Cited by 417Bacillus and Francisella bacterial researchEnzyme Structure and FunctionProtein Structure and Dynamics

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Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin

Drum, Chester L., Yan, Shui-Zhong, Bard, Joel, Shen, Yue-Quan, Lu, Dan, Soelaiman, Sandriyana, Grabarek, Zenon, Bohm, Andrew, Tang, Wei-Jen·2002·Nature

DOI 10.1038/415396a

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Abstract

Oedema factor, a calmodulin-activated adenylyl cyclase, is important in the pathogenesis of anthrax. Here we report the X-ray structures of oedema factor with and without bound calmodulin. Oedema factor shares no significant structural homology with mammalian adenylyl cyclases or other proteins. In the active site, 3'-deoxy-ATP and a single metal ion are well positioned for catalysis with histidine 351 as the catalytic base. This mechanism differs from the mechanism of two-metal-ion catalysis proposed for mammalian adenylyl cyclases. Four discrete regions of oedema factor form a surface that recognizes an extended conformation of calmodulin, which is very different from the collapsed conformation observed in other structures of calmodulin bound to effector peptides. On calmodulin binding, an oedema factor helical domain of relative molecular mass 15,000 undergoes a 15 A translation and a 30 degrees rotation away from the oedema factor catalytic core, which stabilizes a disordered loop and leads to enzyme activation. These allosteric changes provide the first molecular details of how calmodulin modulates one of its targets.

