IL-13 signaling in liver fibrogenesis

Frontiers in Immunology

Volumn 3, Issue MAY, 2012, Pages

  Liu, Yan ^a   Munker, Stefan ^a   Müllenbach, Roman ^a,b   Weng, Hong Lei ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Hepatic stellate cell; Schistosomiasis; STAT6; Th2 cell

Indexed keywords

EID: 84870720956     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00116     Document Type: Review

References (71)

1. Akpolat, N., Yahsi, S., Godekmerdan, A., Demirbag, K., and Yalniz, M. (2005). Relationship between serum cytokine levels and histopathologi- cal changes of liver in patients with hepatitis B. World J. Gastroenterol. 11, 3260-3263.
2. Aliprantis, A. O., Wang, J., Fathman, J. W., Lemaire, R., Dorfman, D. M., Lafyatis, R., and Glimcher, L. H. (2007). Transcription factor T-bet regulates skin sclerosis through its function in innate immunity and via IL-13. Proc. Natl. Acad. Sci. U.S.A. 104, 2827-2830.
3. Alves Oliveira, L. F., Moreno, E. C., Gazzinelli, G., Martins-Filho, O. A., Silveira, A. M., Gazzinelli, A., Malaquias, L. C., LoVerde, P., Leite, P. M., and Correa-Oliveira, R. (2006). Cytokine production asso- ciated with periportal fibrosis dur- ing chronic Schistosomiasis man- soni in humans. Infect. Immun. 74, 1215-1221.
4. Bataller, R., and Brenner, D. A. (2005). Liver fibrosis. J. Clin. Invest. 115, 209-218.
5. Belperio, J. A., Dy, M., Burdick, M. D., Xue, Y. Y., Li, K., Elias, J. A., and Keane, M. P. (2002). Interac- tion of IL-13 and C10 in the patho- genesis of bleomycin-induced pul- monary fibrosis. Am. J. Respir. Cell Mol. Biol. 27, 419-427.
6. Bergamini, A., Bolacchi, F., Cerasari, G., Carvelli, C., Faggioli, E., Cepparulo, M., Demin, F., Uccella, I., Bongio- vanni, B., Niutta, P., Capozzi, M., Lupi, M., Piscitelli, E., Rocchi, G., and Angelico, M. (2001). Lack of evidence for the Th2 predominance in patients with chronic hepatitis C. Clin. Exp. Immunol. 123, 451-458.
7. Blease, K., Jakubzick, C., Westwick, J., Lukacs, N., Kunkel, S. L., and Hogaboam,C. M. (2001). Therapeu- tic effect of IL-13 immunoneutral- ization during chronic experimen- tal fungal asthma. J. Immunol. 166, 5219-5224.
8. Blease, K., Schuh, J. M., Jakubzick, C., Lukacs, N. W., Kunkel, S. L., Joshi, B. H., Puri, R. K., Kaplan, M. H., and Hogaboam, C. M. (2002). Stat6-deficient mice develop air- way hyperresponsiveness and peri- bronchial fibrosis during chronic fungal asthma. Am. J. Pathol. 160, 481-490.
9. Booth, M., Mwatha, J. K., Joseph, S., Jones, F. M., Kadzo, H., Ireri, E., Kazibwe, F., Kemijumbi, J., Kariuki, C., Kimani, G., Ouma, J. H., Kabatere- ine, N. B., Vennervald, B. J., and Dunne, D. W. (2004). Periportal fibrosis in human Schistosoma man- soni infection is associated with low IL-10, low IFN-gamma, high TNF- alpha, or low RANTES, depending on age and gender. J. Immunol. 172, 1295-1303.
10. Cheever, A. W., Poindexter, R. W., and Wynn, T. A. (1999). Egg lay- ing is delayed but worm fecun- dity is normal in SCID mice infected with Schistosoma japonicum and S. mansoni with or without recombinant tumor necrosis factor alpha treatment. Infect. Immun. 67, 2201-2208.
