Role of the haem oxygenase/carbon monoxide pathway in Clostridium difficile toxin A-induced enteritis in mice

Journal of Medical Microbiology

Volumn 60, Issue 8, 2011, Pages 1146-1154

  Medeiros, C A ^a,b   Warren, C A ^c   Freire, R ^c   Vieira, C A ^b   Lima, B B ^b   Vale, M L ^b   Ribeiro, R A ^b   Souza, M H ^b   Brito, G A ^b  

^a DEPARTAMENTO DE FÍSICA   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CARBONYL DERIVATIVE; CLOSTRIDIUM DIFFICILE TOXIN A; DIMANGANESE DECACARBONYL; HEME OXYGENASE 1; INTERLEUKIN 1BETA; MYELOPEROXIDASE; PROTOPORPHYRIN ZINC; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EDEMA; ENTERITIS; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME SYNTHESIS; HISTOPATHOLOGY; ILEUM; IMMUNOHISTOCHEMISTRY; INTESTINE EDEMA; INTESTINE INJURY; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIAL TOXINS; CARBON MONOXIDE; DEOXYURIDINE; ENTERITIS; ENTEROTOXINS; HEME OXYGENASE (DECYCLIZING); HEMIN; ILEUM; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; PROTOPORPHYRINS;

EID: 79960405072     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.028910-0     Document Type: Article

References (43)

