Receptor affinity, stability and binding mode of Shiga toxins are determinants of toxicity

Microbial Pathogenesis

Volumn 43, Issue 2, 2007, Pages 88-95

  Shimizu, Takeshi ^a   Sato, Toshio ^b   Kawakami, Satomi ^c   Ohta, Toshiko ^c   Noda, Masatoshi ^a   Hamabata, Takashi ^b  

^a CHIBA UNIVERSITY   (Japan)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Binding property; EHEC; Gb3; Shiga like toxin; Toxicity

Indexed keywords

GLOBOTRIAOSYLCERAMIDE; VEROTOXIN 1; VEROTOXIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; CHIMERA; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS LINKING; CYTOTOXICITY; HYBRID; LETHAL DOSE; MOLECULE; MOUSE; NONHUMAN; PATHOGENICITY; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RECEPTOR AFFINITY; VERO CELL;

ANIMALS; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LETHAL DOSE 50; MALE; MICE; PROTEIN BINDING; RECOMBINANT PROTEINS; SHIGA TOXINS; TRIHEXOSYLCERAMIDES; VERO CELLS;

ESCHERICHIA COLI; MUS;

EID: 34250793994     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2007.04.003     Document Type: Article

References (46)

1. Hofmann S.L. Southwestern internal medicine conference: Shiga-like toxins in hemolytic-uremic syndrome and thrombotic thrombocytopenic purpura. Am J Med Sci 306 (1993) 398-406
2. Keusch G.T., and Acheson D.W. Thrombotic thrombocytopenic purpura associated with Shiga toxins. Semin Hematol 34 (1997) 106-116
3. Lansbury L.E., and Ludlam H. E. coli O157: lessons from the past 15 years. J Infect 34 (1997) 189-193
4. Rooney J.C., Anderson R.M., and Hopkins I.J. Clinical and pathological aspects of central nervous system involvement in the haemolytic uraemic syndrome. Aust Paediatr J 7 (1971) 28-33
5. Upadhyaya K., Barwick K., Fishaut M., Kashgarian M., and Siegel N.J. The importance of nonrenal involvement in hemolytic-uremic syndrome. Pediatrics 65 (1980) 115-120
6. Tesh V.L., and O'Brien A.D. The pathogenic mechanisms of Shiga toxin and the Shiga-like toxins. Mol Microbiol 5 (1991) 1817-1822
7. Jackson M.P., Newland J.W., Holmes R.K., and O'Brien A.D. Nucleotide sequence analysis of the structural genes for Shiga-like toxin I encoded by bacteriophage 933J from E. coli. Microb Pathog 2 (1987) 147-153
8. Endo Y., Tsurugi K., Yutsudo T., Takeda Y., Ogasawara T., and Igarashi K. Site of action of a Vero toxin (VT2) from E. coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem 171 (1988) 45-50
9. Acheson D.W.K., Donohue-Rolfe A., and Keusch G.T. The family of Shiga and Shiga-like toxins. In: Alouf J.E., and Freer J.H. (Eds). Sourcebook of bacterial protein toxins (1991), Academic Press Ltd., London, UK 415-433
10. O'Brien A.D., and Holmes R.K. Shiga and Shiga-like toxins. Microbiol Rev 51 (1987) 206-220
11. Kleanthous H., Smith H.R., Scotland S.M., Gross R.J., Rowe B., Taylor C.M., et al. Haemolytic uraemic syndromes in the British Isles, 1985-8: association with verocytotoxin producing E. coli. Part 2: microbiological aspects. Arch Dis Child 65 (1990) 722-727
12. Ostroff S.M., Tarr P.I., Neill M.A., Lewis J.H., Hargrett-Bean N., and Kobayashi J.M. Toxin genotypes and plasmid profiles as determinants of systemic sequelae in E. coli O157:H7 infections. J Infect Dis 160 (1989) 994-998
