FK506-binding protein 51 interacts with Clostridium botulinum C2 toxin and FK506 inhibits membrane translocation of the toxin in mammalian cells

Cellular Microbiology

Volumn 14, Issue 8, 2012, Pages 1193-1205

  Kaiser, Eva ^a   Böhm, Natalie ^a   Ernst, Katharina ^a   Langer, Simon ^a   Schwan, Carsten ^b   Aktories, Klaus ^b   Popoff, Michel ^c   Fischer, Gunter ^d   Barth, Holger ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c INSTITUT PASTEUR   (France)

^d MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN; CLOSTRIDIUM DIFFICILE TOXIN A; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 51; HEAT SHOCK PROTEIN 90; ISOMERASE INHIBITOR; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM PERFRINGENS TYPE A; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; IN VITRO STUDY; INTOXICATION; MAMMAL CELL; MEMBRANE TRANSPORT; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANIMALS; BOTULINUM TOXINS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; PROTEIN BINDING; TACROLIMUS; TACROLIMUS BINDING PROTEINS; VERO CELLS;

CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM PERFRINGENS; EUKARYOTA; MAMMALIA;

EID: 84863992806     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01788.x     Document Type: Article

References (51)

1. Aktories, K., Bärmann, M., Ohishi, I., Tsuyama, S., Jakobs, K.H., and Habermann, E. (1986) Botulinum C2 toxin ADP-ribosylates actin. Nature 322: 390-392.
2. Barth, H. (2011) Exploring the role of host cell chaperones/PPIases during cellular up-take of bacterial ADP-ribosylating toxins as basis for novel pharmacological strategies to protect mammalian cells against these virulence factors. Naunyn Schmiedebergs Arch Pharmacol 383: 237-245.
3. Barth, H., and Stiles, B.G. (2008) Binary actin-ADP-ribosylating toxins and their use as molecular Trojan horses for drug delivery into eukaryotic cells. Curr Med Chem 15: 459-469.
4. Barth, H., Hofmann, F., Olenik, C., Just, I., and Aktories, K. (1998) The N-terminal part of the enzyme component (C2I) of the binary Clostridium botulinum C2 toxin interacts with the binding component C2II and functions as a carrier system for a Rho ADP-ribosylating C3-like fusion toxin. Infect Immun 66: 1364-1369.
5. Barth, H., Blöcker, D., Behlke, J., Bergsma-Schutter, W., Brisson, A., Benz, R., and Aktories, K. (2000) Cellular uptake of Clostridium botulinum C2 toxin requires oligomerization and acidification. J Biol Chem 275: 18704-18711.
6. Barth, H., Roebling, R., Fritz, M., and Aktories, K. (2002) The binary Clostridium botulinum C2 toxin as a protein delivery system: identification of the minimal protein region necessary for interaction of toxin components. J Biol Chem 277: 5074-5081.
7. Blöcker, D., Barth, H., Maier, E., Benz, R., Barbieri, J.T., and Aktories, K. (2000) The C-terminus of component C2II of Clostridium botulinum C2 toxin is essentiell for receptor binding. Infect Immun 68: 4566-4573.
8. Blöcker, D., Bachmeyer, C., Benz, R., Aktories, K., and Barth, H. (2003a) Channel formation by the binding component of Clostridium botulinum C2 toxin: glutamate 307 of C2II affects channel properties in vitro and pH-dependent C2I translocation in vivo. Biochemistry 42: 5368-5377.
9. Blöcker, D., Pohlmann, K., Haug, G., Bachmeyer, C., Benz, R., Aktories, K., and Barth, H. (2003b) Clostridium botulinum C2 toxin: low pH-induced pore formation is required for translocation of the enzyme component C2I into the cytosol of host cells. J Biol Chem 278: 32266-32274.
10. Callebaut, I., Renoir, J.M., Lebeau, M.C., Massol, N., Burny, A., Baulieu, E.E., and Mornon, J.P. (1992) An immunophilin that binds M(r) 90, 000 heat shock protein: main structural features of a mammalian p59 protein. Proc Natl Acad Sci USA 89: 6270-6274.
