Bacterial pore-forming toxins: The (w)hole story?

Cellular and Molecular Life Sciences

Volumn 65, Issue 3, 2008, Pages 493-507

  Gonzalez, M R ^a   Bischofberger, M ^a   Pernot, L ^a   Van Der Goot, F G ^a   Freche B ^a  

^a EPFL   (Switzerland)

Author keywords

Aerolysin; Caspase 1; Cellular response; Cholesterol dependent cytolysin; Pore forming toxins

Indexed keywords

AEROLYSIN; ANTHRAX TOXIN; BACTERIAL TOXIN; CELL CYCLE PROTEIN; CHOLERA TOXIN; DIPHTHERIA TOXIN; LISTERIOLYSIN O; MITOGEN ACTIVATED PROTEIN KINASE P38; PNEUMOLYSIN; PORE FORMING TOXIN; STREPTOLYSIN O; UNCLASSIFIED DRUG;

AUTOPHAGY; CELL ACTIVITY; CELL REGENERATION; CELL SURVIVAL; CELL SWELLING; CHANNEL GATING; CLOSTRIDIUM PERFRINGENS; CYTOLYSIS; EUKARYOTIC CELL; LIPID METABOLISM; MEMBRANE DAMAGE; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, BACTERIAL; AUTOPHAGY; BACTERIA; BACTERIAL TOXINS; MODELS, MOLECULAR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 39149142237     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-7434-y     Document Type: Review

References (171)

1. Van der Goot, F. G. E. (2001) Pore Forming Toxins. Springer Verlag, Berlin.
2. Sher, D., Fishman, Y., Zhang, M., Lebendiker, M., Gaathon, A., Mancheno, J. M. and Zlotkin, E. (2005) Hydralysins, a new category of beta-pore-forming toxins in cnidaria. J. Biol. Chem. 280, 22847-22855.
3. Sousa, M. V., Richardson, M., Fontes, W. and Morhy, L. (1994) Homology between the seed cytolysin enterolobin and bacterial aerolysins. J. Protein Chem. 13, 659-667.
4. Mancheno, J. M., Tateno, H., Goldstein, I. J., Martinez-Ripoll, M. and Hermoso, J. A. (2005) Structural analysis of the Laetiporus sulphureus hemolytic pore-forming lectin in complex with sugars. J. Biol. Chem. 280, 17251-17259.
5. Pipkin, M. E. and Lieberman, J. (2007) Delivering the kiss of death: Progress on understanding how perforin works. Curr. Opin. Immunol. 19, 301-308.
6. Parker, M. W. and Feil, S. C. (2005) Pore-forming protein toxins: From structure to function. Prog. Biophys. Mol. Biol. 88, 91-142.
7. Lakey, J. H. and Slatin, S. L. (2001) Pore-forming colicins and their relatives. Curr. Top. Microbiol. Immunol. 257, 131-161.
8. Collier, R. J. (2001) Understanding the mode of action of diphtheria toxin: A perspective on progress during the 20th century. Toxicon 39, 1793-1803.
9. Schendel, S. L., Xie, Z., Montal, M. O., Matsuyama, S., Montal, M. and Reed, J. C. (1997) Channel formation by antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. USA 94, 5113-5118.
10. Wiener, M., Freymann, D., Ghosh, P. and Stroud, R. M. (1997) Crystal structure of colicin Ia. Nature 385, 461-464.
11. Hilsenbeck, J. L., Park, H., Chen, G., Youn, B., Postle, K. and Kang, C. (2004) Crystal structure of the cytotoxic bacterial protein colicin B at 2.5 Å resolution. Mol. Microbiol. 51, 711-720.
12. Vetter, I. R., Parker, M. W., Tucker, A. D., Lakey, J. H., Pattus, F. and Tsernoglou, D. (1998) Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6, 863-874.
13. Galitsky, N., Cody, V., Wojtczak, A., Ghosh, D., Luft, J. R., Pangborn, W. and English, L. (2001) Structure of the insecticidal bacterial delta-endotoxin Cry3Bb1 of Bacillus thuringiensis. Acta Crystallogr. D Biol. Crystallogr. 57, 1101-1109.
14. Schulz, G. E. (2002) The structure of bacterial outer membrane proteins. Biochim. Biophys. Acta 1565, 308-317.
15. Abrami, L., Fivaz, M., Decroly, E., Seidah, N. G., Jean, F., Thomas, G., Leppla, S. H., Buckley, J. T. and van der Goot, F. G. (1998) The pore-forming toxin proaerolysin is activated by furin. J. Biol. Chem. 273, 32656-32661.
16. Howard, S. P. and Buckley, J. T. (1985) Activation of the hole-forming toxin aerolysin by extracellular processing. J. Bacteriol. 163, 336-340.
