Flagellin suppresses experimental asthma by generating regulatory dendritic cells and T cells

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 2, 2016, Pages 426-435

  Shim, Jae Uoong ^a   Lee, Shee Eun ^b   Hwang, Won ^c,e   Lee, Changhon ^e,f   Park, Jung Won ^d   Sohn, Jung Ho ^d   Nam, Jong Hee ^a   Kim, Young ^a   Rhee, Joon Haeng ^a   Im, Sin Hyeog ^e,f   Koh, Young Il ^a  

^a Chonnam National University Medical School   (South Korea)

^b Chonnam National University   (South Korea)

^c Gwangju Institute of Science and Technology (GIST)   (South Korea)

^d Yonsei University College of Medicine   (South Korea)

^e Institute for Basic Science   (South Korea)

^f Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Asthma; dendritic cells; flagellin; regulatory T cells; Toll like receptor 5

Indexed keywords

BASILIXIMAB; CD14 ANTIGEN; FLAGELLIN; FLAGELLIN B; INTERLEUKIN 10; OVALBUMIN; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG; ALLERGEN; FLAB FLAGELLIN; LIGAND;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DERMATOPHAGOIDES; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG INHIBITION; DRUG MEGADOSE; EXPERIMENTAL ASTHMA; FEMALE; HOUSE DUST ALLERGY; HUMAN; HUMAN CELL; INCUBATION TIME; LOW DRUG DOSE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY DENDRITIC CELL; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; TH1 CELL; TH17 CELL; TH2 CELL; VIBRIO VULNIFICUS; WILD TYPE; ADOPTIVE TRANSFER; ANIMAL; ASTHMA; CASE CONTROL STUDY; DISEASE MODEL; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PYROGLYPHIDAE;

ADOPTIVE TRANSFER; ALLERGENS; ANIMALS; ASTHMA; CASE-CONTROL STUDIES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; FLAGELLIN; IMMUNOMODULATION; LIGANDS; MICE; MICE, KNOCKOUT; OVALBUMIN; PYROGLYPHIDAE; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTOR 5;

EID: 84957936317     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.07.010     Document Type: Article

References (47)

