SHIGA TOXIN MODE OF ACTION IN E. COLI O157:H7 DISEASE

Tom G. Obrig

Department of Microbiology and Immunology, University of Rochester, Box 672, 601 Elmwood Avenue, Rochester, NY 14642

Received 12/2/97 Accepted 12/8/97

10. REFERENCES

1. Kononwalchuk, J., J.I. Speirs. & S. Stavric: Vero response to a cytotoxin of Escherichia coli. Infect. Immun 18,775-779 (1977).

2. O'Brien, A.D., V.L. Tesh, A. Donohue-Rolfe, M.P. Jackson, S. Olsnes, K. Sandvig, A.A. Lindberg & G.T. Keusch: Shiga toxin: Biochemistry, genetics, mode of action, and role in pathogenesis. Curr Topics Microbio. Immunol 180,65-94 (1992)

3. Whittam, T.S., M.L. Wolfe, I.K. Wachsmuth, F. Orskow, I. Orskov & R.A. Wilson: Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect Immun 61,1619-1629 (1993)

4. Girbes, T., J.M. Ferreras, R. Iglesias, L. Citores, C. De Torre, M.L. Carbajales, P. Jiminez, F.M. Benito & R. Munoz: Recent advances in the uses and applications of ribosome-inactivating proteins from plants. Cellular Molec Biol 42,461-471 (1996)

5. Pickering, L.K, T.G. Obrig & F.B. Stapleton: . Hemolytic uremic syndrome and enterohemorrhagic Escherichia coli (CME review article). Ped Infect Dis J 13,459-476 (1994)

6. Fontaine, A., J. Arondel, & P.J. Sansonetti: 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 (1988)

7. Richardson, S.E., T.A. Rotman, V. Jay, C.R. Smith, L.E. Becker, M. Petric, N.F. Olivieri & M.A. Karmali: Experimental verocytotoxemia in rabbits. Infect Immun 60,4154-4167 (1992)

8. Jackson, M. P.: Structure-function of Shiga toxin and the Shiga-like toxins. Microbiol Path 8,235-242 (1990)

9. Lingwood, C. A.: Verotoxins and their glycolipid receptors. Adv Lipid Res 25:189-211 (1993)

10. O'Brien, A.D., G.D. LaVeck, D.E. Griffin & M.R. Thompson: Characterization of Shigella dysenteriae 1 (Shiga) toxin purified by anti-Shiga toxin affinity chromatography. Infect Immun 30,170-179 (1980)

11. Olsnes, S., R. Reisbig & K. Eiklid: Subunit structure of Shigella cytotoxin. J Biol Chem, 256, 8732-8738 (1981)

12. Keusch, G.T., M. Jacewicz, D.W. Acheson, A. Donohue-Rolfe, A. V. Kane & G. McCluer: Globotriaosylceramide, Gb3, is an alternative functional receptor for Shiga-like toxin 2e. Infect Immun 63,1138-1141 (1995).

13. Weinstein, D.L., M.P. Jackson, J.E. Samuel, R.K. Holmes & A.D. O'Brien: Cloning and sequencing of a Shiga-like toxin type II variant from an Escherichia coli strain responsible for edema disease of swine. J Bact 170,4223-4230 (1988)

14. Endo, Y., K. Tsurugi, T. Yutsudo, Y. Takeda, T. Ogasawara & K. Igarashi: Site of action of Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. Eur J Biochem 171,45-50 (1988).

15. Obrig, T.G., T.P. Moran & J.E. Brown: The mode of action of Shiga toxin on peptide elongation of eukaryotic protein synthesis. Biochem J 244:287-294 (1987)

16. Obrig, T.G.: Toxins that inhibit host protein synthesis. In: Bacterial Pathogenesis: Part A, Identification and Regulation of Virulence Factors. Eds: Clark V.L., Bavoil P.M., Methods in Enzymol 235,647-656 (1994)

17. Olsnes, S. and A. Phil: Different biological properties of the two constitutent peptide chains of ricin, a toxic protein inhibiting protein synthesis. Biochemistry 12,3121-3126 (1973)

18. Obrig, T.G., J.D. Irvin & B. Hardesty: The effect of an antiviral peptide on elongation enzymes EF-1 and EF-2. Arch Biochem Biophys 155,278-289 (1973)

19. Calderwood, S.B.J., F. Auclair, A. Donohue-Rolfe, G.T. Keusch & J.J. Mekalanos: Nucleotide sequence of the Shiga-like toxin genes of Escherichia coli. Proc Natl Acad Sci USA 84,4364-4368 (1987)

20. Karmali, M.A., M. Petric, C. Lim, P.C. Fleming, G.S. Arbus & H. Lior: The association between idiopathic hemolytic uremic syndrome and infection by Verotoxin-producing Escherichia coli. J Infect Dis 151,775-778 (1985).

