TGF-β-dependent dendritic cell chemokinesis in murine models of airway disease

Journal of Immunology

Volumn 195, Issue 3, 2015, Pages 1182-1190

  Hashimoto, Mitsuo ^a   Yanagisawa, Haruhiko ^a   Minagawa, Shunsuke ^a   Sen, Debasish ^a   Ma, Royce ^a   Murray, Lynne A ^b,c   Tsui, Ping ^b   Lou, Jianlong ^a   Marks, James D ^a   Baron, Jody L ^a   Krummel, Matthew F ^a   Nishimura, Stephen L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MEDIMMUNE   (United States)

^c MEDIMMUNE LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAVBETA8 INTEGRIN; CELL PROTEIN; CHEMOKINE RECEPTOR CCR6; CIGARETTE SMOKE; INTEGRIN; INTERLEUKIN 1BETA; PROTEIN ITGB8; TOLL LIKE RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CCL20 PROTEIN, MOUSE; CCR6 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; INTEGRIN ALPHAVBETA8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; POLYINOSINIC POLYCYTIDYLIC ACID; SMOKE; TLR3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHEMOKINESIS; CHEMOTAXIS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CYTOKINE RESPONSE; DENDRITIC CELL; LUNG CIRCULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADAPTIVE IMMUNITY; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL MOTION; DISEASE MODEL; ENZYME ACTIVATION; FIBROBLAST; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; PATHOLOGY; RADIOGRAPHY; SMOKE;

ADAPTIVE IMMUNITY; ANIMALS; CELL MOVEMENT; CHEMOKINE CCL20; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FIBROBLASTS; INTEGRINS; INTERLEUKIN-1BETA; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLY I-C; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RECEPTORS, CCR6; SMOKE; TOLL-LIKE RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA;

EID: 84937690765     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500348     Document Type: Article

References (50)

