Abstract
Toxins were the first bacterial virulence factors to be identified and were also the first link between bacteria and cell biology. Cellular microbiology was, in fact, naturally born a long time ago with the study of toxins, and only recently, thanks to the sophisticated new technologies, has it expanded to include the study of many other aspects of the interactions between bacteria and host cells. This chapter covers mostly the molecules that have been classically known as toxins; however, the last section also mentions some recently identified molecules that cause cell intoxication and have many but not all of the properties of classical toxins. Tables 22.1 and 22.2 show the known properties of all bacterial toxins described in this chapter, while Fig. 22.1 shows the subunit composition and the spatial organization of toxins whose structures have been solved either by X-ray crystallography or by quick-freeze deep-etch electron microscopy.
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References
Abrahmsen L, Dohlsten M, Segren S, Bjork P, Jonsson E, Kalland T (1995) Characterization of two distinct MHC class II binding sites in the superantigen staphylococcal enterotoxin A. EMBO J 14(13):2978–2986
Aili M, Telepnev M, Hallberg B, Wolf-Watz H, Rosqvist R (2003) In vitro GAP activity towards RhoA, Rac1 and Cdc42 is not a prerequisite for YopE induced HeLa cell cytotoxicity. Microb Pathog 34(6):297–308
Aktories K, Barmann M, Ohishi I, Tsuyama S, Jakobs KH, Habermann E (1986) Botulinum C2 toxin ADP-ribosylates actin. Nature 322:390–392
Aktories K (1994) Clostridial ADP-ribosylating toxins: effects on ATP and GTP-binding proteins. Mol Cell Biochem 138:167–176
Aktories K, Wegner A (1992) Mechanisms of the cytopathic action of actin-ADP-ribosylating toxins. Mol Microbiol 6(20):2905–2908
Allured VS, Collier RJ, Carroll SF, McKay DB (1986) Structure of exotoxin A of Pseudomonas aeruginosa at 3.0-Å resolution. Proc Natl Acad Sci USA 83(5):1320–1324
Alouf JE, Müller-Alouf H (2003) Staphylococcal and streptococcal superantigens: molecular, biological and clinical aspects. Int J Med Microbiol 292(7–8):429–440
Althaus FR, Richter C (1987) ADP-ribosylation of proteins: enzymology and biological significance. Mol Biol Biochem Biophys 37:1–237
Altwegg M, Geiss HK (1989) Aeromonas as a human pathogen. Crit Rev Microbiol 16:253–258
Antoine R, Tallett A, van Heyningen S, Locht C (1993) Evidence for a catalytic role of glutamic acid 129 in the NAD-glycohydrolase activity of the pertussis toxin S1 subunit. J Biol Chem 268:24149–24155
Atassi MZ, Oshima M (1999) Sructure, activity, and immune (T and B cell) recognition of botulinum neurotoxins. Crit Rev Immunol 19:219–260
Baker NR, Minor V, Deal C, Shahrabadi MS, Simpson DA, Woods DE (1991) Pseudomonas aeruginosa exoenzyme S is an adhesin. Infect Immun 59:2859–2863
Baldwin RL, Kobrin MS, Tran T, Pastan I, Korc M (1996) Cytotoxic effects of TGF-alpha-Pseudomonas exotoxin A fusion protein in human pancreatic carcinoma cells. Pancreas 13:16–21
Ballard J, Crabtree J, Roe BA, Tweten RK (1995) epticum alpha-toxin exhibits similarity with that of Aeromonas hydrophila aerolysin. Infect Immun 63:340–344
Barry EM, Weiss AA, Ehrmann IE, Gray MC, Hewlett EL, Goodwin MS (1991) Bordetella pertussis adenylate cyclase toxin and hemolytic activities require a second gene, cyaC, for activation. J Bacteriol 173:720–726
Barth H, Preiss JC, Hofmann F, Aktories K (1998) Characterization of the catalytic site of the ADP-ribosyltransferase Clostridium botulinum C2 toxin by site-directed mutagenesis. J Biol Chem 273:29506–29511
Barz C, Abahji TN, Trulzsch K, Heesemann J (2000) The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac-1. FEBS Lett 482(1–2):139–143
Beecher DJ, Wong AC (1997) Tripartite hemolysin BL from Bacillus cereus. Hemolytic analysis of component interactions and a model for its characteristic paradoxical zone phenomenon. J Biol Chem 272(1):233–239
Beecher DJ, Wong AC (2000) Tripartite haemolysin BL: isolation and characterization of two distinct homologous sets of components from a single Bacillus cereus isolate. Microbiology 146(Pt 6):1371–1380
Bejerano M, Nisan I, Ludwig A, Goebel W, Hanski E (1999) Characterization of the C-terminal domain essential for toxic activity of adenylate cyclase toxin. Mol Microbiol 31(1):381–392
Bell CE, Eisenberg D (1996) Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Biochemistry 35:1137–1149
Bell CE, Eisenberg D (1997) Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Adv Exp Med Biol 419:35–43
Bennett MJ, Eisenberg D (1994) Refined structure of monomeric diphtheria toxin at 2.3 Å resolution. Protein Sci 3:1464–1475
Bhakdi S, Grimminger F, Suttorp N, Walmrath D, Seeger W (1994) Proteinaceous bacterial toxins and pathogenesis of sepsis syndrome and septic shock: the unknown connection. Med Microbiol Immunol (Berl) 183:119–144
Billington SJ, Jost BH, Songer JG (2000) Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol Lett 182:197–205
Blackman MA, Woodland DL (1995) In vivo effects of superantigens. Life Sci 57:1717–1735
Blanke SR, Huang K, Wilson BA, Papini E, Covacci A, Collier RJ (1994) Active-site mutations of the diphtheria toxin catalytic domain: role of histidine-21 in nicotinamide adenine dinucleotide binding and ADP-ribosylation of elongation factor 2. Biochemistry 33:5155–5161
Bliska JB (1995) Crystal structure of the Yersinia tyrosine phosphatase. Trends Microbiol 3:125–127
Bohach GA, Fast DJ, Nelson RD, Schlievert PM (1990) Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit Rev Microbiol 17(4):251–272
Booth BA, Boesman-Finkelstein M, Finkelstein RA (1984) Vibrio cholerae hemagglutinin/protease nicks cholera enterotoxin. Infect Immun 45:558–560
Bourdet-Sicard R, Rudiger M, Jockusch BM, Gounon P, Sansonetti PJ, Nhieu GT (1999) Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization. EMBO J 18:5853–5862
Braun V, Focareta T (1991) Pore-forming bacterial protein hemolysins (cytolysins). Crit Rev Microbiol 18:115–158
Brossier F, Weber-Levy M, Mock M, Sirard JC (2000) Role of toxin functional domains in anthrax pathogenesis. Infect Immun 68:1781–1786
Brown BA, Bodley JW (1979) Primary structure at the site in beef and wheat elongation factor 2 of ADP-ribosylation by diphtheria toxin. FEBS Lett 103:253–255
Bricker AL, Cywes C, Ashbaugh CD, Wessels MR (2002) NAD+-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol Microbiol 44(1):257–269
Buchwald G, Friebel A, Galán JE, Hardt WD, Wittinghofer A, Scheffzek K (2002) Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J 21(13):3286–3295
Buetow L, Flatau G, Chiu K, Boquet P, Ghosh P (2001) Structure of the Rho-activating domain of Escherichia coli cytotoxic necrotizing factor 1. Nat Struct Biol 8(7):584–588
Burnette WN, Cieplak W, Mar VL, Kaljot KT, Sato H, Keith JM (1988) Pertussis toxin S1 mutant with reduced enzyme activity and a conserved protective epitope. Science 242:72–74
Burnette WN, Mar VL, Platler BW, Schlotterbeck JD, McGinley MD, Stoney KS, Rohde MF, Kaslow HR (1991) Site-specific mutagenesis of the catalytic subunit of cholera toxin: substituting lysine for arginine 7 causes loss of activity. Infect Immun 59:4266–4270
Burns EH Jr, Marciel AM, Musser JM (1996) Activation of a 66-kilodalton human endothelial cell matrix metalloprotease by Streptococcus pyogenes extracellular cysteine protease. Infect Immun 64:4744–4750
Cabiaux V, Wolff C, Ruysschaert JM (1997) Interaction with a lipid membrane: a key step in bacterial toxins virulence. Int J Biol Macromol 21:285–298
Cahan R, Axelrad I, Safrin M, Ohman DE, Kessler E (2001) A secreted aminopeptidase of Pseudomonas aeruginosa. Identification, primary structure, and relationship to other aminopeptidases. J Biol Chem 276(47):43645–43652
Caprioli A, Donelli G, Falbo V, Possenti R, Roda LG, Roscetti G, Ruggeri FM (1984) A cell division-active protein from E coli. Biochem Biophys Res Commun 118:587–593
Carnoy C, Mullet C, Muller-Alouf H, Leteurtre E, Simonet M (2000) Superantigen YPMa exacerbates the virulence of Yersinia pseudotuberculosis in mice. Infect Immun 68(5):2553–2559
Carrero JA, Calderon B, Unanue ER (2004) Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J Immunol 172(8):4866–4874
Carroll SF, Collier RJ (1984) NAD binding site of diphtheria toxin: identification of a residue within the nicotinamide subsite by photochemical modification with NAD. Proc Natl Acad Sci USA 81:3307–3311
Carroll SF, McCloskey JA, Crain PF, Oppenheimer NJ, Marschner TM, Collier RJ (1985) Photoaffinity labeling of diphtheria toxin fragment A with NAD: structure of the photoproduct at position 148. Proc Natl Acad Sci USA 82:7237–7241
Cascon A, Yugueros J, Temprano A, Sanchez M, Hernanz C, Luengo JM, Naharro G (2000) A major secreted elastase is essential for pathogenicity of Aeromonas hydrophila. Infect Immun 68(6):3233–3241
Chang YF, Young R, Post D, Struck DK (1987) Identification and characterization of the Pasteurella haemolytica leukotoxin. Infect Immun 55:2348–2354
Chang YF, Young R, Struck DK (1989) Cloning and characterization of a hemolysin gene from Actinobacillus (Haemophilus) pleuropneumoniae. DNA 8:635–647
Chaudhary VK, FitzGerald DJ, Adhya S, Pastan I (1987) Activity of a recombinant fusion protein between transforming growth factor type alpha and Pseudomonas toxin. Proc Natl Acad Sci USA 84:4538–4542
Chaudhary VK, Mizukami T, Fuerst TR, FitzGerald DJ, Moss B, Pastan I, Berger EA (1988) Selective killing of HIV-infected cells by recombinant human CD4-Pseudomonas exotoxin hybrid protein. Nature 335:369–372
