Calmodulin-induced conformational and hydrodynamic changes in the catalytic domain of Bordetella pertussis adenylate cyclase toxin

Biochemistry

Volumn 49, Issue 2, 2010, Pages 318-328

  Karst, Johanna C ^a   Sotomayor Pérez, Ana Cristina ^a   Inaki Guijarro J ^a   Raynal, Bertrand ^a   Chenal, Alexandre ^a   Ladant, Daniel ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION MECHANISMS; ADENYLATE CYCLASE; BIOPHYSICAL PROPERTIES; CATALYTIC DOMAINS; CAUSATIVE AGENTS; CELL INVASION; CYTOSOLS; HYDRODYNAMIC PROPERTIES; MOLECULAR BASIS; N-TERMINALS; PLASMA MEMBRANES; SECONDARY AND TERTIARY STRUCTURES; STRUCTURAL TRANSITIONS; WHOOPING COUGH;

CELL MEMBRANES; COMPLEXATION; FETAL MONITORING; FLUID DYNAMICS; HYDRATES; HYDRODYNAMICS;

CALMODULIN;

ADENYLATE CYCLASE TOXIN; CALMODULIN;

ARTICLE; BIOPHYSICS; BORDETELLA PERTUSSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME MECHANISM; HYDRODYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; ENZYME ACTIVE SITE; ENZYMOLOGY; GEL CHROMATOGRAPHY; GENETICS; ION EXCHANGE CHROMATOGRAPHY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; SPECTROPHOTOMETRY;

ACIS; BORDETELLA PERTUSSIS; EUKARYOTA;

ADENYLATE CYCLASE TOXIN; BORDETELLA PERTUSSIS; CALMODULIN; CATALYTIC DOMAIN; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, ION EXCHANGE; CIRCULAR DICHROISM; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; PROTEIN CONFORMATION; SPECTROPHOTOMETRY;

EID: 75349096080     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9016389     Document Type: Article

References (43)