17. Shatursky, O., Heuck, A. P., Shepard, L. A., Rossjohn, J., Parker, M. W., Johnson, A. E. and Tweten, R. K. (1999) The mechanism of membrane insertion for a cholesterol-dependent cytolysin: A novel paradigm for pore-forming toxins. Cell 99, 293-299.
18. Iacovache, I., Paumard, P., Scheib, H., Lesieur, C., Sakai, N., Matile, S., Parker, M. W. and van der Goot, F. G. (2006) A rivet model for channel formation by aerolysin-like pore-forming toxins. EMBO J. 25, 457-466.
19. Nassi, S., Collier, R. J. and Finkelstein, A. (2002) PA63 channel of anthrax toxin: An extended beta-barrel. Biochemistry 41, 1445-1450.
20. Melton, J. A., Parker, M. W., Rossjohn, J., Buckley, J. T. and Tweten, R. K. (2004) The identification and structure of the membrane-spanning domain of the Clostridium septicum alpha toxin. J. Biol. Chem. 279, 14315-14322.
21. Moniatte, M., van der Goot, F. G., Buckley, J. T., Pattus, F. and van Dorsselaer, A. (1996) Characterisation of the heptameric pore-forming complex of the Aeromonas toxin aerolysin using MALDI-TOF mass spectrometry. FEBS Lett. 384, 269-272.
22. Valeva, A., Palmer, M. and Bhakdi, S. (1997) Staphylococcal alpha-toxin: Formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36, 13298-13304.
23. Wilmsen, H. U., Leonard, K. R., Tichelaar, W., Buckley, J. T. and Pattus, F. (1992) The aerolysin membrane channel is formed by heptamerization of the monomer. EMBO J. 11, 2457-2463.
24. Olofsson, A., Hebert, H. and Thelestam, M. (1993) The projection structure of perfringolysin O (Clostridium perfringens theta-toxin). FEBS Lett. 319, 125-127.
25. Sekiya, K., Satoh, R., Danbara, H. and Futaesaku, Y. (1993) A ring-shaped structure with a crown formed by streptolysin O on the erythrocyte membrane. J. Bacteriol. 175, 5953-5961.
26. Walev, I., Bhakdi, S. C., Hofmann, F., Djonder, N., Valeva, A., Aktories, K. and Bhakdi, S. (2001) Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O. Proc. Natl. Acad. Sci. USA 98, 3185-3190.
27. Collier, R. J. (1990) Diphtheria toxin: Structure and function of a cytocidal protein. In: ADP-Ribosylating Toxins and G Proteins: Insights into Signal Transduction, pp. 3-19, Moss, J. and Vaughan, M. (eds.), American Society of Microbiology, Washington D.C.
28. Petosa, C., Collier, R. J., Klimpel, K. R., Leppla, S. H. and Liddington, R. C. (1997) Crystal structure of the anthrax toxin protective antigen. Nature 385, 833-838.
29. Santelli, E., Bankston, L. A., Leppla, S. H. and Liddington, R. C. (2004) Crystal structure of a complex between anthrax toxin and its host cell receptor. Nature 430, 905-908.
30. Milne, J. C., Furlong, D., Hanna, P. C., Wall, J. S. and Collier, R. J. (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J. Biol. Chem. 269, 20607-20612.
31. Abrami, L., Lindsay, M., Parton, R. G., Leppla, S. H. and van der Goot, F. G. (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.
32. Abrami, L., Reig, N. and van der Goot, F. G. (2005) Anthrax toxin: The long and winding road that leads to the kill. Trends Microbiol. 13, 72-78.
33. Cornelis, G. R. (2006) The type III secretion injectisome. Nat. Rev. Microbiol. 4, 811-825.
34. Galan, J. E. (2001) Salmonella interactions with host cells: Type III secretion at work. Annu. Rev. Cell Dev. Biol. 17, 53-86.
35. 2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis. J. Bacteriol. 176, 569-579.
36. Van Gijsegem, F., Gough, C., Zischek, C., Niqueux, E., Arlat, M., Genin, S., Barberis, P., German, S., Castello, P. and Boucher, C. (1995) The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15, 1095-1114.
37. Faudry, E., Job, V., Dessen, A., Attree, I. and Forge, V. (2007) Type III secretion system translocator has a molten globule conformation both in its free and chaperone-bound forms. FEBS J. 274, 3601-3610.
38. Barrows, B. D., Griffitts, J. S. and Aroian, R. V. (2006) Caenorhabditis elegans carbohydrates in bacterial toxin resistance. Methods Enzymol. 417, 340-358.
39. Scobie, H. M. and Young, J. A. (2005) Interactions between anthrax toxin receptors and protective antigen. Curr. Opin. Microbiol. 8, 106-112.
40. Nelson, K. L., Raja, S. M. and Buckley, J. T. (1997) The glycosylphosphatidylinositol-anchored surface glycoprotein Thy-1 is a receptor for the channel-forming toxin aerolysin. J. Biol. Chem. 272, 12170-12174.
