Chapter 10 : The Evolution of Bacterial Toxins

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The prevailing paradigm of bacterial evolution is clonal descent with periodic modification, punctuated with discrete occurrences of horizontal genetic transmission. This latter phenomenon, termed "mosaicism," is reported with increasing frequency among bacterial toxins. Toxins are generally thought to execute one of two principal pathogenic functions: host avoidance and host damage. However, a prominent theme of bacterial toxin research in the last decade is the identification of multiple patho-genetic functions for bacterial toxins. In terms of evolution, it may be most efficient to adopt virulence factors from another pathogenic organism or to embue an existing one with additional functions. It should be noted that, of the extant STa molecules, none is clearly primative in the evolutionary sense, yet it is interesting to note that, like guanylin, EAST-1 contains four cysteine residues, rather than the six present in STaH and STaP. The typical RTX toxin is encoded by a four-gene operon comprising, in order, the modifying enzyme, the toxin structural gene, and the two components of the secretion system. The accessory genes are highly conserved among the RTX toxins, whereas there is substantial diversity among the toxin structural genes. The fundamental mechanisms of bacterial evolution operate on toxin genes as they do on all genetic loci.

Citation: Stine O, Nataro J. 2006. The Evolution of Bacterial Toxins, p 167-188. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch10
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(A) Schematic representation of the mosaic structures of alleles representative of the major allelic groups of leukotoxin in The different colors indicate sequence identity and the likely origins of the recombinant segments. The number of sites different from those in the corresponding region of the likely donor allele(s) and the degree of divergence are indicated below certain recombinant segments; all other segments exhibited 100% sequence identity to the corresponding regions of the donor alleles. Numbers above the proposed recombination sites indicate the position of the last nucleotide at the downstream end of the recombination segment. (B) Proposed sequence of recombination events in the evolution of to the formation of the and -type alleles (see panel A) in the ovine-specific lineages of leukotoxins and the bovine-specific allele This analysis suggests not only substantial mosaicism of the toxins, but also host-switching phenomena from ovine- to bovine- and back to ovine-specific alleles. Reprinted from reference with permission.

Citation: Stine O, Nataro J. 2006. The Evolution of Bacterial Toxins, p 167-188. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch10
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Image of FIGURE 2

Phylogenic tree of the clostridial neurotoxins drawn with the Phylip program. Reprinted from reference with permission.

Citation: Stine O, Nataro J. 2006. The Evolution of Bacterial Toxins, p 167-188. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch10
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Image of FIGURE 3

Phylogenetic trees of the SPATE proteins generated using ClustalX analysis of amino acid sequences from full-length SPATE passenger domains (A) or the N-terminal one-third (B) corresponding to amino acid 242 of the Pet toxin. Substrates subject to proteolysis are indicated in panel B. Reprinted from reference with permission of the publisher.

Citation: Stine O, Nataro J. 2006. The Evolution of Bacterial Toxins, p 167-188. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch10
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1. Acheson, D. W.,, A. V. Kane, and, G. T. Keusch. 2000. Shiga toxins. Methods Mol. Biol. 145: 4163.
2. Aimoto, S.,, T. Takao,, Y. Shimonishi,, S. Hara,, T. Takeda,, Y. Takeda, and, T. Miwatani. 1982. Amino-acid sequence of a heat-stable enterotoxin produced by human enterotoxigenic Escherichia coli. Eur. J. Biochem. 129: 257263.
3. Al-Hasani, K.,, I. R. Henderson,, H. Sakellaris,, K. Rajakumar,, T. Grant,, J. P. Nataro,, R. Robins-Browne, and, B. Adler. 2000. The sigA gene which is borne on the she pathogenicity island of Shigella flexneri 2a encodes an exported cytopathic protease involved in intestinal fluid accumulation. Infect. Immun. 68: 24572463.
4. Alonso, S.,, K. Pethe,, N. Mielcarek,, D. Raze, and, C. Locht. 2001. Role of ADP-ribosyltransferase activity of pertussis toxin in toxin-adhesin redundancy with filamentous hemagglutinin during Bordetella pertussis infection. Infect. Immun. 69: 60386043.
5. Arita, M.,, T. Honda,, T. Miwatani,, K. Ohmori,, T. Takao, and, Y. Shimonishi. 1991. Purification and characterization of a new heat-stable enterotoxin produced by Vibrio cholerae non-O1 serogroup Hakata. Infect. Immun. 59: 21862188.
6. Arita, M.,, T. Honda,, T. Miwatani,, T. Takeda,, T. Takao, and, Y. Shimonishi. 1991. Purification and characterization of a heat-stable enterotoxin of Vibrio mimicus. FEMS Microbiol. Lett. 63: 105110.
7. Atassi, M. Z., and, M. Oshima. 1999. Structure, activity, and immune (T and B cell) recognition of botulinum neurotoxins. Crit. Rev. Immunol. 19: 219260.
8. Bagley, K. C.,, S. F. Abdelwahab,, R. G. Tuskan,, T. R. Fouts, and, G. K. Lewis. 2002. Pertussis toxin and the adenylate cyclase toxin from Bordetella pertussis activate human monocyte-derived dendritic cells and dominantly inhibit cytokine production through a cAMP-dependent pathway. J. Leukoc. Biol. 72: 962969.
9. Balint, J. P.,, J. L. Kosiba, and, M. B. Cohen. 1997. The heat-stable enterotoxin-guanylin receptor is expressed in rat hepatocytes and in a rat hepatoma (H-35) cell line. J. Recept. Signal Trans-duct. Res. 17: 609630.
10. Barbieri, J. T.,, M. J. Riese, and, K. Aktories. 2002. Bacterial toxins that modify the actin cytoskeleton. Annu. Rev. Cell Dev. Biol. 18: 315344.
11. Barry, E. M.,, A. A. Weiss,, I. E. Ehrmann,, M. C. Gray,, E. L. Hewlett, and, M. S. Goodwin. 1991. Bordetella pertussis adenylate cyclase toxin and hemolytic activities require a second gene, cyaC, for activation. J. Bacteriol. 173: 720726.
