Enhanced production of CCL18 by tolerogenic dendritic cells is associated with inhibition of allergic airway reactivity

Journal of Allergy and Clinical Immunology

Volumn 130, Issue 6, 2012, Pages 1384-1393

  Bellinghausen, Iris ^a   Reuter, Sebastian ^a   Martin, Helen ^a   Maxeiner, Joachim ^a   Luxemburger, Uli ^a   Türeci, Özlem ^a   Grabbe, Stephan ^a   Taube, Christian ^a,b   Saloga, Joachim ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

allergy; Chemokines; dendritic cells; humanized mice; regulation; TH1 TH2 cells

Indexed keywords

ALLERGEN; CHEMOKINE RECEPTOR CCL18; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 5; OX40 LIGAND; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG;

ALLERGIC AIRWAY REACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY PLETHYSMOGRAPHY; CD4+ T LYMPHOCYTE; CELL ASSAY; CELL MATURATION; CELL PROLIFERATION; CHEMOTAXIS; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE ASSOCIATION; DONOR; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; LUNG LAVAGE; MONOCYTE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT ALLERGY; TH2 CELL; TOLEROGENIC DENDRITIC CELL; UPREGULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CHEMOKINES, CC; COCULTURE TECHNIQUES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-10; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICROARRAY ANALYSIS; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTES, REGULATORY; TRANSCRIPTOME;

EID: 84870297310     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2012.08.039     Document Type: Article

References (30)

