Epithelial transglutaminase 2 is needed for T cell interleukin-17 production and subsequent pulmonary inflammation and fibrosis in bleomycin-treated mice

Journal of Experimental Medicine

Volumn 208, Issue 18, 2011, Pages 1707-1719

  Oh, Keunhee ^a   Park, Hyung Bae ^a   Byoun, Ok Jin ^a   Shin, Dong Myung ^a   Jeong, Eui Man ^a   Kim, Young Whan ^a   Kim, Yon Su ^a   Melino, Gerry ^b   Kim, In Gyu ^a   Lee, Dong Sup ^a  

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

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; INTERLEUKIN 17; INTERLEUKIN 6; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; EPITHELIUM CELL; FIBROBLAST; FIBROGENESIS; LUNG FIBROSIS; LUNG INJURY; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; T LYMPHOCYTE;

AMINES; ANIMALS; BIOTIN; BLEOMYCIN; BLOTTING, WESTERN; BRONCHOALVEOLAR LAVAGE; COLLAGEN; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GTP-BINDING PROTEINS; HISTOLOGICAL TECHNIQUES; INTERLEUKIN-17; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PNEUMONIA; POLYMERASE CHAIN REACTION; PULMONARY FIBROSIS; RNA; T-LYMPHOCYTES; TRANSGLUTAMINASES;

EID: 79961159239     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101457     Document Type: Article

References (46)