12. Bauer, M. E., and, R. A. Welch. 1996. Association of RTX toxins with erythrocytes. Infect. Immun. 64: 46654672.
13. Beck, M.,, J. F. van den Bosch,, I. M. Jongenelen,, P. L. Loeffen,, R. Nielsen,, J. Nicolet, and, J. Frey. 1994. RTX toxin genotypes and phenotypes in Actinobacillus pleuropneumoniae field strains. J. Clin. Microbiol. 32: 27492754.
14. Benjelloun-Touimi, Z.,, P. J. Sansonetti, and, C. Parsot. 1995. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol. Microbiol. 17: 123135.
15. Benjelloun-Touimi, Z.,, M. S. Tahar,, C. Montecucco,, P. J. Sansonetti, and, C. Parsot. 1998. SepA, the 110 kDa protein secreted by Shigella flexneri: two-domain structure and proteolytic activity. Microbiology 144: 18151822.
16. Bhuiyan, N. A.,, M. Ansaruzzaman,, M. Kamruzzaman,, K. Alam,, N. R. Chowdhury,, M. Nishibuchi,, S. M. Faruque,, D. A. Sack,, Y. Takeda, and, G. B. Nair. 2002. Prevalence of the pandemic genotype of Vibrio parahaemolyticus in Dhaka, Bangladesh, and significance of its distribution across different serotypes. J. Clin. Microbiol. 40: 284286.
17. Bobak, D. A. 1999. Clostridial toxins: molecular probes of Rho-dependent signaling and apoptosis. Mol. Cell. Biochem. 193: 3742.
18. Bowman, C. C., and, J. D. Clements. 2001. Differential biological and adjuvant activities of cholera toxin and Escherichia coli heat-labile enterotoxin hybrids. Infect. Immun. 69: 15281535.
19. Brunder, W.,, H. Schmidt, and, H. Karch. 1997. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol. Microbiol. 24: 767778.
20. Burrows, L. L., and, R. Y. Lo. 1992. Molecular characterization of an RTX toxin determinant from Actinobacillus suis. Infect. Immun. 60: 21662173.
21. Busch, C., and, K. Aktories. 2000. Microbial toxins and the glycosylation of rho family GTPases. Curr. Opin. Struct. Biol. 10: 528535.
22. Chang, Y. F.,, J. Shi,, D. P. Ma,, S. J. Shin, and, D. H. Lein. 1993. Molecular analysis of the Actinobacillus pleuropneumoniae RTX toxin-III gene cluster. DNA Cell Biol. 12: 351362.
23. Chaves-Olarte, E.,, E. Freer,, A. Parra,, C. Guzman-Verri,, E. Moreno, and, M. Thelestam. 2002. R-Ras glucosylation and transient RhoA activation determine the cytopathic effect produced by toxin B variants from toxin A-negative strains of Clostridium difficile. J. Biol. Chem. 78: 79567963.
24. Chaves-Olarte, E.,, M. Weidmann,, C. Eichel-Streiber, and, M. Thelestam. 1997. Toxins A and B from Clostridium difficile differ with respect to enzymatic potencies, cellular substrate specificities, and surface binding to cultured cells. J. Clin. Investig. 100: 17341741.
25. Ciesla, W. P., Jr., and, D. A. Bobak. 1998. Clostridium difficile toxins A and B are cation-dependent UDP-glucose hydrolases with differing catalytic activities. J. Biol. Chem. 273: 1602116026.
26. Cohen, M. B. 1992. The heat-stable enterotoxin receptor: a probe for ligand hunting. J. Pediatr. Gastroenterol. Nutr. 15: 337338.
27. Crane, J. K.,, M. S. Wehner,, E. J. Bolen,, J. J. Sando,, J. Linden,, R. L. Guerrant, and, C. L. Sears. 1992. Regulation of intestinal guanylate cyclase by the heat-stable enterotoxin of Escherichia coli (STa) and protein kinase C. Infect. Immun. 60: 50045012.
28. Cullen, J. M., and, A. N. Rycroft. 1994. Phagocytosis by pig alveolar macrophages of Actinobacillus pleuropneumoniae serotype 2 mutant strains defective in haemolysin II (ApxII) and pleurotoxin (ApxIII). Microbiology 140: 237244.
29. Currie, M. G.,, K. F. Fok,, J. Kato,, R. J. Moore,, F. K. Hamra,, K. L. Duffin, and, C. E. Smith. 1992. Guanylin: an endogenous activator of intestinal guanylate cyclase. Proc. Natl. Acad. Sci. USA 89: 947951.
30. Czuprynski, C. J., and, R. A. Welch. 1995. Biological effects of RTX toxins: the possible role of lipopolysaccharide. Trends Microbiol. 3: 480483.
31. Davies, R. L.,, S. Campbell, and, T. S. Whittam. 2002. Mosaic structure and molecular evolution of the leukotoxin operon (lktCABD) in Mann-heimia (Pasteurella) haemolytica, Mannheimia glucosida, and Pasteurella trehalosi. J. Bacteriol. 184: 266277.
32. Davies, R. L.,, T. S. Whittam, and, R. K. Selander. 2001. Sequence diversity and molecular evolution of the leukotoxin (lktA) gene in bovine and ovine strains of Mannheimia (Pasteurella) haemolytica. J. Bacteriol. 183: 13941404.
33. Davis, B. M.,, H. H. Kimsey,, W. Chang, and, M. K. Waldor. 1999. The Vibrio cholerae O139 Calcutta bacteriophage CTXphi is infectious and encodes a novel repressor. J. Bacteriol. 181: 67796787.
34. Davis, B. M.,, K. E. Moyer,, E. F. Boyd, and, M. K. Waldor. 2000. CTX prophages in classical biotype Vibrio cholerae: functional phage genes but dysfunctional phage genomes. J. Bacteriol. 182: 69926998.