11. Cheever, A. W., Williams, M. E., Wynn, T. A., Finkelman, F. D., Seder, R. A., Cox, T. M., Hieny, S., Caspar, P., and Sher, A. (1994). Anti-IL-4 treatment of Schistosoma mansoni-infected mice inhibits development of T cells and non-B, non-T cells expressing Th2 cytokines while decreasing egginduced hepatic fibrosis. J. Immunol. 153, 753-759.
12. Chiaramonte, M. G., Cheever, A. W., Malley, J. D., Donaldson, D. D., and Wynn, T. A. (2001). Stud- ies of murine schistosomiasis reveal interleukin-13 blockade as a treat- ment for established and progres- sive liver fibrosis. Hepatology 34, 273-282.
13. Chiaramonte, M. G., Donaldson, D. D., Cheever, A. W., and Wynn, T. A. (1999a). An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2- dominated inflammatory response. J. Clin. Invest. 104, 777-785.
14. Chiaramonte, M. G., Schopf, L. R., Neben, T. Y., Cheever, A. W., Don- aldson, D. D., and Wynn, T. A. (1999b). IL-13 is a key regulatory cytokine for Th2 cell-mediated pul- monary granuloma formation and IgE responses induced by Schisto- soma mansoni eggs. J. Immunol. 162, 920-930.
15. Chiaramonte, M. G., Mentink-Kane, M., Jacobson, B. A., Cheever, A. W., Whitters, M. J., Goad, M. E., Wong, A., Collins, M., Donaldson, D. D., Grusby, M. J., and Wynn, T. A. (2003). Regulation and function of the interleukin 13 receptor alpha 2 during a T helper cell type 2- dominant immune response. J. Exp. Med. 197, 687-701.
16. Coutinho, H. M., Acosta, L. P., Wu, H. W., McGarvey, S. T., Su, L., Langdon, G. C., Jiz, M. A., Jarilla, B., Olveda, R. M., Friedman, J. F., and Kurtis, J. D. (2007). Th2 cytokines are asso- ciated with persistent hepatic fibro- sis in human Schistosoma japonicum infection. J. Infect. Dis. 195,288-295
17. De Jesus, A. R., Magalhaes, A., Miranda, D. G., Miranda, R. G., Araujo, M. I., de Jesus, A. A., Silva, A., Santana, L. B., Pearce, E., and Carvalho, E. M. (2004). Association of type 2 cytokines with hepatic fibrosis in human Schistosoma mansoni infec- tion. Infect. Immun. 72, 3391-3397
18. De Lalla, C., Galli, G., Aldrighetti, L., Romeo, R., Mariani, M., Monno, A., Nuti, S., Colombo, M., Callea, F., Porcelli, S. A., Panina-Bordignon, P., Abrignani, S., Casorati, G., and Dellabona, P. (2004). Production of profibrotic cytokines by invari- ant NKT cells characterizes cirrhosis progression in chronic viral hepati- tis. J. Immunol. 173, 1417-1425.
19. Donaldson, D. D., Whitters, M. J., Fitz, L. J., Neben, T. Y., Finnerty, H., Henderson, S. L., O'Hara, R. M. Jr., Beier, D. R., Turner, K. J., Wood, C. R., and Collins, M. (1998). The murine IL-13 receptor alpha 2: molecular cloning, characterization, and comparison with murine IL-13 receptor alpha 1. J. Immunol. 161, 2317-2324
20. Durante-Mangoni, E., Wang, R., Shaulov, A., He, Q., Nasser, I., Afd- hal, N., Koziel, M. J., and Exley, M. A. (2004). Hepatic CD1d expression in hepatitis C virus infection and recognition by resident proinflam- matory CD1d-reactive T cells. J. Immunol. 173, 2159-2166.