13. Boerlin P., McEwen S.A., Boerlin-Petzold F., Wilson J.B., Johnson R.P., and Gyles C.L. Associations between virulence factors of Shiga toxin-producing E. coli and disease in humans. J Clin Microbiol 37 (1999) 497-503
14. Nakajima H., Kiyokawa N., Katagiri Y.U., Taguchi T., Suzuki T., Sekino T., et al. Kinetic analysis of binding between Shiga toxin and receptor glycolipid Gb3Cer by surface plasmon resonance. J Biol Chem 276 (2001) 42915-42922
15. Nishikawa K., Matsuoka K., Kita E., Okabe N., Mizuguchi M., Hino K., et al. A therapeutic agent with oriented carbohydrates for treatment of infections by Shiga toxin-producing E. coli O157:H7. Proc Natl Acad Sci USA 99 (2002) 7669-7674
16. Shimizu T., Hamabata T., Yoshiki A., Hori T., Ito S., Takeda Y., et al. An association of 27- and 40-kDa molecules with glycolipids that bind A-B bacterial enterotoxins to cultured cells. Biochim Biophys Acta 1612 (2003) 186-194
17. Wadolkowski E.A., Sung L.M., Burris J.A., Samuel J.E., and O'Brien A.D. Acute renal tubular necrosis and death of mice orally infected with E. coli strains that produce Shiga-like toxin type II. Infect Immun 58 (1990) 3959-3965
18. Tesh V.L., Burris J.A., Owens J.W., Gordon V.M., Wadolkowski E.A., O'Brien A.D., et al. Comparison of the relative toxicities of Shiga-like toxins type I and type II for mice. Infect Immun 61 (1993) 3392-3402
19. Louise C.B., and Obrig T.G. Specific interaction of E. coli O157:H7-derived Shiga-like toxin II with human renal endothelial cells. J Infect Dis 172 (1995) 1397-1401
20. Head S.C., Karmali M.A., and Lingwood C.A. Preparation of VT1 and VT2 hybrid toxins from their purified dissociated subunits. Evidence for B subunit modulation of a subunit function. J Biol Chem 266 (1991) 3617-3621
21. Weinstein D.L., Jackson M.P., Perera L.P., Holmes R.K., and O'Brien A.D. In vivo formation of hybrid toxins comprising Shiga toxin and the Shiga-like toxins and role of the B subunit in localization and cytotoxic activity. Infect Immun 57 (1989) 3743-3750
22. Fraser M.E., Fujinaga M., Cherney M.M., Melton-Celsa A.R., Twiddy E.M., O'Brien A.D., et al. Structure of Shiga toxin type 2 (Stx2) from E. coli O157:H7. J Biol Chem 279 (2004) 27511-27517
23. Acheson D.W., Moore R., De Breucker S., Lincicome L., Jacewicz M., Skutelsky E., et al. Translocation of Shiga toxin across polarized intestinal cells in tissue culture. Infect Immun 64 (1996) 3294-3300
24. Hurley B.P., Jacewicz M., Thorpe C.M., Lincicome L.L., King A.J., Keusch G.T., et al. Shiga toxins 1 and 2 translocate differently across polarized intestinal epithelial cells. Infect Immun 67 (1999) 6670-6677
25. te Loo D.M., Monnens L.A., van Der Velden T.J., Vermeer M.A., Preyers F., Demacker P.N., et al. Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic-uremic syndrome. Blood 95 (2000) 3396-3402
26. te Loo D.M., Heuvelink A.E., de Boer E., Nauta J., van der Walle J., Schroder C., et al. Vero cytotoxin binding to polymorphonuclear leukocytes among households with children with hemolytic-uremic syndrome. J Infect Dis 184 (2001) 446-450
27. Rutjes N.W., Binnington B.A., Smith C.R., Maloney M.D., and Lingwood C.A. Differential tissue targeting and pathogenesis of verotoxins 1 and 2 in the mouse animal model. Kidney Int 62 (2002) 832-845