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[20] Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Z., & Minor, W. (1997) · Methods in Enzymology · doi:10.1016/s0076-6879(97)76066-x · Cited by 33,475
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse‐Kunstleve, R. W., Jiang, J., Kuszewski, J. J., Nilges, M., Pannu, N., et al. (1998) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998003254 · Cited by 15,723
Improved methods for building protein models in electron density maps and the location of errors in these models
Jones, T. A., Zou, J.-Y., Cowan, S. W., & Kjeldgaard, M. (1991) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767390010224 · Cited by 12,616
Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons
Nicholls, A. O., Sharp, K. A., & Honig, B. H. (1991) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340110407 · Cited by 5,230
The atomic structure of protein-protein recognition sites 1 1Edited by A. R. Fersht
Conte, L. L., Chothia, C., & Janin, J. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2439 · Cited by 1,967
Three-dimensional structure of calmodulin
Babu, Y. S., Sack, J. S., Greenhough, T. J., Bugg, C. E., Means, A. R., & Cook, W. J. (1985) · Nature · doi:10.1038/315037a0 · Cited by 1,038
Target Enzyme Recognition by Calmodulin: 2.4 Å Structure of a Calmodulin-Peptide Complex
Meador, W. E., Means, A. R., & Quiocho, F. A. (1992) · Science · doi:10.1126/science.1519061 · Cited by 1,032
Proteolytic Inactivation of MAP-Kinase-Kinase by Anthrax Lethal Factor
Duesbery, N. S., Webb, C. P., Leppla, S. H., Gordon, V. M., Klimpel, K. R., Copeland, T. D., Ahn, N. G., Oskarsson, M. K., Fukasawa, K., Paull, K. D., et al. (1998) · Science · doi:10.1126/science.280.5364.734 · Cited by 1,007
Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells.
Leppla, S. H. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.10.3162 · Cited by 935
Sequence motifs for calmodulin recognition
Rhoads, A. R., & Friedberg, F. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.5.9141499 · Cited by 875
Anthrax
Dixon, T. C., Meselson, M. S., Guillemin, J. H., & Hanna, P. C. (1999) · New England Journal of Medicine · doi:10.1056/nejm199909093411107 · Cited by 871
Crystal Structure of the Catalytic Domains of Adenylyl Cyclase in a Complex with G sα ·GTPγS
Tesmer, J. J. G., Sunahara, R. K., Gilman, A. G., & Sprang, S. R. (1997) · Science · doi:10.1126/science.278.5345.1907 · Cited by 792
Structure of RGS4 Bound to AlF4−-Activated Giα1: Stabilization of the Transition State for GTP Hydrolysis
Tesmer, J. J. G., Berman, D. M., Gilman, A. G., & Sprang, S. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80204-4 · Cited by 782
Further additions to MolScript version 1.4, including reading and contouring of electron-density maps
Esnouf, R. M. (1999) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998017363 · Cited by 754
Calcium-induced conformational transition revealed by the solution structure of apo calmodulin
Zhang, M., Tanaka, T., & Ikura, M. (1995) · Nature Structural & Molecular Biology · doi:10.1038/nsb0995-758 · Cited by 696
Solution structure of calcium-free calmodulin
Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C. B., & Bax, A. (1995) · Nature Structural & Molecular Biology · doi:10.1038/nsb0995-768 · Cited by 662
Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons
Deisseroth, K. A., Heist, E. K., & Tsien, R. W. (1998) · Nature · doi:10.1038/32448 · Cited by 656
Modulation of Calmodulin Plasticity in Molecular Recognition on the Basis of X-Ray Structures
Meador, W. E., Means, A. R., & Quiocho, F. A. (1993) · Science · doi:10.1126/science.8259515 · Cited by 608
Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin
Schumacher, M. A., Rivard, A. F., Bächinger, H. P., & Adelman, J. P. (2001) · Nature · doi:10.1038/35074145 · Cited by 604
EF-hand calcium-binding proteins
Lewit‐Bentley, A., & Réty, S. (2000) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(00)00142-1 · Cited by 572
Superconducting Single Crystals of Tl2Ba2CaCu2O8 and YBa2Cu4O8: Crystal Structures in the Vicinity of Tc
Molchanov, V. N., & Simonov, V. I. (1998) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767398011465 · Cited by 548
ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system
Yahr, T. L., Vallis, A. J., Hancock, M. K., Barbieri, J. T., & Frank, D. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.23.13899 · Cited by 464
Expression and characterization of calmodulin-activated (type I) adenylylcyclase
Tang, W., Krupiński, J., & Gilman, A. G. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)93016-4 · Cited by 443
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DeMaria, C. D., Soong, T. W., Alseikhan, B. A., Alvania, R. S., & Yue, D. T. (2001) · Nature · doi:10.1038/35078091 · Cited by 407
Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion
Peters, C., & Mayer, A. (1998) · Nature · doi:10.1038/25133 · Cited by 386
Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase
Meng, W., Sawasdikosol, S., Burakoff, S. J., & Eck, M. J. (1999) · Nature · doi:10.1038/18050 · Cited by 306
Two-Metal-Ion Catalysis in Adenylyl Cyclase
Tesmer, J. J. G., Sunahara, R. K., Johnson, R. A., Gosselin, G., Gilman, A. G., & Sprang, S. R. (1999) · Science · doi:10.1126/science.285.5428.756 · Cited by 306
Bordetella pertussis adenylate cyclase: a toxin with multiple talents
Ladant, D., & Ullmann, A. (1999) · Trends in Microbiology · doi:10.1016/s0966-842x(99)01468-7 · Cited by 293
Calcium-induced structural changes and domain autonomy in calmodulin
Finn, B. E., Evenäs, J., Drakenberg, T., Waltho, J. P., Thulin, E., & Forsén, S. (1995) · Nature Structural & Molecular Biology · doi:10.1038/nsb0995-777 · Cited by 270
Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan.
Huang, X. Y., Poy, F., Zhang, R., Joachimiak, A., Sudol, M., & Eck, M. J. (2000) · Nature Structural Biology · doi:10.1038/77923 · Cited by 269
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Ikura, M., Osawa, M., Tokumitsu, H., Swindells, M. B., Kurihara, H., Orita, M., Shibanuma, T., & Furuya, T. (1999) · Nature Structural Biology · doi:10.1038/12271 · Cited by 238
Catalytic Mechanism and Regulation of Mammalian Adenylyl Cyclases
Tang, W., & Hurley, J. H. (1998) · Molecular Pharmacology · doi:10.1124/mol.54.2.231 · Cited by 203
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Calmodulin and Signal Transduction
(1998) · Elsevier eBooks · doi:10.1016/c2009-0-02125-4 · Cited by 176
A novel endonuclease mechanism directly visualized for I-PpoI.
Galburt, E. A., Chevalier, B. S., Tang, W., Jurica, M. S., Flick, K. E., Monnat, R. J., & Stoddard, B. L. (1999) · Nature Structural Biology · doi:10.1038/70027 · Cited by 118
Self-citation
Identification of residues essential for catalysis and binding of calmodulin in Bordetella pertussis adenylate cyclase by site‐directed mutagenesis.
Glaser, P., Elmaoglou-Lazaridou, A., Krin, E., Ladant, D., Bârzu, O., & Danchin, A. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03459.x · Cited by 105
The active site of Serratia endonuclease contains a conserved magnesium-water cluster
Miller, M. D., Cai, J., & Krause, K. L. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1999.2729 · Cited by 85
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
Trewhella, J., Blumenthal, D. A., Rokop, S. E., & Seeger, P. A. (1990) · Biochemistry · doi:10.1021/bi00492a003 · Cited by 73
The Conserved Asparagine and Arginine Are Essential for Catalysis of Mammalian Adenylyl Cyclase
Yan, S.-Z., Huang, Z.-H., Shaw, R. S., & Tang, W. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.19.12342 · Cited by 69
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Drum, C. L., Yan, S.-Z., Sarac, R., Mabuchi, Y., Beckingham, K., Bohm, A., Grabarek, Z., & Tang, W. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004778200 · Cited by 67
Self-citation
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Montgomery, H. J., Romanov, V., & Guillemette, J. G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.7.5052 · Cited by 66
Structural analysis of adenylate cyclases from Trypanosoma brucei in their monomeric state
Bieger, B., & Essen, L. (2001) · The EMBO Journal · doi:10.1093/emboj/20.3.433 · Cited by 59
Molecular replacement by evolutionary search
Kissinger, C. R., Gehlhaar, D. K., Smith, B. A., & Bouzida, D. (2001) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444901012458 · Cited by 56
Characterization of ATP and calmodulin-binding properties of a truncated form of Bacillus anthracis adenylate cyclase
Labruyère, E., Mock, M., Ladant, D., Michelson, S., Gilles, A. M., Laoide, B. M., & Bârzu, O. (1990) · Biochemistry · doi:10.1021/bi00472a024 · Cited by 47
Functional consequences of single amino acid substitutions in calmodulin‐activated adenylate cyclase of Bordetella pertussis.
Glaser, P., Munier‐Lehmann, H., Gilles, A., Krin, E., Porumb, T., Bârzu, O., Sarfati, R. S., Pellecuer, C., & Danchin, A. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07692.x · Cited by 38
The role of histidine 63 in the catalytic mechanism of Bordetella pertussis adenylate cyclase.
Munier‐Lehmann, H., Bouhss, A., Krin, E., Danchin, A., Gilles, A., Glaser, P., & Bârzu, O. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)50166-1 · Cited by 33
Activation of Myosin Light Chain Kinase Requires Translocation of Bound Calmodulin
Krueger, J. K., Gallagher, S. C., Zhi, G., Geguchadze, R., Persechini, A., Stull, J. T., & Trewhella, J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c000857200 · Cited by 33
The binding of myristoylated N‐terminal nonapeptide from neuron‐specific protein CAP‐23/NAP‐22 to calmodulin does not induce the globular structure observed for the calmodulin—nonmyristoylated peptide complex
Hayashi, N., Izumi, Y., Titani, K., & Matsushima, N. (2000) · Protein Science · doi:10.1110/ps.9.10.1905 · Cited by 23
Crystallization and preliminary X-ray study of the edema factor exotoxin adenylyl cyclase domain fromBacillus anthracisin the presence of its activator, calmodulin
Drum, C. L., Shen, Y., Rice, P. A., Bohm, A., & Tang, W. (2001) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444901014937 · Cited by 23
Self-citation
Calmodulin Binds to Caldesmon in an Antiparallel Manner
Wang, E., Zhuang, S., Kordowska, J., Grabarek, Z., & Wang, C. A. (1997) · Biochemistry · doi:10.1021/bi963075h · Cited by 22
Self-citation
Features of calmodulin that are important in the activation of the catalytic subunit of phosphorylase kinase.
Farrar, Y. J. K., Lukas, T. J., Craig, T. A., Watterson, D. M., & Carlson, G. M. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53588-2 · Cited by 21
Structural characterization by nuclear magnetic resonance spectroscopy of a genetically engineered high-affinity calmodulin-binding peptide derived from Bordetella pertussis adenylate cyclase
Munier‐Lehmann, H., Bouhss, A., Gilles, A., Palibroda, N., Bârzu, O., Mispelter, J., & Craescu, C. T. (1995) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(95)90004-7 · Cited by 6

