Pathogenic pore-forming proteins: Function and host response

Cell Host and Microbe

Volumn 12, Issue 3, 2012, Pages 266-275

  Bischofberger, Mirko ^a   Iacovache, Ioan ^a   Gisou Van Der Goot, F ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AEROLYSIN; ALPHA HEMOLYSIN; ALPHA TOXIN; CALCIUM; CALPAIN; CASPASE 3; CASPASE 8; CASPASE 9; CHOLERA TOXIN; CLOSTRIDIUM PERFRINGENS TOXIN; COLICIN A; DIPHTHERIA TOXIN; ENTEROLOBIN; EQUINATOXIN; HYDRALYSIN; INITIATION FACTOR 2ALPHA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERMEDILYSIN; LISTERIOLYSIN O; LYSENIN; PERFORIN; PLEUROTOLYSIN; PORE FORMING CYTOTOXIC PROTEIN; POTASSIUM; PROTEIN BAK; PROTEIN BAX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SPHINGOMYELIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACID BASE BALANCE; APOPTOSIS; ARTICLE; AUTOPHAGY; BACILLUS THURINGIENSIS; CALCIUM TRANSPORT; CELL DEATH; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL METABOLISM; CELL PROLIFERATION; CELL SURVIVAL; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR MOUSE; CYTOPLASM; ENDOCYTOSIS; ENDOSOME; ENERGY METABOLISM; ENZYME ACTIVATION; IMMUNE RESPONSE; INFLAMMATION; INTERNALIZATION; LEGIONELLA PNEUMOPHILA; LIPID RAFT; LISTERIA MONOCYTOGENES; LYSOSOME; MEMBRANE DAMAGE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

BACTERIA (MICROORGANISMS);

EID: 84866418820     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.08.005     Document Type: Review

References (118)

1. L. Abrami, M. Fivaz, and F.G. van der Goot Adventures of a pore-forming toxin at the target cell surface Trends Microbiol. 8 2000 168 172
2. L. Abrami, and F.G. van Der Goot Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin J. Cell Biol. 147 1999 175 184
3. J.L. Aguilar, R. Kulkarni, T.M. Randis, S. Soman, A. Kikuchi, Y. Yin, and A.J. Ratner Phosphatase-dependent regulation of epithelial mitogen-activated protein kinase responses to toxin-induced membrane pores PLoS ONE 4 2009 e8076
4. E.B. Babiychuk, K. Monastyrskaya, S. Potez, and A. Draeger Intracellular Ca(2+) operates a switch between repair and lysis of streptolysin O-perforated cells Cell Death Differ. 16 2009 1126 1134
5. E.B. Babiychuk, K. Monastyrskaya, S. Potez, and A. Draeger Blebbing confers resistance against cell lysis Cell Death Differ. 18 2011 80 89
6. A. Bellier, C.S. Chen, C.Y. Kao, H.N. Cinar, and R.V. Aroian Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans PLoS Pathog. 5 2009 e1000689
7. A.W. Bernheimer Some aspects of the history of membrane-damaging toxins Med. Microbiol. Immunol. (Berl.) 185 1996 59 63
8. C.L. Birmingham, V. Canadien, N.A. Kaniuk, B.E. Steinberg, D.E. Higgins, and J.H. Brumell Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles Nature 451 2008 350 354
9. L.J. Bischof, C.Y. Kao, F.C. Los, M.R. Gonzalez, Z. Shen, S.P. Briggs, F.G. van der Goot, and R.V. Aroian Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo PLoS Pathog. 4 2008 e1000176
10. P. Boquet, and V. Ricci Intoxication strategy of Helicobacter pylori VacA toxin Trends Microbiol. 20 2012 165 174
11. A. Bouter, C. Gounou, R. Bérat, S. Tan, B. Gallois, T. Granier, B.L. d'Estaintot, E. Pöschl, B. Brachvogel, and A.R. Brisson Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair Nat Commun. 2 2011 270