35. Davis, J.,, A. L. Smith,, W. R. Hughes, and, M. Golomb. 2001. Evolution of an autotransporter: domain shuffling and lateral transfer from pathogenic Haemophilus to Neisseria. J. Bacteriol. 183: 46264635.
36. de Sauvage, F. J.,, R. Horuk,, G. Bennett,, C. Quan,, J. P. Burnier, and, D. V. Goeddel. 1992. Characterization of the recombinant human receptor for Escherichia coli heat-stable enterotoxin. J. Biol. Chem. 267: 64796482.
37. Djafari, S.,, F. Ebel,, C. Deibel,, S. Kramer,, M. Hudel, and, T. Chakraborty. 1997. Characterization of an exported protease from Shiga toxin-producing Escherichia coli. Mol. Microbiol. 25: 771784.
38. Donnenberg, M. S., and, T. S. Whittam. 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Investig. 107: 539548.
39. Dutta, P. R.,, R. Cappello,, F. Navarro-Garcia, and, J. P. Nataro. 2002. Functional comparison of serine protease autotransporters of enterobacteriaceae. Infect. Immun. 70: 71057113.
40. Dziejman, M.,, E. Balon,, D. Boyd,, C. M. Fraser,, J. F. Heidelberg, and, J. J. Mekalanos. 2002. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl. Acad. Sci. USA 99: 15561561.
41. Ehrmann, I. E.,, M. C. Gray,, V. M. Gordon,, L. S. Gray, and, E. L. Hewlett. 1991. Hemolytic activity of adenylate cyclase toxin from Bordetella pertussis. FEBS Lett. 278: 7983.
42. Eklund, M. W., and, F. T. Poysky. 1974. Interconversion of type C and D strains of Clostridium botulinum by specific bacteriophages. Appl. Microbiol. 27: 251258.
43. Eklund, M. W.,, F. T. Poysky,, J. A. Meyers, and, G. A. Pelroy. 1974. Interspecies conversion of Clostridium botulinum type C to Clostridium novyi type A by bacteriophage. Science 186: 456458.
44. Eklund, M. W.,, F. T. Poysky,, L. M. Mseitif, and, M. S. Strom. 1988. Evidence for plasmid-mediated toxin and bacteriocin production in Clostridium botulinum type G. Appl. Environ. Microbiol. 54: 14051408.
45. Eklund, M. W.,, F. T. Poysky, and, S. M. Reed. 1972. Bacteriophage and the toxigenicity of Clostridium botulinum type D. Nat. New Biol. 235: 1617.
46. Eklund, M. W.,, F. T. Poysky,, S. M. Reed, and, C. A. Smith. 1971. Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science 172: 480482.
47. Eslava, C.,, F. Navarro-Garcia,, J. R. Czeczulin,, I. R. Henderson,, A. Cravioto, and, J. P. Nataro. 1998. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66: 31553163.
48. Faruque, S. M.,, Asadulghani, M., M. Rahman,, M. K. Waldor, and, D. A. Sack. 2000. Sunlight-induced propagation of the lysogenic phage encoding cholera toxin. Infect. Immun. 68: 47954801.
49. Faruque, S. M.,, J. Zhu,, Asadulghani, M., Kamruzzaman, and J., J. Mekalanos. 2003. Examination of diverse toxin-coregulated pilus-positive Vibrio cholerae strains fails to demonstrate evidence for Vibrio pathogenicity island phage. Infect. Immun. 71: 29932999.
50. Fasshauer, D.,, R. B. Sutton,, A. T. Brunger, and, R. Jahn. 1998. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. USA 95: 1578115786.
51. Fink, D. L.,, L. D. Cope,, E. J. Hansen, and, J. W. Geme III. 2001. The Haemophilus influenzae Hap autotransporter is a chymotrypsin clan serine protease and undergoes autoproteolysis via an intermolecular mechanism. J. Biol. Chem. 276: 3949239500.
52. Frey, J.,, J. T. Bosse,, Y. F. Chang,, J. M. Cullen,, B. Fenwick,, G. F. Gerlach,, D. Gygi,, F. Haesebrouck,, T. J. Inzana,, R. Jansen, et al. 1993. Actinobacillus pleuropneumoniae RTX-toxins: uniform designation of haemolysins, cytolysins, pleurotoxin and their genes. J. Gen. Microbiol. 139 (Pt. 8): 17231728.
53. Fullner, K. J.,, J. C. Boucher,, M. A. Hanes,, G. K. Haines III,, B. M. Meehan,, C. Walchle,, P. J. Sansonetti, and, J. J. Mekalanos. 2002. The contribution of accessory toxins of Vibrio cholerae O1 El Tor to the proinflammatory response in a murine pulmonary cholera model. J. Exp. Med. 195: 14551462.
54. Fullner, K. J.,, W. I. Lencer, and, J. J. Mekalanos. 2001. Vibrio cholerae-induced cellular responses of polarized T84 intestinal epithelial cells are dependent on production of cholera toxin and the RTX toxin. Infect. Immun. 69: 63106317.
55. Gentschev, I.,, G. Dietrich, and, W. Goebel. 2002. The E. coli alpha-hemolysin secretion system and its use in vaccine development. Trends Microbiol. 10: 3945.
56. Gentschev, I.,, G. Dietrich,, H. J. Mollenkopf,, Z. Sokolovic,, J. Hess,, S. H. Kaufmann, and, W. Goebel. 1997. The Escherichia coli hemolysin secretion apparatus—a versatile antigen delivery system in attenuated Salmonella. Behring Inst. Mitt.: 103113.
57. Gill, D. M. 1982. Bacterial toxins: a table of lethal amounts. Microbiol. Rev. 46: 8694.
58. Gimenez, D. F. 1976. Serological classification and typing of Clostridium botulinum. Dev. Biol. Stand. 32: 175183.
59. Gray, M. C.,, W. Ross,, K. Kim, and, E. L. Hewlett. 1999. Characterization of binding of adenylate cyclase toxin to target cells by flow cytometry. Infect. Immun. 67: 43934399.