Chaudhary VK, Jinno Y, FitzGerald D, Pastan I (1990) Pseudomonas exotoxin contains a specific sequence at the carboxyl terminus that is required for cytotoxicity. Proc Natl Acad Sci USA 87:308–312
Cherla RP, Lee SY, Tesh VL (2003) Shiga toxins and apoptosis. FEMS Microbiol Lett 228(2):159–166
Choe S, Bennett MJ, Fujii G, Curmi PM, Kantardjieff KA, Collier RJ, Eisenberg D (1992) The crystal structure of diphtheria toxin. Nature 357:216–222
Christov NK, Imaishi H, Ohkawa H (1999) Green-tissue-specific expression of a reconstructed cry1C gene encoding the active fragment of Bacillus thuringiensis delta-endotoxin in haploid tobacco plants conferring resistance to Spodoptera litura. Biosci Biotechnol Biochem 63:1433–1444
Cieplak W, Burnette WN, Mar VL, Kaljot KT, Morris CF, Chen KK, Sato H, Keith JM (1988) Identification of a region in the S1 subunit of pertussis toxin that is required for enzymatic activity and that contributes to the formation of a neutralizing antigenic determinant. Proc Natl Acad Sci USA 85:4667–4671
Ciesla WP Jr, Bobak DA (1998) Clostridium difficile toxins A and B are cation-dependent UDP-glucose hydrolases with differing catalytic activities. J Biol Chem 273:16021–16026
Coburn PS, Hancock LE, Booth MC, Gilmore MS (1999) A novel means of self-protection, unrelated to toxin activation, confers immunity to the bactericidal effects of the Enterococcus faecalis cytolysin. Infect Immun 67(7):3339–3347
Cohen SH, Tang YJ, Silva J Jr (2000) Analysis of the pathogenicity locus in Clostridium difficile strains. J Infect Dis 181:659–663
Cole BC, Atkin CL (1991) The Mycoplasma arthritidis T-cell mitogen, MAM: a model superantigen. Immunol Today 12(8):271–276
Collier RJ, Westbrook EM, McKay DB, Eisenberg D (1982) X-ray grade crystals of diphtheria toxin. J Biol Chem 257:5283–5285
Collier RJ (1999) Mechanism of membrane translocation by anthrax toxin: insertion and pore formation by protective antigen. J Appl Microbiol 87:283
Collier RJ, Young JA (2003) Anthrax toxin. Annu Rev Cell Dev Biol 19:45–70
Cooney J, Kienle Z, Foster TJ, O’Toole PW (1993) The gamma-hemolysin locus of Staphylococcus aureus comprises three linked genes, two of which are identical to the genes for the F and S components of leukocidin. Infect Immun 61:768–771
Coote JG (1992) Structural and functional relationships among the RTX toxin determinants of Gram-negative bacteria. FEMS Microbiol Rev 8:137–161
Cortajarena AL, Goni FM, Ostolaza H (2003) A receptor-binding region in Escherichia coli alpha-haemolysin. J Biol Chem 278(21):19159–19163
Cortes-Bratti X, Chaves-Olarte E, Lagergard T, Thelestam M (1999) The cytolethal distending toxin from the chancroid bacterium Haemophilus ducreyi induces cell-cycle arrest in the G2 phase. J Clin Invest 103(1):107–115
Covacci A, Rappuoli R (1993) Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol Microbiol 8:429–434
Covacci A, Censini S, Bugnoli M, Petracca R, Burroni D, Macchia G, Massone A, Papini E, Xiang Z, Figura N et al (1993) Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci USA 90:5791–5795
Covacci A, Rappuoli R (2000) Tyrosine-phosphorylated bacterial proteins: Trojan horses for the host cell. J Exp Med 191:587–592
Cover TL, Blaser MJ (1992) Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem 267:10570–10575
Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP (1992) Crystal structures explain functional properties of two E. coli porins. Nature 358:727–733
Crawford JA, Kaper JB (2002) The N-terminus of enteropathogenic Escherichia coli (EPEC) Tir mediates transport across bacterial and eukaryotic cell membranes. Mol Microbiol 46(3):855–868
Cunningham K, Lacy DB, Mogridge J, Collier RJ (2002) Mapping the lethal factor and edema factor binding sites on oligomeric anthrax protective antigen. Proc Natl Acad Sci USA 99(10):7049–7053
Dallas WS, Falkow S (1980) Amino acid sequence homology between cholera toxin and Escherichia coli heat-labile toxin. Nature 288:499–501
De Rycke J, Guillot JF, Boivin R (1987) Cytotoxins in non-enterotoxigenic strains of Escherichia coli isolated from feces of diarrheic calves. Vet Microbiol 15:137–150
Ding X, Zeng H, Schiering N, Ringe D, Murphy JR (1996) Identification of the primary metal ion-activation sites of the diphtheria tox repressor by X-ray crystallography and site-directed mutational analysis. Nat Struct Biol 3:382–387
Dinges MM, Orwin PM, Schlievert PM (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13(1):16–34
Di Pierro M, Lu R, Uzzau S, Wang W, Margaretten K, Pazzani C, Maimone F, Fasano A (2001) Zonula occludens toxin structure-function analysis. Identification of the fragment biologically active on tight junctions and of the zonulin receptor binding domain. J Biol Chem 276(22):19160–19165
Domenighini M, Magagnoli C, Pizza M, Rappuoli R (1994) Common features of the NAD-binding and catalytic site of ADP-ribosylating toxins. Mol Microbiol 14:41–50
Domenighini M, Pizza M, Jobling MG, Holmes RK, Rappuoli R (1995) Identification of errors among database sequence entries and comparison of correct amino acid sequences for the heat-labile enterotoxins of Escherichia coli and Vibrio cholerae. Mol Microbiol 15:1165–1167
Donadini R, Liew CW, Kwan AH, Mackay JP, Fields BA (2004) Crystal and solution structures of a superantigen from Yersinia pseudotuberculosis reveal a jelly-roll fold. Structure (Camb) 12(1):145–156
Douce G, Giuliani MM, Giannelli V, Pizza MG, Rappuoli R, Dougan G (1998) Mucosal immunogenicity of genetically detoxified derivatives of heat labile toxin from Escherichia coli. Vaccine 16:1065–1073
Douglas CM, Collier RJ (1987) Exotoxin A of Pseudomonas aeruginosa: substitution of glutamic acid 553 with aspartic acid drastically reduces toxicity and enzymatic activity. J Bacteriol 169:4967–4971
Douglas CM, Collier RJ (1990) Pseudomonas aeruginosa exotoxin A: alterations of biological and biochemical properties resulting from mutation of glutamic acid 553 to aspartic acid. Biochemistry 29:5043–5049
Doye A, Mettouchi A, Bossis G, Clement R, Buisson-Touati C, Flatau G, Gagnoux L, Piechaczyk M, Boquet P, Lemichez E (2002) CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 111(4):553–564
Drobniewski FA, Ellar DJ (1989) Purification and properties of a 28-kilodalton hemolytic and mosquitocidal protein toxin of Bacillus thuringiensis subsp. darmstadiensis 73-E10-2. J Bacteriol 171:3060–3067
Drum CL, Yan SZ, Bard J, Shen YQ, Lu D, Soelaiman S, Grabarek Z, Bohm A, Tang WJ (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415(6870):396–402
Du J, Knowles BH, Li J, Ellar DJ (1999) Biochemical characterization of Bacillus thuringiensis cytolytic toxins in association with a phospholipid bilayer. Biochem J 338(Pt 1):185–193
Duche D, Corda Y, Geli V, Baty D (1999) Integration of the colicin A pore-forming domain into the cytoplasmic membrane of Escherichia coli. J Mol Biol 285:1965–1975
Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, Copeland TD, Ahn NG, Oskarsson MK, Fukasawa K, Paull KD, Vande Woude GF (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:734–737
Dussurget O, Cabanes D, Dehoux P, Lecuit M, Buchrieser C, Glaser P, Cossart P (2002) European Listeria genome consortium. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol Microbiol 45(4):1095–10106
el Baya A, Linnemann R, von Olleschik-Elbheim L, Robenek H, Schmidt MA (1997) Endocytosis and retrograde transport of pertussis toxin to the Golgi complex as a prerequisite for cellular intoxication. Eur J Cell Biol 73(1):40–48
Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, Igarashi K (1988) Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem 171:45–50
Escuyer V, Duflot E, Sezer O, Danchin A, Mock M (1988) Structural homology between virulence-associated bacterial adenylate cyclases. Gene 71:293–298
Evans HR, Sutton JM, Holloway DE, Ayriss J, Shone CC, Acharya KR (2003) The crystal structure of C3stau2 from Staphylococcus aureus and its complex with NAD. J Biol Chem 278(46):45924–45930
Evdokimov AG, Anderson DE, Routzahn KM, Waugh DS (2001) Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J Mol Biol 312(4):807–821
Evdokimov AG, Tropea JE, Routzahn KM, Waugh DS (2002) Crystal structure of the Yersinia pestis GTPase activator YopE. Protein Sci 11(2):401–408
Falbo V, Famiglietti M, Caprioli A (1992) Gene block encoding production of cytotoxic necrotizing factor 1 and hemolysin in Escherichia coli isolates from extraintestinal infections. Infect Immun 60:2182–2187
Fallman M, Andersson K, Hakansson S, Magnusson KE, Stendahl O, Wolf-Watz H (1995) Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect Immun 63:3117–3124
Felmlee T, Pellett S, Welch RA (1985) Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol 163:94–105
Felmlee T, Welch RA (1988) Alterations of amino acid repeats in the Escherichia coli hemolysin affect cytolytic activity and secretion. Proc Natl Acad Sci USA 85:5269–5273
Field M, Rao MC, Chang EB (1989a) Intestinal electrolyte transport and diarrheal disease (1). N Engl J Med 321:800–806
Field M, Rao MC, Chang EB (1989b) Intestinal electrolyte transport and diarrheal disease (2). N Engl J Med 321:879–883
Fields BA, Malchiodi EL, Li H, Ysern X, Stauffacher CV, Schlievert PM, Karjalainen K, Mariuzza RA (1996) Crystal structure of a T-cell receptor beta-chain complexed with a superantigen. Nature 384:188–192
Finck-Barbancon V, Duportail G, Meunier O, Colin DA (1993) Pore formation by a two-component leukocidin from Staphylococcus aureus within the membrane of human polymorphonuclear leukocytes. Biochim Biophys Acta 1182:275–282
Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, Cover TL, Solcia E (1999) Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol 188:220–226
Fivaz M, Abrami L, Tsitrin Y, van der Goot FG (2001) Aerolysin from Aeromonas hydrophila and related toxins. Curr Top Microbiol Immunol 257:35–52
Flores-Diaz M, Alape-Giron A (2003) Role of Clostridium perfringens phospholipase C in the pathogenesis of gas gangrene. Toxicon 42(8):979–986
Fontana MR, Manetti R, Giannelli V, Magagnoli C, Marchini A, Olivieri R, Domenighini M, Rappuoli R, Pizza M (1995) Construction of nontoxic derivatives of cholera toxin and characterization of the immunological response against the A subunit. Infect Immun 63:2356–2360
Fotinou C, Emsley P, Black I, Ando H, Ishida H, Kiso M, Sinha KA, Fairweather NF, Isaacs NW (2001) The crystal structure of tetanus toxin Hc fragment complexed with a synthetic GT1b analogue suggests cross-linking between ganglioside receptors and the toxin. J Biol Chem 276(34):32274–32281
Fraser ME, Chernaia MM, Kozlov YV, James MN (1994) Crystal structure of the holotoxin from Shigella dysenteriae at 2.5 Å resolution. Nat Struct Biol 1:59–64
Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401
Frey J, Kuhnert P (2002) RTX toxins in Pasteurellaceae. Int J Med Microbiol 292(3–4):149–158
Frisan T, Cortes-Bratti X, Chaves-Olarte E, Stenerlow B, Thelestam M (2003) The Haemophilus ducreyi cytolethal distending toxin induces DNA double-strand breaks and promotes ATM-dependent activation of RhoA. Cell Microbiol 5(10):695–707
Fu Y, Galan JE (1999) A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401:293–297
Fu H, Coburn J, Collier RJ (1993) The eukaryotic host factor that activates exoenzyme S of Pseudomonas aeruginosa is a member of the 14-3-3 protein family. Proc Natl Acad Sci USA 90(6):2320–2324
Fujinaga Y, Wolf AA, Rodighiero C, Wheeler H, Tsai B, Allen L, Jobling MG, Rapoport T, Holmes RK, Lencer WI (2003) Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm. Mol Biol Cell 14(12):4783–4793
Galloway TS, van Heyningen S (1987) Binding of NAD+ by cholera toxin. Biochem J 244:225–230
Galyov EE, Hakansson S, Wolf-Watz H (1994) Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol 176:4543–4548
Ganesan AK, Frank DW, Misra RP, Schmidt G, Barbieri JT (1998) Pseudomonas aeruginosa exoenzyme S ADP-ribosylates Ras at multiple sites. J Biol Chem 273:7332–7337
Gedde MM, Higgins DE, Tilney LG, Portnoy DA (2000) Role of listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 68:999–1003
Geoffroy C, Mengaud J, Alouf JE, Cossart P (1990) Alveolysin, the thiol-activated toxin of Bacillus alvei, is homologous to listeriolysin O, perfringolysin O, pneumolysin, and streptolysin O and contains a single cysteine. J Bacteriol 172(12):7301–7735
Giannelli V, Fontana MR, Giuliani MM, Guangcai D, Rappuoli R, Pizza M (1997) Protease susceptibility and toxicity of heat-labile enterotoxins with a mutation in the active site or in the protease-sensitive loop. Infect Immun 65:331–334
Gilbert RJ (2002) Pore-forming toxins. Cell Mol Life Sci 59(5):832–844
Glaser P, Sakamoto H, Bellalou J, Ullmann A, Danchin A (1988) Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J 7:3997–4004
Goehring UM, Schmidt G, Pederson KJ, Aktories K, Barbieri JT (1999) The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J Biol Chem 274:36369–36372
Goodwin MS, Weiss AA (1990) Adenylate cyclase toxin is critical for colonization and pertussis toxin is critical for lethal infection by Bordetella pertussis in infant mice. Infect Immun 58:3445–3447
Gordon VM, Nelson KL, Buckley JT, Stevens VL, Tweten RK, Elwood PC, Leppla SH (1999) Clostridium septicum alpha toxin uses glycosylphosphatidylinositol-anchored protein receptors. J Biol Chem 274(38):27274–27280
Gouaux E (1998) Alpha-Hemolysin from Staphylococcus aureus: an archetype of beta-barrel, channel-forming toxins. J Struct Biol 121:110–122
Goyard S, Orlando C, Sabatier JM, Labruyere E, Alayer J, Fontan G, van Rietschoten J, Mock M, Danchin A, Ullmann A et al (1989) Identification of a common domain in calmodulin activated eukaryotic and bacterial adenylate cyclases. Biochemistry 28:1964–1967
Gray GS, Kehoe M (1984) Primary sequence of the alpha-toxin gene from Staphylococcus aureus wood 46. Infect Immun 46:615–618
Gray GL, Smith DH, Baldridge JS, Harkins RN, Vasil ML, Chen EY, Heyneker HL (1984) Cloning, nucleotide sequence, and expression in Escherichia coli of the exotoxin A structural gene of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 81:2645–2649
Grochulski P, Masson L, Borisova S, Pusztai-Carey M, Schwartz JL, Brousseau R, Cygler M (1995) Bacillus thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation. J Mol Biol 254:447–464
Guan KL, Dixon JE (1990) Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249:553–556
Guichon A, Hersh D, Smith MR, Zychlinsky A (2001) Structure-function analysis of the Shigella virulence factor IpaB. J Bacteriol 183(4):1269–1276
Guidry JJ, Cardenas L, Cheng E, Clements JD (1997) Role of receptor binding in toxicity, immunogenicity, and adjuvanticity of Escherichia coli heat-labile enterotoxin. Infect Immun 65:4943–4950
Gulke I, Pfeifer G, Liese J, Fritz M, Hofmann F, Aktories K, Barth H (2001) Characterization of the enzymatic component of the ADP-ribosyltransferase toxin CDTa from Clostridium difficile. Infect Immun 69(10):6004–6011
Haghjoo E, Galan JE (2004) Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci USA 101(13):4614–4619
Hagnerelle X, Plisson C, Lambert O, Marco S, Rigaud JL, Johannes L, Levy D (2002) Two-dimensional structures of the Shiga toxin B-subunit and of a chimera bound to the glycolipid receptor Gb3. J Struct Biol 139(2):113–121
Hallett M (1999) One man’s poison–clinical applications of botulinum toxin. N Engl J Med 341(2):118–120
Halpern JL, Loftus A (1993) Characterization of the receptor-binding domain of tetanus toxin. J Biol Chem 268:11188–11192
Halpern JL, Neale EA (1995) Neurospecific binding, internalization, and retrograde axonal transport. Curr Top Microbiol Immunol 195:221–241
Hamm HE, Gilchrist A (1996) Heterotrimeric G proteins. Curr Opin Cell Biol 8:189–196
Han XY, Galloway DR (1995) Active site mutations of Pseudomonas aeruginosa exotoxin A: analysis of the His440 residue. J Biol Chem 270:679–684
Han S, Arvai AS, Clancy SB, Tainer JA (2001) Crystal structure and novel recognition motif of rho ADP-ribosylating C3 exoenzyme from Clostridium botulinum: structural insights for recognition specificity and catalysis. J Mol Biol 305(1):95–107
Hanna P (1999) Lethal toxin actions and their consequences. J Appl Microbiol 87:285–287
Hardt WD, Galan JE (1997) A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA 94:9887–9892
Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE (1998) S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93:815–826
Hardy SP, Lund T, Granum PE (2001) CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiol Lett 197(1):47–51
Harford S, Dykes CW, Hobden AN, Read MJ, Halliday IJ (1989) Inactivation of the Escherichia coli heat-labile enterotoxin by in vitro mutagenesis of the A-subunit gene. Eur J Biochem 183:311–316
Haslinger B, Strangfeld K, Peters G, Schulze-Osthoff K, Sinha B (2003) Staphylococcus aureus alpha-toxin induces apoptosis in peripheral blood mononuclear cells: role of endogenous tumour necrosis factor-alpha and the mitochondrial death pathway. Cell Microbiol 5(10):729–741
Hatheway CL (1995) Botulism: the present status of the disease. Curr Top Microbiol Immunol 195:55–75
Hayaishi O, Ueda K (1977) Poly(ADP-ribose) and ADP-ribosylation of proteins. Annu Rev Biochem 46:95–116
Henderson B, Nair SP, Ward JM, Wilson M (2003) Molecular pathogenicity of the oral opportunistic pathogen Actinobacillus actinomycetemcomitans. Annu Rev Microbiol 57:29–55
Hermant D, Menard R, Arricau N, Parsot C, Popoff MY (1995) Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol Microbiol 4:781–789
Herreros J, Lalli G, Schiavo G (2000) C-terminal half of tetanus toxin fragment C is sufficient for neuronal binding and interaction with a putative protein receptor. Biochem J 347:199–204
Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96:2396–2401
Heuck AP, Tweten RK, Johnson AE (2003) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J Biol Chem 278(33):31218–31225
Hewlett EL, Sauer KT, Myers GA, Cowell JL, Guerrant RL (1983) Induction of a novel morphological response in Chinese hamster ovary cells by pertussis toxin. Infect Immun 40:1198–1203
Hilbi H, Moss JE, Hersh D, Chen Y, Arondel J, Banerjee S, Flavell RA, Yuan J, Sansonetti PJ, Zychlinsky A (1998) Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273(49):32895–32900
Hill J, Andrew PW, Mitchell TJ (1994) Amino acids in pneumolysin important for hemolytic activity identified by random mutagenesis. Infect Immun 62:757–758
Hofmann C, Vanderbruggen H, Hofte H, Van Rie J, Jansens S, Van Mellaert H (1988) Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high-affinity binding sites in the brush bordermembrane of target insect midguts. Proc Natl Acad Sci USA 85:7844–7848
Hoffmann C, Pop M, Leemhuis J, Schirmer J, Aktories K, Schmidt G (2004) The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J Biol Chem 279(16):16026–16032
Hofte H, Whiteley HR (1989) Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev 53:242–255
Holmgren J (1981) Actions of cholera toxin and the prevention and treatment of cholera. Nature 292:413–417