41. Tweten, R. K., Parker, M. W. and Johnson, A. E. (2001) The cholesterol-dependent cytolysins. Curr. Top. Microbiol. Immunol. 257, 15-33.
42. Valeva, A., Hellmann, N., Walev, I., Strand, D., Plate, M., Boukhallouk, F., Brack, A., Hanada, K., Decker, H. and Bhakdi, S. (2006) Evidence that clustered phosphocholine head groups serve as sites for binding and assembly of an oligomeric protein pore. J. Biol. Chem. 281, 26014-26021.
43. Abrami, L. and van Der Goot, F. G. (1999) Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol. 147, 175-184.
44. Lafont, F., Abrami, L. and van der Goot, F. G. (2004) Bacterial subversion of lipid rafts. Curr. Opin. Microbiol. 7, 4-10.
45. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H. and Gouaux, J. E. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866.
46. Valeva, A., Pongs, J., Bhakdi, S. and Palmer, M. (1997) Staphylococcal alpha-toxin: The role of the N-terminus in formation of the heptameric pore - A fluorescence study. Biochim. Biophys. Acta 1325, 281-286.
47. Gurcel, L., Iacovache, I. and van der Goot, F. G. (2005) Aerolysin and related Aeromonas toxins. In: The Comprehensive Sourcebook of Bacterial Protein Toxins, Alouf, J. E. and Freer, J. H. (eds.), Academic Press, London.
48. Howard, S. P. and Buckley, J. T. (1985) Protein export by a gram-negative bacterium: Production of aerolysin by Aeromonas hydrophila. J. Bacteriol. 161, 1118-1124.
49. Hardie, K. R., Schulze, A., Parker, M. W. and Buckley, J. T. (1995) Vibrio spp. secrete proaerolysin as a folded dimer without the need for disulphide bond formation. Mol. Microbiol. 17, 1035-1044.
50. Howard, S. P., Critch, J. and Bedi, A. (1993) Isolation and analysis of eight exe genes and their involvement in extracellular protein secretion and outer membrane assembly in Aeromonas hydrophila. J. Bacteriol. 175, 6695-6703.
51. Jiang, B. and Howard, S. P. (1992) The Aeromonas hydrophila exeE gene, required both for protein secretion and normal outer membrane biogenesis, is a member of a general secretion pathway. Mol. Microbiol. 6, 1351-1361.
52. Abrami, L., Fivaz, M., Glauser, P. E., Parton, R. G. and van der Goot, F. G. (1998) A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J. Cell Biol. 140, 525-540.
53. Cowell, S., Aschauer, W., Gruber, H. J., Nelson, K. L. and Buckley, J. T. (1997) The erythrocyte receptor for the channel-forming toxin aerolysin is a novel glycosylphosphatidylinositol-anchored protein. Mol. Microbiol. 25, 343-350.
54. Diep, D. B., Nelson, K. L., Raja, S. M., Pleshak, E. N. and Buckley, J. T. (1998) Glycosylphosphatidylinositol anchors of membrane glycoproteins are binding determinants for the channel-forming toxin aerolysin. J. Biol. Chem. 273, 2355-2360.
55. Barry, R., Moore, S., Alonso, A., Ausio, J. and Buckley, J. T. (2001) The channel-forming protein proaerolysin remains a dimer at low concentrations in solution. J. Biol. Chem. 276, 551-554.
56. van der Goot, F. G., Ausio, J., Wong, K. R., Pattus, F. and Buckley, J. T. (1993) Dimerization stabilizes the pore-forming toxin aerolysin in solution. J. Biol. Chem. 268, 18272-9.
57. Fivaz, M., Velluz, M. C. and van der Goot, F. G. (1999) Dimer dissociation of the pore-forming toxin aerolysin precedes receptor binding. J. Biol. Chem. 274, 37705-37708.
58. Parker, M. W., Buckley, J. T., Postma, J. P., Tucker, A. D., Leonard, K., Pattus, F. and Tsernoglou, D. (1994) Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature 367, 292-295.
59. Gordon, V. M., Nelson, K. L., Buckley, J. T., Stevens, V. L., Tweten, R. K., Elwood, P. C. and Leppla, S. H. (1999) Clostridium septicum alpha toxin uses glycosylphosphatidylinositol-anchored protein receptors. J. Biol. Chem. 274, 27274-27280.
60. Abrami, L., Velluz, M. C., Hong, Y., Ohishi, K., Mehlert, A., Ferguson, M., Kinoshita, T. and Gisou van der Goot, F. (2002) The glycan core of GPI-anchored proteins modulates aerolysin binding but is not sufficient: The polypeptide moiety is required for the toxin-receptor interaction. FEBS Lett. 512, 249-254.