28. Pellizzari A., Pang H., and Lingwood C.A. Binding of verocytotoxin 1 to its receptor is influenced by differences in receptor fatty acid content. Biochemistry 31 (1992) 1363-1370
29. Kiarash A., Boyd B., and Lingwood C.A. 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 (1994) 11138-11146
30. Binnington B., Lingwood D., Nutikka A., and Lingwood C.A. Effect of globotriaosyl ceramide fatty acid alpha-hydroxylation on the binding by verotoxin 1 and verotoxin 2. Neurochem Res 27 (2002) 807-813
31. Katagiri Y.U., Mori T., Nakajima H., Katagiri C., Taguchi T., Takeda T., et al. Activation of Src family kinase yes induced by Shiga toxin binding to globotriaosyl ceramide (Gb3/CD77) in low density, detergent-insoluble microdomains. J Biol Chem 274 (1999) 35278-35282
32. Anderson R.G. The caveolae membrane system. Annu Rev Biochem 67 (1998) 199-225
33. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
34. Torgersen M.L., Lauvrak S.U., and Sandvig K. The A-subunit of surface-bound Shiga toxin stimulates clathrin-dependent uptake of the toxin. FEBS J 272 (2005) 4103-4113
35. Daeron M. Fc receptor biology. Annu Rev Immunol 15 (1997) 203-234
36. Park J.G., and Schreiber A.D. Determinants of the phagocytic signal mediated by the type IIIA Fc gamma receptor, Fc gamma RIIIA: sequence requirements and interaction with protein-tyrosine kinases. Proc Natl Acad Sci USA 92 (1995) 7381-7385
37. Majeed M., Caveggion E., Lowell C.A., and Berton G. Role of Src kinases and Syk in Fcgamma receptor-mediated phagocytosis and phagosome-lysosome fusion. J Leukoc Biol 70 (2001) 801-811
38. Strzelecka-Kiliszek A., Kwiatkowska K., and Sobota A. Lyn and Syk kinases are sequentially engaged in phagocytosis mediated by Fc gamma R. J Immunol 169 (2002) 6787-6794
39. Lauvrak S.U., Walchli S., Iversen T.G., Slagsvold H.H., Torgersen M.L., Spilsberg B., et al. Shiga toxin regulates its entry in a Syk-dependent manner. Mol Biol Cell 17 (2006) 1096-1109
40. Noda M., Yutsudo T., Nakabayashi N., Hirayama T., and Takeda Y. Purification and some properties of Shiga-like toxin from E. coli 0157:H7 that is immunologically identical to Shiga toxin. Microb Pathog 2 (1987) 339-349
41. Yutsudo T., Nakabayashi N., Hirayama T., and Takeda Y. Purification and some properties of a Vero toxin from E. coli O157:H7 that is immunologically unrelated to Shiga toxin. Microb Pathog 3 (1987) 21-30
42. Miyake M., Utsuno E., and Noda M. Binding of avian ovomucoid to shiga-like toxin type 1 and its utilization for receptor analog affinity chromatography. Anal Biochem 281 (2000) 202-208
43. Mylvaganam M., Hansen H.C., Binnington B., Magnusson G., Nyholm P.G., and Lingwood C.A. Interaction of the verotoxin 1B subunit with soluble aminodeoxy analogues of globotriaosyl ceramides. Biochem J 368 (2002) 769-776
44. Finney D.J. Probit analysis. 3rd ed (1971), Cambridge University Press, London, UK
45. Griffin P.M., Ostroff S.M., Tauxe R.V., Greene K.D., Wells J.G., Lewis J.H., et al. Illnesses associated with E. coli O157:H7 infections. A broad clinical spectrum. Ann Intern Med 109 (1988) 705-712
46. Shimizu T, Kawakami S, Sato T, Sasaki T, Higashide M, Hamabata T. et al. Serine 31 residue of B subunit of Shiga toxin 2 is essential for the secretion in Enterohemorrhagic Escherichia coli. Infect Immun 2007;75:2189-200.