Cytidylyl and uridylyl cyclase activity of bacillus anthracis edema factor and bordetella pertussis CyaA

Biochemistry

Volumn 49, Issue 26, 2010, Pages 5494-5503

  Göttle, Martin ^a   Dove, Stefan ^a   Kees, Frieder ^a   Schlossmann, Jens ^a   Geduhn, Jens ^a   König, Burkhard ^a   Shen, Yuequan ^b   Tang, Wei Jen ^c   Kaever, Volkhard ^d   Seifert, Roland ^d  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b NANKAI UNIVERSITY   (China)

^c UNIVERSITY OF CHICAGO   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLYL CYCLASE; BACILLUS ANTHRACIS; BACTERIAL TOXIN; CELL-PERMEABLE; CYCLASE ACTIVITY; CYCLASES; CYCLIC ADENOSINE; CYCLIC NUCLEOTIDE; CYTIDINE; EDEMA FACTORS; GUANOSINES; HUMAN NEUTROPHIL; IMMUNE RESPONSE; MAMMALIAN CELL FUNCTION; MONOPHOSPHATES; SECOND MESSENGER; SUBSTRATE SPECIFICITY; SUPEROXIDE PRODUCTION;

BACTERIOLOGY; FETAL MONITORING; LIQUID CHROMATOGRAPHY; MAMMALS; MASS SPECTROMETRY; METABOLITES; NUCLEOTIDES; OXYGEN; TOXIC MATERIALS;

SUBSTRATES;

ADENYLATE CYCLASE; BACTERIAL ENZYME; BACTERIAL TOXIN; CYCLIC CMP; CYCLIC NUCLEOTIDE; CYTIDYLYL CYCLASE; EDEMA FACTOR; LYASE; UNCLASSIFIED DRUG; URIDYLYL CYCLASE;

ARTICLE; BACILLUS ANTHRACIS; BORDETELLA PERTUSSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; RADIOMETRY;

ADENYLATE CYCLASE TOXIN; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CYCLIC AMP; HUMANS; IMMUNITY; NUCLEOTIDES, CYCLIC; PHOSPHORUS-OXYGEN LYASES; SUBSTRATE SPECIFICITY; URIDINE MONOPHOSPHATE;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS; MAMMALIA;

EID: 77954178718     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100684g     Document Type: Article

References (36)