1. Miniño, A. M., J. Xu, and K. D. Kochanek. 2010. Deaths: preliminary data for 2008. Natl. Vital Stat. Rep. 59: 1-52.
2. Ito, K., M. Ito, W. M. Elliott, B. Cosio, G. Caramori, O. M. Kon, A. Barczyk, S. Hayashi, I. M. Adcock, J. C. Hogg, and P. J. Barnes. 2005. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N. Engl. J. Med. 352: 1967-1976.
3. Postma, D. S., and W. Timens. 2006. Remodeling in asthma and chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 3: 434-439.
4. Araya, J., S. Cambier, J. A. Markovics, P. Wolters, D. Jablons, A. Hill, W. Finkbeiner, K. Jones, V. C. Broaddus, D. Sheppard, et al. 2007. Squamous metaplasia amplifies pathologic epithelial-mesenchymal interactions in COPD patients. J. Clin. Invest. 117: 3551-3562.
5. Papi, A., C. M. Bellettato, F. Braccioni, M. Romagnoli, P. Casolari, G. Caramori, L. M. Fabbri, and S. L. Johnston. 2006. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am. J. Respir. Crit. Care Med. 173: 1114-1121.
6. Lucattelli, M., S. Cicko, T. Müller, M. Lommatzsch, G. De Cunto, S. Cardini, W. Sundas, M. Grimm, R. Zeiser, T. Dürk, et al. 2011. P2X7 receptor signaling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am. J. Respir. Cell Mol. Biol. 44: 423-429.
7. Geraghty, P., A. J. Dabo, and J. D'Armiento. 2011. TLR4 protein contributes to cigarette smoke-induced matrix metalloproteinase-1 (MMP-1) expression in chronic obstructive pulmonary disease. J. Biol. Chem. 286: 30211-30218.
8. Kang, M. J., C. G. Lee, J. Y. Lee, C. S. Dela Cruz, Z. J. Chen, R. Enelow, and J. A. Elias. 2008. Cigarette smoke selectively enhances viral PAMP- and virusinduced pulmonary innate immune and remodeling responses in mice. J. Clin. Invest. 118: 2771-2784.
9. Churg, A., S. Zhou, X. Wang, R. Wang, and J. L. Wright. 2009. The role of interleukin-1b in murine cigarette smoke-induced emphysema and small airway remodeling. Am. J. Respir. Cell Mol. Biol. 40: 482-490.
10. Doz, E., N. Noulin, E. Boichot, I. Guénon, L. Fick, M. Le Bert, V. Lagente, B. Ryffel, B. Schnyder, V. F. Quesniaux, and I. Couillin. 2008. Cigarette smokeinduced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J. Immunol. 180: 1169-1178.
11. Kolb, M., P. J. Margetts, D. C. Anthony, F. Pitossi, and J. Gauldie. 2001. Transient expression of IL-1b induces acute lung injury and chronic repair leading to pulmonary fibrosis. J. Clin. Invest. 107: 1529-1536.
12. Mu, D., S. Cambier, L. Fjellbirkeland, J. L. Baron, J. S. Munger, H. Kawakatsu, D. Sheppard, V. C. Broaddus, and S. L. Nishimura. 2002. The integrin avb8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-b1. J. Cell Biol. 157: 493-507.
13. Munger, J. S., J. G. Harpel, F. G. Giancotti, and D. B. Rifkin. 1998. Interactions between growth factors and integrins: latent forms of transforming growth factor-b are ligands for the integrin avb1. Mol. Biol. Cell 9: 2627-2638.
14. Wipff, P. J., D. B. Rifkin, J. J. Meister, and B. Hinz. 2007. Myofibroblast contraction activates latent TGF-b1 from the extracellular matrix. J. Cell Biol. 179: 1311-1323.
15. Munger, J. S., X. Huang, H. Kawakatsu, M. J. Griffiths, S. L. Dalton, J. Wu, J. F. Pittet, N. Kaminski, C. Garat, M. A. Matthay, et al. 1999. The integrin avb6 binds and activates latent TGF b1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96: 319-328.
16. Aluwihare, P., Z. Mu, Z. Zhao, D. Yu, P. H.Weinreb, G. S. Horan, S. M. Violette, and J. S. Munger. 2009. Mice that lack activity of avb6- and avb8-integrins reproduce the abnormalities of Tgfb1- and Tgfb3-null mice. J. Cell Sci. 122: 227-232.
17. Kitamura, H., S. Cambier, S. Somanath, T. Barker, S. Minagawa, J. Markovics, A. Goodsell, J. Publicover, L. Reichardt, D. Jablons, et al. 2011. Mouse and human lung fibroblasts regulate dendritic cell trafficking, airway inflammation, and fibrosis through integrin avb8-mediated activation of TGF-b. J. Clin. Invest. 121: 2863-2875.
18. Kudo, M., A. C. Melton, C. Chen, M. B. Engler, K. E. Huang, X. Ren, Y. Wang, X. Bernstein, J. T. Li, K. Atabai, et al. 2012. IL-17A produced by ab T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat. Med. 18: 547-554.
19. Melton, A. C., S. L. Bailey-Bucktrout, M. A. Travis, B. T. Fife, J. A. Bluestone, and D. Sheppard. 2010. Expression of avb8 integrin on dendritic cells regulates Th17 cell development and experimental autoimmune encephalomyelitis in mice. J. Clin. Invest. 120: 4436-4444.
20. Travis, M. A., B. Reizis, A. C. Melton, E. Masteller, Q. Tang, J. M. Proctor, Y. Wang, X. Bernstein, X. Huang, L. F. Reichardt, et al. 2007. Loss of integrin avb8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449: 361-365.
21. Minagawa, S., J. Lou, R. I. Seed, A. Cormier, S. Wu, Y. Cheng, L. Murray, P. Tsui, J. Connor, R. Herbst, et al. 2014. Selective targeting of TGF-b activation to treat fibroinflammatory airway disease. Sci. Transl. Med. 6: 241ra279. doi: 10.1126/scitranslmed.3008074
22. Brand, O. J., S. Somanath, C. Moermans, H. Yanagisawa, M. Hashimoto, S. Cambier, J. Markovics, A. J. Bondesson, A. Hill, D. Jablons, et al. 2015. Transforming growth factor-b and interleukin-1b signaling pathways converge on the chemokine ccl20 promoter. J. Biol. Chem. 290: 14717-14728.