21. Fallon, P. G., Emson, C. L., Smith, P., and McKenzie, A. N. (2001). IL-13 overexpression predisposes to anaphylaxis following antigen sensitization. J. Immunol. 166, 2712-2716.
22. Fallon, P. G., Richardson, E. J., McKen- zie, G. J., and McKenzie, A. N. (2000). Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL- 4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164, 2585-2591.
23. Fichtner-Feigl, S., Strober, W., Kawakami, K., Puri, R. K., and Kitani, A. (2006). IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat. Med. 12, 99-106.
24. Friedman, S. L. (2008). Mechanisms of hepatic fibrogenesis. Gastroenterol- ogy 134, 1655-1669.
25. Fritz, D. K., Kerr, C., Fattouh, R., Llop-Guevara, A., Khan, W. I., Jor- dana, M., and Richards, C. D. (2011). A mouse model of air- way disease: oncostatin M-induced pulmonary eosinophilia, goblet cell hyperplasia, and airway hyperre- sponsiveness are STAT6 dependent, and interstitial pulmonary fibrosis is STAT6 independent. J. Immunol. 186, 1107-1118.
26. Gressner, A. M., Weiskirchen, R., Bre- itkopf, K., and Dooley, S. (2002). Roles of TGF-beta in hepatic fibrosis. Front. Biosci. 7, d793-d807.
27. Hasegawa, M., Fujimoto, M., Kikuchi, K.,and Takehara,K. (1997). Elevated serum levels of interleukin 4 (IL- 4), IL-10, and IL-13 in patients with systemic sclerosis. J. Rheumatol. 24, 328-332.
28. Hauber, H. P., Gholami, D., Meyer, A., and Pforte, A. (2003). Increased interleukin-13 expression in patients with sarcoidosis. Thorax 58, 519-524.
29. Heller, F., Florian, P., Bojarski, C., Richter, J., Christ, M., Hillenbrand, B., Mankertz, J., Gitter, A. H., Burgel, N., Fromm, M., Zeitz, M., Fuss, I., Strober, W., and Schulzke, J. D. (2005). Interleukin-13 is the key effector Th2 cytokine in ulcera- tive colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129, 550-564.
30. Hershey, G. K. (2003). IL-13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. 111, 677-690; quiz 691.
31. Ingram, J. L., Rice, A. B., Geisenhof- fer, K., Madtes, D. K., and Bon- ner, J. C. (2004). IL-13 and IL-1beta promote lung fibroblast growth through coordinated up-regulation of PDGF-AA and PDGF-Ralpha. FASEB J. 18, 1132-1134.
32. Inoue, M., Kanto, T., Miyatake, H., Itose, I., Miyazaki, M., Yakushijin, T., Sakakibara, M., Kuzushita, N., Hiramatsu, N., Takehara, T., Kasahara,A., and Hayashi, N. (2006). Enhanced ability of peripheral invariant nat- ural killer T cells to produce IL-13 in chronic hepatitis C virus infection. J. Hepatol. 45, 190-196.
33. Iredale, J. P. (2007). Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J. Clin. Invest. 117, 539-548.
34. Isomaki, P., Luukkainen, R., Toiva- nen, P., and Punnonen, J. (1996). The presence of interleukin-13 in rheumatoid synovium and its anti- inflammatory effects on synovial fluid macrophages from patients with rheumatoid arthritis. Arthritis Rheum. 39, 1693-1702.
35. Jakubzick, C., Choi, E. S., Carpenter, K. J., Kunkel, S. L., Evanoff, H., Martinez, F. J., Flaherty, K. R., Toews, G. B., Colby, T.V., Travis,W. D., Joshi, B. H.,Puri,R. K.,and Hogaboam,C. M. (2004). Human pulmonary fibrob- lasts exhibit altered interleukin-4 and interleukin-13 receptor sub- unit expression in idiopathic inter- stitial pneumonia. Am. J. Pathol. 164, 1989-2001.
