Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin

EMBO Journal

Volumn 24, Issue 18, 2005, Pages 3190-3201

  Guo, Qing ^a   Shen, Yuequan ^a   Lee, Young Sam ^a   Gibbs, Craig S ^b   Mrksich, Milan ^a   Tang, Wei Jen ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b GILEAD SCIENCES   (United States)

Author keywords

Adenylyl cyclase toxin; Calmodulin; Catalytic activation; CyaA; Pertussis

Indexed keywords

ADEFOVIR DIPHOSPHATE; ADENYLATE CYCLASE TOXIN; ANTHRAX EDEMA FACTOR; ANTIVIRUS AGENT; BIOLOGICAL FACTOR; CALCIUM; CALMODULIN; PROTEIN CYAA; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BORDETELLA PERTUSSIS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG BINDING; HYDROPHOBICITY; MOLECULAR INTERACTION; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

ADENYLATE CYCLASE TOXIN; AMINO ACID SEQUENCE; BORDETELLA PERTUSSIS; CALMODULIN; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; VIPER VENOMS;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS;

EID: 25144469471     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600800     Document Type: Article

References (52)

1. Abrami L, Reig N, van der Goot FG (2005) Anthrax toxin: the long and winding road that leads to the kill. Trends Microbiol 13: 72-78
2. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529
3. Bhattacharya S, Bunick CG, Chazin WJ (2004) Target selectivity in EF-hand calcium binding proteins. Biochim Biophys Acta 1742: 69-79
4. Bouhss A, Krin E, Munier H, Gilles AM, Danchin A, Glaser P, Barzu O (1993) Cooperative phenomena in binding and activation of Bordetella pertussis adenylate cyclase by calmodulin. J Biol Chem. 268: 1690-1694
5. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921
6. Carbonetti NH, Artamonova GV, Andreasen C, Bushar N (2005) Pertussis toxin and adenylate cyclase toxin provide a one-two punch for establishment of Bordetella pertussis infection of the respiratory tract. Infect Immun 73: 2698-2703
7. Crivici A, Ikura M (1995) Molecular and structural basis of target recognition by calmodulin. Annu Rev Biophys Biomol Struct 24: 85-116
8. Drum CL, Yan SZ, Bard J, Shen Y, 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
9. Drum CL, Yan SZ, Sarac R, Mabuchi Y, Beckingham K, Bohm A, Grabarek Z, Tang W-J (2000) An extended conformation of calmodulin induces interactions between the structural domains of adenylyl cyclase from Bacillus anthracis to promote catalysis. J Biol Chem 275: 36334-36340
10. Gallay J, Vincent M, Li de la Sierra IM, Munier-Lehmann H, Renouard M, Sakamoto H, Barzu O, Gilles AM (2004) Insight into the activation mechanism of Bordetella pertussis adenylate cyclase by calmodulin using fluorescence spectroscopy. Eur J Biochem 271: 821-833
11. Glaser P, Elmaoglou-Lazaridou A, Krin E, Ladant D, Barzu O, 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
12. Glaser P, Munier H, Gilles AM, Krin E, Porumb T, Barzu O, Sarfati R, Pellecuer C, Danchin A (1991) Functional consequences of single amino acid substitutions in calmodulin-activated adenylate cyclase of Bordetella pertussis. EMBO J 10: 1683-1688
13. Guermonprez P, Khelef N, Blouin E, Rieu P, Ricciardi-Castagnoli P, Guiso N, Ladant D, Leclerc C (2001) The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J Exp Med 193: 1035-1044
14. Guo Q, Shen Y, Zhukovskaya NL, Florián J, Tang W-J (2004) Structural and kinetic analyses of the interaction of anthrax adenylyl cyclase toxin with reaction products, cAMP and pyrophosphate. J Biol Chem 279: 29427-29435
15. Hoeflich KP, Ikura M (2002) Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108: 739-742
16. Ikura M, Clore GM, Gronenborn AM, Zhu G, Klee CB, Bax A (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256: 632-638
17. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119
18. Jurado LA, Chockalingam PS, Jarrett HW (1999) Apocalmodulin. Physiol Rev 79: 661-682
19. Karimova G, Pidoux J, Ullmann A, Ladant D (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756
20. La Fortelle E, Bricogne G (1997) Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD methods. Methods Enzymol 276: 472-494
21. Ladant D (1988) Interaction of Bordetella pertussis adenylate cyclase with calmodulin. Identification of two separated calmodulin-binding domains. J Biol Chem 263: 2612-2618