1. C.M. Lloyd, and E.M. Hessel Functions of T cells in asthma: more than just T(H)2 cells Nat Rev Immunol 10 2010 838 848
2. W. Eder, M.J. Ege, and E. von Mutius The asthma epidemic N Engl J Med 355 2006 2226 2235
3. S.T. Holgate The epidemic of allergy and asthma Nature 402 1999 B2 B4
4. E. von Mutius, and D. Vercelli Farm living: effects on childhood asthma and allergy Nat Rev Immunol 10 2010 861 868
5. T. Shirakawa, T. Enomoto, S. Shimazu, and J.M. Hopkin The inverse association between tuberculin responses and atopic disorder Science 275 1997 77 79
6. G. Hansen, V.P. Yeung, G. Berry, D.T. Umetsu, and R.H. DeKruyff Vaccination with heat-killed Listeria as adjuvant reverses established allergen-induced airway hyperreactivity and inflammation: role of CD8+ T cells and IL-18 J Immunol 164 2000 223 230
7. S.O. Shaheen, P. Aaby, A.J. Hall, D.J. Barker, C.B. Heyes, A.W. Shiell, and et al. Measles and atopy in Guinea-Bissau Lancet 347 1996 1792 1796
8. H. Qiu, R. Kuolee, G. Harris, H. Zhou, H. Miller, G.B. Patel, and et al. Acinetobacter baumannii infection inhibits airway eosinophilia and lung pathology in a mouse model of allergic asthma PLoS One 6 2011 e22004
9. I.C. Arnold, N. Dehzad, S. Reuter, H. Martin, B. Becher, C. Taube, and et al. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells J Clin Invest 121 2011 3088 3093
10. R.H. Wilson, S. Maruoka, G.S. Whitehead, J.F. Foley, G.P. Flake, M.L. Sever, and et al. The Toll-like receptor 5 ligand flagellin promotes asthma by priming allergic responses to indoor allergens Nat Med 18 2012 1705 1710
11. S.E. Lee, S.Y. Kim, B.C. Jeong, Y.R. Kim, S.J. Bae, O.S. Ahn, and et al. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity Infect Immun 74 2006 694 702
12. S.E. Lee, Y.I. Koh, M.K. Kim, Y.R. Kim, S.Y. Kim, J.H. Nam, and et al. Inhibition of airway allergic disease by co-administration of flagellin with allergen J Clin Immunol 28 2008 157 165
13. S. Schulke, M. Burggraf, Z. Waibler, A. Wangorsch, S. Wolfheimer, U. Kalinke, and et al. A fusion protein of flagellin and ovalbumin suppresses the TH2 response and prevents murine intestinal allergy J Allergy Clin Immunol 128 2011 1340 1348.e12
14. S.W. Lun, C.K. Wong, F.W. Ko, D.S. Hui, and C.W. Lam Expression and functional analysis of toll-like receptors of peripheral blood cells in asthmatic patients: implication for immunopathological mechanism in asthma J Clin Immunol 29 2009 330 342
15. C. Roduit, J. Wohlgensinger, R. Frei, S. Bitter, C. Bieli, S. Loeliger, and et al. Prenatal animal contact and gene expression of innate immunity receptors at birth are associated with atopic dermatitis J Allergy Clin Immunol 127 2011 179 185.e1
16. M. Hedl, and C. Abraham Negative regulation of human mononuclear phagocyte function Mucosal Immunol 6 2013 205 223
17. F. Nomura, S. Akashi, Y. Sakao, S. Sato, T. Kawai, M. Matsumoto, and et al. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression J Immunol 164 2000 3476 3479
18. A.H. Dalpke, M.D. Lehner, T. Hartung, and K. Heeg Differential effects of CpG-DNA in Toll-like receptor-2/-4/-9 tolerance and cross-tolerance Immunology 116 2005 203 212
19. S.C. Eisenbarth, D.A. Piggott, J.W. Huleatt, I. Visintin, C.A. Herrick, and K. Bottomly Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen J Exp Med 196 2002 1645 1651
20. C.D. Codispoti, L. Levin, G.K. LeMasters, P. Ryan, T. Reponen, M. Villareal, and et al. Breast-feeding, aeroallergen sensitization, and environmental exposures during infancy are determinants of childhood allergic rhinitis J Allergy Clin Immunol 125 2010 1054 1060.e1
21. J.T. Bates, S. Uematsu, S. Akira, and S.B. Mizel Direct stimulation of tlr5+/+ CD11c+ cells is necessary for the adjuvant activity of flagellin J Immunol 182 2009 7539 7547
22. L. Cosmi, F. Liotta, E. Maggi, S. Romagnani, and F. Annunziato Th17 cells: new players in asthma pathogenesis Allergy 66 2011 989 998
23. A.E. Morelli, and A.W. Thomson Tolerogenic dendritic cells and the quest for transplant tolerance Nat Rev Immunol 7 2007 610 621
24. A.L. Mellor, and D.H. Munn IDO expression by dendritic cells: tolerance and tryptophan catabolism Nat Rev Immunol 4 2004 762 774
25. S. Sharma, S.C. Yang, L. Zhu, K. Reckamp, B. Gardner, F. Baratelli, and et al. Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer Cancer Res 65 2005 5211 5220
