Induction of IL-13 triggers TGF-β1-dependent tissue fibrosis in chronic 2,4,6-trinitrobenzene sulfonic acid colitis

Journal of Immunology

Volumn 178, Issue 9, 2007, Pages 5859-5870

  Fichtner Feigl, Stefan ^a,b   Fuss, Ivan J ^a   Young, Cheryl A ^a   Watanabe, Tomohiro ^a   Geissler, Edward K ^b   Schlitt, Hans Jürgen ^b   Kitani, Atsushi ^a   Strober, Warren ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; FC RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 25; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; IMMUNOPATHOGENESIS; INFLAMMATION; INTESTINAL FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH1 CELL; WESTERN BLOTTING;

EID: 34247586091     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.9.5859     Document Type: Article

References (56)

1. Podolsky, D. K. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347: 417-429.
2. Fiocchi, C. 1998. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115: 182-205.
3. Beck, P. L., and D. K. Podolsky. 1999. Growth factors in inflammatory bowel disease. Inflamm. Bowel Dis. 5: 44-60.
4. Harper, P. H., V. W. Fazio, I. C. Lavery, D. G. Jagelman, F. L. Weakley, R. G. Farmer, and K. A. Easley. 1987. The long-term outcome in Crohn's disease. Dis. Colon Rectum 30: 174-179.
5. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3: 521-533.
6. 1 production and fibrosis. Nat. Med. 12: 99-106.
7. Macdonald, T. T. 2006. Decoy receptor springs to life and eases fibrosis. Nat. Med. 12: 13-14.
8. Boirivant, M., I. J. Fuss, A. Chu, and W. Strober. 1998. Oxazolone colitis: a murine model of T helper cell type 2 colitis treatable with antibodies to interleukin 4. J. Exp. Med. 188: 1929-1939.
9. Neurath, M., I. Fuss, and W. Strober. 2000. TNBS-colitis. Int. Rev. Immunol. 19: 51-62.
10. Fichtner-Feigl, S., I. J. Fuss, J. C. Preiss, W. Strober, and A. Kitani. 2005. Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-κB decoy oligonucleotides. J. Clin. Invest. 115: 3057-3071.
11. Neurath, M. F., and S. Pettersson. 1997. Predominant role of NF-κB p65 in the pathogenesis of chronic intestinal inflammation. Immunobiology 198: 91-98.
12. Neurath, M. F., S. Pettersson, K. H. Meyer zum Buschenfelde, and W. Strober. 1996. Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-κB abrogates established experimental colitis in mice. Nat. Med. 2: 998-1004.
13. Lawrance, I. C., F. Wu, A. Z. Leite, I. Willis, G. A. West, C. Fiocchi, and S. Chakravarti. 2003. A murine model of chronic inflammation-induced intestinal fibrosis down-regulated by antisense NF-κB. Gastroenterology 125: 1750-1761.
14. Shimamura, M., R. Morishita, M. Endoh, K. Oshima, M. Aoki, S. Waguri, Y. Uchiyama, and Y. Kaneda. 2003. HVJ-envelope vector for gene transfer into central nervous system. Biochem. Biophys. Res. Commun. 300: 464-471.
15. Kitani, A., I. Fuss, K. Nakamura, F. Kumaki, T. Usui, and W. Strober. 2003. Transforming growth factor (TGF)-β1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-β1-mediated fibrosis. J. Exp. Med. 198: 1179-1188.
16. Watanabe, T., A. Kitani, P. J. Murray, and W. Strober. 2004. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat. Immunol. 5: 800-808.
17. Fuss, I. J., T. Marth, M. F. Neurath, G. R. Pearlstein, A. Jain, and W. Strober. 1999. Anti-interleukin 12 treatment regulates apoptosis of Th1 T cells in experimental colitis in mice. Gastroenterology 117: 1078-1088.
18. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.
19. Fort, M. M., J. Cheung, D. Yen, J. Li, S. M. Zurawski, S. Lo, S. Menon, T. Clifford, B. Hunte, R. Lesley, et al. 2001. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15: 985-995.
