Shiga toxin 1 and ricin A chain bind to human polymorphonuclear leucocytes through a common receptor

Biochemical Journal

Volumn 432, Issue 1, 2010, Pages 173-180

  Arfilli, Valentina ^a   Carnicelli, Domenica ^a   Rocchi, Laura ^a   Ricci, Francesca ^b   Pagliaro, Pasqualepaolo ^b   Tazzari, Pier Luigi ^b   Brigotti, Maurizio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Haemolytic uraemic syndrome; Neutrophil; Ribosome inactivating protein; Ricin; Shiga toxin; Toll like receptor (TLR)

Indexed keywords

HAEMOLYTIC URAEMIC SYNDROME; NEUTROPHIL; RIBOSOME-INACTIVATING PROTEIN; RICIN; SHIGA TOXIN; TOLL-LIKE RECEPTORS;

BINDING ENERGY; BINDING SITES; BIOCHEMISTRY; CELL DEATH; ESCHERICHIA COLI; INTERFERONS;

TOXIC MATERIALS;

DIPHTHERIA TOXIN; GELONIN; MANNOSE RECEPTOR; MEMBRANE RECEPTOR; N ETHYLMALEIMIDE; RIBOSOME INACTIVATING PROTEIN; RICIN A; SAPORIN; SAPORIN S6; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VEROTOXIN 1;

ALPHA CHAIN; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL INTERACTION; CHILD; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LEUKOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RECEPTOR BINDING;

APOPTOSIS; BINDING, COMPETITIVE; DIPHTHERIA TOXIN; FLOW CYTOMETRY; HUMANS; IODINE RADIOISOTOPES; LECTINS, C-TYPE; MANNOSE-BINDING LECTINS; NEUTROPHILS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RADIOLIGAND ASSAY; RECEPTORS, CELL SURFACE; RICIN; SHIGA TOXIN 1; TOLL-LIKE RECEPTORS;

ESCHERICHIA COLI;

EID: 78649756962     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100455     Document Type: Article

References (45)

