Anthrax edema toxin modulates PKA- and CREB- dependent signaling in two phases

PLoS ONE

Volumn 3, Issue 10, 2008, Pages

  Puhar, Andrea ^a,b   Dal Molin, Federica ^a   Horvath, Stéphanie ^a   Landants, Daniel ^b   Montecucco, Cesare ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE TOXIN; ANTHRAX EDEMA TOXIN; CHOLERA TOXIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FORSKOLIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PERTUSSIS TOXIN; PROTEIN P90; S6 KINASE; STRESS ACTIVATED PROTEIN KINASE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; ADENYLATE CYCLASE; CREB1 PROTEIN, HUMAN; CYCLIC AMP; EDEMA FACTOR, BACTERIAL;

ANTHRAX; ARTICLE; BINDING SITE; CELL LEVEL; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; T LYMPHOCYTE ACTIVATION; DNA RESPONSIVE ELEMENT; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYME SPECIFICITY; METABOLISM; PHOSPHORYLATION; PROTEIN BINDING; TIME; TRANSCRIPTION INITIATION;

BORDETELLA PERTUSSIS;

ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FORSKOLIN; GENES, REPORTER; HUMANS; JURKAT CELLS; PHOSPHORYLATION; PROTEIN BINDING; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 55849114413     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003564     Document Type: Article

References (66)

