IL-17 producing γδ T cells are required for a controlled inflammatory response after bleomycin-induced lung injury

Inflammation

Volumn 31, Issue 3, 2008, Pages 167-179

  Braun, Ruedi K ^a   Ferrick, Christina ^b   Neubauer, Paul ^a   Sjoding, Michael ^a   Sterner Kock, Anja ^c   Kock, Martin ^c   Putney, Lei ^b   Ferrick, David A ^d   Hyde, Dallas M ^b   Love, Robert B ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d Seahorse Bioscience   (United States)

Author keywords

T cell; Bleomycin; IL 17; Lung fibrosis

Indexed keywords

BLEOMYCIN; INTERLEUKIN 17; INTERLEUKIN 6; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; KNOCKOUT MOUSE; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROBLAST; LUNG INFILTRATE; LUNG INJURY; MOUSE; NONHUMAN; PNEUMONIA; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BLEOMYCIN; CELL PROLIFERATION; COLLAGEN; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; INTERLEUKIN-17; INTERLEUKIN-6; LUNG; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PNEUMONIA; PULMONARY FIBROSIS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TIME FACTORS;

MUS;

EID: 43349089429     PISSN: 03603997     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10753-008-9062-6     Document Type: Article

References (63)

1. Langhorne, J., P. Mombaerts, and S. Tonegawa. 1995. alpha beta and gamma delta T cells in the immune response to the erythrocytic stages of malaria in mice. Int. Immunol. 7:1005-1011.
2. Mombaerts, P., J. Arnoldi, F. Russ, S. Tonegawa, and S. H. Kaufmann. 1993. Different roles of alpha beta and gamma delta T cells in immunity against an intracellular bacterial pathogen. Nature 365:53-56.
3. Korn, T., M. Oukka, and E. Bettelli. 2007. Th17 cells: effector T cells with inflammatory properties. Semin. Immunol. 19:362-371.
4. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6:1133-1141.
5. Roark, C. L., J. D. French, M. A. Taylor, A. M. Bendele, W. K. Born, and R. L. O'Brien. 2007. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J. Immunol. 179:5576-5583.
6. Lockhart, E., A. M. Green, and J. L. Flynn. 2006. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177:4662-4669.
7. Kelly, M. N., J. K. Kolls, K. Happel, J. D. Schwartzman, P. Schwarzenberger, C. Combe, M. Moretto, and I. A. Khan. 2005. Interleukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection. Infect. Immun. 73:617-621.
8. Ye, P., P. B. Garvey, P. Zhang, S. Nelson, G. Bagby, W. R. Summer, P. Schwarzenberger, J. E. Shellito, and J. K. Kolls. 2001. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25:335-340.
9. Huang, W., L. Na, P. L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190:624-631.
10. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, J. E. Shellito, G. J. Bagby, S. Nelson, K. Charrier, J. J. Peschon, and J. K. Kolls. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194:519-527.
11. 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.
12. Bi, Y., G. Liu, and R. Yang. 2007. Th17 cell induction and immune regulatory effects. J. Cell. Physiol. 211:273-278.
13. Born, W. K., C. L. Reardon, and R. L. O'Brien. 2006. The function of gammadelta T cells in innate immunity. Curr. Opin. Immunol. 18:31-38.
14. Nanno, M., T. Shiohara, H. Yamamoto, K. Kawakami, and H. Ishikawa. 2007. gammadelta T cells: firefighters or fire boosters in the front lines of inflammatory responses. Immunol. Rev. 215:103-113.