21. Kleanthous, H., H.R. Smith & S.M. Scotland: Haemolytic uraemic syndromes in the British Isles, 1985-8: association with verocytotoxin producing Escherichia coli Part 2:microbiological aspects. Arch Dis Child 65,722-727 (1990)

22. Tesh, V.L., J.A. Burris, J.W. Owens, V.M. Gordon, E.A. Wadolkowski, A.D. O'Brien & J.E. Samuel: Comparison of the relative toxicities of Shiga-like toxins type I and type II for mice. Infect Immun 61,3392-402 (1993)

23. Louise, C.B. & T.G. Obrig: Specific interaction of E. coli O157:H7-derived Shiga-like toxin-2 with human renal endothelial cells. J Infect Dis 172:1397-1401 (1995)

24. Obrig, T.G., C.B. Louise,C.A. Lingwood, B. Boyd, L. Barley-Maloney & T.O. Daniel: Endothelial heterogeneity in Shiga toxin receptors and responses. J Biol Chem 268,15484-15488 (1993)

25. R. Habib: Pathology of the hemolytic uremic syndrome. In: Hemolytic-uremic syndrome and thrombotic thrombocytopenic purpura. Eds: Kaplan B.S., Trompeter R.S. & Moake, J.L. Marcel Dekker, New York, (1992)

26. Lingwood, C.A., H. Law, S. Richardson, M. Petric, J.L. Brunton, & M. Karmali: Glycolipid binding of purified and recombinant Escherichia coli produced verotoxin in vitro. J Biol Chem 262,8834-8839 (1987)

27. Lingwood, C.A.: Verotoxins and their glycolipid receptors. Adv Lipid Res 25,189-211 (1993)

28. Stein, P.E., A. Boodhoo, G.J. Tyrell, J.L. Brunton & R.J. Read: Crystal structure of the cell-binding B oligomer of verotoxin-1 from E. coli. Nature 355,748-750 (1992)

29. Kiarash A, B. Boyd & C.A. Lingwood: Glycosphingolipid receptor function is modified by fatty acid content. Verotoxin 1 and verotoxin 2c preferentially recognize different globotriaosyl ceramide fatty acid homologues. J Biol Chem 269,11138-11146 (1994)

30. Kaplan, B.S., R.S. Trompeter & J.L. Moake: Hemolytic uremic syndrome and thrombotic thrombocytopenic purpura. Marcel Dekker, New York (1992)

31. Boyd, B. and C. Lingwood: Verotoxin receptor glycolipid in human renal tissue. Nephron 51,207-210 (1989)

32. Obrig, T.G., C.B. Louise, C.A. Lingwood, T.O. Daniel, S.A. Kaye, B. Boyd & M.P. Jackson: Shiga toxin-endothelial cell interactions. In: Recent Advances in Verocytotoxin-producing E. coli Infections. Eds: Karmali, M.A. & Goglio, A.G., Elsevier, Amsterdam (1994)

33. Sandvig, K, O. Garred, K Prydz, J.V. Kozlov, S.H. Hansen & B. van Deurs: Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature 358,510-512 (1992)

34. Eiklid, K & S. Olsnes: Interaction of Shigella shigae cytotoxin with receptors on sensitive and insensitive cells. J Receptor Res 1, 199-213 (1980)

35. Garred, O, E. Dubinina, A. Polesslaya, S. Olsnes, J. Kozlov & K. Sandvig: Role of the disulfide bond in Shiga toxin-A chain for toxin entry into cells. J Biol Chem 272:11414-11419 (1997)

36. Garred, O, E. Dubinina, P.K. Holm, S. Olsnes, B. van Deurs, J. Kozlov & K. Sandvig: Role of processing and intracellular transport for optimal toxicity of Shiga and toxin mutants. Exptl Cell Res 218,39-49 (1995)

37. Stenger, K-O., F. Windler, H. Karch, H. von Wulffen & J. Heesemann: Hemolytic uremic syndrome associated with an infection by verotoxin producing Escherichia coli O111 in a woman on oral contraceptives. Clin Nephrol 29,153-158 (1988)