Hooper KP, Eidels L (1995) Localization of a critical diphtheria toxin-binding domain to the C-terminus of the mature heparin-binding EGF-like growth factor region of the diphtheria toxin receptor. Biochem Biophys Res Commun 206:710–717
Horiguchi Y (2001) Escherichia coli cytotoxic necrotizing factors and Bordetella dermonecrotic toxin: the dermonecrosis-inducing toxins activating Rho small GTPases. Toxicon 39(11):1619–1627
Horstman AL, Kuehn MJ (2002) Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway. J Biol Chem 277(36):32538–32545
Hotze EM, Heuck AP, Czajkowsky DM, Shao Z, Johnson AE, Tweten RK (2002) Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J Biol Chem 277(13):11597–11605
Hume PJ, McGhie EJ, Hayward RD, Koronakis V (2003) The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol Microbiol 49(2):425–439
Iandolo JJ (1989) Genetic analysis of extracellular toxins of Staphylococcus aureus. Annu Rev Microbiol 43:375–402
Ilver D, Barone S, Mercati D, Lupetti P, Telford JL (2004) Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism. Cell Microbiol 6(2):167–174
Inocencio NM, Moehring JM, Moehring TJ (1994) Furin activates Pseudomonas exotoxin A by specific cleavage in vivo and in vitro. J Biol Chem 269(50):31831–31835
Issartel JP, Koronakis V, Hughes C (1991) Activation of Escherichia coli prohaemolysin to the mature toxin by acyl carrier protein-dependent fatty acylation. Nature 351:759–761
Ito A, Sasaguri Y, Kitada S, Kusaka Y, Kuwano K, Masutomi K, Mizuki E, Akao T, Ohba M (2004) A Bacillus thuringiensis crystal protein with selective cytocidal action to human cells. J Biol Chem 279(20):21282–21286
Johnson VG, Nicholls PJ (1994) Histidine 21 does not play a major role in diphtheria toxin catalysis. J Biol Chem 269:4349–4354
Just I, Mohr C, Schallehn G, Menard L, Didsbury JR, Vandekerckhove J, van Damme J, Aktories K (1992) Purification and characterization of an ADP-ribosyltransferase produced by Clostridium limosum. J Biol Chem 267:10274–10280
Just I, Fritz G, Aktories K, Giry M, Popoff MR, Boquet P, Hegenbarth S, von Eichel-Streiber C (1994) Clostridium difficile toxin B acts on the GTP-binding protein Rho. J Biol Chem 269:10706–10712
Just I, Selzer J, Jung M, van Damme J, Vandekerckhove J, Aktories K (1995a) Rho-ADP-ribosylating exoenzyme from Bacillus cereus: purification, characterization, and identification of the NAD-binding site. Biochemistry 34:334–340
Just I, Selzer J, von Eichel-Streiber C, Aktories K (1995b) The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile. J Clin Invest 95:1026–1031
Just I, Selzer J, Wilm M, von Eichel-Streiber C, Mann M, Aktories K (1995c) Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375:500–503
Kabsch W, Vandekerckhove J (1992) Structure and function of actin. Annu Rev Biophys Biomol Struct 21:49–76
Kachlany SC, Fine DH, Figurski DH (2000) Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitans. Infect Immun 68(11):6094–6100
Kagawa TF, Cooney JC, Baker HM, McSweeney S, Liu M, Gubba S, Musser JM, Baker EN (2000) From the cover: crystal structure of the zymogen form of the group A Streptococcus virulence factor SpeB: an integrin-binding cysteine protease. Proc Natl Acad Sci USA 97:2235–2240
Karmali MA, Arbus GS, Ish-Shalom N, Fleming PC, Malkin D, Petric M, Cheung R, Louie S, Humphreys GR, Strachan M (1988) A family outbreak of hemolytic-uremic syndrome associated with verotoxin-producing Escherichia coli serotype 0157:H7. Pediatr Nephrol 2:409–414
Katada T, Tamura M, Ui M (1983) The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein. Arch Biochem Biophys 224:290–298
Katzin BJ, Collins EJ, Robertus JD (1991) Structure of ricin A-chain at 2.5 A. Proteins 10(3):251–259
Kehoe MA, Miller L, Walker JA, Boulnois GJ (1987) Nucleotide sequence of the streptolysin O (SLO) gene: structural homologies between SLO and other membrane-damaging, thiol-activated toxins. Infect Immun 55:3228–3232
Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511–520
Khelef N, Zychlinsky A, Guiso N (1993) Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect Immun 61:4064–4071
Khoshoo V, Bhan MK, Mathur M, Raj P (1988) A fatal severe enteropathy associated with enteropathogenic E. coli. Indian Pediatr 25:308–309
Kim S, Chamberlain AK, Bowie JU (2004) Membrane channel structure of Helicobacter pylori vacuolating toxin: role of multiple GXXXG motifs in cylindrical channels. Proc Natl Acad Sci USA 101(16):5988–5991
Kirby JE (2004) Anthrax lethal toxin induces human endothelial cell apoptosis. Infect Immun 72(1):430–439
Klapproth JM, Donnenberg MS, Abraham JM, Mobley HL, James SP (1995) Products of enteropathogenic Escherichia coli inhibit lymphocyte activation and lymphokine production. Infect Immun 63:2248–2254
Klapproth JM, Scaletsky IC, McNamara BP, Lai LC, Malstrom C, James SP, Donnenberg MS (2000) A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect Immun 68:2148–2155
Klimpel KR, Molloy SS, Thomas G, Leppla SH (1992) Anthrax toxin protective antigen is activated by a cell surface protease with the sequence specificity and catalytic properties of furin. Proc Natl Acad Sci USA 89:10277–10281
Klimpel KR, Arora N, Leppla SH (1994) Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol Microbiol 13:1093–1100
Knapp O, Maier E, Polleichtner G, Masin J, Sebo P, Benz R (2003) Channel formation in model membranes by the adenylate cyclase toxin of Bordetella pertussis: effect of calcium. Biochemistry 42(26):8077–8084
Knoop FC, Owens M, Crocker IC (1993) Clostridium difficile: clinical disease and diagnosis. Clin Microbiol Rev 6:251–265
Koni PA, Ellar DJ (1993) Cloning and characterization of a novel Bacillus thuringiensis cytolytic delta-endotoxin. J Mol Biol 229:319–327
Koni PA, Ellar DJ (1994) Biochemical characterization of Bacillus thuringiensis cytolytic delta-endotoxins. Microbiology 140:1869–1880
Korostoff J, Wang JF, Kieba I, Miller M, Shenker BJ, Lally ET (1998) Actinobacillus actinomycetemcomitans leukotoxin induces apoptosis in HL-60 cells. Infect Immun 66(9):4474–4483
Kotzin BL, Leung DY, Kappler J, Marrack P (1993) Superantigens and their potential role in human disease. Adv Immunol 54:99–166
Kozlov YV, Chernaia MM, Fraser ME, James MN (1993) Purification and crystallization of Shiga toxin from Shigella dysenteriae. J Mol Biol 232:704–706
Krieglstein KG, DasGupta BR, Henschen AH (1994) Covalent structure of botulinum neurotoxin type A: location of sulfhydryl groups, and disulfide bridges and identification of C-termini of light and heavy chains. J Protein Chem 13:49–57
Kulich SM, Frank DW, Barbieri JT (1993) Purification and characterization of exoenzyme S from Pseudomonas aeruginosa 388. Infect Immun 61:307–312
Kulich SM, Yahr TL, Mende-Mueller LM, Barbieri JT, Frank DW (1994) Cloning the structural gene for the 49-kDa form of exoenzyme S (exoS) from Pseudomonas aeruginosa strain 388. J Biol Chem 269:10431–10437
Kumar P, Ahuja N, Bhatnagar R (2002) Anthrax edema toxin requires influx of calcium for inducing cyclic AMP toxicity in target cells. Infect Immun 70(9):4997–5007
Lacy DB, Tepp W, Cohen AC, DasGupta BR, Stevens RC (1998) Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat Struct Biol 5:898–902
Lacy DB, Stevens RC (1999) Sequence homology and structural analysis of the clostridial neurotoxins. J Mol Biol 291(5):1091–1104
Ladant D, Ullmann A (1999) Bordatella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol 7:172–176
Ladhani S, Joannou CL, Lochrie DP, Evans RW, Poston SM (1999) Clinical, microbial, and biochemical aspects of the exfoliative toxins causing staphylococcal scalded-skin syndrome. Clin Microbiol Rev 12:224–242
Lai CY, Cancedda F, Duffy LK (1981) ADP-ribosyl transferase activity of cholera toxin polypeptide A1 and the effect of limited trypsinolysis. Biochem Biophys Res Commun 102:1021–1027
Lalli G, Bohnert S, Deinhardt K, Verastegui C, Schiavo G (2003) The journey of tetanus and Botulinum neurotoxins in neurons. Trends Microbiol 11(9):431–437
Lara-Tejero M, Galan JE (2001) CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun 69(7):4358–4365
Lee RB, Hassane DC, Cottle DL, Pickett CL (2003) Interactions of Campylobacter jejuni cytolethal distending toxin subunits CdtA and CdtC with HeLa cells. Infect Immun 71(9):4883–4890
Lencer WI, Constable C, Moe S, Jobling MG, Webb HM, Ruston S, Madara JL, Hirst TR, Holmes RK (1995) Targeting of cholera toxin and Escherichia coli heat labile toxin in polarized epithelia: role of COOH-terminal KDEL. J Cell Biol 131:951–962
Leppla SH, Arora N, Varughese M (1999) Anthrax toxin fusion proteins for intracellular delivery of macromolecules. J Appl Microbiol 87:284
Leslie D, Fairweather N, Pickard D, Dougan G, Kehoe M (1989) Phospholipase C and haemolytic activities of Clostridium perfringens alpha-toxin cloned in Escherichia coli: sequence and homology with a Bacillus cereus phospholipase C. Mol Microbiol 3:383–392
Leung DY, Meissner HC, Fulton DR, Murray DL, Kotzin BL, Schlievert PM (1993) Toxic shock syndrome toxin-secreting Staphylococcus aureus in Kawasaki syndrome. Lancet 342:1385–1388
Li M, Dyda F, Benhar I, Pastan I, Davies DR (1995) The crystal structure of Pseudomonas aeruginosa exotoxin domain III with nicotinamide and AMP: conformational differences with the intact exotoxin. Proc Natl Acad Sci USA 92:9308–9312
Li J, Koni PA, Ellar DJ (1996) Structure of the mosquitocidal delta-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. J Mol Biol 257:129–152
Li H, Llera A, Tsuchiya D, Leder L, Ysern X, Schlievert PM, Karjalainen K, Mariuzza RA (1998) Three-dimensional structure of the complex between a T cell receptor beta chain and the superantigen staphylococcal enterotoxin B. Immunity 9:807–816