60. Gray, W. R.,, A. Luque,, B. M. Olivera,, J. Barrett, and, L. J. Cruz. 1981. Peptide toxins from Conus geographus venom. J. Biol. Chem. 256: 47344740.
61. Greenberg, R. N.,, M. Hill,, J. Crytzer,, W. J. Krause,, S. L. Eber,, F. K. Hamra, and, L. R. Forte. 1997. Comparison of effects of uroguanylin, guanylin, and Escherichia coli heat-stable enterotoxin STa in mouse intestine and kidney: evidence that uroguanylin is an intestinal natriuretic hormone. J. Investig. Med. 45: 276282.
62. Grimminger, F.,, C. Scholz,, S. Bhakdi, and, W. Seeger. 1991. Subhemolytic doses of Escherichia coli hemolysin evoke large quantities of lipoxygenase products in human neutrophils. J. Biol. Chem. 266: 1426214269.
63. Grimminger, F.,, U. Sibelius,, S. Bhakdi,, N. Suttorp, and, W. Seeger. 1991. Escherichia coli hemolysin is a potent inductor of phosphoinosi-tide hydrolysis and related metabolic responses in human neutrophils. J. Clin. Invest. 88: 15311539.
64. Grimminger, F.,, M. Thomas,, R. Obernitz,, D. Walmrath,, S. Bhakdi, and, W. Seeger. 1990. Inflammatory lipid mediator generation elicited by viable hemolysin-forming Escherichia coli in lung vasculature. J. Exp. Med. 172: 11151125.
65. Grimminger, F.,, D. Walmrath,, R. G. Birkemeyer,, S. Bhakdi, and, W. Seeger. 1990. Leukotriene and hydroxyeicosatetraenoic acid generation elicited by low doses of Escherichia coli hemolysin in rabbit lungs. Infect. Immun. 58: 26592663.
66. Guarino, A.,, R. Giannella, and, M. R. Thompson. 1989. Citrobacter freundii produces an 18-amino-acid heat-stable enterotoxin identical to the 18-amino-acid Escherichia coli heat-stable enterotoxin (ST Ia). Infect. Immun. 57: 649652.
67. Gutell, R. R.,, B. Weiser,, C. R. Woese, and, H. F. Noller. 1985. Comparative anatomy of 16-S-like ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 32: 155216.
68. Guyer, D. M.,, I. R. Henderson,, J. P. Nataro, and, H. L. Mobley. 2000. Identification of sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol. Microbiol. 38: 5366.
69. Hauser, D.,, M. W. Eklund,, P. Boquet, and, M. R. Popoff. 1994. Organization of the botulinum neurotoxin C1 gene and its associated non-toxic protein genes in Clostridium botulinum C 468. Mol. Gen. Genet. 243: 631640.
70. Hauser, D.,, M. Gibert,, M. W. Eklund,, P. Boquet, and, M. R. Popoff. 1993. Comparative analysis of C3 and botulinal neurotoxin genes and their environment in Clostridium botulinum types C and D. J. Bacteriol. 175: 72607268.
71. Hauser, D.,, M. Gibert,, J. C. Marvaud,, M. W. Eklund, and, M. R. Popoff. 1995. Botulinal neurotoxin C1 complex genes, clostridial neurotoxin homology and genetic transfer in Clostridium botulinum. Toxicon 33: 515526.
72. Heidelberg, J. F.,, J. A. Eisen,, W. C. Nelson,, R. A. Clayton,, M. L. Gwinn,, R. J. Dodson,, D. H. Haft,, E. K. Hickey,, J. D. Peterson,, L. Umayam,, S. R. Gill,, K. E. Nelson,, T. D. Read,, H. Tettelin,, D. Richardson,, M. D. Ermolaeva,, J. Vamathevan,, S. Bass,, H. Qin,, I. Dragoi,, P. Sellers,, L. McDonald,, T. Utterback,, R. D. Fleishmann,, W. C. Nierman, and, O. White. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477483.
73. Henderson, I.,, S. M. Whelan,, T. O. Davis, and, N. P. Minton. 1996. Genetic characterisation of the botulinum toxin complex of Clostridium botulinum strain NCTC 2916. FEMS Microbiol. Lett. 140: 151158.
74. Henderson, I. R.,, R. Cappello, and, J. P. Nataro. 2000. Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol. 8: 529532.
75. Henderson, I. R.,, J. Czeczulin,, C. Eslava,, F. Noriega, and, J. P. Nataro. 1999. Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect. Immun. 67: 55875596.
76. Henderson, I. R.,, S. Hicks,, F. Navarro-Garcia,, W. P. Elias,, A. D. Philips, and, J. P. Nataro. 1999. Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect. Immun. 67: 53385344.
77. Henderson, I. R., and, J. P. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69: 12311243.
78. Henderson, I. R.,, F. Navarro-Garcia, and, J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6: 370378.
79. Hewlett, E., and, J. Wolff. 1976. Soluble adeny-late cyclase from the culture medium of Bordetella pertussis: purification and characterization. J. Bacteriol. 127: 890898.
80. Hewlett, E. L.,, V. M. Gordon,, J. D. McCaffery,, W. M. Sutherland, and, M. C. Gray. 1989. Adenylate cyclase toxin from Bordetella pertussis. Identification and purification of the holotoxin molecule. J. Biol. Chem. 264: 1937919384.
81. Hewlett, E. L.,, L. Gray,, M. Allietta,, I. Ehrmann,, V. M. Gordon, and, M. C. Gray. 1991. Adenylate cyclase toxin from Bordetella pertussis. Conformational change associated with toxin activity. J. Biol. Chem. 266: 1750317508.
82. Hewlett, E. L.,, K. J. Kim,, S. J. Lee, and, M. C. Gray. 2000. Adenylate cyclase toxin from Bordetella pertussis: current concepts and problems in the study of toxin functions. Int. J. Med. Microbiol. 290: 333335.
