Pore-forming activity of clostridial binary toxins

Biochimica et Biophysica Acta - Biomembranes

Volumn 1858, Issue 3, 2016, Pages 512-525

  Knapp, O ^a   Benz, R ^b   Popoff, M R ^a  

^a INSTITUT PASTEUR   (France)

^b JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

Bacillus anthracis toxins; Binary toxin; Clostridium botulinum C2 toxin; Clostridium difficile transferase; Clostridium spiroforme toxin; Iota toxin; Pore forming toxins

Indexed keywords

AEROLYSIN; ANTHRAX TOXIN; BACTERIAL TOXIN; CELL RECEPTOR; CHLOROQUINE; CHOLESTEROL; CLOSTRIDIUM BOTULINUM C2 TOXIN; CLOSTRIDIUM DIFFICILE TRANSFERASE; CLOSTRIDIUM PERFRINGENS IOTA TOXIN; CLOSTRIDIUM SPIROFORME TOXIN; CYCLODEXTRIN DERIVATIVE; CYTOLYSIN; EPSILON TOXIN; MEPACRINE; PORE FORMING TOXIN; UNCLASSIFIED DRUG; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PORE FORMING CYTOTOXIC PROTEIN;

ACTIN FILAMENT; ADENOSINE DIPHOSPHATE RIBOSYLATION; BACTERIAL STRAIN; BACTERIAL STRUCTURES; BACTERIAL VIRULENCE; CELLULAR DISTRIBUTION; CYTOSOL; CYTOTOXICITY; DRUG PROTEIN BINDING; ENDOSOME; HUMAN; INTERNALIZATION; LIPID BILAYER; MICROBIAL ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN TRANSPORT; REVIEW; ANIMAL; CELL MEMBRANE; CHEMISTRY; CLOSTRIDIUM; ENZYMOLOGY; METABOLISM; PROTEIN MULTIMERIZATION;

ADP RIBOSE TRANSFERASES; ANIMALS; BACTERIAL TOXINS; CELL MEMBRANE; CLOSTRIDIUM; HUMANS; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN MULTIMERIZATION;

EID: 84956739494     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.08.006     Document Type: Review

References (143)

1. J.G. Songer Clostridia as agents of zoonotic disease Vet. Microbiol. 140 2010 399 404
2. J.G. Songer, and D.W. Miskimmins Clostridium perfringens type E enteritis in calves: two cases and a brief review of the literature Anaerobe 10 2004 239 242
3. M.R. Popoff, and P. Bouvet Genetic characteristics of toxigenic Clostridia and toxin gene evolution Toxicon 75 2013 63 89
4. M. Gibert, S. Perelle, G. Daube, and M.R. Popoff Clostridium spiroforme toxin genes are related to C. perfringens iota toxin genes but have a different genomic localization Syst. Appl. Microbiol. 20 1997 337 347
5. M.R. Popoff, and P. Boquet Clostridium spiroforme toxin is a binary toxin which ADP-ribosylates cellular actin Biochem. Biophys. Res. Commun. 152 1988 1361 1368
6. S. Baudieri, S.P. Borriello, A. Pantosti, I. Luzzi, G.P. Testore, and G. Panichi Diarrhea associated with toxigenic Clostridium spiroforme J. Infect. 12 1986 278 279
7. R.J. Carman, S. Perelle, and M.R. Popoff Binary toxins from Clostridium spiroforme and Clostridium perfringens J.I. Rood, B.A. McClane, J.G. Songer, R.W. Titball, The Clostridia Molecular biology and Pathogenesis 1997 Academic Press London 359 367
8. M.S. Bain, R.D. Naylor, and N.J. Griffiths Clostridium spiroforme infection in rabbits Vet. Rec. 142 1998 47
9. S. Perelle, M. Gibert, P. Bourlioux, G. Corthier, and M.R. Popoff Production of a complete binary toxin (actin-specific ADP-ribosylating toxin) by Clostridium difficile CD196 Infect. Immun. 65 1997 1402 1407
10. M.R. Popoff, E.J. Rubin, D.M. Gill, and P. Boquet Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain Infect. Immun. 56 1988 2299 2306
11. D.N. Gerding, S. Johnson, M. Rupnik, and K. Aktories Binary toxin CDT: Mechanism, epidemiology, and potential clinical importance Gut Microbes 5 2013 1
12. R.J. Carman, A.L. Stevens, M.W. Lyerly, M.F. Hiltonsmith, B.G. Stiles, and T.D. Wilkins Clostridium difficile binary toxin (CDT) and diarrhea Anaerobe 17 2011 161 165
