Forsen, S. (1995) Calcium-induced structural changes and domain autonomy in calmodulin. Nature Struct. Biol., 2, 777-783.
- Gawienowski, M.C., Szymanski, D., Perera, I.Y. and Zielinski, R.E. (1993) Calmodulin isoforms in Arabidopsis encoded by multiple divergent mRNAs. Plant Mol. Biol., 22, 215-225.
- Geiser, J.R., Tuinen, D., Brockerhoff, S.E., Neff, M.M. and Davis, T.N. (1991) Can calmodulin function without binding calcium? Cell, 65, 949-959.
- Gellman, S.H. (1991) On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry, 30, 6633-6636.
- George, S.E., VanBerkum, M.F.A., Ono, T. et al. (1990) Chimeric calmodulin-cardiac troponin C proteins diffentially activate calmodulin target enzymes. J. Biol. Chem., 265, 9228-9235.
- George, S.E., Su, Z., Fan, D. and Means, A.R. (1993) Calmodulin-cardiac troponin C chimeras. J. Biol. Chem., 268, 25,213-25,220.
- George, S.E., Su, Z., Fan, D., Wang, S. and Johnson, J.D. (1996) The fourth EF-hand of calmodulin and its helix-loop-helix components: impact on calcium binding and enzyme activation. Biochemistry, 35, 8307-8313.
- Gilroy, S. and Trewavas, A. (2001) Signal processing and transduction in plant cells: the end of the beginning? Nature Rev. Mol. Cell Biol., 2, 307-314.
- Goldberg, J., Nairn, A.C. and Kuriyan, J. (1996) Structural basis for the autoinhibition of calcium/calmodulin-dependent protein kinase I. Cell, 84, 875-887.
- Haiech, J., Kilhoffer, M.C., Lukas, T.J., Craig, T.A., Roberts, D.M. and Watterson, D.M. (1991) Restoration of the calcium binding activity of mutant calmodulins toward normal by the presence of a calmodulin binding structure. J. Biol. Chem., 266, 3427-3431.
- Harmon, A.C., Gribskov, M. and Harper, J.F. (2000) CDPKs—a kinase for every Ca2+ signal? Trends Plant Sci., 5, 154-159.
- Heo, W.D., Lee, S.H., Kim, M.C. et al. (1999) Involvement of specific calmodulin isoforms in salicyclic acid-independent activation of plant disease resistance responses. Proc. Natl. Acad. Sci. USA., 96, 766-771.
- Ikura, M. (1996) Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci., 21, 14-17.
- Ikura, M., Spera, S., Barbato, G., Kay, L.E., Krinks, M. and Bax, A. (1991) Secondary structure and side-chain 1H and 13C resonance assignments of calmodulin in solution by heteronuclear multidimentional NMR spectroscopy. Biochemistry, 30, 9216-9228.
- 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, 256, 632-638.
- Janin, J., Wodak, S., Levitt, M. and Maigret, B. (1978) Conformation of amino acid side-chains in proteins. J. Mol. Biol., 125, 357-386.
- Johnson, J.D. and Potter, J.D. (1981) Detection of two classes of Ca2+-binding sites in troponin C with circular dichroism and tyrosine fluorescence. J. Biol. Chem., 253, 3675-3677.
- Johnson, J.D., Snyder, C., Walsh, M. and Flynn, M. (1996) Effects of myosin light chain kinase and peptides on Ca2+ binding sites of calmodulin. J. Biol. Chem., 271, 761-767.
- Jurado, L.A., Chockalingam, P.S. and Jarrett, H.W. (1999) Apocalmodulin. Physiol. Rev., 79, 661-682.
- Kasturi, R., Vasulka, C. and Johnson, J.D. (1993) Ca2+, caldesmon, and myosin light chain kinase exchange with calmodulin. J. Biol. Chem., 268, 7958-7964.
- Kawasaki, H. and Kretsinger, R.H. (1994) Calcium-binding proteins 1: EF-hands. Protein Profile, 1, 343-517.