83. Hewlett, E. L.,, M. A. Urban,, C. R. Manclark, and, J. Wolff. 1976. Extracytoplasmic adenylate cyclase of Bordetella pertussis. Proc. Natl. Acad. Sci. USA 73: 19261930.
84. Heyderman, R. S.,, M. Soriani, and, T. R. Hirst. 2001. Is immune cell activation the missing link in the pathogenesis of post-diarrhoeal HUS? Trends Microbiol. 9: 262266.
85. Hofmann, F.,, C. Busch, and, K. Aktories. 1998. Chimeric clostridial cytotoxins: identification of the N-terminal region involved in protein substrate recognition. Infect. Immun. 66: 10761081.
86. Hsuan, S. L.,, M. S. Kannan,, S. Jeyaseelan,, Y. S. Prakash,, C. Malazdrewich,, M. S. Abrahamsen,, G. C. Sieck, and, S. K. Maheswaran. 1999. Pasteurella haemolytica leuko-toxin and endotoxin induced cytokine gene expression in bovine alveolar macrophages requires NF-kappaB activation and calcium elevation. Microb. Pathog. 26: 263273.
87. Jaeger, J. L., and, D. W. Acheson. 2000. Shiga toxin-producing Escherichia coli. Curr. Infect. Dis. Rep. 2: 6167.
88. Jansen, R.,, J. Briaire,, E. M. Kamp,, A. L. Gielkens, and, M. A. Smits. 1993. Cloning and characterization of the Actinobacillus pleuropneumoniae-RTX-toxin III (ApxIII) gene. Infect. Immun. 61: 947954.
89. Jansen, R.,, J. Briaire,, A. B. van Geel,, E. M. Kamp,, A. L. Gielkens, and, M. A. Smits. 1994. Genetic map of the Actinobacillus pleuropneumoniae RTX-toxin (Apx) operons: characterization of the ApxIII operons. Infect. Immun. 62: 44114418.
90. Jeyaseelan, S.,, S. L. Hsuan,, M. S. Kannan,, B. Walcheck,, J. F. Wang,, M. E. Kehrli,, E. T. Lally,, G. C. Sieck, and, S. K. Maheswaran. 2000. Lymphocyte function-associated antigen 1 is a receptor for Pasteurella haemolytica leukotoxin in bovine leukocytes. Infect. Immun. 68: 7279.
91. Jeyaseelan, S.,, M. S. Kannan,, S. L. Hsuan,, A. K. Singh,, T. F. Walseth, and, S. K. Maheswaran. 2001. Pasteurella (Mannheimia) haemolytica leukotoxin-induced cytolysis of bovine leukocytes: role of arachidonic acid and its regulation. Microb. Pathog. 30: 5969.
92. Johnson, S., and, D. N. Gerding. 1998. Clostridium difficile–associated diarrhea. Clin. Infect. Dis. 26: 10271034; quiz 10351036.
93. Just, I.,, F. Hofmann, and, K. Aktories. 2000. Molecular mode of action of the large clostridial cytotoxins. Curr. Top. Microbiol. Immunol. 250: 5583.
94. Khelef, N.,, P. Gounon, and, N. Guiso. 2001. Internalization of Bordetella pertussis adenylate cyclase-haemolysin into endocytic vesicles contributes to macrophage cytotoxicity. Cell Microbiol. 3: 721730.
95. Kimsey, H. H.,, G. B. Nair,, A. Ghosh, and, M. K. Waldor. 1998. Diverse CTXphis and evolution of new pathogenic Vibrio cholerae. Lancet 352: 457458.
96. Koehler, T. M. 2002. Bacillus anthracis genetics and virulence gene regulation. Curr. Top. Microbiol. Immunol. 271: 143164.
97. Kokai-Kun, J. F.,, A. R. Melton-Celsa, and, A. D. O’Brien. 2000. Elastase in intestinal mucus enhances the cytotoxicity of Shiga toxin type 2d. J. Biol. Chem. 275: 37133721.
98. Konig, B.,, A. Drynda,, A. Ambrosch, and, W. Konig. 1999. Toxin-induced modulation of inflammatory processes, p. 637–656. In J. E. Alouf and, J. H. Freer (ed.), The Comprehensive Sourcebook of Bacterial Protein Toxins, 2nd ed. Academic Press, London, United Kingdom.
99. Lacy, D. B., and, R. C. Stevens. 1999. Sequence homology and structural analysis of the clostridial neurotoxins. J. Mol. Biol. 291: 10911104.
100. Lacy, D. B., and, R. C. Stevens. 1998. Unraveling the structures and modes of action of bacterial toxins. Curr. Opin. Struct. Biol. 8: 778784.
101. Levine, M. M.,, H. L. DuPont,, S. B. Formal,, R. B. Hornick,, A. Takeuchi,, E. J. Gangarosa,, M. J. Snyder, and, J. P. Libonati. 1973. Pathogenesis of Shigella dysenteriae 1 (Shiga) dysentery. J. Infect. Dis. 127: 261270.
102. Lin, W.,, K. J. Fullner,, R. Clayton,, J. A. Sexton,, M. B. Rogers,, K. E. Calia,, S. B. Calderwood,, C. Fraser, and, J. J. Mekalanos. 1999. Identification of a vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc. Natl. Acad. Sci. USA 96: 10711076.
103. Lindgren, S. W.,, J. E. Samuel,, C. K. Schmitt, and, A. D. O’Brien. 1994. The specific activities of Shiga-like toxin type II (SLT-II) and SLT-II-related toxins of enterohemorrhagic Escherichia coli differ when measured by Vero cell cytotoxicity but not by mouse lethality. Infect. Immun. 62: 623631.
104. Ludwig, A., and, W. Goebel. 2000. Dangerous signals from E. coli toxin. Nat. Med. 6: 741742.
105. Ludwig, A., and, W. Goebel. 1999. The family of the multigenic encoded RTX toxins, p. 330–348. In J. E. Alouf and, J. H. Freer (ed.), The Comprehensive Sourcebook of Bacterial Protein Toxins, 2nd ed. Academic Press, London, United Kingdom.