13. G.P. Carter, D. Lyras, D.L. Allen, K.E. Mackin, P.M. Howarth, J.R. O'Connor, and J.I. Rood Binary toxin production in Clostridium difficile is regulated by CdtR, a LytTR family response regulator J. Bacteriol. 189 2007 7290 7301
14. D.S. Metcalf, and J.S. Weese Binary toxin locus analysis in Clostridium difficile J. Med. Microbiol. 60 2011 1137 1145
15. I. Ohishi Response of mouse intestinal loop to botulinum C2 toxin: enterotoxic activity induced by cooperation of nonlinked protein components Infect. Immun. 40 1983 691 695
16. I. Ohishi Lethal and vascular permeability activities of botulinum C2 toxin induced by separate injections of the two toxin components Infect. Immun. 40 1983 336 339
17. I. Ohishi, M. Iwasaki, and G. Sakaguchi Purification and characterization of two components of botulinum C2 toxin Infect. Immun. 30 1980 668 673
18. K. Aktories, M. Bärmann, I. Ohishi, S. Tsuyama, K.H. Jakobs, and E. Habermann Botulinum C2 toxin ADP-ribosylates actin Nature 322 1986 390 392
19. S. Nakamura, T. Serikawa, K. Yamakawa, S. Nishida, S. Kozaki, and S. Sakaguchi Sporulation and C2 toxin production by Clostridium botulinum type C strains producing no C1 toxin Microbiol. Immunol. 22 1978 591 596
20. Y. Sakaguchi, T. Hayashi, Y. Yamamoto, K. Nakayama, K. Zhang, S. Ma, H. Arimitsu, and K. Oguma Molecular analysis of an extrachromosomal element containing the C2 toxin gene discovered in Clostridium botulinum type C J. Bacteriol. 191 2009 3282 3291
21. I. Ohishi, and Y. Hama Purification and characterization of heterologous components IIs of botulinum C2 toxin Microbiol. Immunol. 36 1992 221 229
22. M.R. Popoff Molecular biology of actin-ADP-ribosylating toxins K. Aktories, I. Just, Bacterial Protein Toxins 2000 Springer Berlin 275 302
23. S. Perelle, S. Scalzo, S. Kochi, M. Mock, and M.R. Popoff Immunological and functional comparison between Clostridium perfringens iota toxin, C. spiroforme toxin, and anthrax toxins FEMS Microbiol. Lett. 146 1997 117 121
24. A. Kronhardt, M. Rolando, C. Beitzinger, C. Stefani, M. Leuber, G. Flatau, M.R. Popoff, R. Benz, and E. Lemichez Cross-reactivity of anthrax and C2 toxin: protective antigen promotes the uptake of botulinum C2I toxin into human endothelial cells PLoS One 6 2011 e23133
25. M.W. Eklund, and J. Dowell Avian Botulism 1987 Charles C. Thomas Springfield, Ill.
26. I. Ohishi Response of mouse intestinal loop to botulinum C2 toxin: enterotoxic activity induced by cooperation of non linked protein components Infect. Immun. 40 1983 691 695
27. I. Ohishi, and Y. Odagiri Histopathological effect of botulinum C2 toxin on mouse intestines Infect. Immun. 43 1984 54 58
28. S.H. Leppla Bacillus anthracis toxins J.E. Alouf, M.R. Popoff, The Source Book of Bacterial Protein Toxins 2006 Elsevier Academic Press Amsterdam 323 347
29. S. Liu, M. Moayeri, and S.H. Leppla Anthrax lethal and edema toxins in anthrax pathogenesis Trends Microbiol. 22 2014 317 325
30. S. Han, J.A. Craig, C.D. Putnam, N.B. Carozzi, and J.A. Tainer Evolution and mechanism from structures of an ADP-ribosylating toxin and NAD complex Nat. Struct. Biol. 6 1999 932 936
31. G. Warren, M. Koziel, M.A. Mullins, G. Nye, B. Carr, N. Desai, K. Kostichka, N. Duck, and J.J. Estruch Novel Pesticidal Proteins and Strains 1996 World Intellectual Property Organization (Patent application, WO 96/10083)
32. M. Leuber, F. Orlik, B. Schiffler, A. Sickmann, and R. Benz Vegetative insecticidal protein (Vip1Ac) of Bacillus thuringiensis HD201: evidence for oligomer and channel formation Biochemistry 45 2006 283 288