1. Trompeter, R. S., Schwartz, R., Chantler, C., Dillon, M. J., Haycock, G. B., Kay, R. and Barratt, T. M. (1983) Haemolytic-uraemic syndrome: an analysis of prognostic features. Arch. Dis. Child. 58, 101-105
2. Tarr, P. I., Gordon, C. A. and Chandler, W. L. (2005) Shiga-toxin-producing Escherichia coliand haemolytic uraemic syndrome. Lancet 365, 1073-1086
3. Noris, M. and Remuzzi, G. (2005) Hemolytic uremic syndrome. J. Am. Soc. Nephrol. 16, 1035-1050
4. Paton, J. C. and Paton, A. W. (1998) Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11, 450-479
5. Endo, Y., Tsurugi, K., Yutsudo, T., Takeda, Y., Ogasawara, T. and 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
6. Brigotti, M., Alfieri, R., Sestili, P., Bonelli, M., Petronini, P. G., Guidarelli, A., Barbieri, L., Stirpe, F. and Sperti, S. (2002) Damage to nuclear DNA induced by Shiga toxin 1 and ricin in human endothelial cells. FASEB J. 16, 365-372
7. Barbieri, L., Valbonesi, P., Brigotti, M., Montanaro, L., Stirpe, F. and Sperti, S. (1998) Shiga-like toxin I is a polynucleotide:adenosine glycosidase. Mol. Microbiol. 29, 661-662
8. Brigotti, M., Carnicelli, D., Ravanelli, E., Vara, A. G., Martinelli, C., Alfieri, R. R., Petronini, P. G. and Sestili, P. (2007) Molecular damage and induction of proinflammatory cytokines in human endothelial cells exposed to Shiga toxin 1, Shiga toxin 2, and α-sarcin. Infect. Immun. 75, 2201-2207
9. Matussek, A., Lauber, J., Bergau, A., Hansen, W., Rohde, M., Dittmar, K. E., Gunzer, M., Mengel, M., Gatzlaff, P., Hartmann, M. et al. (2003) Molecular and functional analysis of Shiga toxin-induced response patterns in human vascular endothelial cells. Blood 102, 1323-1332
10. Nakao, H. and Takeda, T. (2000) Escherichia coli Shiga toxin. J. Nat. Toxins 9, 299-313
11. Caprioli, A., Luzzi, I., Rosmini, F., Pasquini, P., Cirrincione, R., Gianviti, A., Matteucci, M. C. and Rizzoni, G. (1992) Hemolytic-uremic syndrome and Vero cytotoxin-producing Escherichia coli infection in Italy. J. Infect. Dis. 166, 154-158
12. Karmali, M. A., Petric, M., Lim, C., Fleming, P. C., Arbus, G. S. and Lior, H. (1985) The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J. Infect. Dis. 151, 775-782
13. Brigotti, M., Caprioli, A., Tozzi, A. E., Tazzari, P. L., Ricci, F., Conte, R., Carnicelli, D., Procaccino, M. A., Minelli, F., Ferretti, A. V. et al. (2006) Shiga toxins present in the gut and in the polymorphonuclear leukocytes circulating in the blood of children with hemolytic-uremic syndrome. J. Clin. Microbiol. 44, 313-317
14. Tazzari, P. L., Ricci, F., Carnicelli, D., Caprioli, A., Tozzi, A. E., Rizzoni, G., Conte, R. and Brigotti, M. (2004) Flow cytometry detection of Shiga toxins in the blood from children with hemolytic uremic syndrome. Cytometry B Clin. Cytom. 61, 40-44
15. Te Loo, D. M., van Hinsbergh, V. W., Van Den Heuvel, L. P. and Monnens, L.A. (2001) Detection of verocytotoxin bound to circulating polymorphonuclear leukocytes of patients with hemolytic uremic syndrome. J. Am. Soc. Nephrol. 12, 800-806
16. te Loo, D. M., Monnens, L. A., Van Der Velden, T. J., Vermeer, M. A., Preyers, F., Demacker, P. N., Van Den Heuvel, L. P. and van Hinsbergh, V. W. (2000) Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome. Blood 95, 3396-3402
17. Brigotti, M., Carnicelli, D., Ravanelli, E., Barbieri, S., Ricci, F., Bontadini, A., Tozzi, A. E., Scavia, G., Caprioli, A. and Tazzari, P. L. (2008) Interactions between Shiga toxins and human polymorphonuclear leukocytes. J. Leukocyte Biol. 84, 1019-1027
18. Griener, T. P., Mulvey, G. L., Marcato, P. and Armstrong, G. D. (2007) Differential binding of Shiga toxin 2 to human and murine neutrophils. J. Med. Microbiol. 56, 1423-1430
19. Fernandez, G. C., Gomez, S. A., Rubel, C. J., Bentancor, L. V., Barrionuevo, P., Alduncin, M., Grimoldi, I., Exeni, R., Isturiz, M. A. and Palermo, M. S. (2005) Impaired neutrophils in children with the typical form of hemolytic uremic syndrome. Pediatr. Nephrol. 20, 1306-1314
20. Flagler, M. J., Strasser, J. E., Chalk, C. L. and Weiss, A. A. (2007) Comparative analysis of the abilities of Shiga toxins 1 and 2 to bind to and influence neutrophil apoptosis. Infect. Immun. 75, 760-765
21. Geelen, J. M., Van Der Velden, T. J., Te Loo, D. M., Boerman, O. C., Van Den Heuvel, L. P. and Monnens, L. A. (2007) Lack of specific binding of Shiga-like toxin (verocytotoxin) and non-specific interaction of Shiga-like toxin 2 antibody with human polymorphonuclear leucocytes. Nephrol. Dial. Transplant. 22, 749-755