1. Swartz MN (2001) Recognition and management of anthrax-an update. N Engl J Med 345: 1621-1626.
2. Turnbull PC (2002) Introduction: anthrax history, disease and ecology. Curr Top Microbiol Immunol 271: 1-19.
3. Burnett JC, Henchal EA, Schmaljohn AL, Bavari S (2005) The evolving field of biodefence: therapeutic developments and diagnostics. Nat Rev Drug Discov 4: 281-297.
4. Fouet A, Mock M (2006) Regulatory networks for virulence and persistence of Bacillus anthracis. Curr Opin Microbiol 9: 160-166.
5. Young JA, Collier RJ (2007) Anthrax Toxin: Receptor Binding, Internalization, Pore Formation, and Translocation. Annu Rev Biochem 76: 243-265.
6. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA (2001) Identification of the cellular receptor for anthrax toxin. Nature 414: 225-229.
7. Scobie HM, Rainey GJ, Bradley KA, Young JA (2003) Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci USA 100: 5170-5174.
8. Wei W, Lu Q, Chaudry GJ, Leppla SH, Cohen SN (2006) The LDL receptor-related protein LRP6 mediates internalization and lethality of anthrax toxin. Cell 124: 1141-1154.
9. Young JJ, Bromberg-White JL, Zylstra C, Church JT, Boguslawski E, et al. (2007) LRP5 and LRP6 are not required for protective antigen-mediated internalization or lethality of anthrax lethal toxin. PLoS Pathog 3: e27 doi:10.1371/journal.ppat.0030027.
10. Ryan PL, Young JA (2008) Evidence against a human cell-specific role for LRP6 in anthrax toxin entry. PLoS ONE 3: e1817.
11. Krantz BA, Melnyk RA, Zhang S, Juris SJ, Lacy DB, et al. (2005) A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309: 777-781.
12. Rainey GJ, Wigelsworth DJ, Ryan PL, Scobie HM, Collier RJ, et al. (2005) Receptor-specific requirements for anthrax toxin delivery into cells. Proc Natl Acad Sci USA 102: 13278-13283.
13. Abrami L, Lindsay M, Parton RG, Leppla SH, van der Goot FG (2004) Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway. J Cell Biol 166: 645-651.
14. 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.
15. Puhar A, Montecucco C (2007) Where and how do anthrax toxins exit endosomes to intoxicate host cells? Trends Microbiol 15: 477-482.
16. Dal Molin F, Tonello F, Ladant D, Zornetta I, Zamparo I, et al. (2006) Cell entry and cAMP imaging of anthrax edema toxin. EMBO J 25: 5405-5413.
17. Guidi-Rontani C, Weber-Levy M, Mock M, Cabiaux V (2000) Translocation of Bacillus anthracis lethal and oedema factors across endosome membranes. Cell Microbiol 2: 259-264.
18. Baldari CT, Tonello F, Paccani SR, Montecucco C (2006) Anthrax toxins: A paradigm of bacterial immune suppression. Trends Immunol 27: 434-440.
19. Turk BE (2007) Manipulation of host signalling pathways by anthrax toxins. Biochem J 402: 405-417.
20. Vitale G, Bernardi L, Napolitani G, Mock M, Montecucco C (2000) Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem J 352 Pt 3: 739-745.
21. Firoved AM, Miller GF, Moayeri M, Kakkar R, Shen Y, et al. (2005) Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am J Pathol 167: 1309-1320.
22. Comer JE, Chopra AK, Peterson JW, Konig R (2005) Direct inhibition of T-lymphocyte activation by anthrax toxins in vivo. Infect Immun 73: 8275-8281.
23. + T cells. J Immunol 174: 4966-4971.
24. Paccani SR, Tonello F, Ghittoni R, Natale M, Muraro L, et al. (2005) Anthrax toxins suppress T lymphocyte activation by disrupting antigen receptor signaling. J Exp Med 201: 325-331.
25. Rossi Paccani S, Tonello F, Patrussi L, Capitani N, Simonato M, et al. (2007) Anthrax toxins inhibit immune cell chemotaxis by perturbing chemokine receptor signalling. Cell Microbiol 9: 924-929.
26. Lissandron V, Terrin A, Collini M, D'Alfonso L, Chirico G, et al. (2005) Improvement of a FRET-based indicator for cAMP by linker design and stabilization of donor-acceptor interaction. J Mol Biol 354: 546-555.
27. Tonello F, Naletto L, Romanello V, Dal Molin F, Montecucco C (2004) Tyrosine-728 and glutamic acid-735 are essential for the metalloproteolytic activity of the lethal factor of Bacillus anthracis. Biochem Biophys Res Commun 313: 496-502.
28. Karimova G, Fayolle C, Gmira S, Ullmann A, Leclerc C, et al. (1998) Charge-dependent translocation of Bordetella pertussis adenylate cyclase toxin into eukaryotic cells: implication for the in vivo delivery of CD8(+) T cell epitopes into antigen-presenting cells. Proc Natl Acad Sci USA 95: 12532-12537.
29. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, et al. (1999) Short Protocols in Molecular Biology. Fourth Edition ed: John Wiley & Sons, Inc.
30. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
31. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
32. El-Azami-El-Idrissi M, Bauche C, Loucka J, Osicka R, Sebo P, et al. (2003) Interaction of Bordetella pertussis Adenylate Cyclase with CD11b/CD18: Role of Toxin Acylation and Identification of the Main Integrin Interaction Domain. J Biol Chem 278: 38514-38521.
33. Guermonprez P, Khelef N, Blouin E, Rieu P, Ricciardi-Castagnoli P, et al. (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.
34. Lauer S, Goldstein B, Nolan RL, Nolan JP (2002) Analysis of Cholera Toxin-Ganglioside Interactions by Flow Cytometry. Biochemistry 41: 1742-1751.