1. Ladant, D., and Ullmann, A. (1999) Bordetella pertussis adenylate cyclase: A toxin with multiple talents. Trends Microbiol. 7, 172-176.
2. Vojtova, J., Kamanova, J., and Sebo, P. (2006) Bordetella adenylate cyclase toxin: A swift saboteur of host defense. Curr. Opin. Microbiol. 9, 69-75.
3. Harvill, E. T., Cotter, P. A., Yuk, M. H., and Miller, J. F. (1999) Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect. Immun. 67, 1493-1500.
4. Perkins, D. J., Gray, M. C., Hewlett, E. L., and Vogel, S. N. (2007) Bordetella pertussis adenylate cyclase toxin (ACT) induces cyclooxygenase-2 (COX-2) in murine macrophages and is facilitated by ACT interaction with CD11b/CD18 (Mac-1). Mol. Microbiol. 66, 1003-1015.
5. Cheung, G. Y., Dickinson, P., Sing, G., Craigon, M., Ghazal, P., Parton, R., and Coote, J. G. (2008) Transcriptional responses of murine macrophages to the adenylate cyclase toxin of Bordetella pertussis. Microb. Pathog. 44, 61-70.
6. Rose, T., Sebo, P., Bellalou, J., and Ladant, D. (1995) Interaction of calcium with Bordetella pertussis adenylate cyclase toxin. Characterization of multiple calcium-binding sites and calcium-induced conformational changes. J. Biol. Chem. 270, 26370-26376.
7. Bauche, C., Chenal, A., Knapp, O., Bodenreider, C., Benz, R., Chaffotte, A., and Ladant, D. (2006) Structural and functional characterization of an essential RTX subdomain of Bordetella pertussis adenylate cyclase toxin. J. Biol. Chem. 281, 16914-16926.
8. Chenal, A., Guijarro, J. I., Raynal, B., Delepierre, M., and Ladant, D. (2009) RTX calcium binding motifs are intrinsically disordered in the absence of calcium: Implication for protein secretion. J. Biol. Chem. 284, 1781-1789.
9. Danchin, A. (1993) Phylogeny of adenylyl cyclases. Adv. Second Messenger Phosphoprotein Res. 27, 109-162.
10. Shen, Y., Zhukovskaya, N. L., Guo, Q., Florian, J., and Tang, W. J. (2005) Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor. EMBO J. 24, 929-941.
11. Guo, Q., Shen, Y., Lee, Y. S., Gibbs, C. S., Mrksich, M., and Tang, W. J. (2005) Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin. EMBO J. 24, 3190-3201.
12. Glaser, P., Elmaoglou-Lazaridou, A., Krin, E., Ladant, D., Barzu, O., and Danchin, A. (1989) Identification of residues essential for catalysis and binding of calmodulin in Bordetella pertussis adenylate cyclase by site-directed mutagenesis. EMBO J. 8, 967-972.
13. Glaser, P., Munier, H., Gilles, A. M., Krin, E., Porumb, T., Barzu, O., Sarfati, R., Pellecuer, C., and Danchin, A. (1991) Functional consequences of single amino acid substitutions in calmodulin-activated adenylate cyclase of Bordetella pertussis. EMBO J. 10, 1683-1688.
14. Munier, H., Bouhss, A., Krin, E., Danchin, A., Gilles, A. M., Glaser, P., and Barzu, O. (1992) The role of histidine 63 in the catalytic mechanism of Bordetella pertussis adenylate cyclase. J. Biol. Chem. 267, 9816-9820.
15. Drum, C. L., Yan, S. Z., Bard, J., Shen, Y. Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A., and Tang, W. J. (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415, 396-402.
16. Ladant, D. (1988) Interaction of Bordetella pertussis adenylate cyclase with calmodulin. Identification of two separated calmodulin-binding domains. J. Biol. Chem. 263, 2612-2618.
17. Ladant, D., Michelson, S., Sarfati, R., Gilles, A. M., Predeleanu, R., and Barzu, O. (1989) Characterization of the calmodulin-binding and of the catalytic domains of Bordetella pertussis adenylate cyclase. J. Biol. Chem. 264, 4015-4020.
18. Munier, H., Bouhss, A., Gilles, A. M., Krin, E., Glaser, P., Danchin, A., and Barzu, O. (1993) Structural flexibility of the calmodulinbinding locus in Bordetella pertussis adenylate cyclase. Reconstitution of catalytically active species from fragments or inactive forms of the enzyme. Eur. J. Biochem. 217, 581-586.
19. Bouhss, A., Krin, E., Munier, H., Gilles, A. M., Danchin, A., Glaser, P., and Barzu, O. (1993) Cooperative phenomena in binding and activation of Bordetella pertussis adenylate cyclase by calmodulin. J. Biol. Chem. 268, 1690-1694.
20. Guo, Q., Jureller, J. E., Warren, J. T., Solomaha, E., Florian, J., and Tang, W. J. (2008) Protein-protein docking and analysis reveal that two homologous bacterial adenylyl cyclase toxins interact with calmodulin differently. J. Biol. Chem. 283, 23836-23845.
21. Vougier, S., Mary, J., Dautin, N., Vinh, J., Friguet, B., and Ladant, D. (2004) Essential role of methionine residues in calmodulin binding to Bordetella pertussis adenylate cyclase, as probed by selective oxidation and repair by the peptide methionine sulfoxide reductases. J. Biol. Chem. 279, 30210-30218.
22. Lees, J. G., Miles, A. J., Wien, F., and Wallace, B. A. (2006) A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22, 1955-1962.
23. Lobley, A., Whitmore, L., and Wallace, B. A. (2002) DICHROWEB: An interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18, 211-212.
24. Whitmore, L., and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32, W668-W673.
25. Compton, L. A., and Johnson, W. C., Jr. (1986) Analysis of protein circular dichroism spectra for secondary structure using a simple matrix multiplication. Anal. Biochem. 155, 155-167.
26. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260.
27. Manavalan, P., and Johnson, W. C., Jr. (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra. Anal. Biochem. 167, 76-85.
28. Cao, W., and Demeler, B. (2005) Modeling analytical ultracentrifugation experiments with an adaptive space-time finite element solution of the Lamm equation. Biophys. J. 89, 1589-1602.
29. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78, 1606-1619.
30. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320, 104-124.
31. Bourdeau, R. W., Malito, E., Chenal, A., Bishop, B. L., Musch, M. W., Villereal, M. L., Chang, E. B., Mosser, E. M., Rest, R. F., and Tang, W. J. (2009) Cellular Functions and X-ray Structure of Anthrolysin O, a Cholesterol-dependent Cytolysin Secreted by Bacillus anthracis. J. Biol. Chem. 284, 14645-14656.
32. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible. Biochemistry 31, 5269-5278.
33. Sreerama, N., Manning, M. C., Powers, M. E., Zhang, J. X., Goldenberg, D. P., and Woody, R. W. (1999) Tyrosine, phenylalanine, and disulfide contributions to the circular dichroism of proteins: Circular dichroism spectra of wild-type and mutant bovine pancreatic trypsin inhibitor. Biochemistry 38, 10814-10822.
34. Freskgard, P. O., Martensson, L. G., Jonasson, P., Jonsson, B. H., and Carlsson, U. (1994) Assignment of the contribution of the tryptophan residues to the circular dichroism spectrum of human carbonic anhydrase II. Biochemistry 33, 14281-14288.
35. Tavallaie, M., Chenal, A., Gillet, D., Pereira, Y., Manich, M., Gibert, M., Raffestin, S., Popoff, M. R., and Marvaud, J. C. (2004) Interaction between the two subdomains of the C-terminal part of the botulinum neurotoxin A is essential for the generation of protective antibodies. FEBS Lett. 572, 299-306.
36. Fasman, G. D., Ed. (1996) Circular Dichroism and the Conformational Analysis of Biomolecules, Plenum Press, New York.
37. 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.
38. Meador, W. E., Means, A. R., and Quiocho, F. A. (1992) Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulinpeptide complex. Science 257, 1251-1255.
39. 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.
40. Harding, S. E., and Colfen, H. (1995) Inversion formulae for ellipsoid of revolution macromolecular shape functions. Anal. Biochem. 228, 131-142.
41. Gilles, A. M., Munier, H., Rose, T., Glaser, P., Krin, E., Danchin, A., Pellecuer, C., and Barzu, O. (1990) Intrinsic fluorescence of a truncated Bordetella pertussis adenylate cyclase expressed in Escherichia coli. Biochemistry 29, 8126-8130.
42. Bouhss, A., Vincent, M., Munier, H., Gilles, A. M., Takahashi, M., Barzu, O., Danchin, A., and Gallay, J. (1996) Conformational transitions within the calmodulin-binding site of Bordetella pertussis adenylate cyclase studied by time-resolved fluorescence of Trp242 and circular dichroism. Eur. J. Biochem. 237, 619-628.
43. Gallay, J., Vincent, M., Li de la Sierra, I. M., Munier-Lehmann, H., Renouard, M., Sakamoto, H., Barzu, O., and Gilles, A. M. (2004) Insight into the activation mechanism of Bordetella pertussis adenylate cyclase by calmodulin using fluorescence spectroscopy. Eur. J. Biochem. 271, 821-833.