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Cowtan, K. in Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography No. 31, 34–38 (1994).

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Authors: Drum, C. L., Yan, S.-Z., Bard, J., Shen, Y.-Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A., & Tang, W.-J.
Affiliations: University of Chicago (US)
Boston Biomedical Research Institute (US)
Tufts University (US)
Corresponding author: Tang, Wei-Jen
ORCID: Drum, Chester L.
Grabarek, Zenon
Bohm, Andrew
Tang, Wei-Jen
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2002-01
Volume: 415
Issue: 6870
Pages: 396-402
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/415396a
OpenAlex: W2096942328
Cited by: 413
References: 51
Citations by year: 2025: 4 · 2024: 5 · 2023: 10 · 2022: 11 · 2021: 6 · 2020: 13 · 2019: 12 · 2018: 8 · 2017: 11 · 2016: 12 · 2015: 13 · 2014: 12 · 2013: 14 · 2012: 19
FWCI: 12.98
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: American Cancer Society
American Heart Association
National Institutes of Health
National Institute on Drug Abuse
National Institute of General Medical Sciences
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacillus and Francisella bacterial research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords: anthrax toxin, adenylate cyclase, calmodulin, enzyme activation, allosteric regulation, calmodulin binding site, metal ion catalysis, protein structure
MeSH terms: Adenylyl Cyclases, Amino Acid Sequence, Animals, Antigens, Bacterial, Bacillus anthracis, Bacterial Toxins, Calmodulin, Enzyme Activation, Exotoxins, Humans, Models, Molecular, Molecular Sequence Data, Protein Binding, Protein Conformation, Structure-Activity Relationship, Crystallography, X-Ray, Catalytic Domain, Macromolecular Substances

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Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin

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