33. A.G. Porter, E.W. Davidson, and J.W. Liu Mosquitocidal toxins of Bacilli and their genetic manipulation for effective biological control of mosquitos Microbiol. Rev. 57 1993 838 861
34. C. Berry The bacterium, Lysinibacillus sphaericus, as an insect pathogen J. Invertebr. Pathol. 109 2012 1 10
35. H. Barth, K. Aktories, M.R. Popoff, and B.G. Stiles Binary bacterial toxins: biochemistry, biology, and applications of common Clostridium and Bacillus proteins Microbiol. Mol. Biol. Rev. 68 2004 373 402
36. M.R. Popoff, and P. Bouvet Clostridial toxins Future Microbiol 4 2009 1021 1064
37. H. Vershueren, I. van der Taelen, J. Dewit, J. De Braekeleer, P. De Baetselier, K. Aktories, and I. Just Effects of Clostridium botulinum C2 toxin and cytochalasin D on in vitro invasiveness, motility and F-actin content of a murine T-lymphoma cell line Eur. J. Cell Biol. 66 1995 335 341
38. J.F. Richard, G. Mainguy, M. Gibert, J.C. Marvaud, B.G. Stiles, and M.R. Popoff Transcytosis of iota toxin across polarized CaCo-2 cell monolayers Mol. Microbiol. 43 2002 907 917
39. L. Ermert, H. Brückner, D. Walmrath, F. Grimminger, K. Aktories, N. Suttorp, H.R. Duncker, and W. Seeger Role of endothelial cytoskeleton in high-permeability edema due to botulism C2 toxin in perfused rabbit lungs Am. J. Physiol. 268 1995 L753 L761
40. K. Aktories, and G. Koch Modification of actin and Rho proteins by clostridial ADP-ribosylating toxins J. Moss, B. Iglewski, M. Vaughan, A.T. Tu, Bacterial Toxins and Virulence Factors in Disease vol. 8 1995 Marcel Dekker New York 491 520
41. C. Schwan, B. Stecher, T. Tzivelekidis, M. van Ham, M. Rohde, W.D. Hardt, J. Wehland, and K. Aktories Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria PLoS Pathog. 5 2009 e1000626
42. C. Schwan, T. Nolke, A.S. Kruppke, D.M. Schubert, A.E. Lang, and K. Aktories Cholesterol- and sphingolipid-rich microdomains are essential for microtubule-based membrane protrusions induced by Clostridium difficile transferase (CDT) J. Biol. Chem. 286 2011 29356 29365
43. M. Moayeri, and S.H. Leppla Cellular and systemic effects of anthrax lethal toxin and edema toxin Mol. Aspects Med. 30 2009 439 455
44. M. Gibert, L. Petit, S. Raffestin, A. Okabe, and M.R. Popoff Clostridium perfringens iota-toxin requires activation of both binding and enzymatic components for cytopathic activity Infect. Immun. 68 2000 3848 3853
45. B.G. Stiles, and T.D. Wilkins Clostridium perfringens iota toxin: synergism between two proteins Toxicon 24 1986 767 773
46. I. Ohishi Activation of botulinum C2 toxin by trypsin Infect. Immun. 55 1987 1461 1465
47. C. Petosa, J.R. Collier, K.R. Klimpel, S.H. Leppla, and R.C. Liddington Crystal structure of the anthrax toxin protective antigen Nature (London) 385 1997 833 838
48. K. Cunningham, D.B. Lacy, J. Mogridge, and R.J. Collier Mapping the lethal factor and edema factor binding sites on oligomeric anthrax protective antigen Proc. Natl. Acad. Sci. U. S. A. 99 2002 7049 7053
49. L. Abrami, S. Liu, P. Cosson, S.H. Leppla, and F.G. van der Goot Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process J. Cell Biol. 160 2003 321 328
50. J. Mogridge, K. Cuningham, D.B. Lacy, M. Mourez, and R.J. Collier The lethal and edema factors of anthrax toxin bind only to oligomeric forms of the protective antigen Proc. Natl. Acad. Sci. U. S. A. 99 2002 7045 7048
51. J. Mogridge, K. Cunningham, and R.J. Collier Stoichiometry of anthrax toxin complexes Biochemistry 41 2002 1079 1082