12. J.S. Braun, O. Hoffmann, M. Schickhaus, D. Freyer, E. Dagand, D. Bermpohl, T.J. Mitchell, I. Bechmann, and J.R. Weber Pneumolysin causes neuronal cell death through mitochondrial damage Infect. Immun. 75 2007 4245 4254
13. I.E. Brodsky, N.W. Palm, S. Sadanand, M.B. Ryndak, F.S. Sutterwala, R.A. Flavell, J.B. Bliska, and R. Medzhitov A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system Cell Host Microbe 7 2010 376 387
14. R. Bücker, S.M. Krug, R. Rosenthal, D. Günzel, A. Fromm, M. Zeitz, T. Chakraborty, M. Fromm, H.J. Epple, and J.D. Schulzke Aerolysin from Aeromonas hydrophila perturbs tight junction integrity and cell lesion repair in intestinal epithelial HT-29/B6 cells J. Infect. Dis. 204 2011 1283 1292
15. L. Bumba, J. Masin, R. Fiser, and P. Sebo Bordetella adenylate cyclase toxin mobilizes its beta2 integrin receptor into lipid rafts to accomplish translocation across target cell membrane in two steps PLoS Pathog. 6 2010 e1000901
16. S. Chakrabarti, P. Liehl, N. Buchon, and B. Lemaitre Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut Cell Host Microbe 12 2012 60 70
17. C.S. Chen, A. Bellier, C.Y. Kao, Y.L. Yang, H.D. Chen, F.C. Los, and R.V. Aroian WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans PLoS ONE 5 2010 e9494
18. E. Cocucci, G. Racchetti, and J. Meldolesi Shedding microvesicles: artefacts no more Trends Cell Biol. 19 2009 43 51
19. M. Corrotte, M.C. Fernandes, C. Tam, and N.W. Andrews Toxin pores endocytosed during plasma membrane repair traffic into the lumen of MVBs for degradation Traffic 13 2012 483 494
20. U. Coskun, and K. Simons Cell membranes: the lipid perspective Structure 19 2011 1543 1548
21. R.R. Craven, X. Gao, I.C. Allen, D. Gris, J. Bubeck Wardenburg, E. McElvania-Tekippe, J.P. Ting, and J.A. Duncan Staphylococcus aureus alpha-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells PLoS ONE 4 2009 e7446
22. B.K. Dhakal, and M.A. Mulvey The UPEC pore-forming toxin α-hemolysin triggers proteolysis of host proteins to disrupt cell adhesion, inflammatory, and survival pathways Cell Host Microbe 11 2012 58 69
23. Y. Dragneva, C.D. Anuradha, A. Valeva, A. Hoffmann, S. Bhakdi, and M. Husmann Subcytocidal attack by staphylococcal alpha-toxin activates NF-kappaB and induces interleukin-8 production Infect. Immun. 69 2001 2630 2635
24. T.L. Dunbar, Z. Yan, K.M. Balla, M.G. Smelkinson, and E.R. Troemel C. elegans detects pathogen-induced translational inhibition to activate immune signaling Cell Host Microbe 11 2012 375 386
25. A. Dunne, P.J. Ross, E. Pospisilova, J. Masin, A. Meaney, C.E. Sutton, Y. Iwakura, J. Tschopp, P. Sebo, and K.H. Mills Inflammasome activation by adenylate cyclase toxin directs Th17 responses and protection against Bordetella pertussis J. Immunol. 185 2010 1711 1719
26. F. Essmann, H. Bantel, G. Totzke, I.H. Engels, B. Sinha, K. Schulze-Osthoff, and R.U. Jänicke Staphylococcus aureus alpha-toxin-induced cell death: predominant necrosis despite apoptotic caspase activation Cell Death Differ. 10 2003 1260 1272
27. R. Fiser, J. Masin, L. Bumba, E. Pospisilova, C. Fayolle, M. Basler, L. Sadilkova, I. Adkins, J. Kamanova, and J. Cerny Calcium influx rescues adenylate cyclase-hemolysin from rapid cell membrane removal and enables phagocyte permeabilization by toxin pores PLoS Pathog. 8 2012 e1002580
