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Chapter 23 : Holistic Perspective on the Escherichia coli Hemolysin

Author: Rodney A. Welch1
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Affiliations: 1: Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, Wisconsin 53706
Content Type: Monograph
Publication Year: 1994

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

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Abstract:

This chapter reviews the knowledge of the prototype of the RTX family of pore-forming toxins, the hemolysin, and proposes that new efforts be made to study the significance and roles of the exotoxins, together with those of endotoxins, as an integrated synergistic system of multiple virulence factors. The fundamental approach taken by biochemists and cell biologists interested in understanding the role in pathogenesis of a bacterial virulence factor such as an exoprotein has been to purify the exoprotein and observe its activity on different substrates, cells, and hosts. The RTX-associated diseases include pertussis, juvenile periodontitis, pneumonia, urinary tract infections, and wound infections. The epidemiological evidence for an association between RTX toxin production and isolates that cause disease is strong for all of the organisms except i, , and . The solubilization of hemolysin aggregates by a chaotropic agent such as urea causes an increase in the specific lytic activity of the hemolysin. The erythrocytes transform into echinocytes, in which gross cytoskeletal or membrane irregularities result in rounding of the cell and the formation of multiple teardrop-shaped projections from the cell surface. The cellular transformation is similar to that caused by the treatment of erthrocytes by a calcium ionophore. The motivation for covering the older literature in the chapter is to stimulate thought, experimentation, and discussion about the significance of the ever-present lipopolysaccharide (LPS) molecules on the structure and activity of the hemolysin.

Citation: Welch R. 1994. Holistic Perspective on the Escherichia coli Hemolysin, p 351-364. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch23
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Holistic Perspective on the Escherichia coli Hemolysin
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Citation: Welch R. 1994. Holistic Perspective on the Escherichia coli Hemolysin, p 351-364. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch23
/content/10.1128/9781555818340.chap23.fig23-1
Figure 1

After a 5-min treatment with the hemolysin, sheep erythrocytes were fixed and visualized by scanning electron microscopy ( ). The photograph shows the loss of the concave cellular structure typical of erythrocytes and the formation of multiple teardrop-shaped projections from the cell surface. Bar, 2 μm. The photograph was the gift of Sally Jorgensen, University of Minnesota.

10.1128/9781555818340/fig23-1_thmb.gif
10.1128/9781555818340/fig23-1.gif
Image of Figure 1
Figure 1

After a 5-min treatment with the hemolysin, sheep erythrocytes were fixed and visualized by scanning electron microscopy ( ). The photograph shows the loss of the concave cellular structure typical of erythrocytes and the formation of multiple teardrop-shaped projections from the cell surface. Bar, 2 μm. The photograph was the gift of Sally Jorgensen, University of Minnesota.

Citation: Welch R. 1994. Holistic Perspective on the Escherichia coli Hemolysin, p 351-364. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch23
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References