22. Ladant D, Ullmann A (1999) Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol 7: 172-176
23. Lawrence MC, Colman PM (1993) Shape complementarity at protein/protein interfaces. J Mol Biol 234: 946-950
24. Linder JU, Schultz JE (2003) The class III adenylyl cyclase: multipurpose signalling modules. Cell Signal 15: 1081-1089
25. 2+ /calmodulin. EMBO J 23: 712-718
26. Mattoo S, Foreman-Wykert AK, Cotter PA, Miller JF (2001) Mechanisms of Bordetella pathogenesis. Front Biosci 6: e168-e186
27. Meador WE, Means AR, Quiocho FA (1992) Target enzyme recognition by calmodulin: 2.4Å structure of a calmodulin-peptide complex. Science 257: 1251-1255
28. Munier H, Bouhss A, Krin E, Danchin A, Gilles AM, Glaser P, Barzu O (1992) The role of histidine 63 in the catalytic mechanism of Bordetella pertussis adenylate cyclase. J Biol Chem 267: 9816-9820
29. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, Roy CR (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 102: 826-831
30. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
31. Purdy A, Rohwer F, Edwards R, Azam F, Bartlett DH (2005) A glimpse into the expanded genome content of Vibrio cholerae through identification of genes present in environmental strains. J Bacteriol 187: 2992-3001
32. Rogel A, Meller R, Hanski E (1991) Adenylate cyclase toxin from Bordetella pertussis. The relationship between induction of cAMP and hemolysis. J Biol Chem 266: 3154-3161
33. Sarfati RS, Kansal VK, Munier H, Glaser P, Gilles AM, Labruyere E, Mock M, Danchin A, Barzu O (1990) Binding of 3′-anthraniloyl-2′-deoxy-ATP to calmodulin-activated adenylate cyclase from Bordetella pertussis and Bacillus anthracis. J Biol Chem 265: 18902-18906
34. Schuck P (1997) Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules. Annu Rev Biophys Biomol Struct 26: 541-566
35. 2+/calmodulin. Nature 410: 1120-1124
36. Shen Y, Lee Y-S, Soelaiman S, Bergson P, Lu D, Chen A, Beckingham K, Grabarek Z, Mrksich M, Tang W-J (2002) Physiological calcium concentrations regulate calmodulin binding and catalysis of adenylyl cyclase exotoxins. EMBO J 21: 6721-6732
37. Shen Y, Zhukovskaya NL, Guo Q, Florian J, Tang W-J (2005) Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor. EMBO J 24: 929-941
38. Shen Y, Zhukovskaya NL, Zimmer MI, Soelaiman S, Bergson P, Wang CR, Gibbs CS, Tang WJ (2004) Selective inhibition of anthrax edema factor by adefovir, a drug for chronic hepatitis B virus infection. Proc Natl Acad Sci USA 101: 3242-3247
39. Sinha SC, Wetterer M, Sprang SR, Schultz JE, Linder JU (2005) Origin of asymmetry in adenylyl cyclases: structures of Mycobacterium tuberculosis Rv1900c. EMBO J 24: 663-673
40. Sory MP, Cornelis GR (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594
41. Steegborn C, Litvin TN, Levin LR, Buck J, Wu H (2005) Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat Struct Mol Biol 12: 32-37
42. Steitz TA (1998) A mechanism for all polymerases. Nature 391: 231-232
43. Terwiliger TC (2000) Maximum likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972
44. Tesmer JJ, Sunahara RK, Gilman AG, Sprang SR (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsα- GTPγS. Science 278: 1907-1916
45. Tews I, Findeisen F, Sinning I, Schultz A, Schultz JE, Linder JU (2005) The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 308: 1020-1023
46. Ulmer TS, Soelaiman S, Li S, Klee CB, Tang W-J, Bax A (2003) Calcium dependency of the interaction between calmodulin and anthrax edema factor. J Biol Chem 278: 29261-29266
47. Vordermeier HM, Simsova M, Wilkinson KA, Wilkinson RJ, Hewinson RG, Sebo P, Leclerc C (2004) Recognition of mycobacterial antigens delivered by genetically detoxified Bordetella pertussis adenylate cyclase by T cells from cattle with bovine tuberculosis. Infect Immun 72: 6255-6261
48. Vougier S, Mary J, Dautin N, Vinh J, Friguet B, 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
49. Weeks CM, Miller R (1999) Optimizing Shake-and-Bake for proteins. Acta Crystallogr D 55: 492-500
50. Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW (1998) ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95: 13899-13904
51. 2+-calmodulin. Nat Struct Biol 10: 226-231
52. Yap KL, Yuan T, Mal TK, Vogel HJ, Ikura M (2003) Structural basis for simultaneous binding of two carboxy-terminal peptides of plant glutamate decarboxylase to calmodulin. J Mol Biol 328: 193-204