TLR2-mediated production of IL-27 and chemokines by respiratory epithelial cells promotes bleomycin-induced pulmonary fibrosis in mice

Journal of Immunology

Volumn 187, Issue 8, 2011, Pages 4007-4017

  Kim, Hye Sung ^a   Go, Heounjeong ^a   Akira, Shizuo ^b   Chung, Doo Hyun ^a  

^a Seoul National University College of Medicine   (South Korea)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; CHEMOKINE; HYDROXYPROLINE; INTERFERON REGULATORY FACTOR; INTERLEUKIN 17; INTERLEUKIN 27; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRONCHUS MUCOSA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FLOW CYTOMETRY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLEOMYCIN; BLOTTING, WESTERN; BRONCHOALVEOLAR LAVAGE; CELL SEPARATION; CHEMOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IDIOPATHIC PULMONARY FIBROSIS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-17; INTERLEUKINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 80054759044     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101654     Document Type: Article

References (45)

1. Hattori, N., J. L. Degen, T. H. Sisson, H. Liu, B. B. Moore, R. G. Pandrangi, R. H. Simon, and A. F. Drew. 2000. Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J. Clin. Invest. 106: 1341-1350.
2. Swaisgood, C. M., E. L. French, C. Noga, R. H. Simon, and V. A. Ploplis. 2000. The development of bleomycin-induced pulmonary fibrosis in mice deficient for components of the fibrinolytic system. Am. J. Pathol. 157: 177-187. (Pubitemid 30641735)
3. Lukacs, N. W., C. Hogaboam, S. W. Chensue, K. Blease, and S. L. Kunkel. 2001. Type 1/type 2 cytokine paradigm and the progression of pulmonary fibrosis. Chest 120(1 Suppl)5S-8S. (Pubitemid 32702104)
4. Segel, M. J., G. Izbicki, P. Y. Cohen, R. Or, T. G. Christensen, S. B. Wallach-Dayan, and R. Breuer. 2003. Role of interferon-gamma in the evolution of murine bleomycin lung fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 285: L1255-L1262. (Pubitemid 37448796)
5. Keane, M. P., J. A. Belperio, M. D. Burdick, and R. M. Strieter. 2001. IL-12 attenuates bleomycin-induced pulmonary fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 281: L92-L97.
6. Gharaee-Kermani, M., Y. Nozaki, K. Hatano, and S. H. Phan. 2001. Lung interleukin-4 gene expression in a murine model of bleomycin-induced pulmonary fibrosis. Cytokine 15: 138-147. (Pubitemid 34587495)
7. Huaux, F., T. Liu, B. McGarry, M. Ullenbruch, and S. H. Phan. 2003. Dual roles of IL-4 in lung injury and fibrosis. J. Immunol. 170: 2083-2092. (Pubitemid 36197430)
8. Schnare, M., G. M. Barton, A. C. Holt, K. Takeda, S. Akira, and R. Medzhitov. 2001. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2: 947-950. (Pubitemid 32976167)
9. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
10. Jiang, D., J. Liang, Y. Li, and P. W. Noble. 2006. The role of Toll-like receptors in non-infectious lung injury. Cell Res. 16: 693-701. (Pubitemid 44258922)
11. Yang, H. Z., B. Cui, H. Z. Liu, Z. R. Chen, H. M. Yan, F. Hua, and Z. W. Hu. 2009. Targeting TLR2 attenuates pulmonary inflammation and fibrosis by reversion of suppressive immune microenvironment. J. Immunol. 182: 692-702.
12. Jiang, D., J. Liang, J. Fan, S. Yu, S. Chen, Y. Luo, G. D. Prestwich, M. M. Mascarenhas, H. G. Garg, D. A. Quinn, et al. 2005. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11: 1173-1179. (Pubitemid 43093664)