28. M.F. Fontana, S. Banga, K.C. Barry, X. Shen, Y. Tan, Z.Q. Luo, and R.E. Vance Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila PLoS Pathog. 7 2011 e1001289
29. K. Fujita, J. Katahira, Y. Horiguchi, N. Sonoda, M. Furuse, and S. Tsukita Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein FEBS Lett. 476 2000 258 261
30. N.O. Gekara, K. Westphal, B. Ma, M. Rohde, L. Groebe, and S. Weiss The multiple mechanisms of Ca2+ signalling by listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes Cell. Microbiol. 9 2007 2008 2021
31. M.R. Gonzalez, M. Bischofberger, B. Frêche, S. Ho, R.G. Parton, and F.G. van der Goot Pore-forming toxins induce multiple cellular responses promoting survival Cell. Microbiol. 13 2011 1026 1043
32. N. Groulx, H. McGuire, R. Laprade, J.L. Schwartz, and R. Blunck Single molecule fluorescence study of the Bacillus thuringiensis toxin Cry1Aa reveals tetramerization J. Biol. Chem. 286 2011 42274 42282
33. L. Gurcel, L. Abrami, S. Girardin, J. Tschopp, and F.G. van der Goot Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival Cell 126 2006 1135 1145
34. M.G. Gutierrez, H.A. Saka, I. Chinen, F.C. Zoppino, T. Yoshimori, J.L. Bocco, and M.I. Colombo Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae Proc. Natl. Acad. Sci. USA 104 2007 1829 1834
35. M.A. Hamon, D. Ribet, F. Stavru, and P. Cossart Listeriolysin O: the Swiss army knife of Listeria Trends Microbiol. 20 2012 360 368
36. M.A. Hamon, E. Batsché, B. Régnault, T.N. Tham, S. Seveau, C. Muchardt, and P. Cossart Histone modifications induced by a family of bacterial toxins Proc. Natl. Acad. Sci. USA 104 2007 13467 13472
37. M.A. Hamon, and P. Cossart K+ efflux is required for histone H3 dephosphorylation by Listeria monocytogenes listeriolysin O and other pore-forming toxins Infect. Immun. 79 2011 2839 2846
38. C.S. Hayes, S.K. Aoki, and D.A. Low Bacterial contact-dependent delivery systems Annu. Rev. Genet. 44 2010 71 90
39. T. Hoegen, N. Tremel, M. Klein, B. Angele, H. Wagner, C. Kirschning, H.W. Pfister, A. Fontana, S. Hammerschmidt, and U. Koedel The NLRP3 inflammasome contributes to brain injury in pneumococcal meningitis and is activated through ATP-dependent lysosomal cathepsin B release J. Immunol. 187 2011 5440 5451
40. E.M. Hotze, and R.K. Tweten Membrane assembly of the cholesterol- dependent cytolysin pore complex Biochim. Biophys. Acta 1818 2012 1028 1038
41. D.L. Huffman, L. Abrami, R. Sasik, J. Corbeil, F.G. van der Goot, and R.V. Aroian Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins Proc. Natl. Acad. Sci. USA 101 2004 10995 11000
42. M. Husmann, E. Beckmann, K. Boller, N. Kloft, S. Tenzer, W. Bobkiewicz, C. Neukirch, H. Bayley, and S. Bhakdi Elimination of a bacterial pore-forming toxin by sequential endocytosis and exocytosis FEBS Lett. 583 2009 337 344
43. M. Husmann, K. Dersch, W. Bobkiewicz, E. Beckmann, G. Veerachato, and S. Bhakdi 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 2006 1128 1134
44. 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
45. V. Idone, C. Tam, J.W. Goss, D. Toomre, M. Pypaert, and N.W. Andrews Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis J. Cell Biol. 180 2008 905 914
46. S.S. Im, and T.F. Osborne Protection from bacterial-toxin-induced apoptosis in macrophages requires the lipogenic transcription factor sterol regulatory element binding protein 1a Mol. Cell Biol. 32 2012 2196 2202