Lilic M, Galkin VE, Orlova A, VanLoock MS, Egelman EH, Stebbins CE (2003) Salmonella SipA polymerizes actin by stapling filaments with nonglobular protein arms. Science 301(5641):1918–1921
Lin SL, Le TX, Cowen DS (2003) SptP, a Salmonella typhimurium type III-secreted protein, inhibits the mitogen-activated protein kinase pathway by inhibiting Raf activation. Cell Microbiol 5(4):267–275
Lindsay JA, Ruzin A, Ross HF, Kurepina N, Novick RP (1998) The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29:527–543
Liu S, Kulich SM, Barbieri JT (1996) Identification of glutamic acid 381 as a candidate active site residue of Pseudomonas aeruginosa exoenzyme S. Biochemistry 35:2754–2758
Lobet Y, Cluff CW, Cieplak W Jr (1991) Effect of site-directed mutagenic alterations on ADP-ribosyltransferase activity of the A subunit of Escherichia coli heat-labile enterotoxin. Infect Immun 59(9):2870–2879
Locht C, Keith JM (1986) Pertussis toxin gene: nucleotide sequence and genetic organization. Science 232(4755):1258–1264
Lockman HA, Gillespie RA, Baker BD, Shakhnovich E (2002) Yersinia pseudotuberculosis produces a cytotoxic necrotizing factor. Infect Immun 70(5):2708–2714
Louch HA, Buczko ES, Woody MA, Venable RM, Vann WF (2002) Identification of a binding site for ganglioside on the receptor binding domain of tetanus toxin. Biochemistry 41(46):13644–13652
Ludwig A, Bauer S, Benz R, Bergmann B, Goebel W (1999) Analysis of the SlyA-controlled expression, subcellular localization and pore-forming activity of a 34 kDa haemolysin (ClyA) from Escherichia coli K-12. Mol Microbiol 31:557–567
Lukomski S, Montgomery CA, Rurangirwa J, Geske RS, Barrish JP, Adams GJ, Musser JM (1999) Extracellular cysteine protease produced by Streptococcus pyogenes participates in the pathogenesis of invasive skin infection and dissemination in mice. Infect Immun 67:1779–1788
Lund T, Granum PE (1999) The 105-kDa protein component of Bacillus cereus non-haemolytic enterotoxin (Nhe) is a metalloprotease with gelatinolytic and collagenolytic activity. FEMS Microbiol Lett 178(2):355–361
Lund T, De Buyser ML, Granum PE (2000) A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol Microbiol 38(2):254–261
Lupetti P, Heuser JE, Manetti R, Massari P, Lanzavecchia S, Bellon PL, Dallai R, Rappuoli R, Telford JL (1996) Oligomeric and subunit structure of the Helicobacter pylori vacuolating cytotoxin. J Cell Biol 133:801–807
Lyerly DM, Phelps CJ, Toth J, Wilkins TD (1986) Characterization of toxins A and B of Clostridium difficile with monoclonal antibodies. Infect Immun 54(1):70–76
Madden DL, Horton RE, McCullough NB (1970) Spontaneous infection in ex-germfree guinea pigs due to Clostridium perfringens. Lab Anim Care 20:454–455
Maier E, Reinhard N, Benz R, Frey J (1996) Channel-forming activity and channel size of the RTX toxins ApxI, ApxII, and ApxIII of Actinobacillus pleuropneumoniae. Infect Immun 64(11):4415–4423
Marinaro M, Fasano A, De Magistris MT (2003) Zonula occludens toxin acts as an adjuvant through different mucosal routes and induces protective immune responses. Infect Immun 71(4):1897–1902
Martens JW, Visser B, Vlak JM, Bosch D (1995) Mapping and characterization of the entomocidal domain of the Bacillus thuringiensis CryIA(b) protoxin. Mol Gen Genet 247:482–487
Masignani V, Balducci E, Di Marcello F, Savino S, Serruto D, Veggi D, Bambini S, Scarselli M, Arico B, Comanducci M, Adu-Bobie J, Giuliani MM, Rappuoli R, Pizza M (2003) NarE: a novel ADP-ribosyltransferase from Neisseria meningitidis. Mol Microbiol 50(3):1055–1067
Matsuzaki K, Yoneyama S, Miyajima K (1997) Pore formation and translocation of melittin. Biophys J 73:831–838
Mauss S, Chaponnier C, Just I, Aktories K, Gabbiani G (1990) ADP-ribosylation of actin isoforms by Clostridium botulinum C2 toxin and Clostridium perfringens iota toxin. Eur J Biochem 194:237–241
McDonald C, Vacratsis PO, Bliska JB, Dixon JE (2003) The Yersinia virulence factor YopM forms a novel protein complex with two cellular kinases. J Biol Chem 278(20):18514–18523
Mekalanos JJ, Swartz DJ, Pearson GD, Harford N, Groyne F, de Wilde M (1983) Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature 306:551–557
Melton JA, Parker MW, Rossjohn J, Buckley JT, Tweten RK (2004) The identification and structure of the membrane–spanning domain of the Clostridium septicum alpha toxin. J Biol Chem 279(14):14315–14322
Merritt EA, Sarfaty S, Pizza M, Domenighini M, Rappuoli R, Hol WG (1995) Mutation of a buried residue causes loss of activity but no conformational change in the heat-labile enterotoxin of Escherichia coli. Nat Struct Biol 2:269–272
Michel E, Reich KA, Favier R, Berche P, Cossart P (1990) Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol Microbiol 4:2167–2178
Miles G, Bayley H, Cheley S (2002) Properties of Bacillus cereus hemolysin II: a heptameric transmembrane pore. Protein Sci 11(7):1813–1824
Mills SD, Boland A, Sory MP, van der Smissen P, Kerbourch C, Finlay BB, Cornelis GR (1997) Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc Natl Acad Sci USA 94:12638–12643
Milne JC, Collier RJ (1993) pH-dependent permeabilization of the plasma membrane of mammalian cells by anthrax protective antigen. Mol Microbiol 10:647–653
Milne JC, Furlong D, Hanna PC, Wall JS, Collier RJ (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J Biol Chem 269:20607–20612
Mody CH, Buser DE, Syme RM, Woods DE (1995) Pseudomonas aeruginosa exoenzyme S induces proliferation of human T lymphocytes. Infect Immun 63:1800–1805
Monday SR, Vath GM, Ferens WA, Deobald C, Rago JV, Gahr PJ, Monie DD, Iandolo JJ, Chapes SK, Davis WC, Ohlendorf DH, Schlievert PM, Bohach GA (1999) Unique superantigen activity of staphylococcal exfoliative toxins. J Immunol 162:4550–4559
Montal MS, Blewitt R, Tomich JM, Montal M (1992) Identification of an ion channel-forming motif in the primary structure of tetanus and botulinum neurotoxins. FEBS Lett 313(1):12–18
Montecucco C, Schiavo G (1994) Mechanism of action of tetanus and botulinum neurotoxins. Mol Microbiol 13:1–8
Montecucco C, Schiavo G (1995) Structure and function of tetanus and botulinum neurotoxins. Q Rev Biophys 28(4):423–472
Montecucco C, Schiavo G, Brunner J, Duflot E, Boquet P, Roa M (1986) Tetanus toxin is labeled with photoactivatable phospholipids at low pH. Biochemistry 25(4):919–924
Moon HW, Whipp SC, Argenzio RA, Levine MM, Giannella RA (1983) Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun 41:1340–1351
Mori T, Shoemaker RH, McMahon JB, Gulakowski RJ, Gustafson KR, Boyd MR (1997) Construction and enhanced cytotoxicity of a [cyanovirin-N]-[Pseudomonas exotoxin] conjugate against human immunodeficiency virus-infected cells. Biochem Biophys Res Commun 239:884–888
Moriishi K, Syuto B, Saito M, Oguma K, Fujii N, Abe N, Naiki M (1993) Two different types of ADP-ribosyltransferase C3 from Clostridium botulinum type D lysogenized organisms. Infect Immun 61:5309–5314
Moss J, Vaughan M (1988) ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Adv Enzymol Relat Areas Mol Biol 61:303–379
Murli S, Watson RO, Galan JE (2001) Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell Microbiol 3(12):795–810
Nagahama M, Mukai M, Morimitsu S, Ochi S, Sakurai J (2002) Role of the C–domain in the biological activities of Clostridium perfringens alpha–toxin. Microbiol Immunol 46(10):647–655
Nagahama M, Hayashi S, Morimitsu S, Sakurai J (2003) Biological activities and pore formation of Clostridium perfringens beta toxin in HL 60 cells. J Biol Chem 278(38):36934–36941
Naglich JG, Metherall JE, Russell DW, Eidels L (1992) Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 69:1051–1061
Naylor CE, Eaton JT, Howells A, Justin N, Moss DS, Titball RW, Basak AK (1998) Structure of the key toxin in gas gangrene. Nat Struct Biol 5:738–746
Nemoto Y, Namba T, Kozaki S, Narumiya S (1991) Clostridium botulinum C3 ADP-ribosyltransferase gene: cloning, sequencing, and expression of a functional protein in Escherichia coli. J Biol Chem 266:19312–19319
Nguyen VT, Kamio Y, Higuchi H (2003) Single–molecule imaging of cooperative assembly of gamma–hemolysin on erythrocyte membranes. EMBO J 22(19):4968–4979
Nhieu GT, Sansonetti PJ (1999) Mechanism of Shigella entry into epithelial cells. Curr Opin Microbiol 2:51–55
Nicosia A, Perugini M, Franzini C, Casagli MC, Borri MG, Antoni G, Almoni M, Neri P, Ratti G, Rappuoli R (1986) Cloning and sequencing of the pertussis toxin genes: operon structure and gene duplication. Proc Natl Acad Sci USA 83:4631–4635
Niebuhr K, Giuriato S, Pedron T, Philpott DJ, Gaits F, Sable J, Sheetz MP, Parsot C, Sansonetti PJ, Payrastre B (2002) Conversion of PtdIns(4,5)P(2) into PtdIns(5)P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J 21(19):5069–5078
Norris FA, Wilson MP, Wallis TS, Galyov EE, Majerus PW (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA 95:14057–14059
Ogata M, Chaudhary VK, FitzGerald DJ, Pastan I (1989) Cytotoxic activity of a recombinant fusion protein between interleukin 4 and Pseudomonas exotoxin. Proc Natl Acad Sci USA 86:4215–4219
Ohishi I (1987) Activation of botulinum C2 toxin by trypsin. Infect Immun 55:1461–1465
Okuda J, Kurazono H, Takeda Y (1995) Distribution of the cytolethal distending toxin A gene (cdtA) among species of Shigella and Vibrio, and cloning and sequencing of the cdt gene from Shigella dysenteriae. Microb Pathog 18(3):167–172
Olson R, Nariya H, Yokota K, Kamio Y, Gouaux E (1999) Crystal structure of staphylococcal LukF delineates conformational changes accompanying formation of a transmembrane channel. Nat Struct Biol 6:134–140
