The adenylyl cyclase activity of anthrax edema factor

Molecular Aspects of Medicine

Volumn 30, Issue 6, 2009, Pages 423-430

  Tang, Wei Jen ^a   Guo, Qing ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Anthrax edema factor; Class III adenylyl cyclase; Pertussis CyaA

Indexed keywords

ADENYLATE CYCLASE; CALMODULIN; CYCLIC AMP; PERTUSSIS TOXIN;

ANTHRAX; BACILLUS ANTHRACIS; BACTERIAL TRANSLOCATION; BIOCHEMISTRY; BORDETELLA PERTUSSIS; CELL FUNCTION; CONCENTRATION (PARAMETERS); ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; HOST CELL; HOST RESISTANCE; NONHUMAN; PATHOGENESIS; PERTUSSIS; PROTEIN BINDING; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; ADENYLATE CYCLASE TOXIN; ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; BINDING SITES; BORDETELLA PERTUSSIS; CALMODULIN; CYCLIC AMP; ENZYME ACTIVATION; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS;

EID: 70350712412     PISSN: 00982997     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mam.2009.06.001     Document Type: Review

References (73)

1. Abrami L., Reig N., and van der Goot F.G. Anthrax toxin: the long and winding road that leads to the kill. Trends Microbiol. 13 2 (2005) 72-78
2. Bahler M., and Rhoads A. Calmodulin signaling via the IQ motif. FEBS Lett. 513 1 (2002) 107-113
3. Baldari C.T., Tonello F., Paccani S.R., and Montecucco C. Anthrax toxins: A paradigm of bacterial immune suppression. Trends Immunol. 27 9 (2006) 434-440
4. Benkovic S.J., and Hammes-Schiffer S. A perspective on enzyme catalysis. Science 301 5637 (2003) 1196-1202
5. Biel M., and Michalakis S. Cyclic nucleotide-gated channels. Handb. Exp. Pharmacol. 191 (2009) 111-136
6. Borland, G., Smith, B.O., Yarwood, S.J., 2009. EPAC proteins transduce diverse cellular actions of cAMP. Br. J. Pharmacol., in press.
7. 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. Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis. J. Biol. Chem. 284 (2009) 14645-14656
8. Carbonetti N.H., Artamonova G.V., Andreasen C., and Bushar N. Pertussis toxin and adenylate cyclase toxin provide a one-two punch for establishment of Bordetella pertussis infection of the respiratory tract. Infect. Immun. 73 5 (2005) 2698-2703
9. Chitlaru T., Gat O., Grosfeld H., Inbar I., Gozlan Y., and Shafferman A. Identification of in vivo-expressed immunogenic proteins by serological proteome analysis of the Bacillus anthracis secretome. Infect. Immun. 75 6 (2007) 2841-2852
10. Cooper D.M., Mons N., and Karpen J.W. Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374 6521 (1995) 421-424
11. Crawford M.A., Aylott C.V., Bourdeau R.W., and Bokoch G.M. Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J. Immunol. 176 12 (2006) 7557-7565
12. Dal Molin F., Tonello F., Ladant D., Zornetta I., Zamparo I., Di Benedetto G., Zaccolo M., and Montecucco C. Cell entry and cAMP imaging of anthrax edema toxin. EMBO J. 25 22 (2006) 5405-5413
13. Drum C.L., Yan S.Z., Bard J., Shen Y.Q., Lu D., Soelaiman S., Grabarek Z., Bohm A., and Tang W.J. Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415 6870 (2002) 396-402
14. Drum C.L., Yan S.Z., Sarac R., Mabuchi Y., Beckingham K., Bohm A., Grabarek Z., and Tang W.J. An extended conformation of calmodulin induces interactions between the structural domains of adenylyl cyclase from Bacillus anthracis to promote catalysis. J. Biol. Chem. 275 46 (2000) 36334-36340
