C-terminal repeats of Clostridium difficile toxin a induce production of chemokine and adhesion molecules in endothelial cells and promote migration of leukocytes

Infection and Immunity

Volumn 76, Issue 3, 2008, Pages 1170-1178

  Yeh, Chiou Yueh ^a   Lin, Chun Nan ^b   Chang, Chuan Fa ^b   Lin, Chun Hung ^b   Lien, Huei Ting ^a   Chen, Jen Yang ^c   Chia, Jean San ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b GENOMICS RESEARCH CENTER   (Taiwan)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CALCIUM; CARBOHYDRATE; CELL ADHESION MOLECULE; CHEMOKINE; CLOSTRIDIUM DIFFICILE TOXIN A; GLUCOSYLTRANSFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; LEWIS Y ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; OLIGOSACCHARIDE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; BACTERIAL TOXIN; ENTEROTOXIN; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE;

ANTIGEN EXPRESSION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INTESTINE CELL; LEUKOCYTE MIGRATION; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; BIOSYNTHESIS; BLOOD GROUP LEWIS SYSTEM; CELL LINE; EPITHELIUM CELL; GENETICS; IMMUNOLOGY; LEUKOCYTE; LEUKOCYTE MIGRATION INHIBITION TEST; METABOLISM; NEUTROPHIL CHEMOTAXIS; PROTEIN BINDING;

BACTERIAL TOXINS; CELL LINE; CELL MIGRATION ASSAYS, LEUKOCYTE; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; CLOSTRIDIUM DIFFICILE; ENDOTHELIAL CELLS; ENTEROTOXINS; EPITHELIAL CELLS; HUMANS; LEUKOCYTES; LEWIS BLOOD-GROUP SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PROTEIN BINDING; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID;

EID: 40749124456     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01340-07     Document Type: Article

References (50)

