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Science 10 December 1993:
Vol. 262. no. 5140, pp. 1718 - 1721
DOI: 10.1126/science.8259515
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Articles

Science, Vol 262, Issue 5140, 1718-1721
Copyright © 1993 by American Association for the Advancement of Science

articles

Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures

WE Meador, AR Means, and FA Quiocho

Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030.

Calmodulin is the primary calcium-dependent signal transducer and regulator of a wide variety of essential cellular functions. The structure of calcium-calmodulin bound to the peptide corresponding to the calmodulin-binding domain of brain calmodulin-dependent protein kinase II alpha was determined to 2 angstrom resolution. A comparison to two other calcium-calmodulin structures reveals how the central helix unwinds in order to position the two domains optimally in the recognition of different target enzymes and clarifies the role of calcium in maintaining recognition-competent domain structures.


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Structural Evidence for Non-canonical Binding of Ca2+ to a Canonical EF-hand of a Conventional Myosin.
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A statistical approach to the interpretation of molecular dynamics simulations of calmodulin equilibrium dynamics.
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J. Cell Sci. 118, 3327-3338
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Two-Photon Cross-Correlation Analysis of Intracellular Reactions with Variable Stoichiometry.
S. A. Kim, K. G. Heinze, K. Bacia, M. N. Waxham, and P. Schwille (2005)
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Dynamic Light Scattering Study of Calmodulin-Target Peptide Complexes.
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Fluorescence Intensity and Lifetime Distribution Analysis: Toward Higher Accuracy in Fluorescence Fluctuation Spectroscopy.
K. Palo, L. Brand, C. Eggeling, S. Jager, P. Kask, and K. Gall (2002)
Biophys. J. 83, 605-618
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Identification of Calmodulin Isoform-specific Binding Peptides from a Phage-displayed Random 22-mer Peptide Library.
J. Y. Choi, S. H. Lee, C. Y. Park, W. D. Heo, J. C. Kim, M. C. Kim, W. S. Chung, B. C. Moon, Y. H. Cheong, C. Y. Kim, et al. (2002)
J. Biol. Chem. 277, 21630-21638
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Tryptophan 1093 Is Largely Responsible for the Slow Off Rate of Calmodulin from Plasma Membrane Ca2+ Pump 4b.
A. R. Penheiter, A. J. Caride, A. Enyedi, and J. T. Penniston (2002)
J. Biol. Chem. 277, 17728-17732
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J. K. Kranz, E. K. Lee, A. C. Nairn, and A. J. Wand (2002)
J. Biol. Chem. 277, 16351-16354
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Calcium Binding Is Required for Calmodulin Function in Aspergillus nidulans.
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Eukaryot. Cell 1, 119-125
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Molecular Characterization of Functional Domains in the Protein Kinase SOS2 That Is Required for Plant Salt Tolerance.
Y. Guo, U. Halfter, M. Ishitani, and J.-K. Zhu (2001)
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Identification of a Calmodulin-Regulated Soybean Ca2+-ATPase (SCA1) That Is Located in the Plasma Membrane.
W. S. Chung, S. H. Lee, J. C. Kim, W. Do Heo, M. C. Kim, C. Y. Park, H. C. Park, C. O. Lim, W. B. Kim, J. F. Harper, et al. (2000)
PLANT CELL 12, 1393-1408