Orth K, Palmer LE, Bao ZQ, Stewart S, Rudolph AE, Bliska JB, Dixon JE (1999) Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285:1920–1923
Orth K (2002) Function of the Yersinia effector YopJ. Curr Opin Microbiol 5(1):38–43
Osicková A, Osicka R, Maier E, Benz R, Sebo P (1999) An amphipathic alpha-helix including glutamates 509 and 516 is crucial for membrane translocation of adenylate cyclase toxin and modulates formation and cation selectivity of its membrane channels. J Biol Chem 274(53):37644–37650
Oswald E, De Rycke J (1990) A single protein of 110 kDa is associated with the multinucleating and necrotizing activity coded by the Vir plasmid of Escherichia coli. FEMS Microbiol Lett 56:279–284
Oswald E, Sugai M, Labigne A, Wu HC, Fiorentini C, Boquet P, O’Brien AD (1994) Cytotoxic necrotizing factor type 2 produced by virulent Escherichia coli modifies the small GTP-binding proteins Rho involved in assembly of actin stress fibers. Proc Natl Acad Sci USA 91:3814–3818
Pallen MJ, Lam AC, Loman NJ, McBride A (2001) An abundance of bacterial ADP–ribosyltransferases–implications for the origin of exotoxins and their human homologues. Trends Microbiol 9(7):302–307
Pannifer AD, Wong TY, Schwarzenbacher R, Renatus M, Petosa C, Bienkowska J, Lacy DB, Collier RJ, Park S, Leppla SH, Hanna P, Liddington RC (2001) Crystal structure of the anthrax lethal factor. Nature 414(6860):229–233
Papageorgiou AC, Acharya KR, Shapiro R, Passalacqua EF, Brehm RD, Tranter HS (1995) Crystal structure of the superantigen enterotoxin C2 from Staphylococcus aureus reveals a zinc-binding site. Structure 3:769–779
Papageorgiou AC, Collins CM, Gutman DM, Kline JB, O’Brien SM, Tranter HS, Acharya KR (1999) Structural basis for the recognition of superantigen streptococcal pyrogenic exotoxin A (SpeA1) by MHC class II molecules and T-cell receptors. EMBO J 18(1):9–21
Papini E, Schiavo G, Sandona D, Rappuoli R, Montecucco C (1989) Histidine 21 is at the NAD+ binding site of diphtheria toxin. J Biol Chem 264:12385–12388
Papini E, Schiavo G, Rappuoli R, Montecucco C (1990) Histidine-21 is involved in diphtheria toxin NAD+ binding. Toxicon 28:631–635
Papini E, de Bernard M, Milia E, Bugnoli M, Zerial M, Rappuoli R, Montecucco C (1994) Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc Natl Acad Sci USA 91:9720–9724
Papini E, Satin B, Bucci C, de Bernard M, Telford JL, Manetti R, Rappuoli R, Zerial M, Montecucco C (1997) The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J 16:15–24
Papini E, Zoratti M, Cover TL (2001) In search of the Helicobacter pylori VacA mechanism of action. Toxicon 39(11):1757–1767
Pappenheimer AM Jr (1977) Diphtheria toxin. Annu Rev Biochem 46:69–94
Parker MW, Buckley JT, Postma JP, Tucker AD, Leonard K, Pattus F, Tsernoglou D (1994) Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature 367:292–295
Pedelacq JD, Maveyraud L, Prèvost G, Baba-Moussa L, Gonzalez A, Courcelle E, Shepard W, Monteil H, Samama JP, Mourey L (1999) The structure of a Staphylococcus aureus leucocidin component (LukF-PV) reveals the fold of the water-soluble species of a family of transmembrane pore-forming toxins. Structure Fold Des 7:277–287
Pellizzari R, Rossetto O, Schiavo G, Montecucco C (1999) Tetanus and botulinum neurotoxins: mechanism of action and therapeutic uses. Philos Trans R Soc Lond B Biol Sci 354:259–268
Perelle S, Gibert M, Boquet P, Popoff MR (1993) Characterization of Clostridium perfringens iota-toxin genes and expression in Escherichia coli. Infect Immun 61:5147–5156
Perelle S, Gibert M, Boquet P, Popoff MR (1995) Characterization of Clostridium perfringens iota-toxin genes and expression in Escherichia coli. Infect Immun 61:5147–5156
Petersson K, Hakansson M, Nilsson H, Forsberg G, Svensson LA, Liljas A, Walse B (2001) Crystal structure of a superantigen bound to MHC class II displays zinc and peptide dependence. EMBO J 20(13):3306–3312
Petosa C, Collier RJ, Klimpel KR, Leppla SH, Liddington RC (1997) Crystal structure of the anthrax toxin protective antigen. Nature 385:833–838
Pickett CL, Lee RB, Eyigor A, Elitzur B, Fox EM, Strockbine NA (2004) Patterns of variations in Escherichia coli strains that produce cytolethal distending toxin. Infect Immun 72(2):684–690
Pizza M, Bartoloni A, Prugnola A, Silvestri S, Rappuoli R (1988) Subunit S1 of pertussis toxin: mapping of the regions essential for ADP-ribosyltransferase activity. Proc Natl Acad Sci USA 85:7521–7525
Pizza M, Covacci A, Bartoloni A, Perugini M, Nencioni L, De Magistris MT, Villa L, Nucci D, Manetti R, Bugnoli M et al (1989) Mutants of pertussis toxin suitable for vaccine development. Science 246:497–500
Popoff MR, Boquet P (1988) Clostridium spiroforme toxin is a binary toxin which ADP-ribosylates cellular actin. Biochem Biophys Res Commun 152(3):1361–1368
Popoff MR, Rubin EJ, Gill DM, Boquet P (1988) Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect Immun 56:2299–2306
Popoff MR, Milward FW, Bancillon B, Boquet P (1989) Purification of the Clostridium spiroforme binary toxin and activity of the toxin on HEp-2 cells. Infect Immun 57:2462–2469
Porro M, Saletti M, Nencioni L, Tagliaferri L, Marsili I (1980) Immunogenic correlation between cross-reacting material (CRM197) produced by a mutant of Corynebacterium diphtheriae and diphtheria toxoid. J Infect Dis 142(5):716–724
Prasad GS, Earhart CA, Murray DL, Novick RP, Schlievert PM, Ohlendorf DH (1993) Structure of toxic shock syndrome toxin 1. Biochemistry 32:13761–13766
Prasad GS, Radhakrishnan R, Mitchell DT, Earhart CA, Dinges MM, Cook WJ, Schlievert PM, Ohlendorf DH (1997) Refined structures of three crystal forms of toxic shock syndrome toxin-1 and of a tetramutant with reduced activity. Protein Sci 6:1220–1227
Prèvost G, Cribier B, Couppie P, Petiau P, Supersac G, Finck-Barbancon V, Monteil H, Piemont Y (1995) Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 63:4121–4129
Proft T, Moffatt SL, Berkahn CJ, Fraser JD (1999) Identification and characterization of novel superantigens from Streptococcus pyogenes. J Exp Med 189(1):89–102
Proft T, Webb PD, Handley V, Fraser JD (2003) Two novel superantigens found in both group A and group C Streptococcus. Infect Immun 71(3):1361–1369
Qiu X, Verlinde CL, Zhang S, Schmitt MP, Holmes RK, Hol WG (1995) Three-dimensional structure of the diphtheria toxin repressor in complex with divalent cation co-repressors. Structure 3:87–100
Rappuoli R (1983) Isolation and characterization of Corynebacterium diphtheriae nontandem double lysogens hyperproducing CRM197. Appl Environ Microbiol 46:560–564
Rappuoli R (1997) Rational design of vaccines. Nat Med 3:374–376
Raynaud C, Guilhot C, Rauzier J, Bordat Y, Pelicic V, Manganelli R, Smith I, Gicquel B, Jackson M (2002) Phospholipases C are involved in the virulence of Mycobacterium tuberculosis. Mol Microbiol 45(1):203–217
Redpath MB, Foster TJ, Bailey CJ (1991) The role of the serine protease active site in the mode of action of epidermolytic toxin of Staphylococcus aureus. FEMS Microbiol Lett 65:151–155
Reingold J, Starr N, Maurer J, Lee MD (1999) Identification of a new Escherichia coli She haemolysin homolog in avian E. coli. Vet Microbiol 66:125–134
Richard JF, Petit L, Gibert M, Marvaud JC, Bouchaud C, Popoff MR (1999) Bacterial toxins modifying the actin cytoskeleton. Int Microbiol 2(3):185–194
Robertson D, Leppla SH (1986) Molecular cloning and expression in Escherichia coli of the lethal factor gene of Bacillus anthracis. Gene 44:71–78
Robertson DL, Tippetts MT, Leppla SH (1988) Nucleotide sequence of the Bacillus anthracis edema factor gene (cya): a calmodulin-dependent adenylate cyclase. Gene 73:363–371
Rosqvist R, Forsberg A, Rimpilainen M, Bergman T, Wolf-Watz H (1990) The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol 4:657–667
Rosqvist R, Forsberg A, Wolf-Watz H (1991) Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun 59:4562–4569
Rossetto O, Deloye F, Poulain B, Pellizzari R, Schiavo G, Montecucco C (1995) The metallo-proteinase activity of tetanus and botulism neurotoxins. J Physiol Paris 89:43–50
Rossjohn J, Feil SC, McKinstry WJ, Tweten RK, Parker MW (1997) Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 89:685–692
Rossjohn J, Gilbert RJ, Crane D, Morgan PJ, Mitchell TJ, Rowe AJ, Andrew PW, Paton JC, Tweten RK, Parker MW (1998) The molecular mechanism of pneumolysin, a virulence factor from Streptococcus pneumoniae. J Mol Biol 284:449–461
Roussel A, Anderson BF, Baker HM, Fraser JD, Baker EN (1997) Crystal structure of the streptococcal superantigen SPE-C: dimerization and zinc binding suggest a novel mode of interaction with MHC class II molecules. Nat Struct Biol 4:635–643
Ruckdeschel K, Roggenkamp A, Schubert S, Heesemann J (1996) Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutrophils. Infect Immun 64:724–733
Sakaguchi G (1982) Clostridium botulinum toxins. Pharmacol Ther 19(2):165–194
Schad EM, Zaitseva I, Zaitsev VN, Dohlsten M, Kalland T, Schlievert PM, Ohlendorf DH, Svensson LA (1995) Crystal structure of the superantigen staphylococcal enterotoxin type A. EMBO J 14:3292–3301
Schiavo G, Papini E, Genna G, Montecucco C (1990) An intact interchain disulfide bond is required for the neurotoxicity of tetanus toxin. Infect Immun 58:4136–4141
Schiavo G, Rossetto O, Santucci A, DasGupta BR, Montecucco C (1992) Botulinum neurotoxins are zinc proteins. J Biol Chem 267:23479–23483
