Epithelial cell IκB-kinase β has an important protective role in Clostridium difficile toxin A-induced mucosal injury

Journal of Immunology

Volumn 177, Issue 2, 2006, Pages 1214-1220

  Chae, Sungwon ^a   Eckmann, Lars ^a   Miyamoto, Yukiko ^a   Pothoulakis, Charalabos ^b   Karin, Michael ^c   Kagnoff, Martin F ^a,c,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN A; I KAPPA B KINASE; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTECTIVE AGENT; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL TRANSLOCATION; CELL ACTIVATION; CELL SURVIVAL; CLOSTRIDIUM DIFFICILE; COLITIS; CONTROLLED STUDY; DIARRHEA; ENZYME ACTIVATION; ENZYME SUBUNIT; EPITHELIUM CELL; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOST RESISTANCE; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE LOOP; MOUSE; MOUSE MUTANT; MUCOSA INFLAMMATION; MUCOSAL DISEASE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PSEUDOMEMBRANOUS COLITIS;

EID: 33745853832     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.2.1214     Document Type: Article

References (44)

1. Lyerly, D. M., H. C. Krivan, and T. D. Wilkins. 1988. Clostridium difficile: its disease and toxins. Clin. Microbiol. Rev. 1: 1-18.
2. Kelly, C. P., and J. T. LaMont. 1998. Clostridium difficile infection. Annu. Rev. Med. 49: 375-390.
3. Pothoulakis, C., and J. T. Lamont. 2001. Microbes and microbial toxins: paradigms for microbial-mucosal interactions. II. The integrated response of the intestine to Clostridium difficile toxins. Am. J. Physiol. 280: G178-G183.
4. Just, I., J. Selzer, C. von Eichel-Streiber, and K. Aktories. 1995. The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile. J. Clin. Invest. 95: 1026-1031.
5. Just, I., J. Selzer, M. Wilm, C. von Eichel-Streiber, M. Mann, and K. Aktories. 1995. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375: 500-503.
6. Hecht, G., C. Pothoulakis, J. T. LaMont, and J. L. Madara. 1988. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J. Clin. Invest. 82: 1516-1524.
7. Castagliuolo, I., A. C. Keates, C. C. Wang, A. Pasha, L. Valenick, C. P. Kelly, S. T. Nikulasson, J. T. LaMont, and C. Pothoulakis. 1998. Clostridium difficile toxin A stimulates macrophage-inflammatory protein-2 production in rat intestinal epithelial cells. J. Immunol. 160: 6039-6045.
8. Jefferson, K. K., M. F. Smith, Jr., and D. A. Bobak. 1999. Roles of intracellular calcium and NF-κB in the Clostridium difficile toxin A-induced up-regulation and secretion of IL-8 from human monocytes. J. Immunol. 163: 5183-5191.
9. Mitchell, T. J., J. M. Ketley, S. C. Haslam, J. Stephen, D. W. Burdon, D. C. Candy, and R. Daniel. 1986. Effect of toxin A and B of Clostridium difficile on rabbit ileum and colon. Gut 27: 78-85.
10. Triadafilopoulos, G., C. Pothoulakis, M. J. O'Brien, and J. T. LaMont. 1987. Differential effects of Clostridium difficile toxins A and B on rabbit ileum. Gastroenterology 93: 273-279.
11. Alfa, M. J., A. Kabani, D. Lyerly, S. Moncrief, L. M. Neville, A. Al-Barrak, G. K. Harding, B. Dyck, K. Olekson, and J. M. Embil. 2000. Characterization of a toxin A-negative, toxin B-positive strain of Clostridium difficile responsible for a nosocomial outbreak of Clostridium difficile-associated diarrhea. J. Clin. Microbiol. 38: 2706-2714.
12. + strain of Clostridium difficile. J. Clin. Microbiol. 38: 1696-1697.
13. Savidge, T. C., W. H. Pan, P. Newman, M. O'Brien, P. M. Anton, and C. Pothoulakis. 2003. Clostridium difficile toxin B is an inflammatory enterotoxin in human intestine. Gastroenterology 125: 413-420.
14. Triadafilopoulos, G., C. Pothoulakis, R. Weiss, C. Giampaolo, and J. T. Lamont. 1989. Comparative study of Clostridium difficile toxin A and cholera toxin in rabbit ileum. Gastroenterology 97: 1186-1192.
15. Branka, J. E., G. Vallette, A. Jarry, C. Bou-Hanna, P. Lemarre, P. N. Van, and C. L. Laboisse. 1997. Early functional effects of Clostridium difficile toxin A on human colonocytes. Gastroenterology 112: 1887-1894.
16. Castagliuolo, I., A. C. Keates, B. Qiu, C. P. Kelly, S. Nikulasson, S. E. Leeman, and C. Pothoulakis. 1997. Increased substance P responses in dorsal root ganglia and intestinal macrophages during Clostridium difficile toxin A enteritis in rats. Proc. Natl. Acad. Sci. USA 94: 4788-4793.
17. Castagliuolo, I., M. Riegler, A. Pasha, S. Nikulasson, B. Lu, C. Gerard, N. P. Gerard, and C. Pothoulakis. 1998. Neurokinin-1 (NK-1) receptor is required in Clostridium difficile-induced enteritis. J. Clin. Invest. 101: 1547-1550.