47. S.S. Im, L. Yousef, C. Blaschitz, J.Z. Liu, R.A. Edwards, S.G. Young, M. Raffatellu, and T.F. Osborne Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a Cell Metab. 13 2011 540 549
48. G. Imre, J. Heering, A.N. Takeda, M. Husmann, B. Thiede, D.M. zu Heringdorf, D.R. Green, F.G. van der Goot, B. Sinha, V. Dötsch, and K. Rajalingam Caspase-2 is an initiator caspase responsible for pore-forming toxin-mediated apoptosis EMBO J. 31 2012 2615 2628
49. I. Inoshima, N. Inoshima, G.A. Wilke, M.E. Powers, K.M. Frank, Y. Wang, and J. Bubeck Wardenburg A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice Nat. Med. 17 2011 1310 1314
50. N. Inoshima, Y. Wang, and J.B. Wardenburg Genetic requirement for ADAM10 in severe Staphylococcus aureus skin infection J. Invest. Dermatol. 132 2012 1513 1516
51. T.I. Jeon, and T.F. Osborne SREBPs: metabolic integrators in physiology and metabolism Trends Endocrinol. Metab. 23 2012 65 72
52. R. Jiang, A. Taly, D. Lemoine, A. Martz, O. Cunrath, and T. Grutter Tightening of the ATP-binding sites induces the opening of P2X receptor channels EMBO J. 31 2012 2134 2143
53. B.F. Kafsack, J.D. Pena, I. Coppens, S. Ravindran, J.C. Boothroyd, and V.B. Carruthers Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells Science 323 2009 530 533
54. B.L. Kagan Membrane pores in the pathogenesis of neurodegenerative disease Prog. Mol. Biol. Transl. Sci. 107 2012 295 325
55. C.Y. Kao, F.C. Los, D.L. Huffman, S. Wachi, N. Kloft, M. Husmann, V. Karabrahimi, J.L. Schwartz, A. Bellier, and C. Ha Global functional analyses of cellular responses to pore-forming toxins PLoS Pathog. 7 2011 e1001314
56. S. Kayal, A. Lilienbaum, O. Join-Lambert, X. Li, A. Israël, and P. Berche Listeriolysin O secreted by Listeria monocytogenes induces NF-kappaB signalling by activating the IkappaB kinase complex Mol. Microbiol. 44 2002 1407 1419
57. D. Keefe, L. Shi, S. Feske, R. Massol, F. Navarro, T. Kirchhausen, and J. Lieberman Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis Immunity 23 2005 249 262
58. H. Keiser, G. Weissmann, and A.W. Bernheimer Studies on Lysosomes. Iv. Solubilization of Enzymes during Mitochondrial Swelling and Disruption of Lysosomes by Streptolysin S and Other Hemolytic Agents J. Cell Biol. 22 1964 101 113
59. C.L. Kennedy, D.J. Smith, D. Lyras, A. Chakravorty, and J.I. Rood Programmed cellular necrosis mediated by the pore-forming alpha-toxin from Clostridium septicum PLoS Pathog. 5 2009 e1000516
60. P.A. Keyel, L. Loultcheva, R. Roth, R.D. Salter, S.C. Watkins, W.M. Yokoyama, and J.E. Heuser Streptolysin O clearance through sequestration into blebs that bud passively from the plasma membrane J. Cell Sci. 124 2011 2414 2423
61. N. Kloft, T. Busch, C. Neukirch, S. Weis, F. Boukhallouk, W. Bobkiewicz, I. Cibis, S. Bhakdi, and M. Husmann Pore-forming toxins activate MAPK p38 by causing loss of cellular potassium Biochem. Biophys. Res. Commun. 385 2009 503 506
62. N. Kloft, C. Neukirch, W. Bobkiewicz, G. Veerachato, T. Busch, G. von Hoven, K. Boller, and M. Husmann Pro-autophagic signal induction by bacterial pore-forming toxins Med. Microbiol. Immunol. (Berl.) 199 2010 299 309
63. O. Knapp, E. Maier, S.B. Mkaddem, R. Benz, M. Bens, A. Chenal, B. Geny, A. Vandewalle, and M.R. Popoff Clostridium septicum alpha-toxin forms pores and induces rapid cell necrosis Toxicon 55 2010 61 72