36. Jakubzick, C., Kunkel, S. L., Joshi, B. H., Puri, R. K., and Hogaboam, C. M. (2002). Interleukin-13 fusion cyto- toxin arrests Schistosoma mansoni egg-induced pulmonary granuloma formation in mice. Am. J. Pathol. 161, 1283-1297.
37. Jankovic, D., Kullberg, M. C., Noben- Trauth, N., Caspar, P., Ward, J. M., Cheever, A. W., Paul, W. E., and Sher, A. (1999). Schistosome-infected IL- 4 receptor knockout (KO) mice, in contrast to IL-4 KO mice, fail to develop granulomatous pathol- ogy while maintaining the same lymphokine expression profile. J. Immunol. 163, 337-342.
38. Jin, Z., Sun, R., Wei, H., Gao, X., Chen, Y., and Tian, Z. (2011). Accelerated liver fibrosis in hepatitis B virus transgenic mice: involvement of nat- ural killer T cells. Hepatology 53, 219-229.
39. Joshi, B. H., Hogaboam, C., Dover, P., Husain, S. R., and Puri, R. K. (2006). Role of interleukin-13 in cancer,pul- monary fibrosis, and other T(H)2- type diseases. Vitam. Horm. 74, 479-504.
40. Kanto, T., and Hayashi, N. (2007). Innate immunity in hepatitis C virus infection: interplay among dendritic cells, natural killer cells and natural killer T cells. Hepatol. Res. 37(Suppl. 3), S319-S326.
41. Kaviratne, M., Hesse, M., Leusink, M., Cheever, A. W., Davies, S. J., McKerrow, J. H., Wakefield, L. M., Let- terio, J. J., and Wynn, T. A. (2004). IL-13 activates a mechanism of tis- sue fibrosis that is completely TGF- beta independent. J. Immunol. 173, 4020-4029.
42. Kawashima, R., Kawamura, Y. I., Oshio, T., Son, A., Yamazaki, M., Hagiwara, T., Okada, T., Inagaki-Ohara, K., Wu, P., Szak, S., Kawamura, Y. J., Konishi, F., Miyake, O., Yano, H., Saito, Y., Burkly, L. C., and Dohi, T. (2011). Interleukin-13 damages intestinal mucosa via TWEAK and Fn14 in mice-a pathway associated with ulcerative colitis. Gastroenterol- ogy 141, 2119-2129; e2118.
43. Kelly-Welch, A. E., Hanson, E. M., Boothby, M. R., and Keegan, A. D. (2003). Interleukin-4 and interleukin-13 signaling connec- tions maps. Science 300, 1527-1528
44. Kumar, R. K., Herbert, C., Yang, M., Koskinen, A. M., McKenzie, A. N., and Foster, P. S. (2002). Role of interleukin-13 in eosinophil accu- mulation and airway remodelling in a mouse model of chronic asthma. Clin. Exp. Allergy 32, 1104-1111.
45. Lanone, S., Zheng, T., Zhu, Z., Liu, W., Lee, C. G., Ma, B., Chen, Q., Homer, R. J., Wang, J., Rabach, L. A., Rabach, M. E., Shipley, J. M., Shapiro, S. D., Senior, R. M., and Elias, J. A. (2002). Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J. Clin. Invest. 110, 463-474.
46. Lee, C. G., Homer, R. J., Zhu, Z., Lanone, S., Wang, X., Koteliansky, V., Ship- ley, J. M., Gotwals, P., Noble, P., Chen, Q., Senior, R. M., and Elias, J. A. (2001). Interleukin-13 induces tissue fibrosis by selectively stimu- lating and activating transforming growth factor beta(1). J. Exp. Med. 194, 809-821.
47. Liu, Y., Meyer, C., Muller, A., Herweck, F., Li, Q., Mullenbach, R., Mertens, P. R., Dooley, S., and Weng, H. L. (2011). IL-13 induces connective tis- sue growth factor in rat hepatic stel- late cells via TGF-beta-independent Smad signaling. J. Immunol. 187, 2814-2823.