/content/book/10.1128/9781555818340.chap23
1. Arthur, M.,, C. E. Johnson,, R. H. Rubin,, R. D. Arbeit,, C. Campanelli,, C. Kim,, S. Steinbach,, M. Agarwal,, R. Wilkinson,, and R. Goldstein. 1989. Molecular epidemiology of adhesin and hemolysin virulence factors among uropathogenic Escherichia coli. Infect. Immun. 57: 303– 313.
2. Benz, R.,, A. Schmid,, W. Wagner,, and W. Goebel. 1989. Pore formation by the Escherichia coli hemolysin: evidence for an association-dissociation equilibrium of the pore-forming aggregates. Infect. Immun. 57: 887– 895.
3. Bhakdi, S. Unpublished data.
4. Bhakdi, S.,, N. Mackman,, J. M. Nicaud,, and I. B. Holland. 1986. Escherichia coli hemolysin may damage target cell membranes by generating transmembrane pores. Infect. Immun. 52: 63– 69.
5. Bhakdi, S.,, and E. Martin. 1991. Superoxide generation by human neutrophils induced by low doses of Escherichia coli hemolysin. Infect. Immun. 59: 2955– 2962.
6. Bohach, G. A.,, and I. S. Snyder. 1985. Chemical and immunological analysis of thecomplex structure of Escherichia coli a-hemolysin. J. Bacteriol. 164: 1071– 1080.
7. Bohach, G.,, and I. S. Snyder. 1986. Composition of affinity-purified a-hemolysin of Escherichia coli. Infect. Immun. 53: 435– 437.
8. Burrows, L. L.,, and R. Y. C. Lo. 1992. Molecular characterization of an RTX toxin determinant from Actinobacillus suis. Infect. Immun. 60: 2166– 2173.
9. Camprubi, S.,, J. Tomas,, F. Munoa,, C. Madrid,, and A. Juarez. 1990. Influence of lipopolysaccha-ride on external hemolytic activity of Salmonella typhimurium and Klebsiella pneumoniae. Curr. Microbiol. 20: 1– 3.
10. Cavalier!, S. J.,, and I. S. Snyder. 1982. Cytotoxic activity of partially purified Escherichia coli alpha haemolysin. J. Med. Microbiol. 15: 11– 21.
11. Chang, Y.,, D. Ma,, J. Shi,, and M. M. Chengappa. 1993. Molecular characterization of a leukotoxin gene from a Pasteurella haemolytica-like organism, encoding a new member of the RTX toxin family. Infect. Immun. 61: 2089– 2095.
12. Chang, Y.-F.,, R. Young,, D. Post,, and D. K. Struck. 1987. Identification and characterization of the Pasteurella haemolytica leukotoxin. Infect. Immun. 55: 2348– 2354.
13. Chang, Y.-F.,, R. Young,, and D. K. Struck. 1989. Cloning and characterization of a hemolysin gene from Actinobacillus (Haemophilus) pleuropneumoniae. DNA 8: 635– 647.
14. Falkow, S. 1988. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis. 10: S274– S276.
15. Fasano, A.,, B. Baudry,, D. Pumplin,, S. Wasserman,, B. D. Tall,, J. Ketley,, and J. B. Kaper. 1991. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc. Natl. Acad. Sci. USA 88: 5242– 5246.
16. Felmlee, T.,, S. Pellett,, E. Y. Lee,, and R. A. Welch. 1985. The Escherichia coli hemolysin is released extracellularly without cleavage of a signal peptide. J. Bacteriol. 163: 88– 93.
17. Felmlee, T.,, S. Pellett,, and R. A. Welch. 1985. The nucleotide sequence of an Escherichia coli chromosomal hemolysin. J. Bacteriol. 163: 94– 105.
18. Fontaine, A.,, J. Arondel,, and P. J. Sansonetti. 1988. Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a Tox - mutant of Shigella dysenteriae 1. Infect. Immun. 56: 3099– 3109.
19. Frey, J.,, R. Meier,, D. Gygi,, and J. Nicolet. 1991. Nucleotide sequence of the hemolysin I gene from Actinobacillus pleuropneumoniae. Infect. Immun. 59: 3026– 3032.
20. Glaser, P.,, D. Ladant,, O. Sezer,, F. Pichot,, A. Ullman,, and A. Danchin. 1988. The calmodulin-sensitive adenylate cyclase of Bordetella pertussis: cloning and expression in Escherichia coli. Mol. Microbiol. 2: 19– 30.
21. Gonzalez-Carrero, M. I.,, J. Zabala,, F. de la Cruz,, and J. M. Ortiz. 1985. Purification of a hemolysin from an overproducing E. coli strain. Mol. Gen. Genet. 109: 106– 110.
22. Grlmminger, F.,, U. Sibelius,, S. Bhakdi,, N. Suttorp,, and W. Seeger. 1991. Escherichia coli hemolysin is a potent inductor of phosphoinositide hydrolysis and related metabolic responses in human neutrophils. J. Clin. Invest. 88: 1531– 1539.