64. K.C. Kristan, G. Viero, M. Dalla Serra, P. Macek, and G. Anderluh Molecular mechanism of pore formation by actinoporins Toxicon 54 2009 1125 1134
65. Y.K. Kwak, E. Vikström, K.E. Magnusson, B. Vécsey- Semjén, P. Colque-Navarro, and R. Möllby The Staphylococcus aureus alpha-toxin perturbs the barrier function in Caco-2 epithelial cell monolayers by altering junctional integrity Infect. Immun. 80 2012 1670 1680
66. F. Lafont, L. Abrami, and F.G. van der Goot Bacterial subversion of lipid rafts Curr. Opin. Microbiol. 7 2004 4 10
67. J.H. Lakey, F.G. van der Goot, and F. Pattus All in the family: the toxic activity of pore-forming colicins Toxicology 87 1994 85 108
68. G.Y. Lam, R. Fattouh, A.M. Muise, S. Grinstein, D.E. Higgins, and J.H. Brumell Listeriolysin O suppresses phospholipase C-mediated activation of the microbicidal NADPH oxidase to promote Listeria monocytogenes infection Cell Host Microbe 10 2011 627 634
69. B. Levine, and G. Kroemer Autophagy in the pathogenesis of disease Cell 132 2008 27 42
70. L.A. Ligeon, N. Temime-Smaali, and F. Lafont Ubiquitylation and autophagy in the control of bacterial infections and related inflammatory responses Cell. Microbiol. 13 2011 1303 1311
71. C.F. Lin, C.L. Chen, W.C. Huang, Y.L. Cheng, C.Y. Hsieh, C.Y. Wang, and M.Y. Hong Different types of cell death induced by enterotoxins Toxins (Basel) 2 2010 2158 2176
72. I. Linhartová, L. Bumba, J. Mašín, M. Basler, R. Osička, J. Kamanová, K. Procházková, I. Adkins, J. Hejnová-Holubová, and L. Sadílková RTX proteins: a highly diverse family secreted by a common mechanism FEMS Microbiol. Rev. 34 2010 1076 1112
73. M. Lizak, and T.O. Yarovinsky Phospholipid scramblase 1 mediates type i interferon-induced protection against staphylococcal α-toxin Cell Host Microbe 11 2012 70 80
74. S. Locovei, E. Scemes, F. Qiu, D.C. Spray, and G. Dahl Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex FEBS Lett. 581 2007 483 488
75. F.C. Los, C.Y. Kao, J. Smitham, K.L. McDonald, C. Ha, C.A. Peixoto, and R.V. Aroian RAB-5- and RAB-11-dependent vesicle-trafficking pathways are required for plasma membrane repair after attack by bacterial pore-forming toxin Cell Host Microbe 9 2011 147 157
76. A.J. McCoy, Y. Koizumi, N. Higa, and T. Suzuki Differential regulation of caspase-1 activation via NLRP3/NLRC4 inflammasomes mediated by aerolysin and type III secretion system during Aeromonas veronii infection J. Immunol. 185 2010 7077 7084
77. A.J. McCoy, Y. Koizumi, C. Toma, N. Higa, V. Dixit, S. Taniguchi, J. Tschopp, and T. Suzuki Cytotoxins of the human pathogen Aeromonas hydrophila trigger, via the NLRP3 inflammasome, caspase-1 activation in macrophages Eur. J. Immunol. 40 2010 2797 2803
78. E.A. McNeela, A. Burke, D.R. Neill, C. Baxter, V.E. Fernandes, D. Ferreira, S. Smeaton, R. El-Rachkidy, R.M. McLoughlin, and A. Mori Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4 PLoS Pathog. 6 2010 e1001191
79. P.L. McNeil, and R.A. Steinhardt Plasma membrane disruption: repair, prevention, adaptation Annu. Rev. Cell Dev. Biol. 19 2003 697 731
80. K. Meixenberger, F. Pache, J. Eitel, B. Schmeck, S. Hippenstiel, H. Slevogt, P. N'Guessan, M. Witzenrath, M.G. Netea, and T. Chakraborty Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1beta, depending on listeriolysin O and NLRP3 J. Immunol. 184 2010 922 930