52. C. Schleberger, H. Hochmann, H. Barth, K. Aktories, and G.E. Schulz Structure and action of the binary C2 toxin from Clostridium botulinum J. Mol. Biol. 364 2006 705 715
53. D. Blocker, H. Barth, E. Maier, R. Benz, J.T. Barbieri, and K. Aktories The C terminus of component C2II of Clostridium botulinum C2 toxin is essential for receptor binding Infect. Immun. 68 2000 4566 4573
54. J.C. Marvaud, T. Smith, M.L. Hale, M.R. Popoff, L.A. Smith, and B.G. Stiles Clostridium perfringens iota-toxin: mapping of receptor binding and Ia docking domains on Ib Infect. Immun. 69 2001 2435 2441
55. B. Stiles, M.L. Hale, J.C. Marvaud, and M.R. Popoff Clostridium perfringens iota toxin: binding studies and characterization of cell surface receptor by fluorescence-activated cytometry Infect. Immun. 68 2000 3475 3484
56. P. Papatheodorou, J.E. Carette, G.W. Bell, C. Schwan, G. Guttenberg, T.R. Brummelkamp, and K. Aktories Lipolysis-stimulated lipoprotein receptor (LSR) is the host receptor for the binary toxin Clostridium difficile transferase (CDT) Proc. Natl. Acad. Sci. U. S. A. 108 2011 16422 16427
57. M. Eckhardt, H. Barth, D. Blocker, and K. Aktories Binding of Clostridium botulinum C2 toxin to asparagine-linked complex and hybrid carbohydrates J. Biol. Chem. 275 2000 2328 2334
58. P. Papatheodorou, C. Wilczek, T. Nolke, G. Guttenberg, D. Hornuss, C. Schwan, and K. Aktories Identification of the Cellular Receptor of Clostridium spiroforme Toxin Infect. Immun. 80 2012 1418 1423
59. H. Barth, F. Hofmann, C. Olenik, I. Just, and K. Aktories 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 1998 1364 1369
60. J. Rossjohn, S.C. Feil, W.J. McKinstry, R.K. Tweten, and M.W. Parker Structure of a cholesterol-binding thiol-activated cytolysin and a model of its membrane form Cell 89 1997 685 692
61. C.E. Soltani, E.M. Hotze, A.E. Johnson, and R.K. Tweten Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions Proc. Natl. Acad. Sci. U. S. A. 104 2007 20226 20231
62. J. Rossjohn, G. Polekhina, S.C. Feil, C.J. Morton, R.K. Tweten, and M.W. Parker Structures of perfringolysin O suggest a pathway for activation of cholesterol-dependent cytolysins J. Mol. Biol. 367 2007 1227 1236
63. A.P. Heuck, C.G. Savva, A. Holzenburg, and A.E. Johnson Conformational changes that effect oligomerization and initiate pore formation are triggered throughout perfringolysin O upon binding to cholesterol J. Biol. Chem. 282 2007 22629 22637
64. A.P. Heuck, R.K. Tweten, and A.E. Johnson β-barrel pore-forming toxins: intriguing dimorphic proteins Biochemistry 40 2001 9065 9073
65. O. Shatursky, A. Heuck, L. Shepard, J. Rossjhon, M. Parker, A. Johnson, and R. Tweten The mechanism of membrane insertion of a cholesterol-dependent cytolysin: a novel paradigm for pore-forming toxins Cell 99 1999 293 299
66. E.M. Hotze, A.P. Heuck, D.M. Czajkowsky, Z. Shao, A.E. Johnson, and R.K. Tweten Monomer-monomer interactions drive the prepore to pore conversion of a β-barrel-forming cholesterol-dependent cytolysin J. Biol. Chem. 277 2002 11597 11605
67. D.M. Czajkowsky, E.M. Hotze, Z. Shao, and R.K. Tweten Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane EMBO J. 23 2004 3206 3215
68. T.X. Dang, E.M. Hotze, I. Rouiller, R.K. Tweten, and E.M. Wilson-Kubalek Prepore to pore transition of a cholesterol-dependent cytolysin visualized by electron microscopy J. Struct. Biol. 150 2005 100 108
69. T.K. Sato, R.K. Tweten, and A.E. Johnson Disulfide-bond scanning reveals assembly state and beta-strand tilt angle of the PFO beta-barrel Nat. Chem. Biol. 9 2013 383 389 (310.1038/nchembio.1228 Epub 2013 Apr 1037.)