15. Moore, T. A., B. B. Moore, M. W. Newstead, and T. J. Standiford. 2000. Gamma delta-T cells are critical for survival and early proinflammatory cytokine gene expression during murine Klebsiella pneumonia. J. Immunol. 165:2643-2650.
16. Takano, M., H. Nishimura, Y. Kimura, Y. Mokuno, J. Washizu, S. Itohara, Y. Nimura, and Y. Yoshikai. 1998. Protective roles of gamma delta T cells and interleukin-15 in Escherichia coli infection in mice. Infect. Immun. 66:3270-3278.
17. Nakamura, T., G. Matsuzaki, and K. Nomoto. 1999. The protective role of T-cell receptor Vgamma1+ T cells in primary infection with Listeria monocytogenes. Immunology 96:29-34.
18. Blum, R. H., S. K. Carter, and K. Agre. 1973. A clinical review of bleomycin-a new antineoplastic agent. Cancer 31:903-914.
19. Jones, A. W. 1978. Bleomycin lung damage: the pathology and nature of the lesion. Br. J. Dis. Chest 72:321-326.
20. Braun, R. K., A. Sterner-Kock, P. J. Kilshaw, D. A. Ferrick, and S. N. Giri. 1996. Integrin alpha E beta 7 expression on BAL CD4+, CD8+, and gamma delta T-cells in bleomycin-induced lung fibrosis in mouse. Eur. Respir. J. 9:673-679.
21. Thrall, R. S., and R. W. Barton. 1984. A comparison of lymphocyte populations in lung tissue and in bronchoalveolar lavage fluid of rats at various times during the development of bleomycin-induced pulmonary fibrosis. Am. Rev. Respir. Dis. 129:279-283.
22. Zhu, J., D. A. Cohen, S. N. Goud, and A. M. Kaplan. 1996. Contribution of T lymphocytes to the development of bleomycin-induced pulmonary fibrosis. Ann. N.Y. Acad. Sci. 796:194-202.
23. Raisfeld, I. H. 1980. Pulmonary toxicity of bleomycin analogs. Toxicol. Appl. Pharmacol. 56:326-336.
24. Creemers, L. B., D. C. Jansen, A. Veen-Reurings, B. T. van den, and V. Everts. 1997. Microassay for the assessment of low levels of hydroxyproline. Biotechniques 22:656-658.
25. Bolender, R. P., D. M. Hyde, and R. T. Dehoff. 1993. Lung morphometry: a new generation of tools and experiments for organ, tissue, cell, and molecular biology. Am. J. Physiol. 265:L521-L548.
26. Hyde, D. M., D. J. Magliano, E. Reus, N. K. Tyler, S. Nichols, and W. S. Tyler. 1992. Computer-assisted morphometry: point, intersection, and profile counting and three-dimensional reconstruction. Microsc. Res. Tech. 21:262-270.
27. Yang, H., P. A. Antony, B. E. Wildhaber, and D. H. Teitelbaum. 2004. Intestinal intraepithelial lymphocyte gammadelta-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse. J. Immunol. 172:4151-4158.
28. D'Souza, C. D., A. M. Cooper, A. A. Frank, R. J. Mazzaccaro, B. R. Bloom, and I. M. Orme. 1997. An anti-inflammatory role for gamma delta T lymphocytes in acquired immunity to Mycobacterium tuberculosis. J. Immunol. 158:1217-1221.
29. King, D. P., D. M. Hyde, K. A. Jackson, D. M. Novosad, T. N. Ellis, L. Putney, M. Y. Stovall, L. S. Van Winkle, B. L. Beaman, and D. A. Ferrick. 1999. Cutting edge: protective response to pulmonary injury requires gamma delta T lymphocytes. J. Immunol. 162:5033-5036.
30. Afzali, B., G. Lombardi, R. I. Lechler, and G. M. Lord. 2007. The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin. Exp. Immunol. 148:32-46.
31. Shin, H. C., N. Benbernou, S. Esnault, and M. Guenounou. 1999. Expression of IL-17 in human memory CD45RO+ T lymphocytes and its regulation by protein kinase A pathway. Cytokine 11:257-266.