81. M.B. Mestre, C.M. Fader, C. Sola, and M.I. Colombo Alpha-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells Autophagy 6 2010 110 125
82. 7 receptor in infectious diseases PLoS Pathog. 7 2011 e1002212
83. B.P. Morgan, M. Daha, S. Meri, and A. Nicholson-Weller Into the third century of complement research Immunol. Today 21 2000 603 605
84. K.L. Nelson, and J.T. Buckley Channel formation by the glycosylphosphatidylinositol-anchored protein binding toxin aerolysin is not promoted by lipid rafts J. Biol. Chem. 275 2000 19839 19843
85. O. Opota, I. Vallet-Gély, R. Vincentelli, C. Kellenberger, I. Iacovache, M.R. Gonzalez, A. Roussel, F.G. van der Goot, and B. Lemaitre Monalysin, a novel ß-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality PLoS Pathog. 7 2011 e1002259
86. A. Osickova, J. Masin, C. Fayolle, J. Krusek, M. Basler, E. Pospisilova, C. Leclerc, R. Osicka, and P. Sebo Adenylate cyclase toxin translocates across target cell membrane without forming a pore Mol. Microbiol. 75 2010 1550 1562
87. P. Pelegrin, and A. Surprenant Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor EMBO J. 25 2006 5071 5082
88. H. Pillich, M. Loose, K.P. Zimmer, and T. Chakraborty Activation of the unfolded protein response by Listeria monocytogenes Cell. Microbiol. 14 2012 949 964
89. H. Porta, A. Cancino-Rodezno, M. Soberon, and A. Bravo Role of MAPK p38 in the cellular responses to pore-forming toxins Peptides 32 2010 601 606
90. J.N. Radin, C. González-Rivera, S.E. Ivie, M.S. McClain, and T.L. Cover Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells Infect. Immun. 79 2011 2535 2543
91. A.L. Radtke, K.L. Anderson, M.J. Davis, M.J. DiMagno, J.A. Swanson, and M.X. O'Riordan Listeria monocytogenes exploits cystic fibrosis transmembrane conductance regulator (CFTR) to escape the phagosome Proc. Natl. Acad. Sci. USA 108 2011 1633 1638
92. J. Rassow Helicobacter pylori vacuolating toxin A and apoptosis Cell Commun. Signal. 9 2011 26
93. V.A. Rathinam, S.K. Vanaja, and K.A. Fitzgerald Regulation of inflammasome signaling Nat. Immunol. 13 2012 333-2
94. A.J. Ratner, K.R. Hippe, J.L. Aguilar, M.H. Bender, A.L. Nelson, and J.N. Weiser Epithelial cells are sensitive detectors of bacterial pore-forming toxins J. Biol. Chem. 281 2006 12994 12998
95. N. Reig, and F.G. van der Goot About lipids and toxins FEBS Lett. 580 2006 5572 5579
96. D. Ribet, M. Hamon, E. Gouin, M.A. Nahori, F. Impens, H. Neyret-Kahn, K. Gevaert, J. Vandekerckhove, A. Dejean, and P. Cossart Listeria monocytogenes impairs SUMOylation for efficient infection Nature 464 2010 1192 1195
97. M.V. Rodnin, A. Kyrychenko, P. Kienker, O. Sharma, Y.O. Posokhov, R.J. Collier, A. Finkelstein, and A.S. Ladokhin Conformational switching of the diphtheria toxin T domain J. Mol. Biol. 402 2010 1 7
98. R. Sato SREBPs: protein interaction and SREBPs FEBS J. 276 2009 622 627
99. M. Skals, N.R. Jorgensen, J. Leipziger, and H.A. Praetorius Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis Proc. Natl. Acad. Sci. USA 106 2009 4030 4035
100. M. Skals, J. Leipziger, and H.A. Praetorius Haemolysis induced by α-toxin from Staphylococcus aureus requires P2X receptor activation Pflugers Arch. 462 2011 669 679
101. G. Soong, J. Chun, D. Parker, and A. Prince S. aureus activation of caspase-1/calpain signaling mediates invasion through human keratinocytes J. Infect. Dis. 205 2012 1571 1579