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Three-dimensional Reconstructions of Calcium/Calmodulin-dependent (CaM) Kinase IIalpha and Truncated CaM Kinase IIalpha Reveal a Unique Organization for Its Structural Core and Functional Domains.
S. J. Kolodziej, A. Hudmon, M. N. Waxham, and J. K. Stoops (2000)
J. Biol. Chem. 275, 14354-14359
   Abstract »    Full Text »    PDF »
Ordered and Cooperative Binding of Opposing Globular Domains of Calmodulin to the Plasma Membrane Ca-ATPase.
H. Sun and T. C. Squier (2000)
J. Biol. Chem. 275, 1731-1738
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Regulatory Cascades Involving Calmodulin-Dependent Protein Kinases.
A. R. Means (2000)
Mol. Endocrinol. 14, 4-13
   Full Text »
Tryptophan fluorescence of calmodulin binding domain peptides interacting with calmodulin containing unnatural methionine analogues.
A. M. Weljie and H. J. Vogel (2000)
Protein Eng. Des. Sel. 13, 59-66
   Abstract »    Full Text »    PDF »
Molecular determinants of the modulation of cyclic nucleotide-activated channels by calmodulin.
M. E. Grunwald, H. Zhong, J. Lai, and K.-W. Yau (1999)
PNAS 96, 13444-13449
   Abstract »    Full Text »    PDF »
Structural Examination of Autoregulation of Multifunctional Calcium/Calmodulin-dependent Protein Kinase II.
E. Yang and H. Schulman (1999)
J. Biol. Chem. 274, 26199-26208
   Abstract »    Full Text »    PDF »
Ca2+/Calmodulin-dependent Protein Kinase Cascade in Caenorhabditis elegans. IMPLICATION IN TRANSCRIPTIONAL ACTIVATION.
K. Eto, N. Takahashi, Y. Kimura, Y. Masuho, K.-i. Arai, M.-a. Muramatsu, and H. Tokumitsu (1999)
J. Biol. Chem. 274, 22556-22562
   Abstract »    Full Text »    PDF »
Apocalmodulin.
L. A. Jurado, P. S. Chockalingam, and H. W. Jarrett (1999)
Physiol Rev 79, 661-682
   Abstract »    Full Text »    PDF »
Apocalmodulin Binds to the Myosin Light Chain Kinase Calmodulin Target Site.
P. O. Tsvetkov, I. I. Protasevich, R. Gilli, D. Lafitte, V. M. Lobachov, J. Haiech, C. Briand, and A. A. Makarov (1999)
J. Biol. Chem. 274, 18161-18164
   Abstract »    Full Text »    PDF »
Surface Exposure of the Methionine Side Chains of Calmodulin in Solution. A NITROXIDE SPIN LABEL AND TWO-DIMENSIONAL NMR STUDY.
T. Yuan, H. Ouyang, and H. J. Vogel (1999)
J. Biol. Chem. 274, 8411-8420
   Abstract »    Full Text »    PDF »
Calmodulin-dependent Regulation of Inducible and Neuronal Nitric-oxide Synthase.
S.-J. Lee and J. T. Stull (1998)
J. Biol. Chem. 273, 27430-27437
   Abstract »    Full Text »    PDF »
Importance of Phenylalanine Residues of Yeast Calmodulin for Target Binding and Activation.
H. Okano, M. S. Cyert, and Y. Ohya (1998)
J. Biol. Chem. 273, 26375-26382
   Abstract »    Full Text »    PDF »
14-3-3 Proteins Are Required for Maintenance of Raf-1 Phosphorylation and Kinase Activity.
J. A. Thorson, L. W. K. Yu, A. L. Hsu, N.-Y. Shih, P. R. Graves, J. W. Tanner, P. M. Allen, H. Piwnica-Worms, and A. S. Shaw (1998)
Mol. Cell. Biol. 18, 5229-5238
   Abstract »    Full Text »
Characterization of the Mechanism of Regulation of Ca2+/ Calmodulin-dependent Protein Kinase I by Calmodulin and by Ca2+/Calmodulin-dependent Protein Kinase Kinase.
M. Matsushita and A. C. Nairn (1998)
J. Biol. Chem. 273, 21473-21481
   Abstract »    Full Text »    PDF »
Evolvability.
M. Kirschner and J. Gerhart (1998)
PNAS 95, 8420-8427
   Abstract »    Full Text »    PDF »
A Mechanism for Calmodulin (CaM) Trapping by CaM-kinase II Defined by a Family of CaM-binding Peptides.
M. N. Waxham, A.-l. Tsai, and J. A. Putkey (1998)
J. Biol. Chem. 273, 17579-17584
   Abstract »    Full Text »    PDF »
Crystal structure of troponin C in complex with troponin I fragment at 2.3-A resolution.