61. Hong, Y., Ohishi, K., Inoue, N., Kang, J. Y., Shime, H., Horiguchi, Y., van der Goot, F. G., Sugimoto, N. and Kinoshita, T. (2002) Requirement of N-glycan on GPI-anchored proteins for efficient binding of aerolysin but not Clostridium septicum alpha-toxin. EMBO J. 21, 5047-5056.
62. Fivaz, M., Vilbois, F., Thurnheer, S., Pasquali, C., Abrami, L., Bickel, P. E., Parton, R. G. and van der Goot, F. G. (2002) Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 21, 3989-4000.
63. Buckley, J. T., Wilmsen, H. U., Lesieur, C., Schulze, A., Pattus, F., Parker, M. W. and van der Goot, F. G. (1995) Protonation of histidine-132 promotes oligomerization of the channel-forming toxin aerolysin. Biochemistry 34, 16450-16455.
64. Lesieur, C., Vecsey-Semjen, B., Abrami, L., Fivaz, M. and Gisou van der Goot, F. (1997) Membrane insertion: The strategies of toxins. Mol. Membr. Biol. 14, 45 -64.
65. Ballard, J., Crabtree, J., Roe, B. A. and Tweten, R. K. (1995) The primary structure of Clostridium septicum alpha-toxin exhibits similarity with that of Aeromonas hydrophila aerolysin. Infect. Immun. 63, 340-344.
66. Bayley, H. (1994) Triggers and switches in a self-assembling pore-forming protein. J. Cell Biochem. 56, 177-182.
67. Bhakdi, S. and Tranum-Jensen, J. (1991) Alpha-toxin of Staphylococcus aureus. Microbiol. Rev. 55, 733-751.
68. Walker, B., Braha, O., Cheley, S. and Bayley, H. (1995) An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch. Chem. Biol. 2, 99-105.
69. Walker, B., Krishnasastry, M., Zorn, L. and Bayley, H. (1992) Assembly of the oligomeric membrane pore formed by Staphylococcal alpha-hemolysin examined by truncation mutagenesis. J. Biol. Chem. 267, 21782-21786.
70. Valeva, A., Palmer, M., Hilgert, K., Kehoe, M. and Bhakdi, S. (1995) Correct oligomerization is a prerequisite for insertion of the central molecular domain of staphylococcal alpha-toxin into the lipid bilayer. Biochim. Biophys. Acta 1236, 213-218.
71. Valeva, A., Weisser, A., Walker, B., Kehoe, M., Bayley, H., Bhakdi, S. and Palmer, M. (1996) Molecular architecture of a toxin pore: a 15-residue sequence lines the transmembrane channel of staphylococcal alpha-toxin. EMBO J. 15, 1857-1864.
72. Walker, B., Krishnasastry, M. and Bayley, H. (1993) Functional complementation of staphylococcal alpha-hemolysin fragments. Overlaps, nicks, and gaps in the glycine-rich loop. J. Biol. Chem. 268, 5285-5292.
73. Ward, R. J., Palmer, M., Leonard, K. and Bhakdi, S. (1994) Identification of a putative membrane-inserted segment in the alpha-toxin of Staphylococcus aureus. Biochemistry 33, 7477-7484.
74. Tweten, R. K. (2005) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 73, 6199-6209.
75. Madden, J. C., Ruiz, N. and Caparon, M. (2001) Cytolysin-mediated translocation (CMT): A functional equivalent of type III secretion in gram-positive bacteria. Cell 104, 143-152.
76. Bavdek, A., Gekara, N. O., Priselac, D., Gutierrez Aguirre, I., Darji, A., Chakraborty, T., Macek, P., Lakey, J. H., Weiss, S. and Anderluh, G. (2007) Sterol and pH interdependence in the binding, oligomerization, and pore formation of Listeriolysin O. Biochemistry 46, 4425-4437.
77. Moors, M. A., Levitt, B., Youngman, P. and Portnoy, D. A. (1999) Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect. Immun. 67, 131-139.
78. Walker, J. A., Allen, R. L., Falmagne, P., Johnson, M. K. and Boulnois, G. J. (1987) Molecular cloning, characterization, and complete nucleotide sequence of the gene for pneumolysin, the sulfhydryl-activated toxin of Streptococcus pneumoniae. Infect. Immun. 55, 1184-1189.
79. Iwamoto, M., Ohno-Iwashita, Y. and Ando, S. (1987) Role of the essential thiol group in the thiol-activated cytolysin from Clostridium perfringens. Eur. J. Biochem. 167, 425-430.
80. Sekino-Suzuki, N., Nakamura, M., Mitsui, K. I. and Ohno-Iwashita, Y. (1996) Contribution of individual tryptophan residues to the structure and activity of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin. Eur. J. Biochem. 241, 941-947.