35. Scobie HM, Thomas D, Marlett JM, Destito G, Wigelsworth DJ, et al. (2005) A soluble receptor decoy protects rats against anthrax lethal toxin challenge. J Infect Dis 192: 1047-1051.
36. Wigelsworth DJ, Krantz BA, Christensen KA, Lacy DB, Juris SJ, et al. (2004) Binding stoichiometry and kinetics of the interaction of a human anthrax toxin receptor, CMG2, with protective antigen. J Biol Chem 279: 23349-23356.
37. Shen Y, Zhukovskaya NL, Zimmer MI, Soelaiman S, Bergson P, et al. (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.
38. Fimia GM, Sassone-Corsi P (2001) Cyclic AMP signalling. J Cell Sci 114: 1971-1972.
39. Johannessen M, Delghandi MP, Moens U (2004) What turns CREB on? Cell Signal 16: 1211-1227.
40. Johannessen M, Moens U (2007) Multisite phosphorylation of the cAMP response element-binding protein (CREB) by a diversity of protein kinases. Front Biosci 12: 1814-1832.
41. Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation- dependent factor CREB. Nat Rev Mol Cell Biol 2: 599-609.
42. Delghandi MP, Johannessen M, Moens U (2005) The cAMP signalling pathway activates CREB through PKA, p38 and MSK1 in NIH 3T3 cells. Cell Signal 17: 1343-1351.
43. Bos JL (2003) Epac: a new cAMP target and new avenues in cAMP research. Nat Rev Mol Cell Biol 4: 733-738.
44. Hong J, Doebele RC, Lingen MW, Quilliam LA, Tang WJ, et al. (2007) Anthrax edema toxin inhibits endothelial cell chemotaxis via Epac and Rap1. J Biol Chem 282: 19781-19787.
45. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105.
46. Hughes-Fulford M, Sugano E, Schopper T, Li CF, Boonyaratanakornkit JB, et al. (2005) Early immune response and regulation of IL-2 receptor subunits. Cell Signal 17: 1111-1124.
47. Muthusamy N, Leiden JM (1998) A protein kinase C-, Ras-, and RSK2- dependent signal transduction pathway activates the cAMP-responsive element-binding protein transcription factor following T cell receptor engagement. J Biol Chem 273: 22841-22847.
48. Kaiser M, Wiggin GR, Lightfoot K, Arthur JS, Macdonald A (2007) MSK regulate TCR-induced CREB phosphorylation but not immediate early gene transcription. Eur J Immunol 37: 2583-2595.
49. Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y (1996) The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87: 953-959.
50. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, et al. (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA 102: 4459-4464.
51. Abrahamsen H, Baillie G, Ngai J, Vang T, Nika K, et al. (2004) TCR- and CD28-mediated recruitment of phosphodiesterase 4 to lipid rafts potentiates TCR signaling. J Immunol 173: 4847-4858.
52. Kanda N, Watanabe S (2001) Regulatory roles of adenylate cyclase and cyclic nucleotide phosphodiesterases 1 and 4 in interleukin-13 production by activated human T cells. Biochem Pharmacol 62: 495-507.
53. Dal Molin F, Zornetta I, Puhar A, Tonello F, Zaccolo M, et al. (2008) cAMP imaging of cells treated with pertussis toxin, cholera toxin, and anthrax edema toxin. Biochem Biophys Res Commun 376: 429-433.
54. Baillie GS, Houslay MD (2005) Arrestin times for compartmentalised cAMP signalling and phosphodiesterase-4 enzymes. Curr Opin Cell Biol 17: 129-134.
55. Cooper DM (2005) Compartmentalization of adenylate cyclase and cAMP signalling. Biochem Soc Trans 33: 1319-1322.
56. Wong W, Scott JD (2004) AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5: 959-970.
57. Sayner S, Stevens T (2006) Soluble adenylate cyclase reveals the significance of compartmentalized cAMP on endothelial cell barrier function. Biochem Soc Trans 34: 492-494.
58. Sayner SL, Alexeyev M, Dessauer CW, Stevens T (2006) Soluble adenylyl cyclase reveals the significance of cAMP compartmentation on pulmonary microvascular endothelial cell barrier. Circ Res 98: 675-681.
59. Sayner SL, Frank DW, King J, Chen H, VandeWaa J, et al. (2004) Paradoxical cAMP-induced lung endothelial hyperpermeability revealed by Pseudomonas aeruginosa ExoY. Circ Res 95: 196-203.
60. del Carmen Castellanos M, Lopez-Giral S, Lopez-Cabrera M, de Landazuri MO (2002) Multiple cis-acting elements regulate the expression of the early T cell activation antigen CD69. Eur J Immunol 32: 3108-3117.
61. van Oirschot BA, Stahl M, Lens SM, Medema RH (2001) Protein kinase A regulates expression of p27(kip1) and cyclin D3 to suppress proliferation of leukemic T cell lines. J Biol Chem 276: 33854-33860.
62. Fuld S, Borland G, Yarwood SJ (2005) Elevation of cyclic AMP in Jurkat T-cells provokes distinct transcriptional responses through the protein kinase A (PKA) and exchange protein activated by cyclic AMP (EPAC) pathways. Exp Cell Res 309: 161-173.
63. Tasken K, Stokka AJ (2006) The molecular machinery for cAMP-dependent immunomodulation in T-cells. Biochem Soc Trans 34: 476-479.
64. Maldonado-Arocho FJ, Fulcher JA, Lee B, Bradley KA (2006) Anthrax oedema toxin induces anthrax toxin receptor expression in monocyte-derived cells. Mol Microbiol 61: 324-337.
65. Park JM, Greten FR, Wong A, Westrick RJ, Arthur JS, et al. (2005) Signaling pathways and genes that inhibit pathogen-induced macrophage apoptosis-CREB and NF-kappaB as key regulators. Immunity 23: 319-329.
66. Kim C, Wilcox-Adelman S, Sano Y, Tang WJ, Collier RJ, et al. (2008) Antiinflammatory cAMP signaling and cell migration genes co-opted by the anthrax bacillus. Proc Natl Acad Sci USA 105: 6150-6155.