11. Chambraud, B., Rouvière-Fourmy, N., Radanyi, C., Hsiao, K., Peattie, D.A., Livingston, D.J., and Baulieu, E.E. (1993) Overexpression of p59-HBI (FKBP59), full length and domains, and characterization of PPlase activity. Biochem Biophys Res Commun 196: 160-166.
12. Dmochewitz, L., Lillich, M., Kaiser, E., Jennings, L.D., Lang, A.E., Buchner, J., etal. (2011) Role of CypA and Hsp90 in membrane translocation mediated by anthrax protective antigen. Cell Microbiol 13: 359-373.
13. Eckhardt, M., Barth, H., Blöcker, D., and Aktories, K. (2000) Binding of Clostridium botulinum C2 toxin to asparagine-linked complex and hybrid carbohydrates. J Biol Chem 275: 2328-2334.
14. Edlich, F., Weiwad, M., Wildemann, D., Jarczowski, F., Kilka, S., Moutty, M.C., etal. (2006) The specific FKBP38 inhibitor N-(N, N-dimethylcarboxamidomethyl)cycloheximide has potent neuroprotective and neurotrophic properties in brain ischemia. J Biol Chem 281: 14961-14970.
15. Fahrer, J., Plunien, R., Binder, U., Langer, T., Seliger, H., and Barth, H. (2010) Genetically engineered clostridial C2 toxin as a novel delivery system for living mammalian cells. Bioconjug Chem 21: 130-139.
16. Fischer, G., Bang, H., and Mech, C. (1984) Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides. Biomed Biochim Acta 43: 1101-1111.
17. Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F.X. (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337: 476-478.
18. Galat, A. (2003) Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity-targets-functions. Curr Top Med Chem 3: 1315-1347.
19. Handschumacher, R.E., Harding, M.W., Rice, J., Drugge, R.J., and Speicher, D.W. (1984) Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226: 544-547.
20. Haug, G., Wilde, C., Leemhuis, J., Meyer, D.K., Aktories, K., and Barth, H. (2003a) Cellular uptake of Clostridium botulinum C2 toxin: membrane translocation of a fusion toxin requires unfolding of its dihydrofolate reductase domain. Biochemistry 42: 15284-15291.
21. Haug, G., Leemhuis, J., Tiemann, D., Meyer, D.K., Aktories, K., and Barth, H. (2003b) The host cell chaperone Hsp90 is essential for translocation of the binary Clostridium botulinum C2 toxin into the cytosol. J Biol Chem 278: 32266-32274.
22. Haug, G., Aktories, K., and Barth, H. (2004) The host cell chaperone Hsp90 is necessary for cytotoxic action of the binary iota-like toxins. Infect Immun 72: 3066-3068.
23. Heine, K., Pust, S., Enzenmüller, S., and Barth, H. (2008) ADP-ribosylation of actin by Clostridium botulinum C2 toxin in mammalian cells results in delayed caspase-dependent apoptotic cell death. Infect Immun 76: 4600-4608.
24. Holownia, A., Mroz, R.M., Kolodziejczyk, A., Chyczewska, E., and Braszko, J.J. (2009) Increased FKBP51 in induced sputum cells of chronic obstructive pulmonary disease patients after therapy. Eur J Med Res 14: 108-111.
25. Just, I., Wilm, M., Selzer, J., Rex, G., Von Eichel-Streiber, C., Mann, M., and Aktories, K. (1995) The enterotoxin from Clostridium difficile (ToxA) monoglucosylates the Rho proteins. J Biol Chem 270: 13932-13936.
26. Kaiser, E., Pust, S., Kroll, C., and Barth, H. (2009) Cyclophilin A facilitates translocation of the Clostridium botulinum C2 toxin across membranes of acidified endosomes into the cytosol of mammalian cells. Cell Microbiol 11: 780-795.
27. Kaiser, E., Kroll, C., Ernst, K., Schwan, C., Popoff, M.R., Fischer, G., etal. (2011) Membrane translocation of binary actin-ADP-ribosylating toxins from Clostridium difficile and Clostridium perfringens is facilitated by Cyclophilin A and Hsp90. Infect Immun 79: 3913-3921.
28. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
29. Lang, K., Schmid, F.X., and Fischer, G. (1987) Catalysis of protein folding by prolyl isomerase. Nature 329: 268-270.
30. Mamane, Y., Sharma, S., Petropoulos, L., Lin, R., and Hiscott, J. (2000) Posttranslational regulation of IRF-4 activity by the immunophilin FKBP52. Immunity 12: 129-140.