38. Bridgewater, F.A.J., R.S. Morgan, K.E.K. Rowson & G.P. Wright: The neurotoxin of Shigella shigae. Morphological and functional lesions produced in the central nervous system of rabbits. Br J Exp Pathol 36,447-453 (1955)

39. Pai, C.H., J.K. Kelly & G.L. Meyers: Experimental infection of infant rabbits with Vero toxin-producing Escherichia coli. Infect Immun 51,16-23 (1986)

40. Riley, L.W., R.S. Remis, S.D. Helgerson, H.B. McGee, J.G. Wells, B.R. Davis, R.J. Herbert, E.S. Olcott, L.M. Johnson, N.T. Hargrett, P.A. Blake, & M.C. Cohen: Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308,681-685 (1983)

41. Tschape, H., R. Prager, W. Streckel, A. Fruth, F. Tietze & G. Rohme: Verotoxinogenic Citrobacter freundii associated with severe gastroenteritis and cases of hemolytic uremic syndrome in a nursery school: green butter as the infection source. Epidemiol and Infect 114,441-450 (1995)

42. Taylor, C.M., D.V. Milford, P.E. Rose, T.C.F. Roy & B. Rowe: The expression of blood group P1 in post-enterpathic haemolytic uraemic syndrome. Ped Nephrol 4,59-61 (1990)

43. Newburg, D.S., P. Chaturvedi, E.L. Lopez, S. Devoto, A. Fayad & T.G. Cleary: Susceptibility to hemolytic-uremic syndrome relates to erythrocyte glycosphingolipid patterns. J Infect Dis 168,476-479 (1993)

44. Mahan, J.D. , P.A. van Setten, C. McAllister, L.P.W. van den Huvel & L.A.H. Monnens: Effect of verotoxin-1 on human glomerular capillary endothelial cells. In: Recent Advances in Verocytotoxin-producing E. coli Infections. Eds: Karmali M.A. & Goglio A.G., Elsevier, Amsterdam (1994)

45. Lingwood, C.A. Verotoxin binding in human renal sections. Nephron 66, 21-28 (1994)

46. van Setten, P.A., H.G.G. Verstraten, L.P.W.J van der Heuvel, M.A. Karmali & L.A.H. Monnens: The role of monocytes in the pathogenesis of the haemolytic uremic syndrome (HUS). In: Recent Advances in Verocytotoxin-producing E. coli Infections. Eds: Karmali, M.A. & Goglio A.G., Elsevier, Amsterdam (1994)

47. Harel, Y., M. Silva, B. Giroir, A. Weinberg, T.G. Cleary & B. Beutler: A reporter transgene indicates renal-specific induction of tumor necrosis factor (TNF) by Shiga-like toxin. J Clin Invest 92,2110-2116 (1993)

48. Morigi, M., G. Micheletti, M. Figliuzzi, B. Imberti, M.A.. Karmali, A. Remuzzi, G. Remuzzi & C. Zoja: Verotoxin-1 promotes leukocyte adhesion to cultured endothelial cells under physiological flow conditions. Blood 86,4553-4558 (1996)

49. Schmidt, H., E. Maier, H. Karch & R. Benz: Pore-forming properties of the plasmid-endoded hemolysin of enterohemorrhagic Escherichia coli O157:H7.. Eur J Biochem 241,594-601 (1996)

50. Bauer, M. & R.A. Welch: Characterization of an RTX toxin from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 64,167-175 (1996)

51. Blattner, F.R., G. Plunkett III, C.A. Bloch, N.T. Perna, V. Burland, M. Rilewy, J. Collado-Vides, J.D. Glasner, C.K. Rode, G.F. Mayhew, J. Gregor, N.W. Davis, H.A. Kirkpatrick, M.A. Goeden, D.J. Rose, B. Mau & Y. Shao. The complete genome sequence of Escherichia coli K-12. Science 277,1453-1462 (1997)

52. Obrig, T.G., P.J. Del Vecchio, J.E. Brown, T.P Moran,., B.M. Rowland, T.K. Judge & S.W. Rothman: Direct cytotoxic action of Shiga toxin on human vascular endothelial cells. Infect Immun 56, 2373-2378 (1988)

53. Koster, F., V. Boonpucknavig, S. Sujaho., R. Gilman & M. Rahaman: Renal histopathology in the hemolytic-uremic syndrome following shigellosis. Clin Nephrol 21,126-133 (1984)