81. Jacobs, T., Darji, A., Frahm, N., Rohde, M., Wehland, J., Chakraborty, T. and Weiss, S. (1998) Listeriolysin O: Cholesterol inhibits cytolysis but not binding to cellular membranes. Mol. Microbiol. 28, 1081-1089.
82. Johnson, M. K., Geoffroy, C. and Alouf, J. E. (1980) Binding of cholesterol by sulfhydryl-activated cytolysins. Infect. Immun. 27, 97-101.
83. Giddings, K. S., Zhao, J., Sims, P. J. and Tweten, R. K. (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat. Struct. Mol. Biol. 11, 1173-1178.
84. Polekhina, G., Giddings, K. S., Tweten, R. K. and Parker, M. W. (2005) Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc. Natl. Acad. Sci. USA 102, 600-605.
85. Giddings, K. S., Johnson, A. E. and Tweten, R. K. (2003) Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins. Proc. Natl. Acad. Sci. USA 100, 11315-11320.
86. Shimada, Y., Maruya, M., Iwashita, S. and Ohno-Iwashita, Y. (2002) The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur. J. Biochem. 269, 6195-6203.
87. Waheed, A. A., Shimada, Y., Heijnen, H. F., Nakamura, M., Inomata, M., Hayashi, M., Iwashita, S., Slot, J. W. and Ohno-Iwashita, Y. (2001) Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl. Acad. Sci. USA 98, 4926-4931.
88. Gekara, N. O., Jacobs, T., Chakraborty, T. and Weiss, S. (2005) The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell. Microbiol. 7, 1345-1356.
89. Gekara, N. O. and Weiss, S. (2004) Lipid rafts clustering and signalling by listeriolysin O. Biochem. Soc. Trans. 32, 712-714.
90. Tilley, S. J., Orlova, E. V., Gilbert, R. J., Andrew, P. W. and Saibil, H. R. (2005) Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121, 247-256.
91. Shepard, L. A., Shatursky, O., Johnson, A. E. and Tweten, R. K. (2000) The mechanism of pore assembly for a cholesterol-dependent cytolysin: Formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. Biochemistry 39, 10284-10293.
92. Heuck, A. P., Tweten, R. K. and Johnson, A. E. (2003) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J. Biol. Chem. 278, 31218-31225.
93. Gilbert, R. J. (2002) Pore-forming toxins. Cell. Mol. Life Sci. 59, 832-844.
94. Palmer, M., Harris, R., Freytag, C., Kehoe, M., Tranum-Jensen, J. and Bhakdi, S. (1998) Assembly mechanism of the oligomeric streptolysin O pore: The early membrane lesion is lined by a free edge of the lipid membrane and is extended gradually during oligomerization. EMBO J. 17, 1598-1605.
95. Collier, R. J. and Young, J. A. (2003) Anthrax toxin. Annu. Rev. Cell Dev. Biol. 19, 45-70.
96. Bradley, K. A., Mogridge, J., Mourez, M., Collier, R. J. and Young, J. A. (2001) Identification of the cellular receptor for anthrax toxin. Nature 414, 225-229.
97. Scobie, H. M., Rainey, G. J., Bradley, K. A. and Young, J. A. (2003) Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc. Natl. Acad. Sci. USA 100, 5170-5174.
98. Gordon, V. M., Klimpel, K. R., Arora, N., Henderson, M. A. and Leppla, S. H. (1995) Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect. Immun. 63, 82-87.
99. Milne, J. C. and Collier, R. J. (1993) pH-dependent permeabilization of the plasma membrane of mammalian cells by anthrax protective antigen. Mol. Microbiol. 10, 647-653.
100. Lacy, D. B., Lin, H. C., Melnyk, R. A., Schueler-Furman, O., Reither, L., Cunningham, K., Baker, D. and Collier, R. J. (2005) A model of anthrax toxin lethal factor bound to protective antigen. Proc. Natl. Acad. Sci. USA 102, 16409-16414.
101. Rainey, G. J., Wigelsworth, D. J., Ryan, P. L., Scobie, H. M., Collier, R. J. and Young, J. A. (2005) Receptor-specific requirements for anthrax toxin delivery into cells. Proc. Natl. Acad. Sci. USA 102, 13278-13283.
102. Lacy, D. B., Wigelsworth, D. J., Melnyk, R. A., Harrison, S. C. and Collier, R. J. (2004) Structure of heptameric protective antigen bound to an anthrax toxin receptor: A role for receptor in pH-dependent pore formation. Proc. Natl. Acad. Sci. USA 101, 13147-13151.
103. Abrami, L., Liu, S., Cosson, P., Leppla, S. H. and van der Goot, F. G. (2003) Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 160, 321-328.
104. Blaustein, R. O., Koehler, T. M., Collier, R. J. and Finkelstein, A. (1989) Anthrax toxin: Channel-forming activity of protective antigen in planar phospholipid bilayers. Proc. Natl. Acad. Sci. USA 86, 2209-2213.