D. G. Vassylyev, S. Takeda, S. Wakatsuki, K. Maeda, and Y. Maeda (1998)
PNAS 95, 4847-4852
   Abstract »    Full Text »    PDF »
Regulatory Segments of Ca2+/Calmodulin-dependent Protein Kinases.
G. Zhi, S. M. Abdullah, and J. T. Stull (1998)
J. Biol. Chem. 273, 8951-8957
   Abstract »    Full Text »    PDF »
Characterization of Substrate Phosphorylation and Use of Calmodulin Mutants to Address Implications from the Enzyme Crystal Structure of Calmodulin-dependent Protein Kinase I.
D. Chin, K. E. Winkler, and A. R. Means (1997)
J. Biol. Chem. 272, 31235-31240
   Abstract »    Full Text »    PDF »
Ca2+/Calmodulin Causes Rab3A to Dissociate from Synaptic Membranes.
J. B. Park, C. C. Farnsworth, and J. A. Glomset (1997)
J. Biol. Chem. 272, 20857-20865
   Abstract »    Full Text »    PDF »
The Ca2+-dependent Binding of Calmodulin to an N-terminal Motif of the Heterotrimeric G Protein beta  Subunit.
M. Liu, B. Yu, O. Nakanishi, T. Wieland, and M. Simon (1997)
J. Biol. Chem. 272, 18801-18807
   Abstract »    Full Text »    PDF »
Identification and Characterization of a Calmodulin-binding Domain in Ral-A, a Ras-related GTP-binding Protein Purified from Human Erythrocyte Membrane.
K. L. Wang, M. T. Khan, and B. D. Roufogalis (1997)
J. Biol. Chem. 272, 16002-16009
   Abstract »    Full Text »    PDF »
Differential Activation of NAD Kinase by Plant Calmodulin Isoforms. THE CRITICAL ROLE OF DOMAIN I.
S. H. Lee, H. Y. Seo, J. C. Kim, W. D. Heo, W. S. Chung, K. J. Lee, M. C. Kim, Y. H. Cheong, J. Y. Choi, C. O. Lim, et al. (1997)
J. Biol. Chem. 272, 9252-9259
   Abstract »    Full Text »    PDF »
Functional Consequences of Truncating Amino Acid Side Chains Located at a Calmodulin-Peptide Interface.
D. Chin, D. J. Sloan, F. A. Quiocho, and A. R. Means (1997)
J. Biol. Chem. 272, 5510-5513
   Abstract »    Full Text »    PDF »
Kinetic Control of the Dissociation Pathway of Calmodulin-Peptide Complexes.
S. E. Brown, S. R. Martin, and P. M. Bayley (1997)
J. Biol. Chem. 272, 3389-3397
   Abstract »    Full Text »    PDF »
Methionine to Glutamine Substitutions in the C-terminal Domain of Calmodulin Impair the Activation of Three Protein Kinases.
D. Chin and A. R. Means (1996)
J. Biol. Chem. 271, 30465-30471
   Abstract »    Full Text »    PDF »
A Peptide Model for Calmodulin Trapping by Calcium/Calmodulin-dependent Protein Kinase II.
J. A. Putkey and M. N. Waxham (1996)
J. Biol. Chem. 271, 29619-29623
   Abstract »    Full Text »    PDF »
Binding of Centrins and Yeast Calmodulin to Synthetic Peptides Corresponding to Binding Sites in the Spindle Pole Body Components Kar1p and Spc110p.
B. M. Geier, H. Wiech, and E. Schiebel (1996)
J. Biol. Chem. 271, 28366-28374
   Abstract »    Full Text »    PDF »
The Role of Phe-92 in the Ca[IMAGE]-induced Conformational Transition in the C-terminal Domain of Calmodulin.
D. F. Meyer, Y. Mabuchi, and Z. Grabarek (1996)
J. Biol. Chem. 271, 11284-11290
   Abstract »    Full Text »    PDF »
Blocking the Ca[IMAGE]-induced Conformational Transitions in Calmodulin with Disulfide Bonds.
R.-Y. Tan, Y. Mabuchi, and Z. Grabarek (1996)
J. Biol. Chem. 271, 7479-7483
   Abstract »    Full Text »    PDF »
Effects of Myosin Light Chain Kinase and Peptides on Ca[IMAGE] Exchange with the N- and C-terminal Ca[IMAGE] Binding Sites of Calmodulin.
J. D. Johnson, C. Snyder, M. Walsh, and M. Flynn (1996)
J. Biol. Chem. 271, 761-767
   Abstract »    Full Text »    PDF »
The Calmodulin-Nitric Oxide Synthase Interaction.
Z. Su, M. A. Blazing, D. Fan, and S. E. George (1995)
J. Biol. Chem. 270, 29117-29122
   Abstract »    Full Text »    PDF »