1. Abraham, N. G., Lin, J. H., Schwartzman, M. L., Levere, R. D. & Shibahara, S. (1988). The physiological significance of heme oxygenase. Int J Biochem 20, 543-558.
2. Bradley, P. P., Christensen, R. D. & Rothstein, G. (1982). Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood 60, 618-622.
3. Brito, G. A., Fujji, J., Carneiro-Filho, B. A., Lima, A. A., Obrig, T. & Guerrant, R. L. (2002a). Mechanism of Clostridium difficile toxin Ainduced apoptosis in T84 cells. J Infect Dis 186, 1438-1447.
4. Brito, G. A., Sullivan, G. W., Ciesla, W. P., Jr, Carper, H. T., Mandell, G. L. & Guerrant, R. L. (2002b). Clostridium difficile toxin A alters in vitro-adherent neutrophil morphology and function. J Infect Dis 185, 1297-1306.
5. Castagliuolo, I., Riegler, M., Pasha, A., Nikulasson, S., Lu, B., Gerard, C., Gerard, N. P. & Pothoulakis, C. (1998). Neurokinin-1 (NK-1) receptor is required in Clostridiumdifficile-induced enteritis. J Clin Invest 101, 1547-1550.
6. Cavalcante, I. C., Castro, M. V., Barreto, A. R., Sullivan, G. W., Vale, M., Almeida, P. R., Linden, J., Rieger, J. M., Cunha, F. Q. &other authors (2006). Effect of novel A2A adenosine receptor agonist ATL 313 on Clostridium difficile toxin A-induced murine ileal enteritis. Infect Immun 74, 2606-2612.
7. Dal Secco, D., Paron, J. A., de Oliveira, S. H., Ferreira, S. H., Silva, J. S. & Cunha, F. de Q. (2003). Neutrophil migration in inflammation: nitric oxide inhibits rolling, adhesion and induces apoptosis. Nitric Oxide 9, 153-164.
8. Dearden, D. V., Hayashibara, K., Beauchamp, J. L., Kirchner, N. J., van Koppen, P. A. M. & Bowers, M. T. (1989). Fundamental studies of the energetics and dynamics of ligand dissociation and exchange processes at transition-metal centers in the gas phase: Mn(CO)x+, x51-6. J Am Chem Soc 111, 2401-2409.
9. Flegel, W. A., Müller, F., Däubener, W., Fischer, H. G., Hadding, U. & Northoff, H. (1991). Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect Immun 59, 3659-3666.
10. Freitas, A., Alves-Filho, J. C., Secco, D. D., Neto, A. F., Ferreira, S. H., Barja-Fidalgo, C. & Cunha, F. Q. (2006). Heme oxygenase/carbon monoxide-biliverdin pathway down regulates neutrophil rolling, adhesion and migration in acute inflammation. Br J Pharmacol 149, 345-354.
11. Gomes, A. S., Gadelha, G. G., Lima, S. J., Garcia, J. A., Medeiros, J. V., Havt, A., Lima, A. A., Ribeiro, R. A., Brito, G. A. & other authors (2010). Gastroprotective effect of heme-oxygenase 1/biliverdin/CO pathway in ethanol-induced gastric damage in mice. Eur J Pharmacol 642, 140-145.
12. Hayashi, S., Takamiya, R., Yamaguchi, T., Matsumoto, K., Tojo, S. J., Tamatani, T., Kitajima, M., Makino, N., Ishimura, Y. & Suematsu, M. (1999). Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme. Circ Res 85, 663-671.
13. Hegazi, R. A., Rao, K. N., Mayle, A., Sepulveda, A. R., Otterbein, L. E. & Plevy, S. E. (2005). Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med 202, 1703-1713.
14. Inui, M., Ishida, Y., Kimura, A., Kuninaka, Y., Mukaida, N. & Kondo, T. (2011). Protective roles of CX3CR1-mediated signals in toxin Ainduced enteritis through the induction of heme oxygenase-1 expression. J Immunol 186, 423-431.
15. Johnson, T. R., Mann, B. E., Clark, J. E., Foresti, R., Green, C. J. & Motterlini, R. (2003). Metal carbonyls: a new class of pharmaceuticals? Angew Chem Int Ed Engl 42, 3722-3729.
16. Jun, C. D., Kim, Y., Choi, E. Y., Kim, M., Park, B., Youn, B., Yu, K., Choi, K. S., Yoon, K. H. &other authors (2006). Gliotoxin reduces the severity of trinitrobenzene sulfonic acid-induced colitis in mice: evidence of the connection between heme oxygenase-1 and the nuclear factor-kappaB pathway in vitro and in vivo. Inflamm Bowel Dis 12, 619-629.
17. Kelly, C. P. & LaMont, J. T. (1998). Clostridium difficile infection. Annu Rev Med 49, 375-390.
18. Kelly, C. P., Becker, S., Linevsky, J. K., Joshi, M. A., O'Keane, J. C., Dickey, B. F., LaMont, J. T. & Pothoulakis, C. (1994a). Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit. J Clin Invest 93, 1257-1265.
19. Kelly, C. P., Becker, S., Linevsky, J. K., Joshi, M. A., O'Keane, J. C., Dickey, B. F., LaMont, J. T. & Pothoulakis, C. (1994b). Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit. J Clin Invest 93, 1257-1265.
20. Kirkwood, K. S., Bunnett, N. W., Maa, J., Castagliolo, I., Liu, B., Gerard, N., Zacks, J., Pothoulakis, C. & Grady, E. F. (2001). Deletion of neutral endopeptidase exacerbates intestinal inflammation induced by Clostridium difficile toxin A. Am J Physiol Gastrointest Liver Physiol 281, G544-G551.