70. L. Gurcel, I. Iacovache, and F.G. van der Goot Aerolysin and related Aeromonas toxins J.E. Alouf, M.R. Popoff, The Source Book of Bacterial Protein Toxins 2006 Elsevier, Academic Press Amsterdam 606 620 (in press)
71. O. Knapp, B.G. Stiles, and M.R. Popoff The aerolysin-like toxin family of cytolytic, pore-forming toxins Open Toxinol. J. 3 2010 53 68
72. I. Iacovache, M. Bischofberger, and F.G. van der Goot Structure and assembly of pore-forming proteins Curr. Opin. Struct. Biol. 20 2010 241 246 10.1016/j.sbi.2010.1001.1013 (Epub 2010 Feb 1019)
73. A. Cole Structural studies on epsilon toxin from Clostridium perfringens C. Duchesnes, J. Mainil, M.R. Popoff, R. Titball, Protein Toxins of the Genus Clostridium and Vaccination 2003 Presses de la Faculté de Médecine Vétérinaire Liège 95
74. S.E. Ivie, and M.S. McClain Identification of amino acids important for binding of Clostridium perfringens epsilon toxin to host cells and to HAVCR1 Biochemistry 51 2012 7588 7595
75. O. Knapp, E. Maier, R. Benz, B. Geny, and M.R. Popoff Identification of the channel-forming domain of Clostridium perfringens epsilon-toxin (ETX) Biochim. Biophys. Acta 1788 2009 2584 2593
76. I. Iacovache, P. Paumard, H. Scheib, C. Lesieur, N. Sakai, S. Matile, M.W. Parker, and F.G. van der Goot A rivet model for channel formation by aerolysin-like pore-forming toxins EMBO J. 25 2006 457 466
77. B.G. Stiles, M.L. Hale, J.C. Marvaud, and M.R. Popoff Clostridium perfringens iota toxin: characterization of the cell-associated iota b complex Biochem. J. 367 2002 801 808
78. D. Blocker, J. Behlke, K. Aktories, and H. Barth Cellular uptake of the Clostridium perfringens binary iota-toxin Infect. Immun. 69 2001 2980 2987
79. H. Barth, D. Blocker, J. Behlke, W. Bergsma-Schutter, A. Brisson, R. Benz, and K. Aktories Cellular uptake of Clostridium botulinum C2 toxin requires oligomerization and acidification J. Biol. Chem. 275 2000 18704 18711
80. J.C. Milne, D. Furlong, P.C. Hanna, J.S. Wall, and J. Collier Anthrax protective antigen forms oligomers during intoxication of mammalian cells J. Biol. Chem. 269 1994 20607 20612
81. K.R. Klimpel, S.S. Molloy, G. Thomas, and S.H. Leppla Anthrax toxin protective antigen is activated by a cell surface protease with the sequence specificity and catalytic properties of furin Proc. Natl. Acad. Sci. U. S. A. 89 1992 10277 10281
82. A.F. Kintzer, K.L. Thoren, H.J. Sterling, K.C. Dong, G.K. Feld, Tang II, T.T. Zhang, E.R. Williams, J.M. Berger, and B.A. Krantz The protective antigen component of anthrax toxin forms functional octameric complexes J. Mol. Biol. 392 2009 614 629
83. H. Katayama, B.E. Janowiak, M. Brzozowski, J. Juryck, S. Falke, E.P. Gogol, R.J. Collier, and M.T. Fisher GroEL as a molecular scaffold for structural analysis of the anthrax toxin pore Nat. Struct. Mol. Biol. 15 2008 754 760
84. H. Katayama, J. Wang, F. Tama, L. Chollet, E.P. Gogol, R.J. Collier, and M.T. Fisher Three-dimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles Proc. Natl. Acad. Sci. U. S. A. 107 2010 3453 3457
85. J.A. Young, and R.J. Collier Anthrax toxin: receptor binding, internalization, pore formation, and translocation Annu. Rev. Biochem. 76 2007 243 265
86. T. Neumeyer, F. Tonello, F. Dal Molin, B. Schiffler, F. Orlik, and R. Benz Anthrax lethal factor (LF) mediated block of the anthrax protective antigen (PA) ion channel: effect of ionic strength and voltage Biochemistry 45 2006 3060 3068
87. T. Neumeyer, F. Tonello, F. Dal Molin, B. Schiffler, and R. Benz Anthrax edema factor, voltage-dependent binding to the protective antigen ion channel and comparison to LF binding J. Biol. Chem. 281 2006 32335 32343 (Epub 32006 Sep 32335)
88. R.J. Collier Membrane translocation by anthrax toxin Mol. Aspects Med. 30 2009 413 422