20. Hurst, S. D., T. Muchamuel, D. M. Gorman, J. M. Gilbert, T. Clifford, S. Kwan, S. Menon, B. Seymour, C. Jackson, T. T. Kung, et al. 2002. New IL-17 family members-promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J. Immunol. 169: 443-453.
21. + T cell development and early IL-4 production in CD1-deficient mice. Immunity 6: 459-467.
22. Exley, M. A., Q. He, O. Cheng, R. J. Wang, C. P. Cheney, S. P. Balk, and M. J. Koziel. 2002. Cutting edge: compartmentalization of Th1-like noninvariant CD1d-reactive T cells in hepatitis C virus-infected liver. J. Immunol. 168: 1519-1523.
23. + Th1 cells. J. Virol. 76: 10785-10790.
24. Van Kaer, L. 2004. Regulation of immune responses by CD1d-restricted natural killer T cells. Immunol. Res. 30: 139-153.
25. Chiaramonte, M. G., M. Mentink-Kane, B. A. Jacobson, A. W. Cheever, M. J. Whitters, M. E. Goad, A. Wong, M. Collins, D. D. Donaldson, M. J. Grusby, and T. A. Wynn. 2003. Regulation and function of the interleukin 13 receptor α2 during a T helper cell type 2-dominant immune response. J. Exp. Med. 197: 687-701.
26. Mentink-Kane, M. M., A. W. Cheever, R. W. Thompson, D. M. Hari, N. B. Kabatereine, B. J. Vennervald, J. H. Ouma, J. K. Mwatha, F. M. Jones, D. D. Donaldson, et al. 2004. IL-13 receptor α2 down-modulates granulomatous inflammation and prolongs host survival in schistosomiasis. Proc. Natl. Acad. Sci. USA 101: 586-590.
27. Wynn, T. A., M. Hesse, N. G. Sandler, M. Kaviratne, K. F. Hoffmann, M. G. Chiaramonte, R. Reiman, A. W. Cheever, J. P. Sypek, and M. M. Mentink-Kane. 2004. P-selectin suppresses hepatic inflammation and fibrosis in mice by regulating interferon γ and the IL-13 decoy receptor. Hepatology 39: 676-687.
28. Kitani, A., I. J. Fuss, K. Nakamura, O. M. Schwartz, T. Usui, and W. Strober. 2000. Treatment of experimental (trinitrobenzene sulfonic acid) colitis by intranasal administration of transforming growth factor (TGF)-β1 plasmid: TGF-β1-mediated suppression of T helper cell type 1 response occurs by interleukin (IL)-10 induction and IL-12 receptor β2 chain downregulation. J. Exp. Med. 192: 41-52.
29. Evans, R. A., Y. C. Tian, R. Steadman, and A. O. Phillips. 2003. TGF-β1-mediated fibroblast-myofibroblast terminal differentiation-the role of Smad proteins. Exp. Cell Res. 282: 90-100.
30. Leask, A., and D. J. Abraham. 2004. TGF-β signaling and the fibrotic response. FASEB J. 18: 816-827.
31. Schnaper, H. W., T. Hayashida, S. C. Hubchak, and A. C. Poncelet. 2003. TGF-β signal transduction and mesangial cell fibrogenesis. Am. J. Physiol. 284: F243-F252.
32. Wang, W., V. Koka, and H. Y. Lan. 2005. Transforming growth factor-β and Smad signalling in kidney diseases. Nephrology 10: 48-56.
33. Yingling, J. M., K. L. Blanchard, and J. S. Sawyer. 2004. Development of TGF-β signalling inhibitors for cancer therapy. Nat. Rev. Drug Discov. 3: 1011-1022.
34. Monteleone, G., G. Del Vecchio Blanco, I. Monteleone, D. Fina, R. Caruso, V. Gioia, S. Ballerini, G. Federici, S. Bernardini, F. Pallone, and T. T. MacDonald. 2005. Post-transcriptional regulation of Smad7 in the gut of patients with inflammatory bowel disease. Gastroenterology 129: 1420-1429.
35. Monteleone, G., A. Kumberova, N. M. Croft, C. McKenzie, H. W. Steer, and T. T. MacDonald. 2001. Blocking Smad7 restores TGF-β1 signaling in chronic inflammatory bowel disease. J. Clin. Invest. 108: 601-609.
36. Monteleone, G., F. Pallone, and T. T. MacDonald. 2004. Smad7 in TGF-β-mediated negative regulation of gut inflammation. Trends Immunol. 25: 513-517.
37. Spencer, D. M., G. M. Veldman, S. Banerjee, J. Willis, and A. D. Levine. 2002. Distinct inflammatory mechanisms mediate early versus late colitis in mice. Gastroenterology 122: 94-105.