106. Mangan, D. F.,, N. S. Taichman,, E. T. Lally, and, S. M. Wahl. 1991. Lethal effects of Actinobacillus actinomycetemcomitans leukotoxin on human T lymphocytes. Infect. Immun. 59: 32673272.
107. Marcato, P.,, G. Mulvey, and, G. D. Armstrong. 2002. Cloned Shiga toxin 2 B subunit induces apoptosis in Ramos Burkitt’s lymphoma B cells. Infect. Immun. 70: 12791286.
108. Matteoli, M.,, C. Verderio,, O. Rossetto,, N. Iezzi,, S. Coco,, G. Schiavo, and, C. Montecucco. 1996. Synaptic vesicle endocytosis mediates the entry of tetanus neurotoxin into hippocampal neurons. Proc. Natl. Acad. Sci. USA 93: 1331013315.
109. McVeigh, A.,, A. Fasano,, D. A. Scott,, S. Jelacic,, S. L. Moseley,, D. C. Robertson, and, S. J. Savarino. 2000. IS1414, an Escherichia coli insertion sequence with a heat-stable enterotoxin gene embedded in a transposase-like gene. Infect. Immun. 68: 57105715.
110. Mekalanos, J. J.,, E. J. Rubin, and, M. K. Waldor. 1997. Cholera: molecular basis for emergence and pathogenesis. FEMS Immunol. Med. Microbiol. 18: 241248.
111. Mellies, J. L.,, F. Navarro-Garcia,, I. Okeke,, J. Frederickson,, J. P. Nataro, and, J. B. Kaper. 2001. espC pathogenicity island of enteropathogenic Escherichia coli encodes an enterotoxin. Infect. Immun. 69: 315324.
112. Melton-Celsa, A. R.,, S. C. Darnell, and, A. D. O’Brien. 1996. Activation of Shiga-like toxins by mouse and human intestinal mucus correlates with virulence of enterohemorrhagic Escherichia coli O91:H21 isolates in orally infected, streptomycin-treated mice. Infect. Immun. 64: 15691576.
113. Melton-Celsa, A. R.,, J. F. Kokai-Kun, and, A. D. O’Brien. 2002. Activation of Shiga toxin type 2d (Stx2d) by elastase involves cleavage of the C-terminal two amino acids of the A2 peptide in the context of the appropriate B pentamer. Mol. Microbiol. 43: 207215.
114. Melton-Celsa, A. R.,, J. E. Rogers,, C. K. Schmitt,, S. C. Darnell, and, A. D. O’Brien. 1998. Virulence of Shiga toxin-producing Escherichia coli (STEC) in orally-infected mice correlates with the type of toxin produced by the infecting strain. Jpn. J. Med. Sci. Biol. 51(Suppl.): S108S114.
115. Menestrina, G.,, C. Moser,, S. Pellet, and, R. Welch. 1994. Pore-formation by Escherichia coli hemolysin (HlyA) and other members of the RTX toxins family. Toxicology 87: 249267.
116. Mezoff, A. G.,, R. A. Giannella,, M. N. Eade, and, M. B. Cohen. 1992. Escherichia coli enterotoxin (STa) binds to receptors, stimulates guanyl cyclase, and impairs absorption in rat colon. Gastroenterology 102: 816822.
117. Michel, J. L.,, R. Rappuoli,, J. R. Murphy, and, A. M. Pappenheimer, Jr. 1982. Restriction endonuclease map of the nontoxigenic corynephage gamma c and its relationship to the toxigenic corynephage beta c. J. Virol. 42: 510518.
118. Moriishi, K.,, M. Koura,, N. Abe,, N. Fujii,, Y. Fujinaga,, K. Inoue, and, K. Ogumad. 1996. Mosaic structures of neurotoxins produced from Clostridium botulinum types C and D organisms. Biochim. Biophys. Acta 1307: 123126.
119. Morris, J. G., Jr.,, G. E. Losonsky,, J. A. Johnson,, C. O. Tacket,, J. P. Nataro,, P. Panigrahi, and, M. M. Levin. 1995. Clinical and immunologic characteristics of Vibrio cholerae O139 Bengal infection in North American volunteers. J. Infect. Dis. 171: 903908.
120. Moss, J.,, S. C. Tsai,, P. Bruni,, R. Adamik,, Y. Kanaho,, E. L. Hewlett, and, M. Vaughan. 1985. Pertussis toxin-catalyzed ADP-ribosylation of adenylate cyclase. Effects of guanyl nucleotides and rhodopsin. Dev. Biol. Stand. 61: 4349.
121. Nagai, S.,, T. Yagihashi, and, A. Ishihama. 1993. DNA sequence analysis of an allelic variant of the Actinobacillus pleuropneumoniae-RTX-toxin I (ApxIA) from serotype 10. Microb. Pathog. 15: 485495.
122. Nagy, G.,, U. Dobrindt,, G. Blum-Oehler,, L. Emody,, W. Goebel, and, J. Hacker. 2000. Analysis of the hemolysin determinants of the uropathogenic Escherichia coli strain 536. Adv. Exp. Med. Biol. 485: 5761.
123. Nataro, J. P., and, J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142201.
124. Navarro-Garcia, F.,, C. Eslava,, J. M. Villaseca,, R. Lopez-Revilla,, J. R. Czeczulin,, S. Srinivas,, J. P. Nataro, and, A. Cravioto. 1998. In vitro effects of a high-molecular-weight heat-labile enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66: 31493154.
125. Nencioni, L.,, M. G. Pizza,, G. Volpini,, M. T. De Magistris,, F. Giovannoni, and, R. Rappuoli. 1991. Properties of the B oligomer of pertussis toxin. Infect. Immun. 59: 47324734.