54. Cavanagh, J.B., J.G. Howard & J.L. Whitby: The neurotoxin of Shigella shigae. A comparative study of the effects produced in various laboratory animals. Br J Exp Med 37,272-278 (1956)

55. Richardson, S.E., M.A Karmali, L.E Becker & C.R. Smith: The histopathology of the hemolytic uremic syndrome associated with verotoxin-producing Escherichia coli infections. J Human Pathol 19,1102-1108 (1988)

56. Barrett, T.J., M.E. Potter & N.A. Strockbine: Evidence for participation of the macrophage in Shiga-like toxin-induced lethality in mice. Microb Pathog 9,95-103 (1990)

57. Eiklid, K. & S. Olsnes: Interaction of Shigella shigae cytotoxin with receptors on sensitive and insensitive cells. J Receptor Res 1,199-213 (1980)

58. Louise, C.B. & T.G. Obrig: Shiga toxin-associated hemolytic uremic syndrome: combined cytotoxic effects of Shiga toxin, interleukin-1 beta, and tumor necrosis factor alpha on human vascular endothelial cells in vitro. Infect Immun 59,4173-4179 (1991)

59. Louise,C.B. & T.G. Obrig: Shiga toxin-associated hemolytic uremic syndrome: combined cytotoxic effects of Shiga toxin and lipopolysaccharide (endotoxin) on human vascular endothelial cells in vitro. Infect Immun 60,1536-1543 (1992)

60. Tesh, V.L., J.E. Samuel, L.P. Perera, J.B. Sharefkin & A.D. O'Brien: Evaluation of the role of Shiga and Shiga-like toxins in mediating direct damage to human vascular endothelial cells. J Infect Dis 164,344-352 (1991)

61. van de Kar, N. C. A. J., L.A.H. Monnens, M.A. Karmali & V.W.M Van Hinsbergh: Tumor necrosis factor and interleukin-1 induce expression of the verocytotoxin receptor globotriaosylceramide on human endothelial cells: implications for the pathogenesis of the hemolytic uremic syndrome. Blood 80,2755-2764. (1992)

62. Cybulsky, M.I., M.K.W Chan & H.Z. Movat: Acute inflammation and microthrombosis induced by endotoxin, IL-1, and TNF and their implication in gram-negative infection. J Lab Invest 58,365-378 (1988)

63. Shands, J.W., Jr.: Macrophage procoagulants. Hemostasis 14,373-377 (1984)

64. Bevilacqua, M.P., R.R Schleef, M.A. Gimbrone & D.J. Loskutoff: Regulation of the fibrinolytic system of cultured human vascular endothelium by IL-1. J Clin Invest 78,587-591 (1986)

65. Bevilacqua, M.P., J.S. Pober, G.R Majeau, W. Friers, R.S. Cotran & M.A. Gimbrone Jr.: Recombinant TNF induces procoagulant activity in cultured human vascular endothelium: Characterization and comparison with the actions of IL-1. Proc Natl Acad Sci USA 83,4533-4537 (1986)

66. Nawroth, P.P. & D.M. Stern: Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med 163,740-745 (1986)

67. Pober, J.S. & R.S. Cotran: Cytokines and endothelial cell biology. Physiol Rev 70,427-451 (1990)

68. van de Kar, N.C.A.J., V.W.M. van Hinsbergh, F.T. Brommer & L.A.H. Monnens: The fibrinolytic system in the hemolytic uremic syndrome: in vivo and in vitro studies. Ped Res 36,257-264 (1994)

69. Kaye, S.A., C.B. Louise, B. Boyd, C.A Lingwood & T.G. Obrig: Shiga toxin-associated hemolytic uremic syndrome: Interleukin-1 beta enhancement of Shiga toxin cytotoxicity toward human vascular endothelial cells, in vitro. Infect Immun 61,3886-3891 (1993)

70. van de Kar, N.C.A.J., T. Kooistra, M. Vermeer, W. Lesslauer, L.A.H. Monnens & V.W.M. van Hinsbergh: Tumor necrosis factor induces endothelial galactosyl transferase activity and verocytotoxin receptors. Role of specific tumor necrosis factor receptors and protein kinase C. Blood 85,734-743 (1995)

71. Louise, C.B., M.C. Tran & T.G. Obrig: Sensitization of human umbilical vein endothelial cells to Shiga toxin: involvement of protein kinase C and NF-kappa B. Infect Immun 65,3337-3344 (1997)