105. Krantz, B. A., Trivedi, A. D., Cunningham, K., Christensen, K. A. and Collier, R. J. (2004) Acid-induced unfolding of the amino-terminal domains of the lethal and edema factors of anthrax toxin. J. Mol. Biol. 344, 739-756.
106. Wesche, J., Elliott, J. L., Falnes, P. O., Olsnes, S. and Collier, R. J. (1998) Characterization of membrane translocation by anthrax protective antigen. Biochemistry 37, 15737-15746.
107. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N. and Sasakawa, C. (2005) Escape of intracellular Shigella from autophagy. Science 307, 727-731.
108. Ernst, J. D. (2000) Bacterial inhibition of phagocytosis. Cell. Microbiol. 2, 379-386.
109. Hernandez, L. D., Hueffer, K., Wenk, M. R. and Galan, J. E. (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304, 1805-1807.
110. Cornelis, G. R. (2002) The Yersinia Ysc-Yop 'type III' weaponry. Nat. Rev. Mol. Cell. Biol. 3, 742-752.
111. Troisfontaines, P. and Cornelis, G. R. (2005) Type III secretion: More systems than you think. Physiology (Bethesda) 20, 326-339.
112. Cossart, P. and Sansonetti, P. J. (2004) Bacterial invasion: The paradigms of enteroinvasive pathogens. Science 304, 242-248.
113. Cossart, P. and Lecuit, M. (1998) Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signaling. EMBO J. 17, 3797-3806.
114. Kayal, S., Lilienbaum, A., Poyart, C., Memet, S., Israel, A. and Berche, P. (1999) Listeriolysin O-dependent activation of endothelial cells during infection with Listeria monocytogenes: Activation of NF-kappa B and upregulation of adhesion molecules and chemokines. Mol. Microbiol. 31, 1709-1722.
115. Hamon, M. A., Batsche, E., Regnault, B., Tham, T. N., Seveau, S., Muchardt, C. and Cossart, P. (2007) Histone modifications induced by a family of bacterial toxins. Proc. Natl. Acad. Sci. USA 104, 13467-13472.
116. 2+ oscillations. Cell. Microbiol. 4, 483-491.
117. 2+ oscillations in renal epithelial cells. Nature 405, 694-697.
118. Koschinski, A., Repp, H., Unver, B., Dreyer, F., Brockmeier, D., Valeva, A., Bhakdi, S. and Walev, I. (2006) Why Escherichia coli alpha-hemolysin induces calcium oscillations in mammalian cells - The pore is on its own. FASEB J. 20, 973-975.
119. Lewis, R. S. (2003) Calcium oscillations in T-cells: Mechanisms and consequences for gene expression. Biochem. Soc. Trans. 31, 925-929.
120. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003) Calcium signalling: Dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell. Biol. 4, 517-529.
121. Dramsi, S. and Cossart, P. (2003) Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect. Immun. 71, 3614-3618.
122. Gekara, N. O., Westphal, K., Ma, B., Rohde, M., Groebe, L. and Weiss, S. (2007) The multiple mechanisms of Ca(2+) signalling by listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes. Cell. Microbiol. 9, 2008-2021.
123. Iliev, A. I., Djannatian, J. R., Nau, R., Mitchell, T. J. and Wouters, F. S. (2007) Cholesterol-dependent actin remodeling via RhoA and Rac1 activation by the Streptococcus pneumoniae toxin pneumolysin. Proc. Natl. Acad. Sci. USA 104, 2897-2902.
124. Berry, A. M., Yother, J., Briles, D. E., Hansman, D. and Paton, J. C. (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect. Immun. 57, 2037-2042.
125. Paton, J. C., Andrew, P. W., Boulnois, G. J. and Mitchell, T. J. (1993) Molecular analysis of the pathogenicity of Streptococcus pneumoniae: The role of pneumococcal proteins. Annu. Rev. Microbiol. 47, 89-115.
126. Paton, J. C., Berry, A. M., Lock, R. A., Hansman, D. and Manning, P. A. (1986) Cloning and expression in Escherichia coli of the Streptococcus pneumoniae gene encoding pneumolysin. Infect. Immun. 54, 50-55.
127. Paton, J. C., Lock, R. A. and Hansman, D. J. (1983) Effect of immunization with pneumolysin on survival time of mice challenged with Streptococcus pneumoniae. Infect. Immun. 40, 548-552.
128. Hirst, R. A., Kadioglu, A., O'Callaghan, C. and Andrew, P. W. (2004) The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin. Exp. Immunol. 138, 195-201.
129. Rayner, C. F., Jackson, A. D., Rutman, A., Dewar, A., Mitchell, T. J., Andrew, P. W., Cole, P. J. and Wilson, R. (1995) Interaction of pneumolysin-sufficient and-deficient isogenic variants of Streptococcus pneumoniae with human respiratory mucosa. Infect. Immun. 63, 442-447.