Schlievert PM, Shands KN, Dan BB, Schmid GP, Nishimura RD (1981) Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic-shock syndrome. J Infect Dis 143:509–516
Schlievert PM, Bohach GA, Ohlendorf DH, Stauffacher CV, Leung DY, Murray DL, Prasad GS, Earhart CA, Jablonski LM, Hoffmann ML, Chi YI (1995) Molecular structure of staphylococcus and streptococcus superantigens. J Clin Immunol 15:4S–10S
Schmidt G, Selzer J, Lerm M, Aktories K (1998) The Rho-deamidating cytotoxic necrotizing factor 1 from Escherichia coli possesses transglutaminase activity: cysteine 866 and histidine 881 are essential for enzyme activity. J Biol Chem 273:13669–13674
Schmidt G, Goehring UM, Schirmer J, Lerm M, Aktories K (1999) Identification of the C-terminal part of Bordetella dermonecrotic toxin as a transglutaminase for rho GTPases. J Biol Chem 274:31875–31881
Schmitt W, Haas R (1994) Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol Microbiol 12:307–319
Sears CL (2001) The toxins of bacteroides fragilis. Toxicon 39(11):1737–1746
Segelke B, Knapp M, Kadkhodayan S, Balhorn R, Rupp B (2004) Crystal structure of Clostridium botulinum neurotoxin protease in a product-bound state: evidence for noncanonical zinc protease activity. Proc Natl Acad Sci USA 101(18):6888–6893
Sekine A, Fujiwara M, Narumiya S (1989) Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase. J Biol Chem 264(15):8602–8605
Sekura RD (1985) Pertussis toxin: a tool for studying the regulation of adenylate cyclase. Methods Enzymol 109:558–566
Seriwatana J, Echeverria P, Taylor DN, Rasrinaul L, Brown JE, Peiris JS, Clayton CL (1988) Type II heat-labile enterotoxin-producing Escherichia coli isolated from animals and humans. Infect Immun 56:1158–1161
Shannon JG, Ross CL, Koehler TM, Rest RF (2003) Characterization of anthrolysin O, the Bacillus anthracis cholesterol–dependent cytolysin. Infect Immun 71(6):3183–3189
Shao F, Dixon JE (2003) YopT is a cysteine protease cleaving Rho family GTPases. Adv Exp Med Biol 529:79–84
Shapiro RE, Specht CD, Collins BE, Woods AS, Cotter RJ, Schnaar RL (1997) Identification of a ganglioside recognition domain of tetanus toxin using a novel ganglioside photoaffinity ligand. J Biol Chem 272(48):30380–30386
Shatursky O, Heuck AP, Shepard LA, Rossjohn J, Parker MW, Johnson AE, Tweten RK (1999) The mechanism of membrane insertion for a cholesterol–dependent cytolysin: a novel paradigm for pore–forming toxins. Cell 99(3):293–299
Shenker BJ, Besack D, McKay T, Pankoski L, Zekavat A, Demuth DR (2004) Actinobacillus actinomycetemcomitans cytolethal distending toxin (Cdt): evidence that the holotoxin is composed of three subunits: CdtA, CdtB, and CdtC. J Immunol 172(1):410–417
Shepard LA, Heuck AP, Hamman BD, Rossjohn J, Parker MW, Ryan KR, Johnson AE, Tweten RK (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an alpha-helical to beta-sheet transition identified by fluorescence spectroscopy. Biochemistry 37(41):14563–14574
Siegall CB, Chaudhary VK, FitzGerald DJ, Pastan I (1988) Cytotoxic activity of an interleukin 6-Pseudomonas exotoxin fusion protein on human myeloma cells. Proc Natl Acad Sci USA 85:9738–9742
Siegall CB, Chaudhary VK, FitzGerald DJ, Pastan I (1989) Functional analysis of domains II, Ib, and III of Pseudomonas exotoxin. J Biol Chem 264:14256–14261
Simpson LL (1980) Kinetic studies on the interaction between botulinum toxin type A and the cholinergic neuromuscular junction. J Pharmacol Exp Ther 212:16–21
Sixma TK, Pronk SE, Kalk KH, Wartna ES, van Zanten BA, Witholt B, Hol WG (1991) Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature 351:371–377
Sixma TK, Kalk KH, van Zanten BA, Dauter Z, Kingma J, Witholt B, Hol WG (1993) Refined structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. J Mol Biol 230(3):890–918
Smith HW, Halls S (1967) The transmissible nature of the genetic factor in Escherichia coli that controls haemolysin production. J Gen Microbiol 47:153–161
So M, Dallas WS, Falkow S (1978) Characterization of an Escherichia coli plasmid encoding for synthesis of heat-labile toxin: molecular cloning of the toxin determinant. Infect Immun 21:405–411
Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274:1859–1866
Sorg I, Hoffmann C, Dumbach J, Aktories K, Schmidt G (2003) The C terminus of YopT is crucial for activity and the N terminus is crucial for substrate binding. Infect Immun 71(8):4623–4632
Sory MP, Boland A, Lambermont I, Cornelis GR (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 92:11998–12002
Spicer EK, Noble JA (1982) Escherichia coli heat-labile enterotoxin. Nucleotide sequence of the A subunit gene. J Biol Chem 257(10):5716–5721
Stanley P, Packman LC, Koronakis V, Hughes C (1994) Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 266(5193):1992–1996
Stebbins CE, Galan JE (2000) Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol Cell 6(6):1449–1460
Stein M, Rappuoli R, Covacci A (2000) Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc Natl Acad Sci USA 97:1263–1268
Stein PE, Boodhoo A, Armstrong GD, Heerze LD, Cockle SA, Klein MH, Read RJ (1994) Structure of a pertussis toxin-sugar complex as a model for receptor binding. Nat Struct Biol 1(9):591–596
Stein M, Bagnoli F, Halenbeck R, Rappuoli R, Fantl WJ, Covacci A (2002) c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol Microbiol 43(4):971–980
Steinthorsdottir V, Halldorsson H, Andresson OS (2000) Clostridium perfringens beta-toxin forms multimeric transmembrane pores in human endothelial cells. Microb Pathog 28:45–50
Stevens DL, Mitten J, Henry C (1987) Effects of alpha and theta toxins from Clostridium perfringens on human polymorphonuclear leukocytes. J Infect Dis 156:324–333
Stevens LA, Moss J, Vaughan M, Pizza M, Rappuoli R (1999) Effects of site-directed mutagenesis of Escherichia coli heat-labile enterotoxin on ADP-ribosyltransferase activity and interaction with ADP-ribosylation factors. Infect Immun 67:259–265
Straley SC, Bowmer WS (1986) Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51(2):445–454
Stiles BG, Wilkins TD (1986) Purification and characterization of Clostridium perfringens iota toxin: dependence on two nonlinked proteins for biological activity. Infect Immun 54:683–688
Stockbauer KE, Magoun L, Liu M, Burns EH Jr, Gubba S, Renish S, Pan X, Bodary SC, Baker E, Coburn J, Leong JM, Musser JM (1999) A natural variant of the cysteine protease virulence factor of group A Streptococcus with an arginine-glycine-aspartic acid (RGD) motif preferentially binds human integrins alphavbeta3 and alphaIIbbeta3. Proc Natl Acad Sci USA 96:242–247
Straley SC, Cibull ML (1989) Differential clearance and host-pathogen interactions of YopE-and YopK-YopL Yersinia pestis in BALB/c mice. Infect Immun 57:1200–1210
Stuckey JA, Schubert HL, Fauman EB, Zhang ZY, Dixon JE, Saper MA (1994) Crystal structure of Yersinia protein tyrosine phosphatase at 25 A and the complex with tungstate. Nature 370:571–575
Su XD, Taddei N, Stefani M, Ramponi G, Nordlund P (1994) The crystal structure of a low-molecular-weight phosphotyrosine protein phosphatase. Nature 370:575–578
Sugai M, Enomoto T, Hashimoto K, Matsumoto K, Matsuo Y, Ohgai H, Hong YM, Inoue S, Yoshikawa K, Suginaka H (1990) A novel epidermal cell differentiation inhibitor (EDIN): purification and characterization from Staphylococcus aureus. Biochem Biophys Res Commun 173:92–98
Sugai M, Hashimoto K, Kikuchi A, Inoue S, Okumura H, Matsumoto K, Goto Y, Ohgai H, Moriishi K, Syuto B et al (1992) Epidermal cell differentiation inhibitor ADP-ribosylates small GTP-binding proteins and induces hyperplasia of epidermis. J Biol Chem 267:2600–2604
Sugawara N, Tomita T, Kamio Y (1997) Assembly of Staphylococcus aureus gamma-hemolysin into a pore-forming ring-shaped complex on the surface of human erythrocytes. FEBS Lett 410:333–337
Sundberg E, Jardetzky TS (1999) Structural basis for HLA-DQ binding by the streptococcal superantigen SSA. Nat Struct Biol 6(2):123–129
Sundstrom M, Abrahmsen L, Antonsson P, Mehindate K, Mourad W, Dohlsten M (1996) The crystal structure of staphylococcal enterotoxin type D reveals Zn2+-mediated homodimerization. EMBO J 15:6832–6840
Swaminathan S, Furey W, Pletcher J, Sax M (1992) Crystal structure of staphylococcal enterotoxin B, a superantigen. Nature 359:801–806
Tamura M, Nogimori K, Yajima M, Ase K, Ui M (1983) A role of the B-oligomer moiety of islet-activating protein, pertussis toxin, in development of the biological effects on intact cells. J Biol Chem 258:6756–6761
Tamura M, Ajayi T, Allmond LR, Moriyama K, Wiener–Kronish JP, Sawa T (2004) Lysophospholipase A activity of Pseudomonas aeruginosa type III secretory toxin ExoU. Biochem Biophys Res Commun 316(2):323–331
Telford JL, Ghiara P, Dell’Orco M, Comanducci M, Burroni D, Bugnoli M, Tecce MF, Censini S, Covacci A, Xiang Z et al (1994) Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J Exp Med 179:1653–1658
Thanabalu T, Hindley J, Jackson-Yap J, Berry C (1991) Cloning, sequencing, and expression of a gene encoding a 100-kilodalton mosquitocidal toxin from Bacillus sphaericus SSII-1. J Bacteriol 173:2776–2785
Thanabalu T, Berry C, Hindley J (1993) Cytotoxicity and ADP-ribosylating activity of the mosquitocidal toxin from Bacillus sphaericus SSII-1: possible roles of the 27-and 70-kilodalton peptides. J Bacteriol 175:2314–2320
Titball RW, Fearn AM, Williamson ED (1993) Biochemical and immunological properties of the C-terminal domain of the alpha-toxin of Clostridium perfringens. FEMS Microbiol Lett 110:45–50
Tomita T, Kamio Y (1997) Molecular biology of the pore-forming cytolysins from Staphylococcus aureus, alpha- and gamma-hemolysins and leukocidin. Biosci Biotechnol Biochem 61(4):565–572
