Endothelial damage induced by Shiga toxins delivered by neutrophils during transmigration

Journal of Leukocyte Biology

Volumn 88, Issue 1, 2010, Pages 201-210

  Brigotti, Maurizio ^a   Tazzari, Pier Luigi ^b   Ravanelli, Elisa ^a   Carnicelli, Domenica ^a   Barbieri, Stefania ^a   Rocchi, Laura ^a   Arfilli, Valentina ^a   Scavia, Gaia ^c   Ricci, Francesca ^b   Bontadini, Andrea ^b   Alfieri, Roberta R ^d   Petronini, Pier Giorgio ^d   Pecoraro, Carmine ^e   Tozzi, Alberto E ^f   Caprioli, Alfredo ^c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e SANTOBONO PAUSILIPON CHILDREN S HOSPITAL   (Italy)

^f BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

Author keywords

Degranulation; Endothelial cells; Hemolytic uremic syndrome; Polymorphonuclear leukocytes; Proinflammatory cytokine

Indexed keywords

VEROTOXIN 1; CYTOKINE;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL MIGRATION; CELL VIABILITY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEGRANULATION; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; HEMOLYTIC UREMIC SYNDROME; HUMAN; HUMAN CELL; KIDNEY INJURY; LEUKOCYTE; NEUTROPHIL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; BIOSYNTHESIS; CELL CULTURE; CELL MOTION; CELL SURVIVAL; DRUG EFFECT; METABOLISM; PHYSIOLOGY;

ANIMALIA;

CELL DEGRANULATION; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; CYTOKINES; ENDOTHELIAL CELLS; HEMOLYTIC-UREMIC SYNDROME; HUMANS; NEUTROPHILS; SHIGA TOXIN 1;

EID: 77954662966     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0709475     Document Type: Article

References (40)