48. Mann, D. A., and Marra, F. (2010). Fibrogenic signalling in hepatic stel- late cells. J. Hepatol. 52, 949-950.
49. Matsushita, M., Yamamoto, T., and Nishioka, K. (2004). Upregulation of interleukin-13 and its receptor in a murine model of bleomycin- induced scleroderma. Int. Arch. Allergy Immunol. 135, 348-356.
50. Mentink-Kane, M. M., Cheever, A. W., Thompson, R. W., Hari, D. M., Kabatereine, N. B., Vennervald, B. J., Ouma, J. H., Mwatha, J. K., Jones, F. M., Donaldson, D. D., Grusby, M. J., Dunne, D. W., and Wynn, T. A. (2004). IL-13 receptor alpha 2 down- modulates granulomatous inflam- mation and prolongs host survival in schistosomiasis. Proc. Natl. Acad. Sci. U.S.A. 101, 586-590.
51. Metwali, A., Elliott, D., Blum, A. M., Li, J., Sandor, M., Lynch, R., Noben-Trauth, N., and Weinstock, J. V. (1996). The granulomatous response in murine Schistosomia- sis mansoni does not switch to Th1 in IL-4-deficient C57BL/6 mice. J. Immunol. 157, 4546-4553.
52. Park, S. W., Ahn, M. H., Jang, H. K., Jang, A. S., Kim, D. J., Koh, E. S., Park, J. S., Uh, S. T., Kim, Y. H., Paik, S. H., Shin, H. K., Youm, W., and Park, C. S. (2009). Interleukin-13 and its receptors in idiopathic inter- stitial pneumonia: clinical implica- tions for lung function. J. Korean Med. Sci. 24, 614-620.
53. Pearce, E. J., Cheever, A., Leonard, S.,Covalesky,M.,Fernandez-Botran, R., Kohler, G., and Kopf, M. (1996). Schistosoma mansoni in IL- 4-deficient mice. Int. Immunol. 8, 435-444.
54. Riccieri, V., Rinaldi, T., Spadaro, A., Scrivo, R., Ceccarelli, F., Franco, M. D., Taccari, E., and Valesini, G. (2003). Interleukin-13 in systemic sclerosis: relationship to nailfold capillaroscopy abnormalities. Clin. Rheumatol. 22, 102-106.
55. Roulot, D., Durand, H., Coste, T., Rautureau, J., Strosberg, A. D., Benarous,R.,and Marullo,S. (1995). Quantitative analysis of transform- ing growth factor beta1 messen- ger RNA in the liver of patients with chronic hepatitis C: absence of correlation between high levels and severity of disease. Hepatology 21, 298-305.
56. Saiki, O., Uda, H., Nishimoto, N., Miwa, T., Mima, T., Ogawara, T., Azuma, N., Katada, Y., Sawaki, J., Tsutsui, H., Matsui, K., Maeda, A., and Nakan- ishi, K. (2004). Adult Still's disease reflects a Th2 rather than a Th1 cytokine profile. Clin. Immunol. 112, 120-125.
57. Shimamura, T., Fujisawa, T., Husain, S. R., Kioi, M., Nakajima, A., and Puri, R. K. (2008). Novel role of IL-13 in fibrosis induced by nonalcoholic steatohepatitis and its amelioration by IL-13R-directed cytotoxin in a rat model. J. Immunol. 181, 4656-4665
58. Spadaro, A., Rinaldi, T., Riccieri, V., Taccari, E., and Valesini, G. (2002). Interleukin-13 in autoim- mune rheumatic diseases: relation- ship with the autoantibody profile. Clin. Exp. Rheumatol. 20, 213-216.