89. C. Beitzinger, C. Stefani, A. Kronhardt, M. Rolando, G. Flatau, E. Lemichez, and R. Benz Role of N-terminal His6-Tags in binding and efficient translocation of polypeptides into cells using anthrax protective antigen (PA) PLoS One 7 2012 e46964
90. M. Nagahama, M. Umezaki, R. Tashiro, M. Oda, K. Kobayashi, M. Shibutani, T. Takagishi, K. Ishidoh, M. Fukuda, and J. Sakurai Intracellular trafficking of Clostridium perfringens iota-toxin b Infect. Immun. 80 2012 3410 3416 10.1128/IAI.00483-00412 (Epub 02012 Jul 00423)
91. D. Blocker, K. Pohlmann, G. Haug, C. Bachmeyer, R. Benz, K. Aktories, and H. Barth 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 2003 37360 37367 (Epub 32003 Jul 37317)
92. M. Nagahama, M. Umezaki, M. Oda, K. Kobayashi, S. Tone, T. Suda, K. Ishidoh, and J. Sakurai Clostridium perfringens iota-toxin b induces rapid cell necrosis Infect. Immun. 79 2011 4353 4360
93. M. Gibert, J.C. Marvaud, Y. Pereira, M.L. Hale, B.G. Stiles, P. Boquet, C. Lamaze, and M.R. Popoff Differential requirement for the translocation of clostridial binary toxins: Iota toxin requires a membrane potential gradient FEBS Lett. 581 2007 1287 1296
94. J. Sakurai, and K. Kobayashi Lethal and dermonecrotic activities of Clostridium perfringens iota toxin: biological activities induced by cooperation of two nonlinked components Microbiol. Immunol. 39 1995 249 253
95. O. Knapp, R. Benz, M. Gibert, J.C. Marvaud, and M.R. Popoff Interaction of Clostridium perfringens iota-toxin with lipid bilayer membranes J. Biol. Chem. 277 2002 6143 6152
96. A. Schmid, R. Benz, I. Just, and K. Aktories Interaction of Clostridium botulinum C2 toxin with lipid bilayer membranes J. Biol. Chem. 269 1994 16706 16711
97. M.R. Popoff Clostridial pore-forming toxins: powerful virulence factors Anaerobe 30 2014 220 238
98. L. Petit, E. Maier, M. Gibert, M.R. Popoff, and R. Benz Clostridium perfringens epsilon-toxin induces a rapid change in cell membrane permeability to ions and forms channels in artificial lipid bilayers J. Biol. Chem. 276 2001 15736 15740
99. C. Chassin, M. Bens, J. de Barry, R. Courjaret, J.L. Bossu, F. Cluzeaud, S. Ben Mkaddem, M. Gibert, B. Poulain, M.R. Popoff, and A. Vandewalle Pore-forming epsilon toxin causes membrane permeabilization and rapid ATP depletion-mediated cell death in renal collecting duct cells Am. J. Physiol. Renal Physiol. 293 2007 F927 F937
100. C. Bachmeyer, R. Benz, H. Barth, K. Aktories, M. Gibert, and M.R. Popoff Interaction of Clostridium botulinum C2 toxin with lipid bilayer membranes and Vero cells: inhibition of channel function in chloroquine and related compounds in vitro and toxin action in vivo FASEB J. 15 2001 1658 1660
101. B.G. Stiles, D.J. Wigelsworth, M.R. Popoff, and H. Barth Clostridial binary toxins: iota and C2 family portraits Front. Cell. Infect. Microbiol. 1 2011 2 13
102. M. Gibert, M.N. Monier, R. Ruez, M.L. Hale, B.G. Stiles, A. Benmerah, L. Johannes, C. Lamaze, and M.R. Popoff Endocytosis and toxicity of clostridial binary toxins depend on a clathrin-independent pathway regulated by Rho-GDI Cell. Microbiol. 13 2011 154 170
103. D.J. Wigelsworth, G. Ruthel, L. Schnell, P. Herrlich, J. Blonder, T.D. Veenstra, R.J. Carman, T.D. Wilkins, G.T. Van Nhieu, S. Pauillac, M. Gibert, N. Sauvonnet, B.G. Stiles, M.R. Popoff, and H. Barth CD44 promotes intoxication by the clostridial iota-family toxins PLoS One 7 2012 e51356
104. M. Hale, J.C. Marvaud, M.R. Popoff, and B.G. Stiles Detergent-resistant membrane microdomains facilitate Ib oligomer formation and biological activity of Clostridium perfringens iota-toxin Infect. Immun. 72 2004 2186 2193
105. S. Pust, H. Barth, and K. Sandvig Clostridium botulinum C2 toxin is internalized by clathrin- and Rho-dependent mechanisms Cell. Microbiol. 12 2010 1809 1820
106. G. van der Goot, and J.A. Young Receptors of anthrax toxin and cell entry Mol. Aspects Med. 30 2009 406 412
