Regulatory T cells prevent Inducible BALT formation by dampening neutrophilic inflammation

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4567-4576

  Foo, Shen Yun ^a   Zhang, Vivian ^b   Lalwani, Amit ^b   Lynch, Jason P ^b   Zhuang, Aowen ^b   Lam, Chuan En ^a   Foster, Paul S ^a   King, Cecile ^c   Steptoe, Raymond J ^b   Mazzone, Stuart B ^b   Sly, Peter D ^b   Phipps, Simon ^b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; CXCL13 CHEMOKINE; CXCL9 CHEMOKINE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23P19; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYMPHOTOXIN; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SECONDARY LYMPHOID TISSUE CHEMOKINE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; FEMALE; INDUCIBLE BRONCHUS ASSOCIATED LYMPHOID TISSUE; INFLAMMATION; LYMPHOID TISSUE; MEDIASTINUM LYMPH NODE; MOUSE; MURINE PNEUMONIA VIRUS; NEUTROPHIL; NEUTROPHILIA; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; UPREGULATION; VIRUS LOAD; VIRUS PNEUMONIA; ANIMAL; BIOSYNTHESIS; IMMUNOLOGY; LYMPHOCYTE DEPLETION; MALE; METABOLISM; PATHOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; ANIMALS, NEWBORN; CELLULAR MICROENVIRONMENT; CYTOKINES; INFLAMMATION; LIPOPOLYSACCHARIDES; LYMPHOCYTE DEPLETION; LYMPHOID TISSUE; MALE; MICE; NEUTROPHILS; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 13;

EID: 84928473425     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400909     Document Type: Article

References (54)