1. Bloch, A., Dutschman, G., and Maue, R. (1974) Cytidine 3′,5′-monophosphate (cyclic CMP). II. Initiation of leukemia L-1210 cell growth in vitro Biochem. Biophys. Res. Commun. 59, 955-959
2. Cech, S. Y. and Ignarro, L. J. (1978) Cytidine 3′,5′- monophosphate (cyclic CMP) formation by homogenates of mouse liver Biochem. Biophys. Res. Commun. 80, 119-125
3. Gaion, R. M. and Krishna, G. (1979) Cytidylate cyclase: The product isolated by the method of Cech and Ignarro is not cytidine 3′,5′- monophosphate Biochem. Biophys. Res. Commun. 86, 105-111
4. Newton, R. P., Salih, S. G., Salvage, B. J., and Kingston, E. E. (1984) Extraction, purification and identification of cytidine 3′,5′-cyclic monophosphate from rat tissues Biochem. J. 221, 665-673
5. Newton, R. P., Salvage, B. J., and Hakeem, N. A. (1990) Cytidylate cyclase: Development of assay and determination of kinetic properties of a cytidine 3′,5′-cyclic monophosphate-synthesizing enzyme Biochem. J. 265, 581-586
6. Newton, R. P., Groot, N., van Geyschem, J., Diffley, P. E., Walton, T. J., Bayliss, M. A., Harris, F. M., Games, D. E., and Brenton, A. G. (1997) Estimation of cytidylyl cyclase activity and monitoring of side-product formation by fast-atom bombardment mass spectrometry Rapid Commun. Mass Spectrom. 11, 189-194 (Pubitemid 27155380)
7. Newton, R. P., Bayliss, M. A., Khan, J. A., Bastani, A., Wilkins, A. C., Games, D. E., Walton, T. J., Brenton, A. G., and Harris, F. M. (1999) Kinetic analysis of cyclic CMP-specific and multifunctional phosphodiesterases by quantitative positive-ion fast-atom bombardment mass spectrometry Rapid Commun. Mass Spectrom. 13, 574-584
8. Bond, A. E., Dudley, E., Tuytten, R., Lemiere, F., Smith, C. J., Esmans, E. L., and Newton, R. P. (2007) Mass spectrometric identification of rab23 phosphorylation as a response to challenge by cytidine 3′,5′-cyclic monophosphate in mouse brain Rapid Commun. Mass Spectrom. 21, 2685-2692
9. Ding, S., Bond, A. E., Lemiere, F., Tuytten, R., Esmans, E. L., Brenton, A. G., Dudley, E., and Newton, R. P. (2008) Online immobilized metal affinity chromatography/mass spectrometric analysis of changes elicited by cCMP in the murine brain phosphoproteome Rapid Commun. Mass Spectrom. 22, 4129-4138
10. 4 synthesis Agents Actions 32, 90-91
11. 4,2′- O -dibutyryl cytidine 3′:5′-cyclic monophosphate of neutrophil activation Biochem. Biophys. Res. Commun. 174, 258-267
12. Newton, R. P., Kingston, E. E., Hakeem, N. A., Salih, S. G., Beynon, J. H., and Moyse, C. D. (1986) Extraction, purification, identification and metabolism of 3′,5′-cyclic UMP, 3′,5′-cyclic IMP and 3′,5′-cyclic dTMP from rat tissues Biochem. J. 236, 431-439
13. Ahuja, N., Kumar, P., and Bhatnagar, R. (2004) The adenylate cyclase toxins Crit. Rev. Microbiol. 30, 187-196
14. Ladant, D. and Ullmann, A. (1999) Bordetella pertussis adenylate cyclase: A toxin with multiple talents Trends Microbiol. 7, 172-176
15. Drum, C. L., Yan, S. Z., Sarac, R., Mabuchi, Y., Beckingham, K., Bohm., A., Grabarek, Z., and 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
16. 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
17. Hewlett, E. L., Donato, G. M., and Gray, M. C. (2006) Macrophage cytotoxicity produced by adenylate cyclase toxin from Bordetella pertussis: More than just making cyclic AMP! Mol. Microbiol. 59, 447-459
18. Paccani, S. R., Tonello, F., Ghittoni, R., Natale, M., Muraro, L., DElios, M. M., Tang, W. J., Montecucco, C., and Baldari, C. T. (2005) Anthrax toxins suppress T lymphocyte activation by disrupting antigen receptor signalling J. Exp. Med. 201, 325-331
19. Tournier, J. N., Quesnel-Hellmann, A., Mathieu, J., Montecucco, C., Tang, W. J., Mock, M., Vidal, D. R., and Goossens, P. L. (2005) Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells J. Immunol. 174, 4934-4941
20. Johnson, R. A. and Shoshani, I. (1990) Inhibition of Bordetella pertussis and Bacillus anthracis adenylyl cyclases by polyadenylate and P-site agonists J. Biol. Chem. 265, 19035-19039
21. Gille, A., Lushington, G. H., Mou, T. C., Doughty, M. B., Johnson, R. A., and Seifert, R. (2004) Differential inhibition of adenylyl cyclase isoforms and soluble guanylyl cyclase by purine and pyrimidine nucleotides J. Biol. Chem. 279, 19955-19969
22. Mou, T. C., Gille, A., Fancy, D. A., Seifert, R., and Sprang, S. R. (2005) Structural basis for the inhibition of mammalian membrane adenylyl cyclase by 2′(3′)- O -(N -Methylanthraniloyl)-guanosine 5′-triphosphate J. Biol. Chem. 280, 7253-7261
23. Mou, T. C., Gille, A., Suryanarayana, S., Richter, M., Seifert, R., and Sprang, S. R. (2006) Broad specificity of mammalian adenylyl cyclase for interaction with 2′,3′-substituted purine- and pyrimidine nucleotide inhibitors Mol. Pharmacol. 70, 878-886
24. Gille, A. and Seifert, R. (2003) 2′(3′)- O -(N -methylanthraniloyl)-substituted GTP analogs: A novel class of potent competitive adenylyl cyclase inhibitors J. Biol. Chem. 278, 12672-12679
25. Shen, Y., Zhukovskaya, N. L., Zimmer, M. I., Soelaiman, S., Bergson, P., Wang, C. R., Gibbs, C. S., and Tang, W. J. (2004) Selective inhibition of anthrax edema factor by adefovir, a drug for chronic hepatitis B virus infection Proc. Natl. Acad. Sci. U.S.A. 101, 3242-3247
26. Göttle, M., Dove, S., Steindel, P., Shen, Y., Tang, W. J., Geduhn, J., König, B., and Seifert, R. (2007) Molecular analysis of the interaction of Bordetella pertussis adenylyl cyclase with fluorescent nucleotides Mol. Pharmacol. 72, 526-535
27. 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
28. 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
29. Taha, H. M., Schmidt, J., Göttle, M., Suryanarayana, S., Shen, Y., Tang, W. J., Gille, A., Geduhn, J., König, B., Dove, S., and Seifert, R. (2009) Molecular analysis of the interaction of anthrax adenylyl cyclase toxin, edema factor, with 2′(3′)- O -(N -(methyl)anthraniloyl)-substituted purine and pyrimidine nucleotides Mol. Pharmacol. 75, 693-703
30. Drum, C. L., Shen, Y., Rice, P. A., Bohm, A., and Tang, W. J. (2001) Crystallization and preliminary X-ray study of the edema factor exotoxin adenylyl cyclase domain from Bacillus anthracis in the presence of its activator, calmodulin Acta Crystallogr. D57, 1881-1884
31. Alvarez, R. and Daniels, D. V. (1990) A single column method for the assay of adenylate cyclase Anal. Biochem. 187, 98-103
32. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M. J., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins and nucleic acids J. Am. Chem. Soc. 117, 5179-5197
33. Zea, C. J., Camci-Unal, G., and Pohl, N. L. (2008) Thermodynamics of binding of divalent magnesium and manganese to uridine phosphates: Implications for diabetes-related hypomagnesaemia and carbohydrate biocatalysis Chem. Cent. J. 2, 15
34. Sinha, S. C., Wetterer, M., Sprang, S. R., Schultz, J. E., and Linder, J. U. (2005) Origin of asymmetry in adenylyl cyclases: Structures of Mycobacterium tuberculosis Rv1900c EMBO J. 24, 663-673
35. Dessauer, C. W., Scully, T. T., and Gilman, A. G. (1997) Interactions of forskolin and ATP with the cytosolic domains of mammalian adenylyl cyclase J. Biol. Chem. 272, 22272-22277
36. Suryanarayana, S., Göttle, M., Hübner, M., Gille, A., Mou, T.-C., Sprang, S. R., Richter, M., and Seifert, R. (2009) Differential inhibition of various adenylyl cyclase isoforms and soluble guanylyl cyclase by 2′,3′- O -(2,4,6-trinitrophenyl)-substituted nucleoside 5′-triphosphates J. Pharmacol. Exp. Ther. 330, 687-695