Tran Van Nhieu G, Ben-Ze’ev A, Sansonetti PJ (1997) Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J 16:2717–2729
Truitt RL, Hanke C, Radke J, Mueller R, Barbieri JT (1998) Glycosphingolipids as novel targets for T-cell suppression by the B subunit of recombinant heat-labile enterotoxin. Infect Immun 66:1299–1308
Tsai SC, Noda M, Adamik R, Chang PP, Chen HC, Moss J, Vaughan M (1988) Stimulation of choleragen enzymatic activities by GTP and two soluble proteins purified from bovine brain. J Biol Chem 263:1768–1772
Tsuge H, Nagahama M, Nishimura H, Hisatsune J, Sakaguchi Y, Itogawa Y, Katunuma N, Sakurai J (2003) Crystal structure and site-directed mutagenesis of enzymatic components from Clostridium perfringens iota-toxin. J Mol Biol 325(3):471–483
Tweten RK, Barbieri JT, Collier RJ (1985) Diphtheria toxin. Effect of substituting aspartic acid for glutamic acid 148 on ADP-ribosyltransferase activity. J Biol Chem 260:10392–10394
Tweten RK (2001) Clostridium perfringens beta toxin and Clostridium septicum alpha toxin: their mechanisms and possible role in pathogenesis. Vet Microbiol 82(1):1–9
Ueda K, Hayaishi O (1985) ADP-ribosylation. Annu Rev Biochem 54:73–100
Umland TC, Wingert LM, Swaminathan S, Furey WF, Schmidt JJ, Sax M (1997) Structure of the receptor binding fragment HC of tetanus neurotoxin. Nat Struct Biol 4:788–792
Unnikrishnan M, Altmann DM, Proft T, Wahid F, Cohen J, Fraser JD, Sriskandan S (2002) The bacterial superantigen streptococcal mitogenic exotoxin Z is the major immunoactive agent of Streptococcus pyogenes. J Immunol 169(5):2561–2569
Van den Akker F, Merritt EA, Pizza M, Domenighini M, Rappuoli R, Hol WG (1995) The Arg7Lys mutant of heat-labile enterotoxin exhibits great flexibility of active site loop 47-56 of the A subunit. Biochemistry 34:10996–11004
Van den Akker F, Pizza M, Rappuoli R, Hol WG (1997) Crystal structure of a non-toxic mutant of heat-labile enterotoxin, which is a potent mucosal adjuvant. Protein Sci 6:2650–2654
Van der Goot FG, Lakey J, Pattus F, Kay CM, Sorokine O, Van Dorsselaer A, Buckley JT (1992) Spectroscopic study of the activation and oligomerization of the channel-forming toxin aerolysin: identification of the site of proteolytic activation. Biochemistry 31:8566–8570
Van der Goot FG, Ausio J, Wong KR, Pattus F, Buckley JT (1993) Dimerization stabilizes the pore-forming toxin aerolysin in solution. J Biol Chem 268:18272–18279
Van Ness BG, Howard JB, Bodley JW (1980) ADP-ribosylation of elongation factor 2 by diphtheria toxin. NMR spectra and proposed structures of ribosyl-diphthamide and its hydrolysis products. J Biol Chem 255:10710–10716
Vath GM, Earhart CA, Rago JV, Kim MH, Bohach GA, Schlievert PM, Ohlendorf DH (1997) The structure of the superantigen exfoliative toxin A suggests a novel regulation as a serine protease. Biochemistry 36:1559–1566
Vath GM, Earhart CA, Monie DD, Iandolo JJ, Schlievert PM, Ohlendorf DH (1999) The crystal structure of exfoliative toxin B: a superantigen with enzymatic activity. Biochemistry 38:10239–10246
Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M, Montecucco C (1999) Anthrax lethal factor cleaves the N-terminus of MAPKKS and induces tyrosine/threonine phosphorylation of MAPKS in cultured macrophages. J Appl Microbiol 87:288
von Eichel-Streiber C, Boquet P, Sauerborn M, Thelestam M (1996) Large clostridial cytotoxins–a family of glycosyltransferases modifying small GTP-binding proteins. Trends Microbiol 4(10):375–382
Wadsworth SJ, Goldfine H (1999) Listeria monocytogenes phospholipase C–dependent calcium signaling modulates bacterial entry into J774 macrophage–like cells. Infect Immun 67(4):1770–1778
Wallace AJ, Stillman TJ, Atkins A, Jamieson SJ, Bullough PA, Green J, Artymiuk PJ (2000) E. coli hemolysin E (HlyE, ClyA, SheA): X-ray crystal structure of the toxin and observation of membrane pores by electron microscopy. Cell 100:265–276
Wandersman C, Delepelaire P (1990) TolC, an Escherichia coli outer membrane protein required for hemolysin secretion. Proc Natl Acad Sci USA 87:4776–4780
Wang JF, Kieba IR, Korostoff J, Guo TL, Yamaguchi N, Rozmiarek H, Billings PC, Shenker BJ, Lally ET (1998) Molecular and biochemical mechanisms of Pasteurella haemolytica leukotoxin-induced cell death. Microb Pathog 25(6):317–331
Weinrauch Y, Zychlinsky A (1999) The induction of apoptosis by bacterial pathogens. Annu Rev Microbiol 53:155–187
Weiss AA, Hewlett EL (1986) Virulence factors of Bordetella pertussis. Annu Rev Microbiol 40:661–681
Weiss MS, Abele U, Weckesser J, Welte W, Schiltz E, Schulz GE (1991) Molecular architecture and electrostatic properties of a bacterial porin. Science 254:1627–1630
Weiss MS, Blanke SR, Collier RJ, Eisenberg D (1995) Structure of the isolated catalytic domain of diphtheria toxin. Biochemistry 34:773–781
Welch RA (1991) Pore-forming cytolysins of gram-negative bacteria. Mol Microbiol 5:521–528
Welch RA, Pellett S (1988) Transcriptional organization of the Escherichia coli hemolysin genes. J Bacteriol 170(4):1622–1630
Wesche J, Elliott JL, Falnes PO, Olsnes S, Collier RJ (1998) Characterization of membrane translocation by anthrax protective antigen. Biochemistry 37:15737–15746
West RE Jr, Moss J, Vaughan M, Liu T, Liu TY (1985) Pertussis toxin-catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADP-ribose acceptor site. J Biol Chem 260:14428–14430
Whalen MC, Wang JF, Carland FM, Heiskell ME, Dahlbeck D, Minsavage GV, Jones JB, Scott JW, Stall RE, Staskawicz BJ (1993) Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol Plant-Microbe Interact 6:616–627
Wick MJ, Hamood AN, Iglewski BH (1990) Analysis of the structure-function relationship of Pseudomonas aeruginosa exotoxin A. Mol Microbiol 4:527–535
Williamson ED, Titball RW (1993) A genetically engineered vaccine against the alpha-toxin of Clostridium perfringens protects mice against experimental gas gangrene. Vaccine 11:1253–1258
Wilson BA, Reich KA, Weinstein BR, Collier RJ (1990) Active-site mutations of diphtheria toxin: effects of replacing glutamic acid-148 with aspartic acid, glutamine, or serine. Biochemistry 29:8643–8651
Wolff C, Wattiez R, Ruysschaert JM, Cabiaux V (2004) Characterization of diphtheria toxin’s catalytic domain interaction with lipid membranes. Biochim Biophys Acta 1661(2):166–177
Woods DE, To M, Sokol PA (1989) Pseudomonas aeruginosa exoenzyme S as a pathogenic determinant in respiratory infections. Antibiot Chemother 42:27–35
Wurtele M, Renault L, Barbieri JT, Wittinghofer A, Wolf E (2001) Structure of the ExoS GTPase activating domain. FEBS Lett 491(1–2):26–29
Xu Y, Barbancon-Finck V, Barbieri JT (1994) Role of histidine 35 of the S1 subunit of pertussis toxin in the ADP-ribosylation of transducin. J Biol Chem 269:9993–9999
Xu-Amano J, Jackson RJ, Fujihashi K, Kiyono H, Staats HF, McGhee JR (1994) Helper Th1 and Th2 cell responses following mucosal or systemic immunization with cholera toxin. Vaccine 12:903–911
Yahr TL, Goranson J, Frank DW (1996) Exoenzyme S of Pseudomonas aeruginosa is secreted by a type III pathway. Mol Microbiol 22:991–1003
Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW (1998) ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95(23):13899–13904
Yamaguchi T, Nishifuji K, Sasaki M, Fudaba Y, Aepfelbacher M, Takata T, Ohara M, Komatsuzawa H, Amagai M, Sugai M (2002) Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect Immun 70(10):5835–5845
Yamaizumi M, Mekada E, Uchida T, Okada Y (1978) One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell. Cell 15:245–250
Yamamoto T, Tamura T, Yokota T (1984) Primary structure of heat-labile enterotoxin produced by Escherichia coli pathogenic for humans. J Biol Chem 259:5037–5044
Yoshida S, Katayama E, Kuwae A, Mimuro H, Suzuki T, Sasakawa C (2002) Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization. EMBO J 21(12):2923–2935
Yoshihara K, Matsushita O, Minami J, Okabe A (1994) Cloning and nucleotide sequence analysis of the colH gene from Clostridium histolyticum encoding a collagenase and a gelatinase. J Bacteriol 176(21):6489–6496
Young VB, Knox KA, Pratt JS, Cortez JS, Mansfield LS, Rogers AB, Fox JG, Schauer DB (2004) In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun 72(5):2521–2527
Zhang RG, Scott DL, Westbrook ML, Nance S, Spangler BD, Shipley GG, Westbrook EM (1995) The three-dimensional crystal structure of cholera toxin. J Mol Biol 251:563–573
Zhang ZY (1995) Are protein-tyrosine phosphatases specific for phosphotyrosine? J Biol Chem 270:16052–16055
Zhang S, Iandolo JJ, Stewart GC (1998) The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (SEJ). FEMS Microbiol Lett 168:227–233
Zhao Y, Li Z, Drozd SJ, Guo Y, Mourad W, Li H (2004) Crystal structure of Mycoplasma arthritidis mitogen complexed with HLA–DR1 reveals a novel superantigen fold and a dimerized superantigen–MHC complex. Structure (Camb) 12(2):277–288
Zhou D, Mooseker MS, Galan JE (1999a) An invasion-associated Salmonella protein modulates the actin-bundling activity of plastin. Proc Natl Acad Sci USA 96:10176–10181
Zhou D, Mooseker MS, Galan JE (1999b) Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283:2092–2095
Zhou D, Chen LM, Hernandez L, Shears SB, Galan JE (2001) A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 39(2):248–259
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Masignani, V., Pizza, M., Rappuoli, R. (2013). Bacterial Toxins. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30144-5_84
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