1. Trompeter, R. S., Schwartz, R., Chantler, C., Dillon, M. J., Haycock, G. B., Kay, R., Barratt, T. M. (1983) Hemolytic-uremic syndrome: an analysis of prognostic features. Arch. Dis. Child. 58, 101-105. (Pubitemid 13152859)
2. Griffin, P. M., Tauxe, R. V. (1991) The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol. Rev. 13, 60-98.
3. Karmali, M. A., Petric, M., Lim, C., Fleming, P. C., Arbus, G. S., Lior, H. (1985) The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J. Infect. Dis. 151, 775-782. (Pubitemid 15094592)
4. Tozzi, A. E., Caprioli, A., Minelli, F., Gianviti, A., De Petris, L., Edefonti, A., Montini, G., Ferretti, A., De Palo, T., Gaido, M., Rizzoni, G. (2003) Shiga toxin-producing Escherichia coli infections associated with hemolytic uremic syndrome, Italy, 1988-2000. Emerg. Infect. Dis. 9, 106-108.
5. Noris, M., Remuzzi, G. (2005) Hemolytic uremic syndrome. J. Am. Soc. Nephrol. 16, 1035-1050.
6. Ray, P. E., Liu, X. H. (2001) Pathogenesis of Shiga toxin-induced hemolytic uremic syndrome. Pediatr. Nephrol. 16, 823-839. (Pubitemid 32895613)
7. Paton, J. C., Paton, A. W. (1998) Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11, 450-479. (Pubitemid 28379095)
8. Endo, Y., Tsurugi, K., Yutsudo, T., Takeda, Y., Ogasawara, T., 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. (Pubitemid 18042873)
9. Brigotti, M., Carnicelli, D., Ravanelli, E., Vara, A. G., Martinelli, C., Alfieri, R. R., Petronini, P. G., 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. (Pubitemid 46744306)
10. Brigotti, M., Alfieri, R., Sestili, P., Bonelli, M., Petronini, P. G., Guidarelli, A., Barbieri, L., Stirpe, F., Sperti, S. (2002) Damage to nuclear DNA induced by Shiga toxin 1 and ricin in human endothelial cells. FASEB J. 16, 365-372. (Pubitemid 34195297)
11. Nakao, H., Takeda, T. (2000) Escherichia coli Shiga toxin. J. Nat. Toxins 9, 299-313.
12. Sestili, P., Alfieri, R., Carnicelli, D., Martinelli, C., Barbieri, L., Stirpe, F., Bonelli, M., Petronini, P. G., Brigotti, M. (2005) Shiga toxin 1 and ricin inhibit the repair of H2O2-induced DNA single strand breaks in cultured mammalian cells. DNA Repair (Amst.) 4, 271-277.
13. Matussek, A., Lauber, J., Bergau, A., Hansen, W., Rohde, M., Dittmar, K. E., Gunzer, M., Mengel, M., Gatzlaff, P., Hartmann, M., Buer, J., Gunzer, F. (2003) Molecular and functional analysis of Shiga toxin-induced response patterns in human vascular endothelial cells. Blood 102, 1323-1332. (Pubitemid 36988039)
14. Zoja, C., Angioletti, S., Donadelli, R., Zanchi, C., Tomasoni, S., Binda, E., Imberti, B., te Loo, M., Monnens, L., Remuzzi, G., Morigi, M. (2002) Shiga toxin-2 triggers endothelial leukocyte adhesion and transmigration via NF-κB dependent up-regulation of IL-8 and MCP-1. Kidney Int. 62, 846-856.
15. Caprioli, A., Luzzi, I., Rosmini, F., Pasquini, P., Cirrincione, R., Gianviti, A., Matteucci, M. C., Rizzoni, G. (1992) Hemolytic-uremic syndrome and Vero cytotoxin-producing Escherichia coli infection in Italy. The HUS Italian Study Group. J. Infect. Dis. 166, 154-158.
16. Te Loo, D. M., van Hinsbergh, V. W., van den Heuvel, L. P., 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.
17. 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., van Hinsbergh, V. W. (2000) Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome. Blood 95, 3396-3402. (Pubitemid 30428469)
18. Geelen, J. M., van der Velden, T. J., Te Loo, D. M., Boerman, O. C., van den Heuvel, L. P., 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 leukocytes. Nephrol. Dial. Transplant. 22, 749-755.
19. Flagler, M. J., Strasser, J. E., Chalk, C. L., 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.
20. Tazzari, P. L., Ricci, F., Carnicelli, D., Caprioli, A., Tozzi, A. E., Rizzoni, G., Conte, R., 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.
21. Brigotti, M., Caprioli, A., Tozzi, A. E., Tazzari, P. L., Ricci, F., Conte, R., Carnicelli, D., Procaccino, M. A., Minelli, F., Ferretti, A. V., Paglialonga, F., Edefonti, A., Rizzoni, G. (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.
22. Griener, T. P., Mulvey, G. L., Marcato, P., Armstrong, G. D. (2007) Differential binding of Shiga toxin 2 to human and murine neutrophils. J. Med. Microbiol. 56, 1423-1430. (Pubitemid 350175065)
23. Brigotti, M., Carnicelli, D., Ravanelli, E., Barbieri, S., Ricci, F., Bontadini, A., Tozzi, A. E., Scavia, G., Caprioli, A., Tazzari, P. L. (2008) Interactions between Shiga toxins and human polymorphonuclear leukocytes. J. Leukoc. Biol. 84, 1019-1027.
24. Fernandez, G. C., Gomez, S. A., Ramos, M. V., Bentancor, L. V., Fernandez-Brando, R. J., Landoni, V. I., Lopez, L., Ramirez, F., Diaz, M., Alduncin, M., Grimoldi, I., Exeni, R., Isturiz, M. A., Palermo, M. S. (2007) The functional state of neutrophils correlates with the severity of renal dysfunction in children with hemolytic uremic syndrome. Pediatr. Res. 61, 123-128.
25. Ryd, M., Alfredsson, H., Blomberg, L., Andersson, A., 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. (Pubitemid 20001079)
26. Maier, J. A., Voulalas, P., Roeder, D., Maciag, T. (1990) Extension of the life-span of human endothelial cells by an interleukin-1 α antisense oligomer. Science 249, 1570-1574.
27. Petronini, P. G., Tramacere, M., Mazzini, A., Piedimonte, G., Silvotti, L., Borghetti, A. F. (1987) Hyperosmolarity-induced stress proteins in chick embryo fibroblasts. Exp. Cell Res. 172, 450-462. (Pubitemid 18025347)
28. Cassatella, M. A., Cappelli, R., Della Bianca, V., Grzeskowiak, M., Dusi, S., Berton, G. (1988) Interferon-γ activates human neutrophil oxygen metabolism and exocytosis. Immunology 63, 499-506.
29. Van Setten, P. A., Monnens, L. A., Verstraten, R. G., van den Heuvel, L. P., 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.
30. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72, 248-254.
31. Borregaard, N., Sorensen, O. E., Theilgaard-Monch, K. (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 28, 340-345. (Pubitemid 47077924)
32. Soehnlein, O., Weber, C., Lindbom, L. (2009) Neutrophil granule proteins tune monocytic cell function. Trends Immunol. 30, 538-546.
33. Soehnlein, O., Zernecke, A., Weber, C. (2009) Neutrophils launch monocyte extravasation by release of granule proteins. Thromb. Haemost. 102, 198-205.
34. Brigotti, M., Carnicelli, D., Ravanelli, E., Vara, A. G., Martinelli, C., Alfieri, R. R., Petronini, P. G., 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. (Pubitemid 46744306)
35. Morigi, M., Galbusera, M., Binda, E., Imberti, B., Gastoldi, S., Remuzzi, A., Zoja, C., Remuzzi, G. (2001) Verotoxin-1-induced up-regulation of adhesive molecules renders microvascular endothelial cells thrombogenic at high shear stress. Blood 98, 1828-1835.
36. Iordanov, M. S., Pribnow, D., Magun, J. L., Dinh, T. H., Pearson, J. A., Chen, S. L., Magun, B. E. (1997) Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the α-sarcin/ricin loop in the 28S rRNA. Mol. Cell. Biol. 17, 3373-3381. (Pubitemid 27215052)
37. Smith, W. E., Kane, A. V., Campbell, S. T., Acheson, D. W., Cochran, B. H., Thorpe, C. M. (2003) Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infect. Immun. 71, 1497-1504.
38. Fernandez, G. C., Gomez, S. A., Rubel, C. J., Bentancor, L. V., Barrionuevo, P., Alduncin, M., Grimoldi, I., Exeni, R., Isturiz, M. A., Palermo, M. S. (2005) Impaired neutrophils in children with the typical form of hemolytic uremic syndrome. Pediatr. Nephrol. 20, 1306-1314.
39. Marcato, P., Vander Helm, K., Mulvey, G. L., Armstrong, G. D. (2003) Serum amyloid P component binding to Shiga toxin 2 requires both a subunit and B pentamer. Infect. Immun. 71, 6075-6078. (Pubitemid 37205665)
40. Taylor Jr., F. B., Tesh, V. L., DeBault, L., Li, A., Chang, A. C., Kosanke, S. D., Pysher, T. J., Siegler, R. L. (1999) Characterization of the baboon responses to Shiga-like toxin: descriptive study of a new primate model of toxic responses to Stx-1. Am. J. Pathol. 154, 1285-1299.