15. Firoved A.M., Miller G.F., Moayeri M., Kakkar R., Shen Y., Wiggins J.F., McNally E.M., Tang W.J., and Leppla S.H. Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am. J. Pathol. 167 5 (2005) 1309-1320
16. Firoved A.M., Moayeri M., Wiggins J.F., Shen Y., Tang W.J., and Leppla S.H. Anthrax edema toxin sensitizes DBA/2J mice to lethal toxin. Infect. Immun. 75 5 (2007) 2120-2125
17. Gallagher D.T., Smith N.N., Kim S.K., Heroux A., Robinson H., and Reddy P.T. Structure of the class IV adenylyl cyclase reveals a novel fold. J. Mol. Biol. 362 1 (2006) 114-122
18. Gat O., Grosfeld H., Ariel N., Inbar I., Zaide G., Broder Y., Zvi A., Chitlaru T., Altboum Z., Stein D., Cohen S., and Shafferman A. Search for Bacillus anthracis potential vaccine candidates by a functional genomic-serologic screen. Infect. Immun. 74 7 (2006) 3987-4001
19. Gruenberg J., and van der Goot F.G. Mechanisms of pathogen entry through the endosomal compartments. Nat. Rev. Mol. Cell. Biol. 7 7 (2006) 495-504
20. Guermonprez P., Khelef N., Blouin E., Rieu P., Ricciardi-Castagnoli P., Guiso N., Ladant D., and Leclerc C. The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J. Exp. Med. 193 9 (2001) 1035-1044
21. Guidi-Rontani C., Weber-Levy M., Mock M., and Cabiaux V. Translocation of Bacillus anthracis lethal and oedema factors across endosome membranes. Cell. Microbiol. 2 3 (2000) 259-264
22. Guo Q., Jureller J.E., Warren J.T., Solomaha E., Florian J., and Tang W.J. Protein-protein docking and analysis reveal that two homologous bacterial adenylyl cyclase toxins interact with calmodulin differently. J. Biol. Chem. 283 35 (2008) 23836-23845
23. Guo Q., Shen Y., Lee Y.S., Gibbs C.S., Mrksich M., and Tang W.J. Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin. EMBO J. 24 18 (2005) 3190-3201
24. Hoeflich K.P., and Ikura M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108 6 (2002) 739-742
25. Hong J., Doebele R.C., Lingen M.W., Quilliam L.A., Tang W.J., and Rosner M.R. Anthrax edema toxin inhibits endothelial cell chemotaxis via Epac and Rap1. J. Biol. Chem. 282 27 (2007) 19781-19787
26. Hoover D.L., Friedlander A.M., Rogers L.C., Yoon I.K., Warren R.L., and Cross A.S. Anthrax edema toxin differentially regulates lipopolysaccharide-induced monocyte production of tumor necrosis factor α and interleukin-6 by increasing intracellular cyclic AMP. Infect. Immun. 62 10 (1994) 4432-4439
27. Kamenetsky M., Middelhaufe S., Bank E.M., Levin L.R., Buck J., and Steegborn C. Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 362 4 (2006) 623-639
28. Kim C., Wilcox-Adelman S., Sano Y., Tang W.J., Collier R.J., and Park J.M. Antiinflammatory cAMP signaling and cell migration genes co-opted by the anthrax bacillus. Proc. Natl. Acad. Sci. USA 105 16 (2008) 6150-6155
29. Knowles J.R. Enzyme catalysis: not different, just better. Nature 350 6314 (1991) 121-124
30. Kuo S.R., Willingham M.C., Bour S.H., Andreas E.A., Park S.K., Jackson C., Duesbery N.S., Leppla S.H., Tang W.J., and Frankel A.E. Anthrax toxin-induced shock in rats is associated with pulmonary edema and hemorrhage. Microb. Pathog. 44 6 (2008) 467-472
31. Ladant D., and Ullmann A. Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol. 7 4 (1999) 172-176
32. Lee Y.S., Bergson P., He W.S., Mrksich M., and Tang W.J. Discovery of a small molecule that inhibits the interaction of anthrax edema factor with its cellular activator, calmodulin. Chem. Biol. 11 8 (2004) 1139-1146