23. Demedts, I. K., K. R. Bracke, G. Van Pottelberge, D. Testelmans, G. M. Verleden, F. E. Vermassen, G. F. Joos, and G. G. Brusselle. 2007. Accumulation of dendritic cells and increased CCL20 levels in the airways of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 175: 998-1005.
24. Bracke, K. R., A. I. D'hulst, T. Maes, K. B. Moerloose, I. K. Demedts, S. Lebecque, G. F. Joos, and G. G. Brusselle. 2006. Cigarette smoke-induced pulmonary inflammation and emphysema are attenuated in CCR6-deficient mice. J. Immunol. 177: 4350-4359.
25. Aubert, J. D., B. I. Dalal, T. R. Bai, C. R. Roberts, S. Hayashi, and J. C. Hogg. 1994. Transforming growth factor beta 1 gene expression in human airways. Thorax 49: 225-232.
26. Schroder, K., R. Zhou, and J. Tschopp. 2010. The NLRP3 inflammasome: a sensor for metabolic danger? Science 327: 296-300.
27. Lambrecht, B. N., and H. Hammad. 2009. Biology of lung dendritic cells at the origin of asthma. Immunity 31: 412-424.
28. Hashimoto, M., H. Yanagisawa, S. Minagawa, D. Sen, A. Goodsell, R. Ma, C. Moermans, K. J. McKnelly, J. L. Baron, M. F. Krummel, and S. L. Nishimura. 2015. A critical role for dendritic cells in the evolution of IL-1b-mediated murine airway disease. J. Immunol. 194: 3962-3969.
29. Zhang, N., and M. J. Bevan. 2012. TGF-b signaling to T cells inhibits autoimmunity during lymphopenia-driven proliferation. Nat. Immunol. 13: 667-673.
30. Vignola, A. M., P. Chanez, G. Chiappara, A. Merendino, E. Pace, A. Rizzo, A. M. la Rocca, V. Bellia, G. Bonsignore, and J. Bousquet. 1997. Transforming growth factor-b expression in mucosal biopsies in asthma and chronic bronchitis. Am. J. Respir. Crit. Care Med. 156: 591-599.
31. Border, W. A., and N. A. Noble. 1994. Transforming growth factor b in tissue fibrosis. N. Engl. J. Med. 331: 1286-1292.
32. Thornton, E. E., M. R. Looney, O. Bose, D. Sen, D. Sheppard, R. Locksley, X. Huang, and M. F. Krummel. 2012. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J. Exp. Med. 209: 1183-1199.
33. Lindquist, R. L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M. L. Dustin, and M. C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5: 1243-1250.
34. Ganter, M. T., J. Roux, B. Miyazawa, M. Howard, J. A. Frank, G. Su, D. Sheppard, S. M. Violette, P. H. Weinreb, G. S. Horan, et al. 2008. Interleukin-1b causes acute lung injury via avb5 and avb6 integrin-dependent mechanisms. Circ. Res. 102: 804-812.
35. Hogg, J. C., F. Chu, S. Utokaparch, R. Woods, W. M. Elliott, L. Buzatu, R. M. Cherniack, R. M. Rogers, F. C. Sciurba, H. O. Coxson, and P. D. Paré. 2004. The nature of small-Airway obstruction in chronic obstructive pulmonary disease. N. Engl. J. Med. 350: 2645-2653.
36. Saxton, M. J. 1997. Single-particle tracking: the distribution of diffusion coefficients. Biophys. J. 72: 1744-1753.
37. Saxton, M. J., and K. Jacobson. 1997. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26: 373-399.
38. Miller, M. J., S. H. Wei, I. Parker, and M. D. Cahalan. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296: 1869-1873.
39. Thurlbeck, W. M., and A. Churg. 2005. Thurlbeck's Pathology of the Lung. Thieme, New York.
40. Holt, P. G., S. Haining, D. J. Nelson, and J. D. Sedgwick. 1994. Origin and steady-state turnover of class II MHC-bearing dendritic cells in the epithelium of the conducting airways. J. Immunol. 153: 256-261.
41. Kallal, L. E., M. A. Schaller, D. M. Lindell, S. A. Lira, and N. W. Lukacs. 2010. CCL20/CCR6 blockade enhances immunity to RSV by impairing recruitment of DC. Eur. J. Immunol. 40: 1042-1052.
42. Phadke, A. P., G. Akangire, S. J. Park, S. A. Lira, and B. Mehrad. 2007. The role of CC chemokine receptor 6 in host defense in a model of invasive pulmonary aspergillosis. Am. J. Respir. Crit. Care Med. 175: 1165-1172.
43. Ballesteros-Tato, A., B. León, F. E. Lund, and T. D. Randall. 2010. Temporal changes in dendritic cell subsets, cross-priming and costimulation via CD70 control CD8+ T cell responses to influenza. Nat. Immunol. 11: 216-224.
44. Lambrecht, B. N., and H. Hammad. 2012. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu. Rev. Immunol. 30: 243-270.
45. Kisseleva, T., M. Cong, Y. Paik, D. Scholten, C. Jiang, C. Benner, K. Iwaisako, T. Moore-Morris, B. Scott, H. Tsukamoto, et al. 2012. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc. Natl. Acad. Sci. USA 109: 9448-9453.
46. Moeller, A., K. Ask, D. Warburton, J. Gauldie, and M. Kolb. 2008. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis? Int. J. Biochem. Cell Biol. 40: 362-382.
47. Araya, J., and S. L. Nishimura. 2010. Fibrogenic reactions in lung disease. Annu. Rev. Pathol. 5: 77-98.
48. Irvin, C. G., and J. H. Bates. 2003. Measuring the lung function in the mouse: the challenge of size. Respir. Res. 4: 4.
49. Araya, J., S. Cambier, A. Morris, W. Finkbeiner, and S. L. Nishimura. 2006. Integrin-mediated transforming growth factor-beta activation regulates homeostasis of the pulmonary epithelial-mesenchymal trophic unit. Am. J. Pathol. 169: 405-415.
50. Zheng, B., Z. Zhang, C. M. Black, B. de Crombrugghe, and C. P. Denton. 2002. Ligand-dependent genetic recombination in fibroblasts : a potentially powerful technique for investigating gene function in fibrosis. Am. J. Pathol. 160: 1609-1617.