38. Bamias, G., C. Martin, M. Mishina, W. G. Ross, J. Rivera-Nieves, M. Marini, and F. Cominelli. 2005. Proinflammatory effects of TH2 cytokines in a murine model of chronic small intestinal inflammation. Gastroenterology 128: 654-666.
39. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
40. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro- and anti-inflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
41. Hue, S., P. Ahern, S. Buonocore, M. C. Kullberg, D. J. Cua, B. S. McKenzie, F. Powrie, and K. J. Maloy. 2006. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203: 2473-2483.
42. Kullberg, M. C., D. Jankovic, C. G. Feng, S. Hue, P. L. Gorelick, B. S. McKenzie, D. J. Cua, F. Powrie, A. W. Cheever, K. J. Maloy, and A. Sher. 2006. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203: 2485-2494.
43. Bettelli, E., and V. K. Kuchroo. 2005. IL-12- and IL-23-induced T helper cell subsets: birds of the same feather flock together. J. Exp. Med. 201: 169-171.
44. Langrish, C. L., B. S. McKenzie, N. J. Wilson, R. de Waal Malefyt, R. A. Kastelein, and D. J. Cua. 2004. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol. Rev. 202: 96-105.
45. Watford, W. T., B. D. Hissong, J. H. Bream, Y. Kanno, L. Muul, and J. J. O'Shea. 2004. Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol. Rev. 202: 139-156.
46. Uhlig, H. H., B. S. McKenzie, S. Hue, C. Thompson, B. Joyce-Shaikh, R. Stepankova, N. Robinson, S. Buonocore, H. Tlaskalova-Hogenova, D. J. Cua, and F. Powrie. 2006. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 25: 309-318.
47. Becker, C., H. Dornhoff, C. Neufert, M. C. Fantini, S. Wirtz, S. Huebner, A. Nikolaev, H. A. Lehr, A. J. Murphy, D. M. Valenzuela, et al. 2006. Cutting edge: IL-23 cross-regulates IL-12 production in T cell-dependent experimental colitis. J. Immunol. 177: 2760-2764.
48. Fuss, I. J., C. Becker, Z. Yang, C. Groden, R. L. Hornung, F. Heller, M. F. Neurath, W. Strober, and P. J. Mannon. 2006. Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with anti-IL-12 p40 monoclonal antibody. Inflamm. Bowel Dis. 12: 9-15.
49. Redecke, V., H. Hacker, S. K. Datta, A. Fermin, P. M. Pitha, D. H. Broide, and E. Raz. 2004. Cutting edge: activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J. Immunol. 172: 2739-2743.
50. Donaldson, D. D., M. J. Whitters, L. J. Fitz, T. Y. Neben, H. Finnerty, S. L. Henderson, R. M. O'Hara, Jr., D. R. Beier, K. J. Turner, C. R. Wood, and M. Collins. 1998. The murine IL-13 receptor α2: molecular cloning, characterization, and comparison with murine IL-13 receptor α1. J. Immunol. 161: 2317-2324.
51. MacDonald, T. T., A. DiSabatino, and J. N. Gordon. 2005. Immunopathogenesis of Crohn's disease. JPEN J. Parenter. Enteral. Nutr. 29: S118-S124.
52. Monteleone, G., G. Del Vecchio Blanco, G. Palmieri, P. Vavassori, I. Monteleone, A. Colantoni, S. Battista, L. G. Spagnoli, M. Romano, M. Borrelli, et al. 2004. Induction and regulation of Smad7 in the gastric mucosa of patients with Helicobacter pylori infection. Gastroenterology 126: 674-682.
53. Park, S. H. 2005. Fine tuning and cross-talking of TGF-β signal by inhibitory Smads. J. Biochem. Mol. Biol. 38: 9-16.
54. Hershey, G. K. IL-13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. 111: 677-690.
55. Heller, F., P. Florian, C. Bojarski, J. Richter, M. Christ, B. Hillenbrand, J. Mankertz, A. H. Gitter, N. Burgel, M. Fromm, et al. 2005. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129: 550-564.
56. Del Zotto, B., G. Mumolo, A. M. Pronio, C. Montesani, R. Tersigni, and M. Boirivant. 2003. TGF-β1 production in inflammatory bowel disease: differing production patterns in Crohn's disease and ulcerative colitis. Clin. Exp. Immunol. 134: 120-126.