1. Rangel-Moreno, J., L. Hartson, C. Navarro, M. Gaxiola, M. Selman, and T. D. Randall. 2006. Inducible bronchus-associated lymphoid tissue (iBALT) in patients with pulmonary complications of rheumatoid arthritis. J. Clin. Invest. 116: 3183-3194.
2. Chvatchko, Y., M. H. Kosco-Vilbois, S. Herren, J. Lefort, and J. Y. Bonnefoy. 1996. Germinal center formation and local immunoglobulin E (IgE) production in the lung after an airway antigenic challenge. J. Exp. Med. 184: 2353-2360.
3. Moyron-Quiroz, J. E., J. Rangel-Moreno, K. Kusser, L. Hartson, F. Sprague, S. Goodrich, D. L. Woodland, F. E. Lund, and T. D. Randall. 2004. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 10: 927-934.
4. Wiley, J. A., L. E. Richert, S. D. Swain, A. Harmsen, D. L. Barnard, T. D. Randall, M. Jutila, T. Douglas, C. Broomell, M. Young, and A. Harmsen. 2009. Inducible bronchus-associated lymphoid tissue elicited by a protein cage nanoparticle enhances protection in mice against diverse respiratory viruses. PLoS One 4: e7142. Available at: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0007142.
5. Halle, S., H. C. Dujardin, N. Bakocevic, H. Fleige, H. Danzer, S. Willenzon, Y. Suezer, G. Hämmerling, N. Garbi, G. Sutter, et al. 2009. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J. Exp. Med. 206: 2593-2601.
6. Corbett, M., and J. P. Kraehenbuhl. 2004. Lung immunity: necessity is the mother of induction. Nat. Med. 10: 904-905.
7. Foo, S. Y., and S. Phipps. 2010. Regulation of inducible BALT formation and contribution to immunity and pathology. Mucosal Immunol. 3: 537-544.
8. Emery, J. L., and F. Dinsdale. 1973. The postnatal development of lymphoreticular aggregates and lymph nodes in infants' lungs. J. Clin. Pathol. 26: 539-545.
9. Tschernig, T., W. J. Kleemann, and R. Pabst. 1995. Bronchus-associated lymphoid tissue (BALT) in the lungs of children who had died from sudden infant death syndrome and other causes. Thorax 50: 658-660.
10. Mebius, R. E. 2003. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3: 292-303.
11. Sawa, S., M. Cherrier, M. Lochner, N. Satoh-Takayama, H. J. Fehling, F. Langa, J. P. Di Santo, and G. Eberl. 2010. Lineage relationship analysis of RORgammat + innate lymphoid cells. Science 330: 665-669.
12. Rangel-Moreno, J., D. M. Carragher, M. de la Luz Garcia-Hernandez, J. Y. Hwang, K. Kusser, L. Hartson, J. K. Kolls, S. A. Khader, and T. D. Randall. 2011. The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat. Immunol. 12: 639-646.
13. Lochner, M., C. Ohnmacht, L. Presley, P. Bruhns, M. Si-Tahar, S. Sawa, and G. Eberl. 2011. Microbiota-induced tertiary lymphoid tissues aggravate inflammatory disease in the absence of RORgamma t and LTi cells. J. Exp. Med. 208: 125-134.
14. Peters, A., L. A. Pitcher, J. M. Sullivan, M. Mitsdoerffer, S. E. Acton, B. Franz, K. Wucherpfennig, S. Turley, M. C. Carroll, R. A. Sobel, et al. 2011. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 35: 986-996.
15. Kocks, J. R., A. C. Davalos-Misslitz, G. Hintzen, L. Ohl, and R. Förster. 2007. Regulatory T cells interfere with the development of bronchus-associated lymphoid tissue. J. Exp. Med. 204: 723-734.
16. Aggarwal, S., N. Ghilardi, M. H. Xie, F. J. de Sauvage, and A. L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278: 1910-1914.
17. McGeachy, M. J., Y. Chen, C. M. Tato, A. Laurence, B. Joyce-Shaikh, W. M. Blumenschein, T. K. McClanahan, J. J. O'Shea, and D. J. Cua. 2009. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10: 314-324.
18. O'Sullivan, B. J., H. E. Thomas, S. Pai, P. Santamaria, Y. Iwakura, R. J. Steptoe, T. W. Kay, and R. Thomas. 2006. IL-1 beta breaks tolerance through expansion of CD25+ effector T cells. J. Immunol. 176: 7278-7287.
19. Pasare, C., and R. Medzhitov. 2003. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
20. Attridge, K., C. J. Wang, L. Wardzinski, R. Kenefeck, J. L. Chamberlain, C. Manzotti,M. Kopf, and L. S.Walker. 2012. IL-21 inhibits T cell IL-2 production and impairs Treg homeostasis. Blood 119: 4656-4664. doi: 4610.1182/blood-2011-4610-388546.
21. Kim, J. M., J. P. Rasmussen, and A. Y. Rudensky. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8: 191-197.
22. Davidson, S., G. Kaiko, Z. Loh, A. Lalwani, V. Zhang, K. Spann, S. Y. Foo, N. Hansbro, S. Uematsu, S. Akira, et al. 2011. Plasmacytoid dendritic cells promote host defense against acute pneumovirus infection via the TLR7-MyD88-dependent signaling pathway. J. Immunol. 186: 5938-5948.
23. McGuire, H. M., S. Walters, A. Vogelzang, C. M. Lee, K. E. Webster, J. Sprent, D. Christ, S. Grey, and C. King. 2011. Interleukin-21 is critically required in autoimmune and allogeneic responses to islet tissue in murine models. Diabetes 60: 867-875.
24. Lührmann, A., T. Tschernig, and R. Pabst. 2002-2003. Stimulation of bronchus-associated lymphoid tissue in rats by repeated inhalation of aerosolized lipopeptide MALP-2. Pathobiology 70: 266-269.
25. Toyoshima, M., K. Chida, and A. Sato. 2000. Antigen uptake and subsequent cell kinetics in bronchus-associated lymphoid tissue. Respirology 5: 141-145.
26. Chen, X., M. Bäumel, D. N. Männel, O. M. Howard, and J. J. Oppenheim. 2007. Interaction of TNF with TNF receptor type 2 promotes expansion and function of mouse CD4+CD25+ T regulatory cells. J. Immunol. 179: 154-161.
27. Khader, S. A., G. K. Bell, J. E. Pearl, J. J. Fountain, J. Rangel-Moreno, G. E. Cilley, F. Shen, S. M. Eaton, S. L. Gaffen, S. L. Swain, et al. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8: 369-377.
28. Joshi, A. D., D. J. Fong, S. R. Oak, G. Trujillo, K. R. Flaherty, F. J. Martinez, and C. M. Hogaboam. 2009. Interleukin-17-mediated immunopathogenesis in experimental hypersensitivity pneumonitis. Am. J. Respir. Crit. Care Med. 179: 705-716.