1. M. Akdis, J. Verhagen, A. Taylor, F. Karamloo, C. Karagiannidis, and R. Crameri Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells J Exp Med 199 2004 1567 1575
2. C. Ozdemir, M. Akdis, and C.A. Akdis T regulatory cells and their counterparts: masters of immune regulation Clin Exp Allergy 39 2009 626 639
3. M.K. Levings, S. Gregori, E. Tresoldi, S. Cazzaniga, C. Bonini, and M.G. Roncarolo Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells Blood 105 2005 1162 1169
4. I. Bellinghausen, B. König, I. Böttcher, J. Knop, and J. Saloga Inhibition of human allergic T-helper type 2 immune responses by induced regulatory T cells requires the combination of interleukin-10-treated dendritic cells and transforming growth factor-beta for their induction Clin Exp Allergy 36 2006 1546 1555
5. K. Wu, Y. Bi, K. Sun, and C. Wang IL-10-producing type 1 regulatory T cells and allergy Cell Mol Immunol 4 2007 269 275
6. O. Palomares, G. Yaman, A.K. Azkur, T. Akkoc, M. Akdis, and C.A. Akdis Role of Treg in immune regulation of allergic diseases Eur J Immunol 40 2010 1232 1240
7. A. Terashima, H. Watarai, S. Inoue, E. Sekine, R. Nakagawa, and K. Hase A novel subset of mouse NKT cells bearing the IL-17 receptor B responds to IL-25 and contributes to airway hyperreactivity J Exp Med 205 2008 2727 2733
8. Y. Tasaki, S. Fukuda, M. Iio, R. Miura, T. Imai, and S. Sugano Chemokine PARC gene (SCYA18) generated by fusion of two MIP-1alpha/LD78alpha-like genes Genomics 55 1999 353 357
9. G.J. Adema, F. Hartgers, R. Verstraten, E. de Vries, G. Marland, and S. Menon A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells Nature 387 1997 713 717
10. E. Schutyser, A. Richmond, and J. Van Damme Involvement of CC chemokine ligand 18 (CCL18) in normal and pathological processes J Leukoc Biol 78 2005 14 26
11. J. Auer, M. Blass, H. Schulze-Koops, S. Russwurm, T. Nagel, and J.R. Kalden Expression and regulation of CCL18 in synovial fluid neutrophils of patients with rheumatoid arthritis Arthritis Res Ther 9 2007 R94
12. M. Goebeler, A. Trautmann, A. Voss, E.V. Brocker, A. Toksoy, and R. Gillitzer Differential and sequential expression of multiple chemokines during elicitation of allergic contact hypersensitivity Am J Pathol 158 2001 431 440
13. K. Pochetuhen, I.G. Luzina, V. Lockatell, J. Choi, N.W. Todd, and S.P. Atamas Complex regulation of pulmonary inflammation and fibrosis by CCL18 Am J Pathol 171 2007 428 437
14. S. Peterson, J.A. Poposki, D.R. Nagarkar, R.T. Chustz, A.T. Peters, and L.A. Suh Increased expression of CC chemokine ligand 18 in patients with chronic rhinosinusitis with nasal polyps J Allergy Clin Immunol 129 2012 119 127
15. P. de Nadai, A.S. Charbonnier, C. Chenivesse, S. Senechal, C. Fournier, and J. Gilet Involvement of CCL18 in allergic asthma J Immunol 176 2006 6286 6293
16. V. Kodelja, C. Muller, O. Politz, N. Hakij, C.E. Orfanos, and S. Goerdt Alternative macrophage activation-associated CC-chemokine-1, a novel structural homologue of macrophage inflammatory protein-1 alpha with a Th2-associated expression pattern J Immunol 160 1998 1411 1418
17. C. Gunther, C. Bello-Fernandez, T. Kopp, J. Kund, N. Carballido-Perrig, and S. Hinteregger CCL18 is expressed in atopic dermatitis and mediates skin homing of human memory T cells J Immunol 174 2005 1723 1728
18. H. Martin, S. Reuter, N. Dehzad, A. Heinz, I. Bellinghausen, and J. Saloga CD4-mediated regulatory T-cell activation inhibits the development of disease in a humanized mouse model of allergic airway disease J Allergy Clin Immunol 129 2012 521 528
19. B. Weigmann, N. Schughart, C. Wiebe, S. Sudowe, H.A. Lehr, and H. Jonuleit Allergen-induced IgE-dependent gut inflammation in a human PBMC-engrafted murine model of allergy J Allergy Clin Immunol 129 2012 1126 1135
20. I. Bellinghausen, U. Brand, K. Steinbrink, A.H. Enk, J. Knop, and J. Saloga Inhibition of human allergic T cell responses by interleukin-10-treated dendritic cells: differences from hydrocortisone-treated dendritic cells J Allergy Clin Immunol 108 2001 242 249
21. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408
22. S.F. Ziegler FOXP3: of mice and men Annu Rev Immunol 24 2006 209 226
23. A.Y. Rudensky Regulatory T cells and Foxp3 Immunol Rev 241 2011 260 268
24. R. Wang, L. Kozhaya, F. Mercer, A. Khaitan, H. Fujii, and D. Unutmaz Expression of GARP selectively identifies activated human FOXP3+ regulatory T cells Proc Natl Acad Sci U S A 106 2009 13439 13444
25. M. Vulcano, S. Struyf, P. Scapini, M. Cassatella, S. Bernasconi, and R. Bonecchi Unique regulation of CCL18 production by maturing dendritic cells J Immunol 170 2003 3843 3849
26. A. Pardo, K.M. Smith, J. Abrams, R. Coffman, M. Bustos, and T.K. McClanahan CCL18/DC-CK-1/PARC up-regulation in hypersensitivity pneumonitis J Leukoc Biol 70 2001 610 616
27. I. Azzaoui, S.A. Yahia, Y. Chang, H. Vorng, O. Morales, and Y. Fan CCL18 differentiates dendritic cells in tolerogenic cells able to prime regulatory T cells in healthy subjects Blood 118 2011 3549 3558
28. Y. Chang, N.P. de, I. Azzaoui, O. Morales, N. Delhem, and H. Vorng The chemokine CCL18 generates adaptive regulatory T cells from memory CD4+ T cells of healthy but not allergic subjects FASEB J 24 2010 5063 5072
29. R.J. Nibbs, T.W. Salcedo, J.D. Campbell, X.T. Yao, Y. Li, and B. Nardelli C-C chemokine receptor 3 antagonism by the beta-chemokine macrophage inflammatory protein 4, a property strongly enhanced by an amino-terminal alanine-methionine swap J Immunol 164 2000 1488 1497
30. O. Bruna-Romero, J. Schmieg, M. Del Val, M. Buschle, and M. Tsuji The dendritic cell-specific chemokine, dendritic cell-derived CC chemokine 1, enhances protective cell-mediated immunity to murine malaria J Immunol 170 2003 3195 3203