23. Hacker, J. C.,, C. Hughes,, H. Hof,, and W. Goebel. 1983. Cloned hemolysin genes from Escherichia coli that cause urinary tract infection determine different levels of toxicity in mice. Infect. Immun. 42: 57– 63.
24. Hewlett, E. L.,, V. M. Gordon,, J. D. McCaffery,, W. M. Sutherland,, and M. C. Gray. 1989. Adenylate cyclase toxin from Bordetella pertussis: identification of the holotoxin molecule. J. Biol. Chem. 264: 19379– 19384.
25. Highlander, S. K.,, M. Chidambaram,, M. J. Engler,, and G. M. Weinstock. 1989. DNA sequence of the Pasteurella haemolytica leukotoxin gene cluster. DNA 8: 15– 28.
26. Holmgren, J.,, and A. Svennerholm. 1977. Mechanism of disease and immunity in cholera: a review. J. Infect. Dis. 136S: 105– 112.
27. Issartel, J.-P.,, V. Koronakis,, and C. Hughes. 1991. Activation of Escherichia coli prohaemolysin to the mature toxin by acyl carrier protein-dependent fatty acylation. Nature (London) 351: 759– 761.
28. Jansen, R.,, J. Brake,, E. M. Kamp,, A. L. Gielkins,, and M. A. Smits. 1993. Cloning and characterization of the Actinobacillus pleuropnettmoniae RTX-toxin III (ApxIII) gene. Infect. Immun. 61: 947– 954.
29. Jonas, D.,, B. Schultheis,, C. Klas,, P. H. Krammer,, and S. Bhakdi. 1993. Cytocidal effects of Escherichia coli hemolysin on human T lymphocytes. Infect. Immun. 61: 1715– 1721.
30. Jorgensen, S. E.,, R. F. Hammer,, and G. K. Wu. 1980. Effects of a single hit from the α-hemolysin produced by Escherichia coli on the morphology of sheep erythrocytes. Infect. Immun. 27: 988– 994.
31. Jorgensen, S. E.,, P. F. Muicahy,, G. K. Wu,, and C. F. Louis. 1983. Calcium accumulation in human and sheep erythrocytes that is induced by Escherichia coli hemolysin. Toxicon 21: 717– 727.
32. Kaper, J. B.,, H. Lockman,, M. M. Baldini,, and M. M. Levine. 1984. A recombinant live oral cholera vaccine. Bio/Technology 2: 345– 349.
33. Kaper, J. B.,, H. Lockman,, M. M. Baldini,, and M. M. Levine. 1984. Recombinant nontoxigenic Vibrio cholerae strains as attenuated cholera vaccines candidates. Nature (London) 308: 655– 658.
34. Koronakis, V.,, M. Cross,, B. Senior,, E. Koranakis,, and C. Hughes. 1987. The secreted hemolysins of Proteus mirabilis, Proteus vulgaris, and Morganella morganii are genetically related to each other and to the α-hemolysin of Escherichia coli. J. Bacteriol. 169: 1509– 1515.
35. Kraig, E.,, T. Dailey,, and D. Kolodrubetz. 1990. Nucleotide sequence of the leukotoxin gene from Actinobacillus actinomycetemcomitans: homology to the α-hemolysin/leukotoxin gene family. Infect. Immun. 58: 920– 929.
36. Levine, M. M.,, J. B. Kaper,, D. Herrington,, G. Losonsky,, J. G. Morris,, M. L. Clements,, R. E. Black,, B. Tall,, and R. Hall. 1988. Volunteer studies of deletion mutants of Vibrio cholerae O1 prepared by recombinant techniques. Infect. Immun. 56: 161– 167.
37. Lo, R. Y., C. C. Strathdee,, and P. Shewen. 1987. Nucleotide sequence of the leukotoxin genes of Pasteurella haemolytica Al. Infect. Immun. 55: 1987– 1996.
38. Ludwig, A.,, R. Benz,, and W. Goebel. 1993. Oligomerization of Escherichia coli (HlyA) is involved in pore formation. Mol. Gen. Genet. 241: 89– 96.
39. Menestrina, G.,, N. Mackman,, I. B. Holland,, and S. Bhakdi. 1987. Escherichia coli haemolysin forms voltage-dependent ion channels in lipid membranes. Biochim. Biophys. Acta 905: 109– 117.
40. Moayeri, M. Unpublished data.
41. Nicaud, J. M.,, N. Mackman,, L. Gray,, and I. B. Holland. 1985. Characterization of HlyC and mechanism of activation and secretion of hemolysin from E. coli 2001. FEBS Lett. 187: 339– 344.
42. Opal, S. M.,, A. S. Cross,, P. Gemski,, and L. W. Lyhte. 1990. Aerobactin and a-hemolysin as virulence determinants in Escherichia coli isolated from human blood, urine, and stool. J. Infect. Dis. 161: 794– 796.
43. Ostolaza, H.,, B. Bartolome,, I. O. de Zarate,, F. de la Cruz,, and F. Goni. 1993. Release of lipid vesicle contents by the bacterial protein toxin a-hemolysin. Biochim. Biophys. Acta 1147: 81– 88.