107. H. Barth, and K. Aktories New insights into the mode of action of the actin ADP-ribosylating virulence factors Salmonella enterica SpvB and Clostridium botulinum C2 toxin Eur. J. Cell Biol. 90 2011 944 950 10.1016/j.ejcb.2010.1011.1007 (Epub 2011 Jan 1017)
108. G. Haug, K. Aktories, and H. Barth The host cell chaperone Hsp90 is necessary for cytotoxic action of the binary iota-like toxins Infect. Immun. 72 2004 3066 3068
109. G. Haug, J. Leemhuis, D. Tiemann, D.K. Meyer, K. Aktories, and H. Barth The host cell chaperone Hsp90 is essential for translocation of the binary Clostridium botulinum C2 toxin into the cytosol J. Biol. Chem. 278 2003 32266 32274
110. E. Kaiser, N. Bohm, K. Ernst, S. Langer, C. Schwan, K. Aktories, M. Popoff, G. Fischer, and H. Barth FK506-binding protein 51 interacts with Clostridium botulinum C2 toxin and FK506 inhibits membrane translocation of the toxin in mammalian cells Cell. Microbiol. 14 2012 1193 1205 10.1111/j.1462-5822.2012.01788.x (Epub 02012 Apr 01712)
111. E. Kaiser, S. Pust, C. Kroll, and H. Barth Cyclophilin A facilitates translocation of the Clostridium botulinum C2 toxin across membranes of acidified endosomes into the cytosol of mammalian cells Cell. Microbiol. 11 2009 790 795
112. S. Zhang, A. Finkelstein, and R.J. Collier Evidence that translocation of anthrax toxin's lethal factor is initiated by entry of its N terminus into the protective antigen channel Proc. Natl. Acad. Sci. U. S. A. 101 2004 16756 16761
113. S. Zhang, E. Udho, Z. Wu, R.J. Collier, and A. Finkelstein Protein translocation through anthrax toxin channels formed in planar lipid bilayers Biophys. J. 87 2004 3842 3849
114. R.J. Collier, and J.A.T. Young Anthrax toxin Annu. Rev. Cell Dev. Biol. 19 2003 45 70
115. M.R. Gonzalez, M. Bischofberger, L. Pernot, F.G. van der Goot, and B. Freche Bacterial pore-forming toxins: the (w)hole story? Cell. Mol. Life Sci. 65 2008 493 507
116. B.J. Nablo, R.G. Panchal, S. Bavari, T.L. Nguyen, R. Gussio, W. Ribot, A. Friedlander, D. Chabot, J.E. Reiner, J.W. Robertson, A. Balijepalli, K.M. Halverson, and J.J. Kasianowicz Anthrax toxin-induced rupture of artificial lipid bilayer membranes J. Chem. Phys. 139 2013 065101
117. E.L. Benson, P.D. Huynh, A. Finkelstein, and J.R. Collier Identification of residues lining the Anthrax Protective Antigen channel Biochemistry 37 1998 3941 3948
118. S.M. Bezrukov, X. Liu, V.A. Karginov, A.N. Wein, S.H. Leppla, M.R. Popoff, H. Barth, and E.M. Nestorovich Interactions of high-affinity cationic blockers with the translocation pores of B. anthracis, C. botulinum, and C. perfringens binary toxins Biophys. J. 103 2012 1208 1217
119. E.M. Nestorovich, and S.M. Bezrukov Obstructing toxin pathways by targeted pore blockage Chem. Rev. 112 2012 6388 6430
120. E.M. Nestorovich, V.A. Karginov, A.M. Berezhkovskii, and S.M. Bezrukov Blockage of anthrax PA63 pore by a multicharged high-affinity toxin inhibitor Biophys. J. 99 2010 134 143
121. D. Blocker, C. Bachmeyer, R. Benz, K. Aktories, and H. Barth 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 2003 5368 5377
122. O. Knapp, E. Maier, E. Waltenberger, C. Mazuet, R. Benz, and M.R. Popoff Residues involved in the pore-forming activity of the Clostridium perfringens iota toxin Cell. Microbiol. 17 2015 288 302
123. B.A. Krantz, R.A. Melnyk, S. Zhang, S.J. Juris, D.B. Lacy, Z. Wu, A. Finkelstein, and R.J. Collier A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore Science 309 2005 777 781
124. J. Sun, A.E. Lang, K. Aktories, and R.J. Collier Phenylalanine-427 of anthrax protective antigen functions in both pore formation and protein translocation Proc. Natl. Acad. Sci. U. S. A. 105 2008 4346 4351