1. Alston, W. K., D. A. Elliott, M. E. Epstein, V. B. Hatcher, M. Tang, and F. D. Lowy. 1997. Extracellular matrix heparan sulfate modulates endothelial cell susceptibility to Staphylococcus aureus. J. Cell. Physiol. 173:102-109.
2. Andrade, M. A., C. Perez-Iratxeta, and C. P. Ponting. 2001. Protein repeats: structures, functions, and evolution. J. Struct. Biol. 134:117-131.
3. Behling-Kelly, E., H. Vonderheid, K. S. Kim, L. B. Corbeil, and C. J. Czuprynski. 2006. Roles of cellular activation and sulfated glycans in Haemophilus somnus adherence to bovine brain microvascular endothelial cells. Infect. Immun. 74:5311-5318.
4. Castagliuolo, I., M. Sardina, P. Brun, C. DeRos, C. Mastrotto, L. Lovato, and G. Palu. 2004. Clostridium difficile toxin A carboxyl-terminus peptide lacking ADP-ribosyltransferase activity acts as a mucosal adjuvant. Infect. Immun. 72:2827-2836.
5. Demarest, S. J., J. Salbato, M. Elia, J. Zhong, T. Morrow, T. Holland, K. Kline, G. Woodnutt, B. E. Kimmel, and G. Hansen. 2005. Structural characterization of the cell wall binding domains of Clostridium difficile toxins A and B; evidence that Ca2+ plays a role in toxin A cell surface association. J. Mol. Biol. 346:1197-1206.
6. Faust, C., B. Ye, and K. P. Song. 1998. The enzymatic domain of Clostridium difficile toxin A is located within its N-terminal region. Biochem. Biophys. Res. Commun. 251:100-105.
7. Flegel, W. A., F. Muller, W. Daubener, H. G. Fischer, U. Hadding, and H. Northoff. 1991. Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect. Immun. 59:3659-3666.
8. Frisch, C., R. Gerhard, K. Aktories, F. Hofmann, and I. Just. 2003. The complete receptor-binding domain of Clostridium difficile toxin A is required for endocytosis. Biochem. Biophys. Res. Commun. 300:706-711.
9. Gaugler, M. H., V. Vereycken-Holler, C. Squiban, and J. Aigueperse. 2004. PECAM-1 (CD31) is required for interactions of platelets with endothelial cells after irradiation. J. Thromb. Haemost. 2:2020-2026.
10. Grafe, M., G. Steinheider, U. Desaga, C. Warnecke, H. B. Lehmkuhl, V. Regitz-Zagrosek, A. G. Hildebrandt, and E. Fleck. 1999. Characterization of two distinct mechanisms for induction of apoptosis in human vascular endothelial cells. Clin. Chem. Lab. Med. 37:505-510.
11. Greco, A., J. G. Ho, S. J. Lin, M. M. Palcic, M. Rupnik, and K. K. Ng. 2006. Carbohydrate recognition by Clostridium difficile toxin A. Nat. Struct. Mol. Biol. 13:460-461.
12. Heidemann, J., W. Domschke, T. Kucharzik, and C. Maaser. 2006. Intestinal microvascular endothelium and innate immunity in inflammatory bowel disease: a second line of defense? Infect. Immun. 74:5425-5432.
13. Ho, J. G., A. Greco, M. Rupnik, and K. K. Ng. 2005. Crystal structure of receptor-binding C-terminal repeats from Clostridium difficile toxin A. Proc. Natl. Acad. Sci. USA 102:18373-18378.
14. Hofmann, F., C. Busch, U. Prepens, I. Just, and K. Aktories. 1997. Localization of the glucosyltransferase activity of Clostridium difficile toxin B to the N-terminal part of the holotoxin. J. Biol. Chem. 272:11074-11078.
15. Jaffe, E. A., R. L. Nachman, C. G. Becker, and C. R. Minick. 1973. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J. Clin. Investig. 52:2745-2756.
16. Jefferson, K. K., M. F. Smith, Jr., and D. A. Bobak. 1999. Roles of intracellular calcium and NF-kappa B in the Clostridium difficile toxin A-induced up-regulation and secretion of IL-8 from human monocytes. J. Immunol. 163:5183-5191.
17. Johnson, S., and D. N. Gerding. 1998. Clostridium difficile-associated diarrhea. Clin. Infect. Dis. 26:1027-1034.
18. Just, I., and R. Gerhard. 2004. Large clostridial cytotoxins. Rev. Physiol. Biochem. Pharmacol. 152:23-47.
19. Kim, J. M., J. Y. Lee, Y. M. Yoon, Y. K. Oh, J. Youn, and Y. J. Kim. 2006. NF-kappa B activation pathway is essential for the chemokine expression in intestinal epithelial cells stimulated with Clostridium difficile toxin A. Scand. J. Immunol. 63:453-460.
20. Krishnaswamy, G., J. Kelley, L. Yerra, J. K. Smith, and D. S. Chi. 1999. Human endothelium as a source of multifunctional cytokines: molecular regulation and possible role in human disease. J. Interferon Cytokine Res. 19:91-104.
21. Krivan, H. C., G. F. Clark, D. F. Smith, and T. D. Wilkins. 1986. Cell surface binding site for Clostridium difficile enterotoxin: evidence for a glycoconjugate containing the sequence Galα1-3Galβ1-4GlcNAc. Infect. Immun. 53: 573-581.
22. Kurose, I., C. Pothoulakis, J. T. LaMont, D. C. Anderson, J. C. Paulson, M. Miyasaka, R. Wolf, and D. N. Granger. 1994. Clostridium difficile toxin A-induced microvascular dysfunction. Role of histamine. I. Clin. Investig. 94:1919-1926.
23. Lima, A. A., D. M. Lyerly, T. D. Wilkins, D. J. Innes, and R. L. Guerrant. 1988. Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro. Infect. Immun. 56:582-588.
24. Linevsky, J. K., C. Pothoulakis, S. Keates, M. Warny, A. C. Keates, J. T. LaMont, and C. P. Kelly. 1997. IL-8 release and neutrophil activation by Clostridium difficile toxin-exposed human monocytes. Am. J. Physiol. 273: G1333-G1340.
25. Lyerly, D. M., H. C. Krivan, and T. D. Wilkins. 1988. Clostridium difficile: its disease and toxins. Clin. Microbiol. Rev. 1:1-18.
26. Lyerly, D. M., J. L. Johnson, S. M. Frey, and T. D. Wilkins. 1990. Vaccination against lethal Clostridium difficile enterocolitis with a nontoxic recombinant peptide of toxin A. Curr. Microbiol. 21:29-32.
27. Main, E. R., S. E. Jackson, and L. Regan. 2003. The folding and design of repeat proteins: reaching a consensus. Curr. Opin. Struct. Biol. 13:482-489.