126. O’Brien, A. D.,, V. L. Tesh,, A. Donohue-Rolfe,, M. P. Jackson,, S. Olsnes,, K. Sandvig,, A. A. Lindberg, and, G. T. Keusch. 1992. Shiga toxin: biochemistry, genetics, mode of action, and role in pathogenesis. Curr. Top. Microbiol. Immunol. 180: 6594.
127. Ohta, H.,, A. Miyagi,, K. Kato, and, K. Fukui. 1996. The relationships between leukotoxin production, growth rate and the bicarbonate concentration in a toxin-production-variable strain of Actinobacillus actinomycetemcomitans. Microbiology 142(Pt. 4): 963970.
128. Okeke, I. N.,, A. Lamikanra,, J. Czeczulin,, F. Dubovsky,, J. B. Kaper, and, J. P. Nataro. 2000. Heterogeneous virulence of enteroaggregative Escherichia coli strains isolated from children in Southwest Nigeria. J. Infect. Dis. 181: 252260.
129. Okeke, I. N., and, J. P. Nataro. 2001. Enteroaggregative Escherichia coli. Lancet Infect. Dis. 1: 304313.
130. Ozaki, H.,, T. Sato,, H. Kubota,, Y. Hata,, Y. Katsube, and, Y. Shimonishi. 1991. Molecular structure of the toxin domain of heat-stable enterotoxin produced by a pathogenic strain of Escherichia coli. A putative binding site for a binding protein on rat intestinal epithelial cell membranes. J. Biol. Chem. 266: 59345941.
131. Pappenheimer, A. M., Jr., and, J. R. Murphy. 1983. Studies on the molecular epidemiology of diphtheria. Lancet 2: 923926.
132. Pellett, S., and, R. A. Welch. 1996. Escherichia coli hemolysin mutants with altered target cell specificity. Infect. Immun. 64: 30813087.
133. Popoff, M. R., and, J.-C. Marvaud. 1999. Structural and genomic features of clostridial neurotoxins, p. 174–201. In J. E. Alouf and, J. H. Freer (ed.), The Comprehensive Sourcebook of Bacterial Protein Toxins, 2nd ed. Academic Press, London, United Kingdom.
134. Qa’Dan, M.,, M. Ramsey,, J. Daniel,, L. M. Spyres,, B. Safiejko-Mroczka,, W. Ortiz-Leduc, and, J. D. Ballard. 2002. Clostridium difficile toxin B activates dual caspase-dependent and caspase-independent apoptosis in intoxicated cells. Cell Microbiol. 4: 425434.
135. Rosoff, P. M.,, R. Walker, and, L. Winberry. 1987. Pertussis toxin triggers rapid second messenger production in human T lymphocytes. J. Immunol. 139: 24192423.
136. Samra, Z.,, S. Talmor, and, J. Bahar. 2002. High prevalence of toxin A-negative toxin B-positive Clostridium difficile in hospitalized patients with gastrointestinal disease. Diagn. Microbiol. Infect. Dis. 43: 189192.
137. Savarino, S. J.,, A. Fasano,, J. Watson,, B. M. Martin,, M. M. Levine,, S. Guandalini, and, P. Guerry. 1993. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc. Natl. Acad. Sci. USA 90: 30933097.
138. Schiavo, G.,, M. Matteoli, and, C. Montecucco. 2000. Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80: 717766.
139. Sears, C. L., and, J. B. Kaper. 1996. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60: 167215.
140. So, M.,, R. Atchison,, S. Falkow,, S. Moseley, and, B. J. McCarthy. 1981. A study of the dissemination of Tn1681: a bacterial transposon encoding a heat-stable toxin among enterotoxigenic Escherichia coli isolates. Cold Spring Harbor Symp. Quant. Biol. 45 (Pt. 1): 5358.
141. So, M.,, F. Heffron, and, B. J. McCarthy. 1979. The E. coli gene encoding heat stable toxin is a bacterial transposon flanked by inverted repeats of IS1. Nature 277: 453456.
142. So, M., and, B. J. McCarthy. 1980. Nucleotide sequence of the bacterial transposon Tn1681 encoding a heat-stable (ST) toxin and its identification in enterotoxigenic Escherichia coli strains. Proc. Natl. Acad. Sci. USA 77: 40114015.
143. Stathopoulos, C.,, D. L. Provence, and, R. Curtiss III. 1999. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect. Immun. 67: 772781.
144. Sun, Y.,, K. D. Clinkenbeard,, C. Clarke,, L. Cudd,, S. K. Highlander, and, S. M. Dabo. 1999. Pasteurella haemolytica leukotoxin induced apoptosis of bovine lymphocytes involves DNA fragmentation. Vet. Microbiol. 65: 153166.
145. Sun, Y.,, K. D. Clinkenbeard,, L. A. Cudd,, C. R. Clarke, and, P. A. Clinkenbeard. 1999. Correlation of Pasteurella haemolytica leukotoxin binding with susceptibility to intoxication of lymphoid cells from various species. Infect. Immun. 67: 62646269.
146. Szabo, G.,, M. C. Gray, and, E. L. Hewlett. 1994. Adenylate cyclase toxin from Bordetella pertussis produces ion conductance across artificial lipid bilayers in a calcium- and polarity-dependent manner. J. Biol. Chem. 269:- 2249622499.
147. Takao, T.,, T. Hitouji,, S. Aimoto,, Y. Shimonishi,, S. Hara,, T. Takeda,, Y. Takeda, and, T. Miwatani. 1983. Amino acid sequence of a heat-stable enterotoxin isolated from enterotoxigenic Escherichia coli strain 18D. FEBS Lett. 152: 15.
148. Takao, T.,, N. Tominaga,, S. Yoshimura,, Y. Shimonishi,, S. Hara,, T. Inoue, and, A. Miyama. 1985. Isolation, primary structure and synthesis of heat-stable enterotoxin produced by Yersinia enterocolitica. Eur. J. Biochem. 152: 199206.