The Regulatory Region of Calcium/Calmodulin-dependent Protein Kinase I Contains Closely Associated Autoinhibitory and Calmodulin-binding Domains.
H. Yokokura, M. R. Picciotto, A. C. Nairn, and H. Hidaka (1995)
J. Biol. Chem. 270, 23851-23859
   Abstract »    Full Text »    PDF »
Interaction of Calmodulin with Its Binding Domain of Rat Cerebellar Nitric Oxide Synthase.
M. Zhang, T. Yuan, J. M. Aramini, and H. J. Vogel (1995)
J. Biol. Chem. 270, 20901-20907
   Abstract »    Full Text »    PDF »
Mutational Analysis of Ca[IMAGE]-independent Autophosphorylation of Calcium/Calmodulin-dependent Protein Kinase II.
S. Mukherji and T. R. Soderling (1995)
J. Biol. Chem. 270, 14062-14067
   Abstract »    Full Text »    PDF »
Calmodulin Binding of a Peptide Derived from the Regulatory Domain of Bordetella pertussis Adenylate Cyclase.
C. T. Craescu, A. Bouhss, J.ël Mispelter, E. Diesis, A. Popescu, M. Chiriac, and O. Bârzu (1995)
J. Biol. Chem. 270, 7088-7096
   Abstract »    Full Text »    PDF »
Calmodulin Stabilizes an Amphiphilic alpha-Helix within RC3/Neurogranin and GAP-43/Neuromodulin Only When Ca[IMAGE] Is Absent.
D. D. Gerendasy, S. R. Herron, P. A. Jennings, and J. G. Sutcliffe (1995)
J. Biol. Chem. 270, 6741-6750
   Abstract »    Full Text »    PDF »
Calcium-Calmodulin Modulation of the Olfactory Cyclic Nucleotide-Gated Cation Channel.
M. Liu, T.-Y. Chen, B. Ahamed, J. Li, and K.-W. Yau (1994)
Science 266, 1348-1354
   Abstract »    PDF »
Activation of Myosin Light Chain Kinase Requires Translocation of Bound Calmodulin.
J. K. Krueger, S. C. Gallagher, G. Zhi, R. Geguchadze, A. Persechini, J. T. Stull, and J. Trewhella (2001)
J. Biol. Chem. 276, 4535-4538
   Abstract »    Full Text »    PDF »
Regulatory Mechanism of Ca2+/Calmodulin-dependent Protein Kinase Kinase.
H. Tokumitsu, M.-a. Muramatsu, M. Ikura, and R. Kobayashi (2000)
J. Biol. Chem. 275, 20090-20095
   Abstract »    Full Text »    PDF »
An Extended Conformation of Calmodulin Induces Interactions between the Structural Domains of Adenylyl Cyclase from Bacillus anthracis to Promote Catalysis.
C. L. Drum, S.-Z. Yan, R. Sarac, Y. Mabuchi, K. Beckingham, A. Bohm, Z. Grabarek, and W.-J. Tang (2000)
J. Biol. Chem. 275, 36334-36340
   Abstract »    Full Text »    PDF »
Identification of the Calmodulin-binding Domain of Recombinant Calcium-independent Phospholipase A2beta . IMPLICATIONS FOR STRUCTURE AND FUNCTION.
C. M. Jenkins, M. J. Wolf, D. J. Mancuso, and R. W. Gross (2001)
J. Biol. Chem. 276, 7129-7135
   Abstract »    Full Text »    PDF »
Energetics of Target Peptide Binding by Calmodulin Reveals Different Modes of Binding.
R. D. Brokx, M. M. Lopez, H. J. Vogel, and G. I. Makhatadze (2001)
J. Biol. Chem. 276, 14083-14091
   Abstract »    Full Text »    PDF »
Molecular Characterization of Calmodulin Trapping by Calcium/Calmodulin-dependent Protein Kinase II.
S. I. Singla, A. Hudmon, J. M. Goldberg, J. L. Smith, and H. Schulman (2001)
J. Biol. Chem. 276, 29353-29360
   Abstract »    Full Text »    PDF »
Mapping of Calmodulin and Gbeta gamma Binding Domains within the C-terminal Region of the Metabotropic Glutamate Receptor 7A.
O. El Far, E. Bofill-Cardona, J. M. Airas, V. O'Connor, S. Boehm, M. Freissmuth, C. Nanoff, and H. Betz (2001)
J. Biol. Chem. 276, 30662-30669
   Abstract »    Full Text »    PDF »
Mapping the interface between calmodulin and MARCKS-related protein by fluorescence spectroscopy.
A. Ulrich, A. A. P. Schmitz, T. Braun, T. Yuan, H. J. Vogel, and G. Vergeres (2000)
PNAS 97, 5191-5196
   Abstract »    Full Text »    PDF »


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