130. Steinfort, C., Wilson, R., Mitchell, T., Feldman, C., Rutman, A., Todd, H., Sykes, D., Walker, J., Saunders, K., Andrew, P. W., Boulnois, G. J. and Cole, P. J. (1989) Effect of Streptococcus pneumoniae on human respiratory epithelium in vitro. Infect. Immun. 57, 2006-2013.
131. Akira, S., Uematsu, S. and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801.
132. Medzhitov, R. (2001) Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135-145.
133. Martinon, F. and Tschopp, J. (2005) NLRs join TLRs as innate sensors of pathogens. Trends Immunol. 26, 447-454.
134. Gurcel, L., Abrami, L., Girardin, S., Tschopp, J. and van der Goot, F. G. (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126, 1135-1145.
135. Walev, I., Reske, K., Palmer, M., Valeva, A. and Bhakdi, S. (1995) Potassium-inhibited processing of IL-1 beta in human monocytes. EMBO J. 14, 1607-1614.
136. Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T. D., Ozoren, N., Jagirdar, R., Inohara, N., Vandenabeele, P., Bertin, J., Coyle, A., Grant, E. P. and Nunez, G. (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7, 576-582.
137. Bonizzi, G. and Karin, M. (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25, 280-288.
138. Dragneva, Y., Anuradha, C. D., Valeva, A., Hoffmann, A., Bhakdi, S. and Husmann, M. (2001) Subcytocidal attack by staphylococcal alpha-toxin activates NF-kappaB and induces interleukin-8 production. Infect. Immun. 69, 2630-2635.
139. Chopra, A. K., Xu, X., Ribardo, D., Gonzalez, M., Kuhl, K., Peterson, J. W. and Houston, C. W. (2000) The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infect. Immun. 68, 2808-2818.
140. Fickl, H., Cockeran, R., Steel, H. C., Feldman, C., Cowan, G., Mitchell, T. J. and Anderson, R. (2005) Pneumolysin-mediated activation of NFkappaB in human neutrophils is antagonized by docosahexaenoic acid. Clin. Exp. Immunol. 140, 274-281.
141. Kayal, S., Lilienbaum, A., Join-Lambert, O., Li, X., Israel, A. and Berche, P. (2002) Listeriolysin O secreted by Listeria monocytogenes induces NF-kappaB signalling by activating the IkappaB kinase complex. Mol. Microbiol. 44, 1407-1419.
142. Martinon, F., Burns, K. and Tschopp, J. (2002) The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10, 417-426.
143. Dinarello, C. A. (1998) Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann. N. Y. Acad. Sci. 856, 1-11.
144. Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., Lee, W. P., Weinrauch, Y., Monack, D. M. and Dixit, V. M. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232.
145. Ozoren, N., Masumoto, J., Franchi, L., Kanneganti, T. D., Body-Malapel, M., Erturk, I., Jagirdar, R., Zhu, L., Inohara, N., Bertin, J., Coyle, A., Grant, E. P. and Nunez, G. (2006) Distinct roles of TLR2 and the adaptor ASC in IL-1beta/IL-18 secretion in response to Listeria monocytogenes. J. Immunol. 176, 4337-4342.
146. Cordoba-Rodriguez, R., Fang, H., Lankford, C. S. and Frucht, D. M. (2004) Anthrax lethal toxin rapidly activates caspase-1/ ICE and induces extracellular release of interleukin (IL)-1beta and IL-18. J. Biol. Chem. 279, 20563-20566.
147. Boyden, E. D. and Dietrich, W. F. (2006) Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38, 240-244.
148. Wickliffe, K. E., Leppla, S. H. and Moayeri, M. (2007) Anthrax lethal toxin-induced inflammasome formation and caspase-1 activation are late events dependent on ion fluxes and the proteasome. Cell Microbiol (in press).
149. Ren, T., Zamboni, D. S., Roy, C. R., Dietrich, W. F. and Vance, R. E. (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediatedmacrophage immunity. PLoS Pathog. 2, e18.
150. Miao, E. A., Alpuche-Aranda, C. M., Dors, M., Clark, A. E., Bader, M. W., Miller, S. I. and Aderem, A. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7, 569-575.
151. Zamboni, D. S., Kobayashi, K. S., Kohlsdorf, T., Ogura, Y., Long, E. M., Vance, R. E., Kuida, K., Mariathasan, S., Dixit, V. M., Flavell, R. A., Dietrich, W. F. and Roy, C. R. (2006) The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7, 318-325.
152. Shin, H. and Cornelis, G. R. (2007) Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of Pro-inflammatory IL-1beta. Cell. Microbiol. (in press).