149. Teel, L. D.,, A. R. Melton-Celsa,, C. K. Schmitt, and, A. D. O’Brien. 2002. One of two copies of the gene for the activatable shiga toxin type 2d in Escherichia coli O91:H21 strain B2F1 is associated with an inducible bacteriophage. Infect. Immun. 70: 42824291.
150. Tesh, V. 1998. Cytokine response to Shiga toxins, p. 226–235. In J. B. Kaper and, A. D. O’Brien (ed.), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains. American Society for Microbiology Press, Washington, D. C.
151. Tesh, V. L.,, J. A. Burris,, J. W. Owens,, V. M. Gordon,, E. A. Wadolkowski,, A. D. O’Brien, and, J. E. Samuel. 1993. Comparison of the relative toxicities of Shiga-like toxins type I and type II for mice. Infect. Immun. 61: 33923402.
152. Thelestam, M., and, E. Chaves-Olarte. 2000. Cytotoxic effects of the Clostridium difficile toxins. Curr. Top. Microbiol. Immunol. 250: 8596.
153. Thom, R. E., and, J. E. Casnellie. 1989. Pertussis toxin activates protein kinase C and a tyrosine protein kinase in the human T cell line Jurkat. FEBS Lett. 244: 181184.
154. Thorpe, C. M.,, B. P. Hurley, and, D. W. Acheson. 2003. Shiga toxin interactions with the intestinal epithelium. Methods Mol. Med. 73: 263273.
155. Tu, A. H.,, C. Hausler,, R. Young, and, D. K. Struck. 1994. Differential expression of the cytotoxic and hemolytic activities of the ApxIIA toxin from Actinobacillus pleuropneumoniae. Infect. Immun. 62: 21192121.
156. van den Berg, B. M.,, H. Beekhuizen,, R. J. Willems,, F. R. Mooi, and, R. van Furth. 1999. Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect. Immun. 67: 10561062.
157. Van Ostaaijen, J.,, J. Frey,, S. Rosendal, and, J. I. MacInnes. 1997. Actinobacillus suis strains isolated from healthy and diseased swine are clonal and carry apxICABDvar. suis and apxIICAvar. suis toxin genes. J. Clin. Microbiol. 35: 11311137.
158. Villaseca, J. M.,, F. Navarro-Garcia,, G. Mendoza-Hernandez,, J. P. Nataro,, A. Cravioto, and, C. Eslava. 2000. Pet toxin from enteroaggregative Escherichia coli produces cellular damage associated with fodrin disruption. Infect. Immun. 68: 59205927.
159. Wagner, P. L.,, D. W. Acheson, and, M. K. Waldor. 1999. Isogenic lysogens of diverse shiga toxin 2-encoding bacteriophages produce markedly different amounts of shiga toxin. Infect. Immun. 67: 67106714.
160. Wagner, P. L.,, J. Livny,, M. N. Neely,, D. W. Acheson,, D. I. Friedman, and, M. K. Waldor. 2002. Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol. Microbiol. 44: 957970.
161. Wagner, P. L., and, M. K. Waldor. 2002. Bacteriophage control of bacterial virulence. Infect. Immun. 70: 39853993.
162. Waldor, M. K. 1998. Bacteriophage biology and bacterial virulence. Trends Microbiol. 6: 295297.
163. Waldor, M. K., and, J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 19101914.
164. Wang, J. F.,, I. R. Kieba,, J. Korostoff,, T. L. Guo,, N. Yamaguchi,, H. Rozmiarek,, P. C. Billings,, B. J. Shenker, and, E. T. Lally. 1998. Molecular and biochemical mechanisms of Pasteurella haemolytica leukotoxin-induced cell death. Microb. Pathog. 25: 317331.
165. Wang, Z.,, C. Clarke, and, K. Clinkenbeard. 1998. Pasteurella haemolytica leukotoxin-induced increase in phospholipase A2 activity in bovine neutrophils. Infect. Immun. 66: 18851890.
166. Wang, Z.,, C. R. Clarke, and, K. D. Clinkenbeard. 1999. Role of phospholipase D in Pasteurella haemolytica leukotoxin-induced increase in phospholipase A(2) activity in bovine neutrophils. Infect. Immun. 67: 37683772.
167. Welch, R. A. 2001. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr. Top. Microbiol. Immunol. 257: 85111.
168. Welch, R. A.,, M. E. Bauer,, A. D. Kent,, J. A. Leeds,, M. Moayeri,, L. B. Regassa, and, D. L. Swenson. 1995. Battling against host phagocytes: the wherefore of the RTX family of toxins? Infect Agents Dis. 4: 254272.
169. Wiegand, R. C.,, J. Kato,, M. D. Huang,, K. F. Fok,, J. F. Kachur, and, M. G. Currie. 1992. Human guanylin: cDNA isolation, structure, and activity. FEBS Lett. 311: 150154.
170. Woese, C. R.,, E. Stackebrandt,, T. J. Macke, and, G. E. Fox. 1985. A phylogenetic definition of the major eubacterial taxa. Syst. Appl. Microbiol. 6: 143151.
171. Yoshimura, S.,, T. Takao,, Y. Shimonishi,, S. Hara,, M. Arita,, T. Takeda,, H. Imaishi,, T. Honda, and, T. Miwatani. 1986. A heat-stable enterotoxin of Vibrio cholerae non-O1: chemical synthesis, and biological and physicochemical properties. Biopolymers 25 (Suppl.): S69S83.
172. Zaretzky, F. R.,, M. C. Gray, and, E. L. Hewlett. 2002. Mechanism of association of adenylate cyclase toxin with the surface of Bordetella pertussis: a role for toxin-filamentous haemagglutinin interaction. Mol. Microbiol. 45: 15891598.


Generic image for table

The STa family of toxins

Citation: Stine O, Nataro J. 2006. The Evolution of Bacterial Toxins, p 167-188. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch10
Generic image for table

Summary of SPATE functions

Citation: Stine O, Nataro J. 2006. The Evolution of Bacterial Toxins, p 167-188. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch10

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