- Köhler, C. and Neuhaus, G. (2000) Characterisation of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana . FEBS Lett., 471, 133-136.
- Kretsinger, R.H. and Nockholds, C.E. (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem., 248, 3313-3326.
- 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.
- Lee, S.H., Johnson, J.D., Walsh, M.P. et al. (2000) Differential regulation of Ca2+/calmodulin-dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem. J., 350, 299-306.
- Lee, S.H., Kim, K.C., Lee, M.S. et al. (1995) Identification of a novel divergent calmodulin isoform from soybean which has differential ability to activate calmodulin-dependent enzymes. J. Biol. Chem., 270, 21,806-21,812.
- Lee, S.H., Seo, H.Y., Kim, J.C. et al. (1997) Differential activation of NAD kinase by plant calmodulin isoforms. J. Biol. Chem., 272, 9252-9259.
- Li, C.-J., Heim, R., Lu, Y., Tsien, R.Y. and Chang, D.C. (1999) Dynamic redistribution of calmodulin in HeLa cells during cell division as revealed by a GFP-calmodulin fusion protein technique. J. Cell Sci., 112, 1567-1577.
- Liao, B., Gawienowski, M.C. and Zielinski, R.E. (1996) Differential stimulation of NAD kinase and binding of peptide substrates by wild-type and mutant plant calmodulin isoforms. Arch. Biochem. Biophys., 327, 53-60.
- Ling, V. and Zielinski, R.E. (1993) Isolation of an Arabidopsis cDNA sequence encoding a 22 kDa calcium-binding protein (CaBP-22) related to calmodulin. Plant Mol. Biol., 22, 207-214.
- Ling, V., Perera, I.Y. and Zielinski, R.E. (1991) Primary structures of Arabidopsis calmodulin isoforms deduced from the sequences of cDNA clones. Plant Physiol., 90, 1196-1202.
- Linse, S. and Forsen, S. (1995) Determinants that govern high-affinity calcium binding. Adv. Second Messenger Phosphoprot. Res., 30, 88-151.
- 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, 257, 1251-1255.
- 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, 262, 1718-1721.
- 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.
- Miyawaki, A., Griesbeck, O., Heim, R. and Tsien, R.Y. (1999) Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc. Natl Acad. Sci. USA, 96, 2135-2140.
- Miyawaki, A., Liopis, J., Heim, R., McCaffery, J.M., Adams, J.A., Ikura, M. and Tsien, R.Y. (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature, 388, 882-887.
- Montigiani, S., Neri, G., Neri, P. and Neri, D. (1996) Alanine substitutions in calmodulin-binding peptides result in unexpected affinity enhancement. J. Mol. Biol., 258, 6-13.
- Moser, M.J., Flory, M.R. and Davis, T.N. (1997) Calmodulin localizes to the spindle pole body of Schizosaccharomyces pombe and performs an essential function in chromosome segregation. J. Cell Sci., 110, 1805-1812.
- Ohki, S., Ikura, M. and Zhang, M. (1997) Identification of Mg2+-binding sites and the role of Mg2+ on target recognition by calmodulin. Biochemistry, 36, 4309-4316.
- Ohya, Y. and Botstein, D. (1994a) Diverse essential functions revealed by complementing yeast calmodulin mutants. Science, 263, 963-966.
- Ohya, Y. and Botstein, D. (1994b) Structure-based systematic isolation of conditional-lethal mutations in the single yeast calmodulin gene. Genetics, 138, 1041-1054.
- Okano, H., Cyert, M.S. and Ohya, Y. (1998) Importance of phenylalanine residues of yeast calmodulin for target binding and activation. J. Biol. Chem., 273, 26,375-26,382.
- Olwin, B.B. and Storm, D.R. (1985) Calcium binding to complexes of calmodulin and calmodulin binding proteins. Biochemistry, 24, 8081-8086.