18. Morteau, O., I. Castagliuolo, A. Mykoniatis, J. Zacks, M. Wlk, B. Lu, C. Pothoulakis, N. P. Gerard, and C. Gerard. 2002. Genetic deficiency in the chemokine receptor CCR1 protects against acute Clostridium difficile toxin A enteritis in mice. Gastroenterology 122: 725-733.
19. Ishida, Y., T. Maegawa, T. Kondo, A. Kimura, Y. Iwakura, S. Nakamura, and N. Mukaida. 2004. Essential involvement of IFN-γ in Clostridium difficile toxin A-induced enteritis. J. Immunol. 172: 3018-3025.
20. Mahida, Y. R., S. Makh, S. Hyde, T. Gray, and S. P. Borriello. 1996. Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment. Gut 38: 337-347.
21. Brito, G. A., J. Fujji, B. A. Carneiro-Filho, A. A. Lima, T. Obrig, and R. L. Guerrant. 2002. Mechanism of Clostridium difficile toxin A-induced apoptosis in T84 cells. J. Infect. Dis. 186: 1438-1447.
22. Karin, M., and A. Lin. 2002. NF-κB at the crossroads of life and death. Nat. Immunol. 3: 221-227.
23. Chen, L. W., L. Egan, Z. W. Li, F. R. Greten, M. F. Kagnoff, and M. Karin. 2003. The two faces of IKK and NF-κB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat. Med. 9: 575-581.
24. Maeda, S., L. Chang, Z. W. Li, J. L. Luo, H. Leffert, and M. Karin. 2003. IKKβ is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFα. Immunity 19: 725-737.
25. Egan, L. J., L. Eckmann, F. R. Greten, S. Chae, Z. W. Li, G. M. Myhre, S. Robine, M. Karin, and M. F. Kagnoff. 2004. IκB-kinaseβ-dependent NF-κB activation provides radioprotection to the intestinal epithelium. Proc. Natl. Acad. Sci. USA 101: 2452-2457.
26. Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109: S81-96.
27. Li, Q., D. Van Antwerp, F. Mercurio, K. F. Lee, and I. M. Verma. 1999. Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science 284: 321-325.
28. Li, Z. W., W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189: 1839-1845.
29. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18: 621-663.
30. He, D., S. Sougioultzis, S. Hagen, J. Liu, S. Keates, A. C. Keates, C. Pothoulakis, and J. T. Lamont. 2002. Clostridium difficile toxin A triggers human colonocyte IL-8 release via mitochondrial oxygen radical generation. Gastroenterology 122: 1048-1057.
31. Keates, A. C., I. Castagliuolo, B. Qiu, S. Nikulasson, A. Sengupta, and C. Pothoulakis. 1998. CGRP up-regulation in dorsal root ganglia and ileal mucosa during Clostridium difficile toxin A-induced enteritis. Am. J. Physiol. 274: G196-G202.
32. Pothoulakis, C., J. T. LaMont, R. Eglow, N. Gao, J. B. Rubins, T. C. Theoharides, and B. F. Dickey. 1991. Characterization of rabbit ileal receptors for Clostridium difficile toxin A: evidence for a receptor-coupled G protein. J. Clin. Invest. 88: 119-125.
33. Greten, F. R., L. Eckmann, T. F. Greten, J. M. Park, Z. W. Li, L. J. Egan, M. F. Kagnoff, and M. Karin. 2004. IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118: 285-296.
34. Morris, G. P., P. L. Beck, M. S. Herridge, W. T. Depew, M. R. Szewczuk, and J. L. Wallace. 1989. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96: 795-803.
35. Hase, K., L. Eckmann, J. D. Leopard, N. Varki, and M. F. Kagnoff. 2002. Cell differentiation is a key determinant of cathelicidin LL-37/human cationic antimicrobial protein 18 expression by human colon epithelium. Infect. Immun. 70: 953-963.
36. Berin, M. C., M. B. Dwinell, L. Eckmann, and M. F. Kagnoff. 2001. Production of MDC/CCL22 by human intestinal epithelial cells. Am. J. Physiol. 280: G1217-G1226.
37. Elewaut, D., J. A. DiDonato, J. M. Kim, F. Truong, L. Eckmann, and M. F. Kagnoff. 1999. NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J. Immunol. 163: 1457-1466.
38. He, D., S. J. Hagen, C. Pothoulakis, M. Chen, N. D. Medina, M. Warny, and J. T. LaMont. 2000. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 119: 139-150.
39. Mahida, Y. R., A. Galvin, S. Makh, S. Hyde, L. Sanfilippo, S. P. Borriello, and H. F. Sewell. 1998. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: early loss of macrophages followed by T-cell apoptosis. Infect. Immun. 66: 5462-5469.
40. Calderon, G. M., J. Torres-Lopez, T. J. Lin, B. Chavez, M. Hernandez, O. Munoz, A. D. Befus, and J. A. Enciso. 1998. Effects of toxin A from Clostridium difficile on mast cell activation and survival. Infect. Immun. 66: 2755-2761.
41. 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.
42. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
43. Alcantara, C., W. F. Stenson, T. S. Steiner, and R. L. Guerrant. 2001. Role of inducible cyclooxygenase and prostaglandins in Clostridium difficile toxin A-induced secretion and inflammation in an animal model. J. Infect. Dis. 184: 648-652.
44. 2 synthesis in colonocytes via reactive oxygen species and activation of p38 MAPK. J. Biol. Chem. 280: 21237-21245.