32. Shibata, K., H. Yamada, H. Hara, K. Kishihara, and Y. Yoshikai. 2007. Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178:4466-4472.
33. Ferrick, D. A., D. P. King, K. A. Jackson, R. K. Braun, S. Tam, D. M. Hyde, and B. L. Beaman. 2000. Intraepithelial gamma delta T lymphocytes: sentinel cells at mucosal barriers. Springer Semin. Immunopathol 22:283-296.
34. Tam, S., D. P. King, and B. L. Beaman. 2001. Increase of {gamma}{delta} T Lymphocytes in murine lungs occurs during recovery from pulmonary infection by nocardia asteroides. Infect. Immun. 69:6165-6171.
35. Hsieh, B., M. D. Schrenzel, T. Mulvania, H. D. Lepper, L. DiMolfetto-Landon, and D. A. Ferrick. 1996. In vivo cytokine production in murine listeriosis. Evidence for immunoregulation by gamma delta+ T cells. J. Immunol. 156:232-237.
36. McKenzie, B. S., R. A. Kastelein, and D. J. Cua. 2005. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27:17-23.
37. Bowman, E. P., A. A. Chackerian, and D. J. Cua. 2006. Rationale and safety of anti-interleukin-23 and anti-interleukin-17A therapy. Curr. Opin. Infect. Dis. 19:245-252.
38. Rohn, T. A., G. T. Jennings, M. Hernandez, P. Grest, M. Beck, Y. Zou, M. Kopf, and M. F. Bachmann. 2006. Vaccination against IL-17 suppresses autoimmune arthritis and encephalomyelitis. Eur. J. Immunol. 36:2857-2867.
39. Schrier, D. J., S. H. Phan, and P. A. Ward. 1982. Cellular sensitivity to collagen in bleomycin-treated rats. J. Immunol. 129:2156-2159.
40. Kravis, T. C., A. Ahmed, T. E. Brown, J. D. Fulmer, and R. G. Crystal. 1976. Pathogenic mechanisms in pulmonary fibrosis: collagen-induced migration inhibition factor production and cytotoxicity mediated by lymphocytes. J. Clin. Invest. 58:1223-1232.
41. Nakos, G., A. Adams, and N. Andriopoulos. 1993. Antibodies to collagen in patients with idiopathic pulmonary fibrosis. Chest 103:1051-1058.
42. Collard, H. R., B. B. Moore, K. R. Flaherty, K. K. Brown, R. J. Kaner, T. E. King Jr., J. A. Lasky, J. E. Loyd, I. Noth, M. A. Olman, G. Raghu, J. Roman, J. H. Ryu, D. A. Zisman, G. W. Hunninghake, T. V. Colby, J. J. Egan, D. M. Hansell, T. Johkoh, N. Kaminski, D. S. Kim, Y. Kondoh, D. A. Lynch, J. Muller-Quernheim, J. L. Myers, A. G. Nicholson, M. Selman, G. B. Toews, A. U. Wells, and F. J. Martinez. 2007. Acute exacerbations of idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 176:636-643.
43. Adamson, I. Y. 1984. Drug-induced pulmonary fibrosis. Environ. Health Perspect. 55:25-36.
44. Ghosh, S., T. Mendoza, L. A. Ortiz, G. W. Hoyle, C. D. Fermin, A. R. Brody, M. Friedman, and G. F. Morris. 2002. Bleomycin sensitivity of mice expressing dominant-negative p53 in the lung epithelium. Am. J. Respir. Crit. Care Med. 166:890-897.
45. Serrano-Mollar, A., M. Nacher, G. Gay-Jordi, D. Closa, A. Xaubet, and O. Bulbena. 2007. Intratracheal transplantation of alveolar Type II cells reverse bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 176:1261-1268.
46. Watanabe, M., M. Ebina, F. M. Orson, A. Nakamura, K. Kubota, D. Koinuma, K. Akiyama, M. Maemondo, S. Okouchi, M. Tahara, K. Matsumoto, T. Nakamura, and T. Nukiwa. 2005. Hepatocyte growth factor gene transfer to alveolar septa for effective suppression of lung fibrosis. Mol. Ther. 12:58-67.
47. Yi, E. S., S. T. Williams, H. Lee, D. M. Malicki, E. M. Chin, S. Yin, J. Tarpley, and T. R. Ulich. 1996. Keratinocyte growth factor ameliorates radiation- and bleomycin-induced lung injury and mortality. Am. J. Pathol. 149:1963-1970.