31. Ni, L., Yang, C.S., Gioeli, D., Frierson, H., Toft, D.O., and Paschal, B.M. (2010) FKBP51 promotes assembly of the Hsp90 chaperone complex and regulates androgen receptor signaling in prostate cancer cells. Mol Cell Biol 30: 1243-1253.
32. Ohishi, I., Iwasaki, M., and Sakaguchi, G. (1980) Purification and characterization of two components of botulinum C2 toxin. Infect Immun 30: 668-673.
33. Papatheodorou, P., Zamboglou, C., Genisyuerek, S., Guttenberg, G., and Aktories, K. (2010) Clostridial glucosylating toxins enter cells via clathrin-mediated endocytosis. PLoS ONE 5: e10673.
34. Perelle, S., Domenighini, M., and Popoff, M.R. (1996) Evidence that Arg-295, Glu-378, and Glu-380 are active-site residues of the ADP-ribosyltransferase activity of iota toxin. FEBS Lett 395: 191-194.
35. Periyasamy, S., Warrier, M., Tillekeratne, M.P., Shou, W., and Sanchez, E.R. (2007) The immunophilin ligands cyclosporin a and FK506 suppress prostate cancer cell growth by androgen receptor-dependent and -independent mechanisms. Endocrinology 148: 4716-4726.
36. Pirkl, F., and Buchner, J. (2001) Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. J Mol Biol 308: 795-806.
37. Popoff, M.R., and Boquet, P. (1988) Clostridium spiroforme toxin is a binary toxin which ADP- ribosylates cellular actin. Biochem Biophys Res Commun 152: 1361-1368.
38. Pratt, W.B., and Toft, D.O. (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18: 306-360.
39. Pust, S., Barth, H., and Sandvig, K. (2010) Clostridium botulinum C2 toxin is internalized by clathrin- and Rho-dependent mechanisms. Cell Microbiol 12: 1809-1820.
40. Ratts, R., Zeng, H., Berg, E.A., Blue, C., McComb, M.E., Costello, C.E., etal. (2003) The cytosolic entry of diphtheria toxin catalytic domain requires a host cell cytosolic translocation factor complex. J Cell Biol 160: 1139-1150.
41. Schleberger, C., Hochmann, H., Barth, H., Aktories, K., and Schulz, G.E. (2006) Structure and action of the binary C2 toxin from Clostridium botulinum. J Mol Biol 364: 705-715.
42. Schmid, F.X. (1993) Prolyl isomerase: enzymatic catalysis of slow protein-folding reactions. Annu Rev Biophys Biomol Struct 22: 123-142.
43. Schmid, F.X., Mayr, L.M., Mucke, M., and Schonbrunner, E.R. (1993) Prolyl isomerases: role in protein folding. Adv Protein Chem 44: 25-66.
44. Stechschulte, L.A., and Sanchez, E.R. (2011) FKBP51- a selective modulator of glucocorticoid and androgen sensitivity. Curr Opin Pharmacol 11: 332-337.
45. Stiles, B.G., and Wilkens, T.D. (1986) Purification and characterization of Clostridium perfringens iota toxin: dependence on two nonlinked proteins for biological activity. Infect Immun 54: 683-688.
46. Vandekerckhove, J., Schering, B., Bärmann, M., and Aktories, K. (1988) Botulinum C2 toxin ADP-ribosylates cytoplasmic β/γ-actin in arginine 177. J Biol Chem 263: 696-700.
47. Wang, P., and Heitman, J. (2005) The cyclophilins. Genome Biol 6: 226.
48. Weiwad, M., Edlich, F., Kilka, S., Erdmann, F., Jarczowski, F., Dorn, M., etal. (2006) Comparative analysis of calcineurin inhibition by complexes of immunosuppressive drugs with human FK506 binding proteins. Biochemistry 45: 15776-15784.
49. Wiedlocha, A., Nilsen, T., Wesche, J., Sorensen, V., Malecki, J., Marcinkowska, E., and Olsnes, S. (2005) Phosphorylation-regulated nucleocytoplasmic trafficking of internalized fibroblast growth factor-1. Mol Biol Cell 16: 794-810.
50. Wiegers, W., Just, I., Müller, H., Hellwig, A., Traub, P., and Aktories, K. (1991) Alteration of the cytoskeleton of mammalian cells cultured in vitro by Clostridium botulinum C2 toxin and C3 ADP-ribosyltransferase. Eur J Cell Biol 54: 237-245.
51. Woodruff, P.G., Boushey, H.A., Dolganov, G.M., Barker, C.S., Yang, Y.H., Donnelly, S., etal. (2007) Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids. Proc Natl Acad Sci USA 104: 15858-15863.