1. Akimov, S.S., and A.M. Belkin. 2001. Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatin-binding domain of fibronectin: a role in TGFbeta-dependent matrix deposition. J. Cell Sci. 114:2989-3000.
2. Aujla, S.J., P.J. Dubin, and J.K. Kolls. 2007. Interleukin-17 in pulmonary host defense. Exp. Lung Res. 33:507-518.
3. Boisvert, W.A., D.M. Rose, A. Boullier, O. Quehenberger, A. Sydlaske, K.A. Johnson, L.K. Curtiss, and R. Terkeltaub. 2006. Leukocyte transglutaminase 2 expression limits atherosclerotic lesion size. Arterioscler. Thromb. Vasc. Biol. 26:563-569.
4. 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.
5. Chen, E.S., B.M. Greenlee, M. Wills-Karp, and D.R. Moller. 2001. Attenuation of lung inflammation and fibrosis in interferon-gamma-deficient mice after intratracheal bleomycin. Am. J. Respir. Cell Mol. Biol. 24:545-555.
6. Chua, F., S.E. Dunsmore, P.H. Clingen, S.E. Mutsaers, S.D. Shapiro, A.W. Segal, J. Roes, and G.J. Laurent. 2007. Mice lacking neutrophil elastase are resistant to bleomycin-induced pulmonary fibrosis. Am. J. Pathol. 170:65-74.
7. Cose, S., C. Brammer, K.M. Khanna, D. Masopust, and L. Lefrançois. 2006. Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur. J. Immunol. 36:1423-1433.
8. Dailey, M.O. 1998. Expression of T lymphocyte adhesion molecules: regulation during antigen-induced T cell activation and differentiation. Crit. Rev. Immunol. 18:153-184.
9. De Laurenzi, V., and G. Melino. 2001. Gene disruption of tissue transglutaminase. Mol. Cell. Biol. 21:148-155.
10. Di Cesare, A., P. Di Meglio, and F.O. Nestle. 2009. The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J. Invest. Dermatol. 129:1339-1350.
11. du Bois, R.M. 2010. Strategies for treating idiopathic pulmonary fibrosis. Nat. Rev. Drug Discov. 9:129-140.
12. Elli, L., C.M. Bergamini, M.T. Bardella, and D. Schuppan. 2009. Transglutaminases in inflammation and fibrosis of the gastrointestinal tract and the liver. Dig. Liver Dis. 41:541-550.
13. Falasca, L., M.G. Farrace, A. Rinaldi, L. Tuosto, G. Melino, and M. Piacentini. 2008. Transglutaminase type II is involved in the pathogenesis of endotoxic shock. J. Immunol. 180:2616-2624.
14. Gaudry, C.A., E. Verderio, D. Aeschlimann, A. Cox, C. Smith, and M. Griffin. 1999. Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal beta-sandwich domain. J. Biol. Chem. 274:30707-30714.
15. Hardie, W.D., S.W. Glasser, and J.S. Hagood. 2009. Emerging concepts in the pathogenesis of lung fibrosis. Am. J. Pathol. 175:3-16.
16. Ientile, R., D. Caccamo, and M. Griffin. 2007. Tissue transglutaminase and the stress response. Amino Acids. 33:385-394.
17. Ivanov, I.I., L. Zhou, and D.R. Littman. 2007. Transcriptional regulation of Th17 cell differentiation. Semin. Immunol. 19:409-417.
18. Johnson, T.S., M. Griffin, G.L. Thomas, J. Skill, A. Cox, B. Yang, B. Nicholas, P.J. Birckbichler, C. Muchaneta-Kubara, and A. Meguid El Nahas. 1997. The role of transglutaminase in the rat subtotal nephrectomy model of renal fibrosis. J. Clin. Invest. 99:2950-2960.
19. Jones, H.A., J.B. Schofield, T. Krausz, A.R. Boobis, and C. Haslett. 1998. Pulmonary fibrosis correlates with duration of tissue neutrophil activation. Am. J. Respir. Crit. Care Med. 158:620-628.
20. Kebir, H., K. Kreymborg, I. Ifergan, A. Dodelet-Devillers, R. Cayrol, M. Bernard, F. Giuliani, N. Arbour, B. Becher, and A. Prat. 2007. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13:1173-1175.
21. Kim, S.Y. 2006. Transglutaminase 2 in inflammation. Front. Biosci. 11:3026-3035.
22. Kim, R., and K.C. Meyer. 2008. Therapies for interstitial lung disease: past, present and future. Ther. Adv. Respir. Dis. 2:319-338.
23. Kojima, S., K. Nara, and D.B. Rifkin. 1993. Requirement for transglutaminase in the activation of latent transforming growth factor-beta in bovine endothelial cells. J. Cell Biol. 121:439-448.
24. Korn, T., E. Bettelli, M. Oukka, and V.K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27:485-517.
25. Kuestner, R.E., D.W. Taft, A. Haran, C.S. Brandt, T. Brender, K. Lum, B. Harder, S. Okada, C.D. Ostrander, J.L. Kreindler, et al. 2007. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J. Immunol. 179:5462-5473.
26. Lee, D.S., C. Ahn, B. Ernst, J. Sprent, and C.D. Surh. 1999. Thymic selection by a single MHC/peptide ligand: autoreactive T cells are low-affinity cells. Immunity. 10:83-92.
27. Li, M.O., Y.Y. Wan, S. Sanjabi, A.K. Robertson, and R.A. Flavell. 2006. Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24:99-146.
28. Lo Re, S., L. Dumoutier, I. Couillin, C. Van Vyve, Y. Yakoub, F. Uwambayinema, B. Marien, S. van den Brûle, J. Van Snick, C. Uyttenhove, et al. 2010. IL-17A-producing gammadelta T and Th17 lymphocytes mediate lung inflammation but not fibrosis in experimental silicosis. J. Immunol. 184:6367-6377.
29. Lorand, L., and R.M. Graham. 2003. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4:140-156.
30. Manzo, A., and C. Pitzalis. 2007. Lymphoid tissue reactions in rheumatoid arthritis. Autoimmun. Rev. 7:30-34.
31. McGeachy, M.J., and D.J. Cua. 2008. Th17 cell differentiation: the long and winding road. Immunity. 28:445-453.
32. Park, S.S., J.M. Kim, D.S. Kim, I.H. Kim, and S.Y. Kim. 2006. Transglutaminase 2 mediates polymer formation of I-kappaBalpha through C-terminal glutamine cluster. J. Biol. Chem. 281:34965-34972.
33. Rogliani, P., M. Mura, M. Assunta Porretta, and C. Saltini. 2008. New perspectives in the treatment of idiopathic pulmonary fibrosis. Ther. Adv. Respir. Dis. 2:75-93.
34. Schnyder-Candrian, S., D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203:2715-2725.
35. Serhan, C.N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6:1191-1197.
36. Shweke, N., N. Boulos, C. Jouanneau, S. Vandermeersch, G. Melino, J.C. Dussaule, C. Chatziantoniou, P. Ronco, and J.J. Boffa. 2008. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am. J. Pathol. 173:631-642.
37. Sonnenberg, G.F., M.G. Nair, T.J. Kirn, C. Zaph, L.A. Fouser, and D. Artis. 2010. Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J. Exp. Med. 207:1293-1305.
38. Staton, T.L., A. Habtezion, M.M. Winslow, T. Sato, P.E. Love, and E.C. Butcher. 2006. CD8+ recent thymic emigrants home to and efficiently repopulate the small intestine epithelium. Nat. Immunol. 7:482-488.
39. Surh, C.D., D.S. Lee, W.P. Fung-Leung, L. Karlsson, and J. Sprent. 1997. Thymic selection by a single MHC/peptide ligand produces a semidiverse repertoire of CD4+ T cells. Immunity. 7:209-219.
40. Thompson, E.D., H.L. Enriquez, Y.X. Fu, and V.H. Engelhard. 2010. Tumor masses support naive T cell infiltration, activation, and differentiation into effectors. J. Exp. Med. 207:1791-1804.
41. Traves, S.L., and L.E. Donnelly. 2008. Th17 cells in airway diseases. Curr. Mol. Med. 8:416-426.
42. Verderio, E.A., T. Johnson, and M. Griffin. 2004. Tissue transglutaminase in normal and abnormal wound healing: review article. Amino Acids. 26:387-404.
43. Weaver, C.T., R.D. Hatton, P.R. Mangan, and L.E. Harrington. 2007. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25:821-852.
44. 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-1betamediated pulmonary fibrosis is IL-17A dependent. J. Exp. Med. 207:535-552.
45. Worbs, T., U. Bode, S. Yan, M.W. Hoffmann, G. Hintzen, G. Bernhardt, R. Förster, and O. Pabst. 2006. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203:519-527.
46. Wynn, T.A. 2007. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J. Clin. Invest. 117:524-529.