- Olwin, B.B., Edelman, A.M., Krebs, E.G. and Storm, D.R. (1984) Quantitation of energy coupling between Ca2+, calmodulin, skeletal muscle myosin light chain kinase, and kinase substrates. J. Biol. Chem., 259, 10,949-10,955.
- 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.
- Osawa, M., Tokumitsu, H., Swindells, M.B. et al. (1999) A novel target recognition revealed by calmodulin in complex with Ca2+-calmodulin-dependent kinase kinase. Nat. Struct. Biol., 6, 819-824.
- Ozawa, T., Sasaki, K. and Umezawa, Y. (1999) Metal ion selectivity for formation of the calmodulin-metal-target peptide ternary complex studied by surface plasmon resonance spectroscopy. Biochim. Biophys. Acta, 1434, 211-230.
- Peersen, O.B., Madsen, T.S. and Falke, J.J. (1997) Intermolecular tuning of calmodulin by target peptides and proteins: differential effects on Ca2+ binding and implications for kinase activation. Prot. Sci., 6, 794-807.
- Perera, I.Y. and Zielinski, R.E. (1992) Structure and expression of the Arabidopsis CaM-3 calmodulin gene. Plant Mol. Biol., 19, 649-664.
- Persechini, A. and Cronk, B. (1999) The relationship between the free concentrations of Ca2+ and Ca2+-calmodulin in intact cells. J. Biol. Chem., 274, 6827-6830.
- Persechini, A. and Kretsinger, R.H. (1988) The central helix of calmodulin functions as a flexible tether. J. Biol. Chem., 263, 12,175-12,178.
- Persechini, A., Blumenthal, D.K., Jarrett, H.W., Klee, C.B., Hardy, D.O. and Kretsinger, R.H. (1989) The effects of deletions in the central helix of calmodulin on enzyme activation and peptide binding. J. Biol. Chem., 264, 8052-8058.
- Persechini, A., Kretsinger, R.H. and Davis, T.N. (1991) Calmodulins with deletions in the central helix functionally replace the native protein in yeast cells. Proc. Natl Acad. Sci. USA, 88, 449-452.
- Persechini, A., White, H.D. and Gansz, K.J. (1996) Different mechanisms for Ca2+ dissociation from complexes of calmodulin with nitric oxide synthase or myosin light chain kinase. J. Biol. Chem., 271, 62-67.
- Privalov, P.L. and Gill, S.J. (1988) Stability of protein structure and hydrophobic interactions. Adv. Protein Chem., 39, 191-234.
- Rasi-Caldogno, F., Carnelli, A. and De Michelis, M.I. (1993) Controlled proteolysis activates the plasma membrane Ca2+ pump of higher plants. Plant Physiol., 103, 385-390.
- Reddy, V.S., Safadi, F., Zielinski, R.E. and Reddy, A.S.N. (1999) Interaction of a kinesin-like protein with calmodulin isoforms from Arabidopsis . J. Biol. Chem., 274, 31,727-31,733.
- Rhoads, A.R. and Friedberg, F. (1997) Sequence motifs for calmodulin recognition. FASEB J., 11, 331-340.
- Rodriguez-Concepcion, M., Yalovsky, S., Zik, M., Fromm, H. and Gruissem, W. (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J., 18, 1996-2007.
- Romoser, V.A., Hinkle, P.M. and Persechini, A. (1997) Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence: A new class of fluorescent indicators. J. Biol. Chem., 272, 13270-13274.
- Sekiya-Kawasaki, M., Botstein, D. and Ohya, Y. (1998) Identification of functional connections between calmodulin and the yeast actin cytoskeleton. Genetics, 150, 43-58.
- Snedden, W.A. and Fromm, H. (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci., 3, 299-304.
- Snedden, W.A., Koutsia, N., Baum, G. and Fromm, H. (1996) Activation of a recombinant petunia glutamate decarboxylase by calcium/calmodulin or by a monoclonal antibody which recognizes that calmodulin binding domain. J. Biol. Chem., 271, 4148-4153.