44. Ostolaza, H.,, B. Bartoleme,, J. Serra,, F. de la Cruz,, and F. Goni. 1991. a-Hemolysin from E. coli: purification and self-aggregation properties. FEBS Lett. 280: 195– 198.
45. Parker, C. T.,, A. W. Kloser,, C. A. Schnaitman,, M. A. Stein,, S. Gottesman,, and B. W. Gibson. 1992. Role of the rfaG and rfaP genes in determination of the lipolysaccharide structure and cell surface properties of Escherichia coli. J. Bacteriol. 174: 2525– 2538.
46. Rennie, R. P.,, and J. P. Arbuthnott. 1974. Partial characterization of Escherichia coli haemolysin. J. Med. Microbiol. 7: 179– 188.
47. Rennie, R. P.,, J. H. Freer,, and J. P. Arbuthnott. 1974. The kinetics of erythrocyte lysis by Escherichia coli haemolysin. J. Med. Microbiol. 7: 189– 195.
48. Rocque, W.,, R. Coughlin,, and E. McGroarty. 1987. Lipopolysaccharide tightly bound to porin monomers and trimers from Escherichia coli K-12. J. Bacteriol. 169: 4003– 4010.
49. Rogel, A.,, J. Schultz,, R. M. Brownlie,, J. G. Coote,, R. Parton,, and E. Hanski. 1989. Bordetella pertussis adenylate cyclase: purification and characterization of the toxic form of the enzyme. EMBO J. 8: 2755– 2760.
50. Short, E. C. Jr.,, and H. J. Kurtz. 1971. Properties of the hemolytic activities of Escherichia coli. Infect. Immun. 3: 678– 687.
51. Smith, H. W.,, and M. B. Huggins. 1985. The toxic role of alpha-haemolysin in the pathogenesis of experimental Escherichia coli infection in mice. J. Gen. Microbiol. 131: 395– 403.
52. Stanley, P. L. D.,, P. Diaz,, M. J. A. Bailey,, D. Gygi,, A. Juarez,, and C. Hughes. 1993. Loss of activity in the secreted form of Escherichia coli haemolysin caused by an rfaP lesion in core lipopolysaccharide assembly. Mol. Microbiol. 10: 781– 787.
53. Swihart, K. G.,, and R. A. Welch. 1990. The HpmA hemolysin is more common than HlyA among Proteus isolates. Infect. Immun. 58: 1853– 1860.
54. Tesh, V. L.,, and A. D. O'Brien. 1991. The pathogenic mechanisms of Shiga toxin and the Shiga-like toxins. Mol. Microbiol. 5: 1817– 1822.
55. Trucksis, M.,, J. E. Galen,, J. Michalski,, A. Fasano,, and J. Kaper. 1993. Accessory cholera entero-toxin (Ace), the third toxin of a Vibrio cholerae virulence cassette. Proc. Natl. Acad. Sci. USA 90: 5267– 5271.
56. Wagner, W.,, M. Kuhn,, and W. Goebel. 1988. Active and inactive forms of hemolysin (HlyA) from Escherichia coli. Biol. Chem. Hoppe-Seyler 369: 39– 46.
57. Wandersman, C.,, and S. Letoffe. 1993. Involvement of lipopolysaccharide in the secretion of Escherichia coli a-hemolysin and Erwinia chrysanthemi protease. Mol. Microbiol. 7: 141– 150.
58. Welch, R. A. 1987. Identification of two different hemolysin determinants in uropathogenic Proteus isolates. Infect. Immun. 55: 2183– 2190.
59. Welch, R. A. 1991. Pore-forming cytolysins of gram-negative bacteria. Mol. Microbiol. 5: 521– 528.
60. Welch, R. A.,, E. P. Dellinger,, B. Minshew,, and S. Falkow. 1981. Hemolysin contributes to virulence of extra-intestinal Escherichia coli infections. Nature (London) 294: 665– 667.
61. Welch, R. A.,, R. Hull,, and S. Falkow. 1983. Molecular cloning and physical characterization of a chromosomal hemolysin from Escherichia coli. Infect. Immun. 42: 178– 186.
62. Welch, R. A.,, S. Pellett,, D. Robbins,, W. Keane,, G. Gekker,, and P. Peterson,. 1989. Epidemiological observations involving the Escherichia coli hemolysin. In E. Kass, and C. Svanborg-Eden (ed.), Host-Parasite Interactions in Urinary Tract Infections. University of Chicago Press, Chicago.
63. White, J. G. 1974. Effects of an ionophore, A23187, on the surface morphology of normal erythrocytes. Am. J. Pathol. 77: 507– 518.
64. Williams, P. H. 1979. Determination of the molecular weight of Escherichia coli α-haemolysin. FEMS Microbiol. Lett. 5: 21– 24.
65. Zwadyk, P.,, and I. S. Snyder. 1971. Purification and kinetic studies of the hemolysin from Escherichia coli. Can. J. Microbiol. 17: 741– 745.