13. Yoshizaki, A., Y. Iwata, K. Komura, F. Ogawa, T. Hara, E. Muroi, M. Takenaka, K. Shimizu, M. Hasegawa, M. Fujimoto, et al. 2008. CD19 regulates skin and lung fibrosis via Toll-like receptor signaling in a model of bleomycin-induced scleroderma. Am. J. Pathol. 172: 1650-1663. (Pubitemid 351793356)
14. Trujillo, G., A. Meneghin, K. R. Flaherty, L. M. Sholl, J. L. Myers, E. A. Kazerooni, B. H. Gross, S. R. Oak, A. L. Coelho, H. Evanoff, E. Day, G. B. Toews, A. D. Joshi, M. A. Schaller, B. Waters, G. Jarai, J. Westwick, S. L. Kunkel, F. J. Martinez, and C. M. Hogaboam. 2010. TLR9 differentiates rapidly from slowly progressing forms of idiopathic pulmonary fibrosis. Sci. Transl. Med. 2: 57ra82.
15. Schwandner, R., R. Dziarski, H. Wesche, M. Rothe, and C. J. Kirschning. 1999. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J. Biol. Chem. 274: 17406-17409.
16. Armstrong, L., A. R. Medford, K. M. Uppington, J. Robertson, I. R. Witherden, T. D. Tetley, and A. B. Millar. 2004. Expression of functional toll-like receptor-2 and -4 on alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 31: 241-245. (Pubitemid 39095455)
17. Homma, T., A. Kato, N. Hashimoto, J. Batchelor, M. Yoshikawa, S. Imai, H. Wakiguchi, H. Saito, and K. Matsumoto. 2004. Corticosteroid and cytokines synergistically enhance toll-like receptor 2 expression in respiratory epithelial cells. Am. J. Respir. Cell Mol. Biol. 31: 463-469. (Pubitemid 39330957)
18. Gribar, S. C., W. M. Richardson, C. P. Sodhi, and D. J. Hackam. 2008. No longer an innocent bystander: epithelial toll-like receptor signaling in the development of mucosal inflammation. Mol. Med. 14: 645-659.
19. Kim, H. Y., S. Kim, and D. H. Chung. 2006. FcgammaRIII engagement provides activating signals to NKT cells in antibody-induced joint inflammation. J. Clin. Invest. 116: 2484-2492. (Pubitemid 44330147)
20. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189. (Pubitemid 43214587)
21. Sutmuller, R. P., M. H. den Brok, M. Kramer, E. J. Bennink, L. W. Toonen, B. J. Kullberg, L. A. Joosten, S. Akira, M. G. Netea, and G. J. Adema. 2006. Toll-like receptor 2 controls expansion and function of regulatory T cells. J. Clin. Invest. 116: 485-494. (Pubitemid 43228366)
22. + regulatory T cells. Proc. Natl. Acad. Sci. USA 103: 7048-7053.
23. + regulatory T cell function via innate TLR2 signaling. J. Clin. Invest. 116: 2022-2032.
24. Loures, F. V., A. Pina, M. Felonato, and V. L. Calich. 2009. TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J. Immunol. 183: 1279-1290.
25. Chapman, H. A. 2011. Epithelial-mesenchymal interactions in pulmonary fibrosis. Annu. Rev. Physiol. 73: 413-435.
26. Pflanz, S., J. C. Timans, J. Cheung, R. Rosales, H. Kanzler, J. Gilbert, L. Hibbert, T. Churakova, M. Travis, E. Vaisberg, et al. 2002. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 16: 779-790. (Pubitemid 34786477)
27. Liu, J., X. Guan, and X. Ma. 2007. Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-gamma-mediated pathways. J. Exp. Med. 204: 141-152. (Pubitemid 46148764)
28. Molle, C., M. Nguyen, V. Flamand, J. Renneson, F. Trottein, D. De Wit, F. Willems, M. Goldman, and S. Goriely. 2007. IL-27 synthesis induced by TLR ligation critically depends on IFN regulatory factor 3. J. Immunol. 178: 7607-7615. (Pubitemid 46898030)
29. Molle, C., M. Goldman, and S. Goriely. 2010. Critical role of the IFN-stimulated gene factor 3 complex in TLR-mediated IL-27p28 gene expression revealing a two-step activation process. J. Immunol. 184: 1784-1792.
30. Wirtz, S., C. Becker, M. C. Fantini, E. E. Nieuwenhuis, I. Tubbe, P. R. Galle, H. J. Schild, M. Birkenbach, R. S. Blumberg, and M. F. Neurath. 2005. EBV-induced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-kappa B activation. J. Immunol. 174: 2814-2824. (Pubitemid 40279698)