29. Hartl, D., S. Krauss-Etschmann, B. Koller, P. L. Hordijk, T. W. Kuijpers, F. Hoffmann, A. Hector, E. Eber, V. Marcos, I. Bittmann, et al. 2008. Infiltrated neutrophils acquire novel chemokine receptor expression and chemokine responsiveness in chronic inflammatory lung diseases. J. Immunol. 181: 8053-8067.
30. Seiler, P., P. Aichele, S. Bandermann, A. E. Hauser, B. Lu, N. P. Gerard, C. Gerard, S. Ehlers, H. J. Mollenkopf, and S. H. Kaufmann. 2003. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur. J. Immunol. 33: 2676-2686.
31. Kelsen, S. G., M. O. Aksoy, M. Georgy, R. Hershman, R. Ji, X. Li, M. Hurford, C. Solomides, W. Chatila, and V. Kim. 2009. Lymphoid follicle cells in chronic obstructive pulmonary disease overexpress the chemokine receptor CXCR3. Am. J. Respir. Crit. Care Med. 179: 799-805.
32. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70.
33. Puga, I., M. Cols, C. M. Barra, B. He, L. Cassis, M. Gentile, L. Comerma, A. Chorny, M. Shan, W. Xu, et al. 2012. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13: 170-180.
34. Tschernig, T., and R. Pabst. 2000. Bronchus-associated lymphoid tissue (BALT) is not present in the normal adult lung but in different diseases. Pathobiology 68: 1-8.
35. Sue-Chu, M., E. M. Karjalainen, A. Altraja, A. Laitinen, L. A. Laitinen, A. B. Naess, L. Larsson, and L. Bjermer. 1998. Lymphoid aggregates in endobronchial biopsies from young elite cross-country skiers. Am. J. Respir. Crit. Care Med. 158: 597-601.
36. Kaiko, G. E., Z. Loh, K. Spann, J. P. Lynch, A. Lalwani, Z. Zheng, S. Davidson, S. Uematsu, S. Akira, J. Hayball, et al. 2013. Toll-like receptor 7 gene deficiency and early-life Pneumovirus infection interact to predispose toward the development of asthma-like pathology in mice. J. Allergy Clin. Immunol. 131: 1331-1339.e10.
37. Fontenot, J. D., J. L. Dooley, A. G. Farr, and A. Y. Rudensky. 2005. Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 202: 901-906.
38. Atarashi, K., T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, Y. Momose, G. Cheng, S. Yamasaki, T. Saito, Y. Ohba, et al. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-341.
39. Rangel-Moreno, J., J. E. Moyron-Quiroz, L. Hartson, K. Kusser, and T. D. Randall. 2007. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. Proc. Natl. Acad. Sci. USA 104: 10577-10582.
40. GeurtsvanKessel, C. H., M. A. Willart, I. M. Bergen, L. S. van Rijt, F. Muskens, D. Elewaut, A. D. Osterhaus, R. Hendriks, G. F. Rimmelzwaan, and B. N. Lambrecht. 2009. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J. Exp. Med. 206: 2339-2349.
41. Grumelli, S., D. B. Corry, L.-Z. Song, L. Song, L. Green, J. Huh, J. Hacken, R. Espada, R. Bag, D. E. Lewis, and F. Kheradmand. 2004. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med. 1: e8. Available at: http://journals.plos.org/plosmedicine/article?id=10.1371/journal.pmed.0010008.
42. Yang, C. W., B. S. Strong, M. J. Miller, and E. R. Unanue. 2010. Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J. Immunol. 185: 2927-2934.
43. Mantovani, A., M. A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11: 519-531.
44. van Gisbergen, K. P., M. Sanchez-Hernandez, T. B. Geijtenbeek, and Y. van Kooyk. 2005. Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 201: 1281-1292.
45. Das, A., L. Kole, L. Wang, R. Barrios, B. Moorthy, and A. K. Jaiswal. 2006. BALT development and augmentation of hyperoxic lung injury in mice deficient in NQO1 and NQO2. Free Radic. Biol. Med. 40: 1843-1856.
46. Shomer, N. H., J. G. Fox, A. E. Juedes, and N. H. Ruddle. 2003. Helicobacter-induced chronic active lymphoid aggregates have characteristics of tertiary lymphoid tissue. Infect. Immun. 71: 3572-3577.
47. Singh, P., Z. Z. Coskun, C. Goode, A. Dean, L. Thompson-Snipes, and G. Darlington. 2008. Lymphoid neogenesis and immune infiltration in aged liver. Hepatology 47: 1680-1690.
48. Pabst, R., D. Durak, A. Roos, A. Lührmann, and T. Tschernig. 2009. TLR2/6 stimulation of the rat lung: effects on lymphocyte subsets, natural killer cells and dendritic cells in different parts of the air-conducting compartments and at different ages. Immunology 126: 132-139.
49. Bracke, K. R., F. M. Verhamme, L. J. Seys, C. Bantsimba-Malanda, D. M. Cunoosamy, R. Herbst, H. Hammad, B. N. Lambrecht, G. F. Joos, and G. G. Brusselle. 2013. Role of CXCL13 in cigarette smoke-induced lymphoid follicle formation and chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 188: 343-355.
50. Odoardi, F., C. Sie, K. Streyl, V. K. Ulaganathan, C. Schläger, D. Lodygin, K. Heckelsmiller, W. Nietfeld, J. Ellwart, W. E. Klinkert, et al. 2012. T cells become licensed in the lung to enter the central nervous system. Nature 488: 675-679.
51. Schwaller, J., P. Schneider, P. Mhawech-Fauceglia, T. McKee, S. Myit, T. Matthes, J. Tschopp, O. Donze, F. A. Le Gal, and B. Huard. 2007. Neutrophil-derived APRIL concentrated in tumor lesions by proteoglycans correlates with human B-cell lymphoma aggressiveness. Blood 109: 331-338.
52. Hardenberg, G., L. van Bostelen, M. Hahne, and J. P. Medema. 2008. Thymus-independent class switch recombination is affected by APRIL. Immunol. Cell Biol. 86: 530-534.
53. Huard, B., T. McKee, C. Bosshard, S. Durual, T. Matthes, S. Myit, O. Donze, C. Frossard, C. Chizzolini, C. Favre, et al. 2008. APRIL secreted by neutrophils binds to heparan sulfate proteoglycans to create plasma cell niches in human mucosa. J. Clin. Invest. 118: 2887-2895.
54. Kimberley, F. C., L. van Bostelen, K. Cameron, G. Hardenberg, J. A. Marquart, M. Hahne, and J. P. Medema. 2009. The proteoglycan (heparan sulfate proteoglycan) binding domain of APRIL serves as a platform for ligand multimerization and cross-linking. FASEB J. 23: 1584-1595.