28. Muller, W. A. 2003. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24:327-334.
29. Munoz, C., D. Pascual-Salcedo, M. C. Castellanos, A. Alfranca, J. Aragones, A. Vara, J. M. Redondo, and M. O. de Landazuri. 1996. Pyrrolidine dithiocarbamate inhibits the production of interleukin-6, interleukin-8, and granulocyte-macrophage colony-stimulating factor by human endothelial cells in response to inflammatory mediators: modulation of NF-kappa B and AP-1 transcription factors activity. Blood 88:3482-3490.
30. Namavar, F., M. Sparrius, E. C. Veerman, B. J. Appelmelk, and C. M. Vandenbroucke-Grauls. 1998. Neutrophil-activating protein mediates adhesion of Helicobacter pylori to sulfated carbohydrates on high-molecular-weight salivary mucin. Infect. Immun. 66:444-447.
31. Pavliakova, D., J. S. Moncrief, D. M. Lyerly, G. Schiffman, D. A. Bryla, J. B. Robbins, and R. Schneerson. 2000. Clostridium difficile recombinant toxin A repeating units as a carrier protein for conjugate vaccines: studies of pneumococcal type 14, Escherichia coli K1, and Shigella flexneri type 2a polysaccharides in mice. Infect. Immun. 68:2161-2166.
32. Perrier, C., N. Sprenger, and B. Corthesy. 2006. Glycans on secretory component participate in innate protection against mucosal pathogens. J. Biol. Chem. 281:14280-14287.
33. Pothoulakis, C., R. J. Gilbert, C. Cladaras, I. Castagliuolo, G. Semenza, Y. Hitti, J. S. Montcrief, J. Linevsky, C. P. Kelly, S. Nikulasson, H. P. Desai, T. D. Wilkins, and J. T. LaMont. 1996. Rabbit sucrase-isomaltase contains a functional intestinal receptor for Clostridium difficile toxin A. I. Clin. Investig. 98:641-649.
34. Price, S. B., C. J. Phelps, T. D. Wilkins, and J. L. Johnson. 1987. Cloning of the carbohydrate-binding portion of the toxin A gene of Clostridium difficile. Curr. Microbiol. 16:55-60.
35. Rupnik, M., S. Pabst, M. Rupnik, C. von Eichel-Streiber, H. Urlaub, and H. D. Soling. 2005. Characterization of the cleavage site and function of resulting cleavage fragments after limited proteolysis of Clostridium difficile toxin B (TcdB) by host cells. Microbiology 151:199-208.
36. Sauerborn, M., P. Leukel, and C. von Eichel-Streiber. 1997. The C-terminal ligand-binding domain of Clostridium difficile toxin A (TcdA) abrogates TcdA-specific binding to cells and prevents mouse lethality. FEMS Microbiol. Lett. 155:45-54.
37. Teneberg, S., I. Lonnroth, J. F. Torres Lopez, U. Galili, M. O. Halvarsson, J. Angstrom, and K. A. Karlsson. 1996. Molecular mimicry in the recognition of glycosphingolipids by Gal alpha 3 Gal beta 4 GlcNAc beta-binding Clostridium difficile toxin A, human natural anti alpha-galactosyl IgG and the monoclonal antibody Gal-13: characterization of a binding-active human glycosphingolipid, non-identical with the animal receptor. Glycobiology 6:599-609.
38. Thelestam, M., and E. Chaves-Olarte. 2000. Cytotoxic effects of the Clostridium difficile toxins. Curr. Top. Microbiol. Immunol. 250:85-96.
39. Tucker, K. D., and T. D. Wilkins. 1991. Toxin A of Clostridium difficile binds to the human carbohydrate antigens I, X, and Y. Infect. Immun. 59:73-78.
40. Veerman, E. C., C. M. Bank, F. Namavar, B. J. Appelmelk, J. G. Bolscher, and A. V. Nieuw Amerongen. 1997. Sulfated glycans on oral mucin as receptors for Helicobacter pylori. Glycobiology 7:737-743.
41. von Eichel-Streiber, C., P. Boquet, M. Sauerborn, and M. Thelestam. 1996. Large clostridial cytotoxins - a family of glycosyltransferases modifying small GTP-binding proteins. Trends Microbiol. 4:375-382.
42. von Eichel-Streiber, C., R. Laufenberg-Feldmann, S. Sartingen, J. Schulze, and M. Sauerborn. 1992. Comparative sequence analysis of the Clostridium difficile toxins A and B. Mol. Gen. Genet. 233:260-268.
43. von Eichel-Streiber, C., and M. Sauerborn. 1990. Clostridium difficile toxin A carries a C-terminal repetitive structure homologous to the carbohydrate binding region of streptococcal glycosyltransferases. Gene 96:107-113.
44. von Eichel-Streiber, C., M. Sauerborn, and H. K. Kuramitsu. 1992. Evidence for a modular structure of the homologous repetitive C-terminal carbohydrate-binding sites of Clostridium difficile toxins and Streptococcus mutans glucosyltransferases. J. Bacteriol. 174:6707-6710.
45. Voth, D. E., and J. D. Ballard. 2005. Clostridium difficile toxins: mechanism of action and role in disease. Clin. Microbiol. Rev. 18:247-263.
46. Ward, S. J., G. Douce, G. Dougan, and B. Wren. 1997. Delivery of non-toxic fragments of Clostridium difficile toxin A to the mucosal immune system. Rev. Med. Microbiol. 8:S34-S36.
47. Ward, S. J., G. Douce, G. Dougan, and B. W. Wren. 1999. Local and systemic neutralizing antibody responses induced by intranasal immunization with the nontoxic binding domain of toxin A from Clostridium difficile. Infect. Immun. 67:5124-5132.
48. Wren, B. W. 1991. A family of clostridial and streptococcal ligand-binding proteins with conserved C-terminal repeat sequences. Mol. Microbiol. 5:797-803.
49. Wren, B. W., R. R. Russell, and S. Tabaqchali. 1991. Antigenic cross-reactivity and functional inhibition by antibodies to Clostridium difficile toxin A, Streptococcus mutans glucan-binding protein, and a synthetic peptide. Infect. Immun. 59:3151-3155.
50. Yeh, C. Y., J. Y. Chen, and J. S. Chia. 2006. Glucosyltransferases of viridans group streptococci modulate interleukin-6 and adhesion molecule expression in endothelial cells and augment monocytic cell adherence. Infect. Immun. 74:1273-1283.