59. Stickel, F., Urbaschek, R., Schuppan, D., Poeschl, G., Oesterling, C., Conradt, C., McCuskey, R. S., Simanowski, U. A., and Seitz, H. K. (2001). Serum collagen type VI and XIV and hyaluronic acid as early indi- cators for altered connective tissue turnover in alcoholic liver disease. Dig. Dis. Sci. 46, 2025-2032.
60. Sugimoto, R., Enjoji, M., Nakamuta, M., Ohta, S., Kohjima, M., Fukushima, M., Kuniyoshi, M., Arimura, E., Morizono,S.,Kotoh,K.,and Nawata, H. (2005). Effect of IL-4 and IL-13 on collagen production in cultured LI90 human hepatic stellate cells. Liver Int. 25, 420-428.
61. Toh, M. L., and Miossec, P. (2007). The role of T cells in rheumatoid arthri- tis: new subsets and new targets. Curr. Opin. Rheumatol. 19, 284-288.
62. Tokayer, A., Carsons, S. E., Chokshi, B., and Santiago-Schwarz, F. (2002). High levels of interleukin 13 in rheumatoid arthritis sera are modulated by tumor necrosis factor antagonist therapy: association with dendritic cell growth activity. J. Rheumatol. 29, 454-461.
63. Weng, H. L., Liu, Y., Chen, J. L., Huang, T., Xu, L. J., Godoy, P., Hu, J. H., Zhou, C., Stickel, F., Marx, A., Bohle, R. M., Zimmer, V., Lammert, F., Mueller, S., Gigou, M., Samuel, D., Mertens, P. R., Singer, M. V., Seitz, H. K., and Dooley, S. (2009). The etiology of liver damage imparts cytokines transforming growth fac- tor beta1 or interleukin-13 as driving forces in fibrogenesis. Hepatology 50, 230-243.
64. Wilson, M. S., Ramalingam, T. R., Riv- ollier, A., Shenderov, K., Mentink-Kane, M. M., Madala, S. K., Cheever, A. W., Artis, D., Kelsall, B. L., and Wynn, T. A. (2011). Colitis and intestinal inflammation in IL10-/- mice results from IL-13Ralpha2- mediated attenuation of IL-13 activ- ity. Gastroenterology 140, 254-264.
65. Wynn, T. A. (2003). IL-13 effector functions. Annu. Rev. Immunol. 21, 425-456.
66. Wynn, T. A. (2004). Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat. Rev. Immunol. 4, 583-594.
67. Wynn, T. A. (2008). Cellular and mol- ecular mechanisms of fibrosis. J. Pathol. 214, 199-210.
68. Wynn, T. A., Hesse, M., Sandler, N. G., Kaviratne, M., Hoffmann, K. F., Chiaramonte, M. G., Reiman, R., Cheever, A. W., Sypek, J. P., and Mentink-Kane, M. M. (2004a). P- selectin suppresses hepatic inflam- mation and fibrosis in mice by regulating interferon gamma and the IL-13 decoy receptor. Hepatology 39, 676-687.
69. Wynn, T. A., Thompson, R. W., Cheever, A. W., and Mentink-Kane, M. M. (2004b). Immunopathogenesis of schistosomiasis. Immunol. Rev. 201, 156-167.
70. Zhang, J. G., Hilton, D. J., Willson, T. A., McFarlane, C., Roberts, B. A., Moritz, R. L., Simpson, R. J., Alexan- der, W. S., Metcalf, D., and Nicola, N. A. (1997). Identification, purifica- tion, and characterization of a solu- ble interleukin (IL)-13-binding pro- tein. Evidence that it is distinct from the cloned Il-13 receptor and Il-4 receptor alpha-chains. J. Biol. Chem. 272, 9474-9480.
71. Zhu, Z., Homer, R. J., Wang, Z., Chen, Q., Geba, G. P., Wang, J., Zhang, Y., and Elias, J. A. (1999). Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecre- tion, subepithelial fibrosis, physi- ologic abnormalities, and eotaxin production. J. Clin. Invest. 103, 779-788.