Tables

Holistic Perspective on the Escherichia coli Hemolysin
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818340.chap23-1,webId=/content/author/10.1128/9781555818340.chap23-1,properties={foaf_givenname=Rodney A., foaf_name=Rodney A. Welch, foaf_surname=Welch, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818340.chap23-aff1]]}]]
Citation: Welch R. 1994. Holistic Perspective on the Escherichia coli Hemolysin, p 351-364. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch23
/content/10.1128/9781555818340.chap23.tab23-1
Table 1

Selected features of toxins from the RTX toxin branch of the RTX exoprotein family

The predicted pi, based on the predicted amino acid sequence of the toxin gene product.

PMNs, polymorphonuclear leukocytes.

A weak hemolytic activity is observed.

No hemolytic activity is observed.

10.1128/9781555818340/tab23-1_thmb.gif
10.1128/9781555818340/tab23-1.gif
Generic image for table
Table 1

Selected features of toxins from the RTX toxin branch of the RTX exoprotein family

The predicted pi, based on the predicted amino acid sequence of the toxin gene product.

PMNs, polymorphonuclear leukocytes.

A weak hemolytic activity is observed.

No hemolytic activity is observed.

Citation: Welch R. 1994. Holistic Perspective on the Escherichia coli Hemolysin, p 351-364. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch23

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