33. Leppla S.H. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. USA 79 10 (1982) 3162-3166
34. Leppla S.H. Bacillus anthracis calmodulin-dependent adenylate cyclase: chemical and enzymatic properties and interactions with eucaryotic cells. Adv. Cyclic. Nucl. Prot. Phosphoryl. Res. 17 (1984) 189-198
35. Linder J.U. Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell. Mol. Life Sci. 63 15 (2006) 1736-1751
36. Maldonado-Arocho F.J., Fulcher J.A., Lee B., and Bradley K.A. Anthrax oedema toxin induces anthrax toxin receptor expression in monocyte-derived cells. Mol. Microbiol. 61 2 (2006) 324-337
37. 2+/calmodulin. EMBO J. 23 (2004) 712-718
38. Mattoo S., Foreman-Wykert A.K., Cotter P.A., and Miller J.F. Mechanisms of Bordetella pathogenesis. Front. Biosci. 6 (2001) e168-e186
39. + channels and calmodulin. J. Physiol. 554 Pt 2 (2004) 255-261
40. Moayeri M., Haines D., Young H.A., and Leppla S.H. Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J. Clin. Invest. 112 5 (2003) 670-682
41. Mock M., Labruyere E., Glaser P., Danchin A., and Ullmann A. Cloning and expression of the calmodulin-sensitive Bacillus anthracis adenylate cyclase in Escherichia coli. Gene 64 2 (1988) 277-284
42. O'Brien J., Friedlander A., Dreier T., Ezzell J., and Leppla S.H. Effects of anthrax toxin components on human neutrophils. Infect. Immun. 47 1 (1985) 306-310
43. Paccani S.R., Tonello F., Ghittoni R., Natale M., Muraro L., d'elios M.M., Tang W.-J., Montecucco C., and Baldari C.T. Anthrax toxins suppress T-lymphocyte activation by disrupting antigen receptor signaling. J. Exp. Med. 201 (2005) 325-331
44. Pezard C., Berche P., and Mock M. Contribution of individual toxin components to virulence of Bacillus anthracis. Infect. Immun. 59 10 (1991) 3472-3477
45. Puhar A., Dal Molin F., Horvath S., Ladants D., and Montecucco C. Anthrax edema toxin modulates PKA- and CREB-dependent signaling in two phases. PLoS ONE 3 10 (2008) e3564
46. Rogel A., Meller R., and Hanski E. Adenylate cyclase toxin from Bordetella pertussis. The relationship between induction of cAMP and hemolysis. J. Biol. Chem. 266 5 (1991) 3154-3161
47. Rossi Paccani S., Tonello F., Patrussi L., Capitani N., Simonato M., Montecucco C., and Baldari C.T. Anthrax toxins inhibit immune cell chemotaxis by perturbing chemokine receptor signalling. Cell. Microbiol. 9 4 (2007) 924-929
48. 2+/calmodulin. Nature 410 (2001) 1120-1124
49. Shen Y., Lee Y.S., Soelaiman S., Bergson P., Lu D., Chen A., Beckingham K., Grabarek Z., Mrksich M., and Tang W.J. Physiological calcium concentrations regulate calmodulin binding and catalysis of adenylyl cyclase exotoxins. EMBO J. 21 24 (2002) 6721-6732
50. Shen Y., Zhukovskaya N.L., Guo Q., Florian J., and Tang W.J. Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor. EMBO J. 24 5 (2005) 929-941
51. Shen Y., Zhukovskaya N.L., Zimmer M.I., Soelaiman S., Bergson P., Wang C.R., Gibbs C.S., and Tang W.J. Selective inhibition of anthrax edema factor by adefovir, a drug for chronic hepatitis B virus infection. Proc. Natl. Acad. Sci. USA 101 9 (2004) 3242-3247
52. Smith H., and Keppie J. Observations on experimental anthrax; demonstration of a specific lethal factor produced in vivo by Bacillus anthracis. Nature 173 4410 (1954) 869-870