153. Goldstein, J. L., DeBose-Boyd, R. A. and Brown, M. S. (2006) Protein sensors for membrane sterols. Cell 124, 35-46.
154. Huffman, D. L., Abrami, L., Sasik, R., Corbeil, J., van der Goot, F. G. and Aroian, R. V. (2004) Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc. Natl. Acad. Sci. USA 101, 10995-11000.
155. Kim, D. H., Feinbaum, R., Alloing, G., Emerson, F. E., Garsin, D. A., Inoue, H., Tanaka-Hino, M., Hisamoto, N., Matsumoto, K., Tan, M. W. and Ausubel, F. M. (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626.
156. Husmann, M., Dersch, K., Bobkiewicz, W., Beckmann, E., Veerachato, G. and Bhakdi, S. (2006) Differential role of p38 mitogen activated protein kinase for cellular recovery from attack by pore-forming S. aureus alpha-toxin or streptolysin O. Biochem. Biophys. Res. Commun. 344, 1128-1134.
157. Ratner, A. J., Hippe, K. R., Aguilar, J. L., Bender, M. H., Nelson, A. L. and Weiser, J. N. (2006) Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J. Biol. Chem. 281, 12994-12998.
158. Stassen, M., Muller, C., Richter, C., Neudorfl, C., Hultner, L., Bhakdi, S., Walev, I. and Schmitt, E. (2003) The streptococcal exotoxin streptolysin O activates mast cells to produce tumor necrosis factor alpha by p38 mitogen-activated protein kinase- and protein kinase C-dependent pathways. Infect. Immun. 71, 6171-6177.
159. Stringaris, A. K., Geisenhainer, J., Bergmann, F., Balshusemann, C., Lee, U., Zysk, G., Mitchell, T. J., Keller, B. U., Kuhnt, U., Gerber, J., Spreer, A., Bahr, M., Michel, U. and Nau, R. (2002) Neurotoxicity of pneumolysin, a major pneumococcal virulence factor, involves calcium influx and depends on activation of p38 mitogen-activated protein kinase. Neurobiol. Dis. 11, 355-368.
160. Haugwitz, U., Bobkiewicz, W., Han, S. R., Beckmann, E., Veerachato, G., Shaid, S., Biehl, S., Dersch, K., Bhakdi, S. and Husmann, M. (2006) Pore-forming Staphylococcus aureusalpha-toxin triggers epidermal growth factor receptor-dependent proliferation. Cell. Microbiol. 8, 1591-1600.
161. Gutierrez, M. G., Saka, H. A., Chinen, I., Zoppino, F. C., Yoshimori, T., Bocco, J. L. and Colombo, M. I. (2007) Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae. Proc. Natl. Acad. Sci. USA 104, 1829-1834.
162. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I. and Deretic, V. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766.
163. Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., Nara, A., Funao, J., Nakata, M., Tsuda, K., Hamada, S. and Yoshimori, T. (2004) Autophagy defends cells against invading group A Streptococcus. Science 306, 1037-1040.
164. Suzuki, T., Franchi, L., Toma, C., Ashida, H., Ogawa, M., Yoshikawa, Y., Mimuro, H., Inohara, N., Sasakawa, C. and Nunez, G. (2007) Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 3, e111.
165. Walev, I., Palmer, M., Martin, E., Jonas, D., Weller, U., Hohn-Bentz, H., Husmann, M. and Bhakdi, S. (1994) Recovery of human fibroblasts from attack by the pore-forming alpha-toxin of Staphylococcus aureus. Microb. Pathog. 17, 187-201.
166. McNeil, P. L. and Steinhardt, R. A. (2003) Plasma membrane disruption: Repair, prevention, adaptation. Annu. Rev. Cell Dev. Biol. 19, 697-731.
167. Lesieur, C., Frutiger, S., Hughes, G., Kellner, R., Pattus, F. and van Der Goot, F. G. (1999) Increased stability upon heptamerization of the pore-forming toxin aerolysin. J. Biol. Chem. 274, 36722-36728.
168. Griffitts, J. S., Haslam, S. M., Yang, T., Garczynski, S. F., Mulloy, B., Morris, H., Cremer, P. S., Dell, A., Adang, M. J. and Aroian, R. V. (2005) Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 307, 922-925.
169. Duncan, J. L. and Schlegel, R. (1975) Effect of streptolysin O on erythrocyte membranes, liposomes, and lipid dispersions. A protein-cholesterol interaction. J. Cell Biol. 67, 160-174.
170. Naglich, J. G., Metherall, J. E., Russell, D. W. and Eidels, L. (1992) Expression cloning of a diphtheria toxin receptor: Identity with a heparin-binding EGF-like growth factor precursor. Cell 69, 1051-1061.
171. Saha, N. and Banerjee, K. K. (1997) Carbohydrate-mediated regulation of interaction of Vibrio cholerae hemolysin with erythrocyte and phospholipid vesicle. J. Biol. Chem. 272, 162-167.