102. F. Stavru, F. Bouillaud, A. Sartori, D. Ricquier, and P. Cossart Listeria monocytogenes transiently alters mitochondrial dynamics during infection Proc. Natl. Acad. Sci. USA 108 2011 3612 3617
103. C. Tam, V. Idone, C. Devlin, M.C. Fernandes, A. Flannery, X. He, E. Schuchman, I. Tabas, and N.W. Andrews Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair J. Cell Biol. 189 2010 1027 1038
104. I. Tattoli, M.T. Sorbara, D. Vuckovic, A. Ling, F. Soares, L.A. Carneiro, C. Yang, A. Emili, D.J. Philpott, and S.E. Girardin Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program Cell Host Microbe 11 2012 563 575
105. M. Thelestam, and R. Mollby Survival of cultured cells after functional and structural disorganization of plasma membrane by bacterial haemolysins and phospholipases Toxicon 21 1983 805 815
106. N. Tomita, K. Abe, Y. Kamio, and M. Ohta Cluster-forming property correlated with hemolytic activity by staphylococcal γ-hemolysin transmembrane pores FEBS Lett. 585 2011 3452 3456
107. B. Turk, S.A. Turk, and V. Turk Protease signalling: the cutting edge EMBO J. 31 2012 1630 1643
108. P. Uhlén, A. Laestadius, T. Jahnukainen, T. Söderblom, F. Bäckhed, G. Celsi, H. Brismar, S. Normark, A. Aperia, and A. Richter-Dahlfors Alpha-haemolysin of uropathogenic E. coli induces Ca2+ oscillations in renal epithelial cells Nature 405 2000 694 697
109. F.G. van der Goot, G. Tran van Nhieu, A. Allaoui, P. Sansonetti, and F. Lafont Rafts can trigger contact-mediated secretion of bacterial effectors via a lipid-based mechanism J. Biol. Chem. 279 2004 47792 47798
110. G. van der Goot, and J.A. Young Receptors of anthrax toxin and cell entry Mol. Aspects Med. 30 2009 406 412
111. J. Verove, C. Bernarde, Y.S. Bohn, F. Boulay, M.J. Rabiet, I. Attree, and F. Cretin Injection of Pseudomonas aeruginosa Exo toxins into host cells can be modulated by host factors at the level of translocon assembly and/or activity PLoS ONE 7 2012 e30488
112. I. Walev, S.C. Bhakdi, F. Hofmann, N. Djonder, A. Valeva, K. Aktories, and S. Bhakdi Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O Proc. Natl. Acad. Sci. USA 98 2001 3185 3190
113. I. Walev, M. Hombach, W. Bobkiewicz, D. Fenske, S. Bhakdi, and M. Husmann Resealing of large transmembrane pores produced by streptolysin O in nucleated cells is accompanied by NF-kappaB activation and downstream events FASEB J. 16 2002 237 239
114. I. Walev, K. Reske, M. Palmer, A. Valeva, and S. Bhakdi Potassium-inhibited processing of IL-1 beta in human monocytes EMBO J. 14 1995 1607 1614
115. T.J. Wiles, B.K. Dhakal, D.S. Eto, and M.A. Mulvey Inactivation of host Akt/protein kinase B signaling by bacterial pore-forming toxins Mol. Biol. Cell 19 2008 1427 1438
116. G.A. Wilke, and J. Bubeck Wardenburg Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury Proc. Natl. Acad. Sci. USA 107 2010 13473 13478
117. A. Yamaji-Hasegawa, A. Makino, T. Baba, Y. Senoh, H. Kimura-Suda, S.B. Sato, N. Terada, S. Ohno, E. Kiyokawa, M. Umeda, and T. Kobayashi Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin J. Biol. Chem. 278 2003 22762 22770
118. T.O. Yarovinsky, M.M. Monick, M. Husmann, and G.W. Hunninghake Interferons increase cell resistance to Staphylococcal alpha-toxin Infect. Immun. 76 2008 571 577