31. Pirhonen, J., J. Sirén, I. Julkunen, and S. Matikainen. 2007. IFN-alpha regulates Toll-like receptor-mediated IL-27 gene expression in human macrophages. J. Leukoc. Biol. 82: 1185-1192. (Pubitemid 350133516)
32. Yoshida, H., S. Hamano, G. Senaldi, T. Covey, R. Faggioni, S. Mu, M. Xia, A. C. Wakeham, H. Nishina, J. Potter, et al. 2001. WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity 15: 569-578. (Pubitemid 33016442)
33. Stumhofer, J. S., A. Laurence, E. H. Wilson, E. Huang, C. M. Tato, L. M. Johnson, A. V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7: 937-945. (Pubitemid 44263907)
34. Fitzgerald, D. C., G. X. Zhang, M. El-Behi, Z. Fonseca-Kelly, H. Li, S. Yu, C. J. Saris, B. Gran, B. Ciric, and A. Rostami. 2007. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol. 8: 1372-1379. (Pubitemid 350131174)
35. Yoshida, H., M. Nakaya, and Y. Miyazaki. 2009. Interleukin 27: a double-edged sword for offense and defense. J. Leukoc. Biol. 86: 1295-1303.
36. Yoshizaki, A., K. Yanaba, Y. Iwata, K. Komura, A. Ogawa, E. Muroi, F. Ogawa, M. Takenaka, K. Shimizu, M. Hasegawa, et al. 2011. Elevated serum interleukin-27 levels in patients with systemic sclerosis: association with T cell, B cell and fibroblast activation. Ann. Rheum. Dis. 70: 194-200.
37. Nichols, J. R., A. L. Aldrich, M. M. Mariani, D. Vidlak, N. Esen, and T. Kielian. 2009. TLR2 deficiency leads to increased Th17 infiltrates in experimental brain abscesses. J. Immunol. 182: 7119-7130.
38. Aliahmadi, E., R. Gramlich, A. Grützkau, M. Hitzler, M. Krüger, R. Baumgrass, M. Schreiner, B. Wittig, R. Wanner, and M. Peiser. 2009. TLR2-activated human langerhans cells promote Th17 polarization via IL-1beta, TGF-beta and IL-23. Eur. J. Immunol. 39: 1221-1230.
39. +) T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease. Immunity 32: 692-702.
40. Teixeira-Coelho, M., A. Cruz, J. Carmona, C. Sousa, D. Ramos-Pereira, A. L. Saraiva, M. Veldhoen, J. Pedrosa, A. G. Castro, and M. Saraiva. 2011. TLR2 deficiency by compromising p19 (IL-23) expression limits Th 17 cell responses to Mycobacterium tuberculosis. Int. Immunol. 23: 89-96.
41. Braun, R. K., C. Ferrick, P. Neubauer, M. Sjoding, A. Sterner-Kock, M. Kock, L. Putney, D. A. Ferrick, D. M. Hyde, and R. B. Love. 2008. IL-17 producing gammadelta T cells are required for a controlled inflammatory response after bleomycin-induced lung injury. Inflammation 31: 167-179.
42. Wilson, M. S., S. K. Madala, T. R. Ramalingam, B. R. Gochuico, I. O. Rosas, A. W. Cheever, and T. A. Wynn. 2010. Bleomycin and IL-1β-mediated pulmonary fibrosis is IL-17A dependent. J. Exp. Med. 207: 535-552.
43. Yoshizaki, A., K. Yanaba, Y. Iwata, K. Komura, A. Ogawa, Y. Akiyama, E. Muroi, T. Hara, F. Ogawa, M. Takenaka, et al. 2010. Cell adhesion molecules regulate fibrotic process via Th1/Th2/Th17 cell balance in a bleomycin-induced scleroderma model. J. Immunol. 185: 2502-2515.
44. Becker, M. N., M. S. Sauer, M. S. Muhlebach, A. J. Hirsh, Q. Wu, M. W. Verghese, and S. H. Randell. 2004. Cytokine secretion by cystic fibrosis airway epithelial cells. Am. J. Respir. Crit. Care Med. 169: 645-653. (Pubitemid 38270902)
45. Tager, A. M., R. L. Kradin, P. LaCamera, S. D. Bercury, G. S. Campanella, C. P. Leary, V. Polosukhin, L. H. Zhao, H. Sakamoto, T. S. Blackwell, and A. D. Luster. 2004. Inhibition of pulmonary fibrosis by the chemokine IP-10/CXCL10. Am. J. Respir. Cell Mol. Biol. 31: 395-404. (Pubitemid 39330949)