22. Akira, S. and Takeda, K. (2004) Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511
23. Creagh, E. M. and O'Neill, L. A. (2006) TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 27, 352-357
24. Gazi, U. and Martinez-Pomares, L. (2009) Influence of the mannose receptor in host immune responses. Immunobiology 214, 554-561
25. Barbieri, L., Battelli, M. G. and Stirpe, F. (1993) Ribosome-inactivating proteins from plants. Biochim. Biophys. Acta 1154, 237-282
26. Peumans, W. J., Hao, Q. and Van Damme, E. J. (2001) Ribosome-inactivating proteins from plants: more than RNA N-glycosidases? FASEB J. 15, 1493-1506
27. Calderwood, S. B., Auclair, F., Donohue-Rolfe, A., Keusch, G. T. and Mekalanos, J. J. (1987) Nucleotide sequence of the Shiga-like toxin genes of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 84, 4364-4368
28. O'Brien, A. D., Tesh, V. L., Donohue-Rolfe, A., Jackson, M. P., Olsnes, S., Sandvig, K., Lindberg, A. A. and Keusch, G. T. (1992) Shiga toxin: biochemistry, genetics, mode of action, and role in pathogenesis. Curr. Top. Microbiol. Immunol. 180, 65-94
29. Simmons, B. M., Stahl, P. D. and Russell, J. H. (1986) Mannose receptor-mediated uptake of ricin toxin and ricin A chain by macrophages. Multiple intracellular pathways for a chain translocation. J. Biol. Chem. 261, 7912-7920
30. Skilleter, D.N., Paine, A.J. and Stirpe, F. (1981) A comparison of the accumulation of ricin by hepatic parenchymal and non-parenchymal cells and its inhibition of protein synthesis. Biochim. Biophys. Acta 677, 495-500
31. Valera, I., Vigo, A. G., Alonso, S., Barbolla, L., Crespo, M. S. and Fernandez, N. (2007) Peptidoglycan and mannose-based molecular patterns trigger the arachidonic acid cascade in human polymorphonuclear leukocytes. J. Leukocyte Biol. 81, 925-933
32. Ryd, M., Alfredsson, H., Blomberg, L., Andersson, A. and Lindberg, A. A. (1989) Purification of Shiga toxin by α-D-galactose-(1-4)-β-D- galactose-(1-4)-β-D-glucose-(1-) receptor ligand-based chromatography. FEBS Lett. 258, 320-322
33. Sperti, S., Montanaro, L. and Rambelli, F. (1986) Dye affinity chromatography of ricin subunits. Biosci. Rep. 6, 1035-1040
34. Brigotti, M., Rambelli, F., Zamboni, M., Montanaro, L. and Sperti, S. (1989) Effect of α-sarcin and ribosome-inactivating proteins on the interaction of elongation factors with ribosomes. Biochem. J. 257, 723-727
35. Pope, C. G. and Stevens, M. F. (1958) The purification of diphtheria toxin and the isolation of crystalline toxin-protein. Br. J. Exp. Pathol. 39, 139-149
36. Cassatella, M. A., Cappelli, R., Della Bianca, V., Grzeskowiak, M., Dusi, S. and Berton, G. (1988) Interferon-γ activates human neutrophil oxygen metabolism and exocytosis. Immunology 63, 499-506
37. van Setten, P. A., Monnens, L. A., Verstraten, R. G., Van Den Heuvel, L. P. and van Hinsbergh, V. W. (1996) Effects of verocytotoxin-1 on nonadherent human monocytes: binding characteristics, protein synthesis, and induction of cytokine release. Blood 88, 174-183
38. Hedblom, M. L., Cawley, D. B., Boguslawski, S. and Houston, L. L. (1978) Binding of ricin A chain to rat liver ribosomes: relationship to ribosome inactivation. J. Supramol. Struct. 9, 253-268
39. Bainton, D. F., Ullyot, J. L. and Farquhar, M. G. (1971) The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J. Exp. Med. 134, 907-934
40. Akgul, C., Moulding, D. A. and Edwards, S. W. (2001) Molecular control of neutrophil apoptosis. FEBS Lett. 487, 318-322
41. Benatti, L., Nitti, G., Solinas, M., Valsasina, B., Vitale, A., Ceriotti, A. and Soria, M. R. (1991) A Saporin-6 cDNA containing a precursor sequence coding for a carboxyl-terminal extension. FEBS Lett. 291, 285-288
42. Stirpe, F., Gasperi-Campani, A., Barbieri, L., Falasca, A., Abbondanza, A. and Stevens, W. A. (1983) Ribosome-inactivating proteins from the seeds of Saponaria officinalis L. (soapwort), of Agrostemma githago L. (corn cockle) and of Asparagus officinalis L. (asparagus), and from the latex of Hura crepitans L. (sandbox tree). Biochem. J. 216, 617-625
43. Hartley, M. R. and Lord, J. M. (2004) Cytotoxic ribosome-inactivating lectins from plants. Biochim. Biophys. Acta 1701, 1-14
44. Macher, B. A. and Klock, J. C. (1980) Isolation and chemical characterization of neutral glycosphingolipids of human neutrophils. J. Biol. Chem. 255, 2092-2096
45. Woo, B. H., Lee, J. T., Na, D. H. and Lee, K. C. (2001) Sepharose-unbinding ricin E as a source for ricin A chain immunotoxin. J. Immunol. Methods 249, 91-98