26. J. Karman, J.L. Jiang, N. Gumlaw, H. Zhao, J. Campos-Rivera, J. Sancho, and et al. Ligation of cytotoxic T lymphocyte antigen-4 to T cell receptor inhibits T cell activation and directs differentiation into Foxp3+ regulatory T cells J Biol Chem 287 2012 11098 11107
27. X. Cao, S.F. Cai, T.A. Fehniger, J. Song, L.I. Collins, D.R. Piwnica-Worms, and et al. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance Immunity 27 2007 635 646
28. G. Amodio, and S. Gregori Human tolerogenic DC-10: perspectives for clinical applications Transplant Res 1 2012 14
29. Proceedings of the ATS workshop on refractory asthma: current understanding, recommendations, and unanswered questions. American Thoracic Society Am J Respir Crit Care Med 162 2000 2341 2351
30. C.M. Hilkens, and J.D. Isaacs Tolerogenic dendritic cell therapy for rheumatoid arthritis: where are we now? Clin Exp Immunol 172 2013 148 157
31. Z. Calamita, H. Saconato, A.B. Pela, and A.N. Atallah Efficacy of sublingual immunotherapy in asthma: systematic review of randomized-clinical trials using the Cochrane Collaboration method Allergy 61 2006 1162 1172
32. M.H. Shamji, and S.R. Durham Mechanisms of immunotherapy to aeroallergens Clin Exp Allergy 41 2011 1235 1246
33. T.A. Le, T. Takai, A.T. Vu, H. Kinoshita, X. Chen, S. Ikeda, and et al. Flagellin induces the expression of thymic stromal lymphopoietin in human keratinocytes via toll-like receptor 5 Int Arch Allergy Immunol 155 2011 31 37
34. K. Maneechotesuwan, V. Wamanuttajinda, K. Kasetsinsombat, S. Huabprasert, M. Yaikwawong, P.J. Barnes, and et al. Der p 1 suppresses indoleamine 2, 3-dioxygenase in dendritic cells from house dust mite-sensitive patients with asthma J Allergy Clin Immunol 123 2009 239 248
35. S. Provoost, T. Maes, Y.M. van Durme, P. Gevaert, C. Bachert, C.B. Schmidt-Weber, and et al. Decreased FOXP3 protein expression in patients with asthma Allergy 64 2009 1539 1546
36. S. Schulke, Z. Waibler, M.S. Mende, G. Zoccatelli, S. Vieths, M. Toda, and et al. Fusion protein of TLR5-ligand and allergen potentiates activation and IL-10 secretion in murine myeloid DC Mol Immunol 48 2010 341 350
37. O. Akbari, R.H. DeKruyff, and D.T. Umetsu Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen Nat Immunol 2 2001 725 731
38. J. Kearley, J.E. Barker, D.S. Robinson, and C.M. Lloyd Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+CD25+ regulatory T cells is interleukin 10 dependent J Exp Med 202 2005 1539 1547
39. H. Huang, W. Dawicki, X. Zhang, J. Town, and J.R. Gordon Tolerogenic dendritic cells induce CD4+CD25hiFoxp3+ regulatory T cell differentiation from CD4+CD25-/loFoxp3- effector T cells J Immunol 185 2010 5003 5010
40. X. Li, A. Yang, H. Huang, X. Zhang, J. Town, B. Davis, and et al. Induction of type 2 T helper cell allergen tolerance by IL-10-differentiated regulatory dendritic cells Am J Respir Cell Mol Biol 42 2010 190 199
41. D.J. Johnson, and P.S. Ohashi Molecular programming of steady-state dendritic cells: impact on autoimmunity and tumor immune surveillance Ann N Y Acad Sci 1284 2013 46 51
42. Hammad H. Presentation at the 2015 Keystone Symposium on "Dendritic cells and macrophages reunited." March 8-15, 2015, Montreal, Canada.
43. M. Akdis, K. Blaser, and C.A. Akdis T regulatory cells in allergy: novel concepts in the pathogenesis, prevention, and treatment of allergic diseases J Allergy Clin Immunol 116 2005 961 969
44. R.L. Coffman, D.A. Lebman, and B. Shrader Transforming growth factor beta specifically enhances IgA production by lipopolysaccharide-stimulated murine B lymphocytes J Exp Med 170 1989 1039 1044
45. Y. Cong, T. Feng, K. Fujihashi, T.R. Schoeb, and C.O. Elson A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota Proc Natl Acad Sci U S A 106 2009 19256 19261
46. S. Lankford, C. Petty, A. LaVoy, S. Reckling, W. Tompkins, and G.A. Dean Cloning of feline FOXP3 and detection of expression in CD4+CD25+ regulatory T cells Vet Immunol Immunopathol 122 2008 159 166
47. N.K. Crellin, R.V. Garcia, O. Hadisfar, S.E. Allan, T.S. Steiner, and M.K. Levings Human CD4+ T cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4+CD25+ T regulatory cells J Immunol 175 2005 8051 8059