53. Soelaiman S., Wei B.Q., Bergson P., Lee Y.S., Shen Y., Mrksich M., Shoichet B.K., and Tang W.J. Structure-based inhibitor discovery against adenylyl cyclase toxins from pathogenic bacteria that cause anthrax and whooping cough. J. Biol. Chem. 278 28 (2003) 25990-25997
54. Stanley J.L., Sargeant K., and Smith H. Purification of factors I and II of the anthrax toxin produced in vivo. J. Gen. Microbiol. 22 (1960) 206-218
55. Steegborn C., Litvin T.N., Levin L.R., Buck J., and Wu H. Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat. Struct. Mol. Biol. 12 1 (2005) 32-37
56. Steitz T.A. A mechanism for all polymerases. Nature 391 6664 (1998) 231-232
57. Sunahara R.K., and Taussig R. Isoforms of mammalian adenylyl cyclase: multiplicities of signaling. Mol. Interv. 2 3 (2002) 168-184
58. Szarowicz S.E., During R.L., Li W., Quinn C.P., Tang W.J., and Southwick F.S. Bacillus anthracis edema toxin impairs neutrophil actin-based motility. Infect Immun. 77 (2009) 2455-2464
59. Tang W.J., and Hurley J.H. Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol. Pharmacol. 54 2 (1998) 231-240
60. Tesmer J.J., Sunahara R.K., Gilman A.G., and Sprang S.R. Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsalpha.GTPgammaS. Science 278 5345 (1997) 1907-1916
61. Tesmer J.J., Sunahara R.K., Johnson R.A., Gosselin G., Gilman A.G., and Sprang S.R. Two-metal-Ion catalysis in adenylyl cyclase. Science 285 5428 (1999) 756-760
62. Tessier J., Green C., Padgett D., Zhao W., Schwartz L., Hughes M., and Hewlett E. Contributions of histamine, prostanoids, and neurokinins to edema elicited by edema toxin from Bacillus anthracis. Infect. Immun. 75 4 (2007) 1895-1903
63. Tews I., Findeisen F., Sinning I., Schultz A., Schultz J.E., and Linder J.U. The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 308 5724 (2005) 1020-1023
64. Tournier J.N., Quesnel-Hellmann A., Mathieu J., Montecucco C., Tang W.J., Mock M., Vidal D.R., and Goossens P.L. Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J. Immunol. 174 8 (2005) 4934-4941
65. Ulmer T.S., Soelaiman S., Li S., Klee C.B., Tang W.J., and Bax A. Calcium dependence of the interaction between calmodulin and anthrax edema factor. J. Biol. Chem. 278 31 (2003) 29261-29266
66. Watson L.E., Kuo S.R., Katki K., Dang T., Park S.K., Dostal D.E., Tang W.J., Leppla S.H., and Frankel A.E. Anthrax toxins induce shock in rats by depressed cardiac ventricular function. PLoS ONE 2 5 (2007) e466
67. Watson L.E., Mock J., Lal H., Lu G., Bourdeau R.W., Tang W.J., Leppla S.H., Dostal D.E., and Frankel A.E. Lethal and edema toxins of anthrax induce distinct hemodynamic dysfunction. Front. Biosci. 12 (2007) 4670-4675
68. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87 3 (2007) 965-1010
69. Wolff J., Cook G.H., Goldhammer A.R., and Berkowitz S.A. Calmodulin activates prokaryotic adenylate cyclase. Proc. Natl. Acad. Sci. USA 77 7 (1980) 3841-3844
70. Yahr, T.L., Vallis, A.J., Hancock, M.K., Barbieri, J.T., Frank, D.W., 1998. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. USA 95 (23), 13899-13904.
71. 2+-calmodulin. Nat. Struct. Biol. 10 (2003) 226-231
72. Yap K.L., Yuan T., Mal T.K., Vogel H.J., and Ikura M. Structural basis for simultaneous binding of two carboxy-terminal peptides of plant glutamate decarboxylase to calmodulin. J. Mol. Biol. 328 (2003) 193-204
73. Young J.A., and Collier R.J. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76 (2007) 243-265