- Su, Z., Fan, D. and George, S.E. (1994) Role of domain 3 of calmodulin in activation of calmodulin-stimulated phosphodiesterase and smooth muscle myosin light chain kinase. J. Biol. Chem., 269, 16,761-16,765.
- Swindells, M.B. and Ikura, M. (1996) Pre-formation of the semi-open conformation by the apocalmodulin C-terminal domain and implications binding IQ-motifs. Nature Struct. Biol., 3, 501-504.
- Sze, H., Liang, F., Hwang, I., Curran, A.C. and Harper, J.F. (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu. Rev. Plant Physiol. Plant Mol. Biol., 51, 433-462.
- Szymanski, D.B., Liao, B. and Zielinski, R.E. (1996) Calmodulin isoforms differentially enhance the binding of cauliflower nuclear proteins and recombinant TGA3 to a region derived from the Arabidopsis CaM3 promoter. Plant Cell, 8, 1069-1077.
- Takezawa, D., Liu, Z.H., An, G. and Poovaiah, B.W. (1995) Calmodulin gene family in potato: developmental and touch-induced expression of the mRNA encoding a novel isoform. Plant Mol. Biol., 27, 693-703.
- Trewavas, A.J. and Malho, R. (1998) Ca2+ signaling in plant cells: the big network! Curr. Opin. Plant Biol., 1, 428-433.
- Tsien, R.Y. (1998) The green fluorescent protein. Annu. Rev. Biochem., 67, 509-544.
- Van Berkum, M.F.A. and Means, A.R. (1991) Three amino acid substitutions in domain I of calmodulin prevent the activation of chicken smooth muscle myosin light chain kinase. J. Biol. Chem., 266, 21,488-21,495.
- Wintrode, P.L. and Privalov, P.L. (1997) Energetics of target peptide recognition by calmodulin: a calorimetric study. J. Mol. Biol., 266, 1050-1062.
- Yuan, T. and Vogel, H. (1998) Calcium-calmodulin-induced dimerization of the carboxyl-terminal domain from petunia glutamate decarboxylase. J. Biol. Chem., 273, 30,328-30,335.
- Yuan, T., Ouyang, H. and Vogel, H. (1999a) Surface exposure of the methionine side chains of calmodulin in solution. J. Biol. Chem., 274, 8411-8420.
- Yuan, T., Walsh, M.P., Sutherland, C., Fabian, H. and Vogel, H.J. (1999b) Calcium-dependent and -independent interactions of the calmodulin-binding domain of cyclic nucleotide phosphodiesterase with calmodulin. Biochemistry, 38, 1446-1455.
- Zhang, M. and Vogel, H.J. (1994) Two-dimensional NMR studies of selenomethionyl calmodulin. J. Mol. Biol., 239, 545-554.
- Zhang, M., Li, M., Wang, J.H. and Vogel, H.J. (1994) The effect of Met → Leu mutations on calmodulin's ability to activate cyclic nucleotide phosphodiesterase. J. Biol. Chem., 269, 15,546-15,552.
- 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.
- Zhang, G., Liu, Y., Ruoho, A.E. and Hurley, J.H. (1997) Structure of the adenylyl cyclase catalytic core. Nature, 386, 247-253.
- Zielinski, R.E. (1998) Calmodulin and calmodulin-binding proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 49, 697-725.
- Zielinski, R.E. (2001) Characterization of three new members of the Arabidopsis thaliana calmodulin gene family: conserved and diverged members of the gene family functionally complement a yeast calmodulin null. Planta (in press). Available electronically (DOI 10.1007/S004250/00636).
- Zik, M., Arazi, T., Snedden, W.A. and Fromm, H. (1998) Two isoforms of glutamate decarboxylase in Arabidopsis are regulated by calcium/calmodulin and differ in organ distribution. Plant Mol. Biol., 37, 967-975.
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