125. T. Neumeyer, B. Schiffler, E. Maier, A.E. Lang, K. Aktories, and R. Benz Clostridium botulinum C2 toxin. Identification of the binding site for chloroquine and related compounds and influence of the binding site on properties of the C2II channel J. Biol. Chem. 283 2008 3904 3914
126. B.R. Sellman, S. Nassi, and R.J. Collier Point mutations in anthrax protective antigen that block translocation J. Biol. Chem. 276 2001 8371 8376
127. C. Bachmeyer, F. Orlik, H. Barth, K. Aktories, and R. Benz Mechanism of C2-toxin inhibition by Fluphenazine and related compounds: investigation of their binding kinetics to the C2II-channel using the current noise analysis J. Mol. Biol. 333 2003 527 540
128. E.M. Nestorovich, and S.M. Bezrukov Designing inhibitors of anthrax toxin Expert Opin. Drug Discovery 9 2014 299 318
129. C. Beitzinger, A. Bronnhuber, K. Duscha, Z. Riedl, M. Huber-Lang, R. Benz, G. Hajos, and H. Barth Designed azolopyridinium salts block protective antigen pores in vitro and protect cells from anthrax toxin PLoS One 8 2013 e66099
130. A. Bronnhuber, E. Maier, Z. Riedl, G. Hajos, R. Benz, and H. Barth Inhibitions of the translocation pore of Clostridium botulinum C2 toxin by tailored azolopyridinium salts protects human cells from intoxication Toxicology 316 2014 25 33
131. E.M. Nestorovich, V.A. Karginov, M.R. Popoff, S.M. Bezrukov, and H. Barth Tailored ss-cyclodextrin blocks the translocation pores of binary exotoxins from C. botulinum and C. perfringens and protects cells from intoxication PLoS One 6 2011 e23927
132. M. Roeder, E.M. Nestorovich, V.A. Karginov, C. Schwan, K. Aktories, and H. Barth Tailored cyclodextrin pore blocker protects mammalian cells from Clostridium difficile binary toxin CDT Toxins (Basel) 6 2014 2097 2114 10.3390/toxins6072097
133. Y. Moran, D. Fredman, P. Szczesny, M. Grynberg, and U. Technau Recurrent horizontal transfer of bacterial toxin genes to eukaryotes Mol. Biol. Evol. 29 2012 2223 2230
134. J. Fahrer, J. Funk, M. Lillich, and H. Barth Internalization of biotinylated compounds into cancer cells is promoted by a molecular Trojan horse based upon core streptavidin and clostridial C2 toxin Naunyn Schmiedebergs Arch. Pharmacol. 383 2010 263 273
135. J. Fahrer, R. Plunien, U. Binder, T. Langer, H. Seliger, and H. Barth Genetically engineered clostridial C2 toxin as a novel delivery system for living mammalian cells Bioconjug. Chem. 21 2010 130 139
136. J. Fahrer, J. Rieger, G. van Zandbergen, and H. Barth The C2-streptavidin delivery system promotes the uptake of biotinylated molecules in macrophages and T-leukemia cells Biol. Chem. 391 2011 1315 1325
137. R.O. Blaustein, T.M. Koehler, R.J. Collier, and A. Finkelstein Anthrax toxin: channel-forming activity of protective antigen in planar phospholipid bilayers Proc. Natl. Acad. Sci. U. S. A. 86 1989 2209 2213
138. K.A. Bradley, J. Mogridge, M. Mourez, R.J. Collier, and J.A.T. Young Identification of the cellular receptor for anthrax toxin Nature (London) 414 2001 225 229
139. A. Finkelstein The channel formed in planar lipid bilayers by the protective antigen component of anthrax toxin Toxicology 87 1994 29 41
140. F. Orlik, B. Schiffler, and R. Benz Anthrax toxin protective antigen: inhibition of channel function by chloroquine and related compounds and study of binding kinetics using the current noise analysis Biophys. J. 88 2005 1715 1724
141. H.M. Scobie, G.J. Rainey, K.A. Bradley, and J.A. Young Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor Proc. Natl. Acad. Sci. U. S. A. 100 2003 5170 5174
142. J. Rossjohn, J.T. Buckley, B. Hazes, A.G. Murzin, R.J. Read, and M.W. Parker Aerolysin and pertussis toxin share a common receptor-binding domain EMBO J. 16 1997 3426 3434
143. L. Shepard, O. Shatursky, A. Johnson, and R. Tweten The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane b-hairpins Biochemistry 39 2000 10284 10293