48. Jameson, J., and W. L. Havran. 2007. Skin gammadelta T-cell functions in homeostasis and wound healing. Immunol. Rev. 215:114-122.
49. Chen, Y., K. Chou, E. Fuchs, W. L. Havran, and R. Boismenu. 2002. Protection of the intestinal mucosa by intraepithelial gamma delta T cells. Proc. Natl. Acad. Sci. U. S. A. 99:14338-14343.
50. Koohsari, H., M. Tamaoka, H. R. Campbell, and J. G. Martin. 2007. The role of gamma delta T cells in airway epithelial injury and bronchial responsiveness after chlorine gas exposure in mice. Respir. Res. 8:21.
51. Inoue, D., M. Numasaki, M. Watanabe, H. Kubo, T. Sasaki, H. Yasuda, M. Yamaya, and H. Sasaki. 2006. IL-17A promotes the growth of airway epithelial cells through ERK-dependent signaling pathway. Biochem. Biophys. Res. Commun. 347:852-858.
52. Manoury, B., S. Nenan, I. Guenon, V. Lagente, and E. Boichot. 2007. Influence of early neutrophil depletion on MMPs/TIMP-1 balance in bleomycin-induced lung fibrosis. Int. Immunopharmacol. 7:900-911.
53. Kolls, J. K., and A. Linden. 2004. Interleukin-17 family members and inflammation. Immunity. 21:467-476.
54. Hyde, D. M., L. A. Miller, R. J. McDonald, M. Y. Stovall, V. Wong, K. E. Pinkerton, C. D. Wegner, R. Rothlein, and C. G. Plopper. 1999. Neutrophils enhance clearance of necrotic epithelial cells in ozone-induced lung injury in rhesus monkeys. Am. J. Physiol. 277:L1190-L1198.
55. Liu, W., A. L. Putnam, Z. Xu-Yu, G. L. Szot, M. R. Lee, S. Zhu, P. A. Gottlieb, P. Kapranov, T. R. Gingeras, B. F. de St Groth, C. Clayberger, D. M. Soper, S. F. Ziegler, and J. A. Bluestone. 2006. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4(+) T reg cells. J. Exp. Med. 203:1701-1711.
56. Gunnarsson, M., S. M. Walther, T. Seidal, G. D. Bloom, and S. Lennquist. 1998. Exposure to chlorine gas: effects on pulmonary function and morphology in anaesthetised and mechanically ventilated pigs. J. Appl. Toxicol. 18:249-255.
57. Crouch, E. 1990. Pathobiology of pulmonary fibrosis. Am. J. Physiol. 259:159-184.
58. Eickelberg, O., A. Pansky, R. Mussmann, M. Bihl, M. Tamm, P. Hildebrand, A. P. Perruchoud, and M. Roth. 1999. Transforming growth factor-beta1 induces interleukin-6 expression via activating protein-1 consisting of JunD homodimers in primary human lung fibroblasts. J. Biol. Chem. 274:12933-12938.
59. Xing, Z., J. Gauldie, G. Cox, H. Baumann, M. Jordana, X. F. Lei, and M. K. Achong. 1998. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 101:311-320.
60. Gurujeyalakshmi, G., Y. Wang, and S. N. Giri. 2000. Taurine and niacin block lung injury and fibrosis by down-regulating bleomycin-induced activation of transcription nuclear factor-kappaB in mice. J. Pharmacol. Exp. Ther. 293:82-90.
61. Tabata, C., Y. Kadokawa, R. Tabata, M. Takahashi, K. Okoshi, Y. Sakai, M. Mishima, and H. Kubo. 2006. All-trans-retinoic acid prevents radiation- or bleomycin-induced pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 174:1352-1360.
62. Sener, G., N. Topaloglu, A. O. Sehirli, F. Ercan, and N. Gedik. 2007. Resveratrol alleviates bleomycin-induced lung injury in rats. Pulm. Pharmacol. Ther. 20:642-649.
63. Tabata, C., R. Tabata, Y. Kadokawa, S. Hisamori, M. Takahashi, M. Mishima, T. Nakano, and H. Kubo. 2007. Thalidomide prevents bleomycin-induced pulmonary fibrosis in mice. J. Immunol. 179:708-714.