21. Kuehne, S. A., Cartman, S. T., Heap, J. T., Kelly, M. L., Cockayne, A. & Minton, N. P. (2010). The role of toxin A and toxin B in Clostridium difficile infection. Nature 467, 711-713.
22. Lyras, D., O'Connor, J. R., Howarth, P. M., Sambol, S. P., Carter, G. P., Phumoonna, T., Poon, R., Adams, V., Vedantam, G. &other authors (2009). Toxin B is essential for virulence of Clostridium difficile. Nature 458, 1176-1179.
23. Maines, M. D., Trakshel, G. M. & Kutty, R. K. (1986). Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 261, 411-419.
24. McCoubrey, W. K., Jr, Huang, T. J. & Maines, M. D. (1997). Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247, 725-732.
25. Morse, D., Pischke, S. E., Zhou, Z., Davis, R. J., Flavell, R. A., Loop, T., Otterbein, S. L., Otterbein, L. E. & Choi, A. M. (2003). Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem 278, 36993-36998.
26. Otterbein, L. E. & Choi, A. M. (2000). Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 279, L1029-L1037.
27. Otterbein, L. E., Bach, F. H., Alam, J., Soares, M., Tao Lu, H., Wysk, M., Davis, R. J., Flavell, R. A. & Choi, A. M. (2000). Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6, 422-428.
28. Paine, A., Eiz-Vesper, B., Blasczyk, R. & Immenschuh, S. (2010). Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 80, 1895-1903.
29. Paul, G., Bataille, F., Obermeier, F., Bock, J., Klebl, F., Strauch, U., Lochbaum, D., Rümmele, P., Farkas, S. & other authors (2005). Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin Exp Immunol 140, 547-555.
30. Pothoulakis, C. & LaMont, J. T. (2001). Microbes and microbial toxins: paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am J Physiol Gastrointest Liver Physiol 280, G178-G183.
31. Pothoulakis, C., Barone, L. M., Ely, R., Faris, B., Clark, M. E., Franzblau, C. & LaMont, J. T. (1986). Purification and properties of Clostridium difficile cytotoxin B. J Biol Chem 261, 1316-1321.
32. Pothoulakis, C., Castagliuolo, I. & LaMont, J. T. (1998). Nerves and intestinal mast cells modulate responses to enterotoxins. News Physiol Sci 13, 58-63.
33. Safieh-Garabedian, B., Poole, S., Allchorne, A., Winter, J. & Woolf, C. J. (1995). Contribution of interleukin-1 beta to the inflammationinduced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol 115, 1265-1275.
34. Siow, R. C., Sato, H. & Mann, G. E. (1999). Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide? Cardiovasc Res 41, 385-394.
35. Soares, M. P., Seldon, M. P., Gregoire, I. P., Vassilevskaia, T., Berberat, P. O., Yu, J., Tsui, T. Y. & Bach, F. H. (2004). Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol 172, 3553-3563.
36. Suematsu, M., Wakabayashi, Y. & Ishimura, Y. (1996). Gaseous monoxides: a new class of microvascular regulator in the liver. Cardiovasc Res 32, 679-686.
37. Vachharajani, T. J., Work, J., Issekutz, A. C. & Granger, D. N. (2000). Heme oxygenase modulates selectin expression in different regional vascular beds. Am J Physiol Heart Circ Physiol 278, H1613-H1617.
38. Varga, C., Laszlo, F., Fritz, P., Cavicchi, M., Lamarque, D., Horvath, K., Posa, A., Berko, A. & Whittle, B. J. (2007). Modulation by heme and zinc protoporphyrin of colonic heme oxygenase-1 and experimental inflammatory bowel disease in the rat. Eur J Pharmacol 561, 164-171.
39. Vicente, A. M., Guillén, M. I., Habib, A. & Alcaraz, M. J. (2003). Beneficial effects of heme oxygenase-1 up-regulation in the development of experimental inflammation induced by zymosan. J Pharmacol Exp Ther 307, 1030-1037.
40. Vijayan, V., Mueller, S., Baumgart-Vogt, E. & Immenschuh, S.(2010). Heme oxygenase-1 as a therapeutic target in inflammatory disorders of the gastrointestinal tract. World J Gastroenterol 16, 3112-3119.
41. Wagener, F. A., van Beurden, H. E., von den Hoff, J. W., Adema, G. J. & Figdor, C. G. (2003). The heme-heme oxygenase system: a molecular switch in wound healing. Blood 102, 521-528.
42. Wang, W. P., Guo, X., Koo, M. W., Wong, B. C., Lam, S. K., Ye, Y. N. & Cho, C. H. (2001). Protective role of heme oxygenase-1 on trinitrobenzene sulfonic acid-induced colitis in rats. Am J Physiol Gastrointest Liver Physiol 281, G586-G594.
43. Willis, D., Moore, A. R., Frederick, R. & Willoughby, D. A. (1996). Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 2, 87-90.