Airway structural cells regulate TLR5-mediated mucosal adjuvant activity

Mucosal Immunology

Volumn 7, Issue 3, 2014, Pages 489-500

  Van Maele, L ^a,b,c,d   Fougeron, D ^a,b,c,d   Janot, L ^e,f   Didierlaurent, A ^g   Cayet, D ^a,b,c,d   Tabareau, J ^a,b,c,d   Rumbo, M ^h   Corvo Chamaillard, S ^a,b,c,d   Boulenouar, S ^a,b,c,d   Jeffs, S ⁱ   Walle, L Vande ^j,k   Lamkanfi, M ^j,k   Lemoine, Y ^a,b,c,d   Erard, F ^e,f   Hot, D ^a,b,c,d   Hussell, T ^g,l   Ryffel, B ^e,f   Benecke, A G ^c   Sirard, J C ^a,b,c,d  

^a INSERM U1019   (France)

^b Institut National de la Sante et de la RechercheMe dicale   (France)

^c CNRS   (France)

^d UNIV LILLE   (France)

^e University of Orle ans   (France)

^f Laboratoire d'Immunologie et Embryologie Moleculaires Orleans   (France)

^g NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^h FACULTAD DE CIENCIAS EXACTAS   (Argentina)

ⁱ IMPERIAL COLLEGE LONDON   (United Kingdom)

^j DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^k GHENT UNIVERSITY   (Belgium)

^l UNIVERSITY OF MANCHESTER   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXOID; FLAGELLIN; GLYCOPROTEIN GP 140; KEYHOLE LIMPET HEMOCYANIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; OVALBUMIN; TETANUS TOXOID; TOLL LIKE RECEPTOR 5;

ADAPTIVE IMMUNITY; AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; EX VIVO STUDY; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IMMUNOREGULATION; LUNG ALVEOLUS EPITHELIUM; LUNG PARENCHYMA; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; ANIMAL; ANTIGEN PRESENTING CELL; CELL LINE; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; KNOCKOUT MOUSE; METABOLISM; RESPIRATORY TRACT MUCOSA;

ADAPTIVE IMMUNITY; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGEN-PRESENTING CELLS; CELL LINE; FLAGELLIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, MUCOSAL; MICE; MICE, KNOCKOUT; PROTEOLYSIS; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 5;

EID: 84899580444     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2013.66     Document Type: Article

References (59)

1. Mbow, M.L., De Gregorio, E, Valiante, N.M. & Rappuoli, R. New adjuvants for human vaccines. Curr Opin Immunol 22, 411-416 (2010).
2. Marichal, T. et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 17, 996-1002 (2011).
3. Beutler, B. et al. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu Rev Immunol 24, 353-389 (2006).
4. Kufer, T.A. & Sansonetti, P.J. NLR functions beyond pathogen recognition. Nat Immunol 12, 121-128 (2011).
5. Moresco, E.M., LaVine, D & Beutler, B. Toll-like receptors. Curr Biol 21, R488-R493 (2011).
6. Abreu, M.T. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10, 131-144 (2010).
7. Helft, J, Ginhoux, F, Bogunovic, M & Merad, M. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol Rev 234, 55-75 (2010).
8. Sporri, R. Reis e Sousa C. Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion ofCD4+ Tcell populations lacking helper function. Nat Immunol 6, 163-170 (2005).
9. Sansonetti, P.J. War and peace at mucosal surfaces. Nat Rev Immunol 4, 953-964 (2004).
10. Lycke, N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 12, 592-605 (2012).
11. Woodrow, K.A., Bennett, K.M. & Lo, D.D. Mucosal vaccine design and delivery. Annu Rev Biomed Eng 14, 17-46 (2012).
12. Ramos, H.C., Rumbo, M & Sirard, J.C. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12, 509-517 (2004).
13. Lamkanfi, M & Dixit, V.M. Inflammasomes and their roles in health and disease. Annu Rev Cell Dev Biol 28, 137-161 (2012).
14. Sanders, C.J., Yu, Y, Moore, D.A. 3rd, Williams, I.R. & Gewirtz, A.T. Humoral immune response to flagellin requires T cells and activation of innate immunity. J Immunol 177, 2810-2818 (2006).
15. Didierlaurent, A. et al. Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J Immunol 172, 6922-6930 (2004).
16. McSorley, S.J., Ehst, B.D., Yu, Y & Gewirtz, A.T. Bacterial flagellin is an effective adjuvant for CD4(+) T cells in vivo. J Immunol 169, 3914-3919 (2002).
17. Vijay-Kumar, M, Carvalho, F.A., Aitken, J.D., Fifadara, N.H. & Gewirtz, A.T. TLR5 or NLRC4 is necessary and sufficient for promotion of humoral immunity by flagellin. Eur J Immunol 40, 3528-3534 (2010).
18. Nempont, C, Cayet, D, Rumbo, M, Bompard, C, Villeret, V & Sirard, J.C. Deletion of flagellin's hypervariable region abrogates antibody-mediated neutralization and systemic activation of TLR5-dependent immunity. J Immunol 181, 2036-2043 (2008).
19. Wilson, R.H. et al. The Toll-like receptor 5 ligand flagellin promotes asthma by priming allergic responses to indoor allergens. NatMed 18, 1705-1710 (2012).
20. Honko, A.N., Sriranganathan, N, Lees, C.J. & Mizel, S.B. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 74, 1113-1120 (2006).
21. Pino, O, Martin, M & Michalek, S.M. Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica Serovar Typhimurium to potentiate mucosal and systemic responses. Infect Immun 73, 6763-6770 (2005).
22. Uematsu, S. et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 9, 769-776 (2008).
23. VanMaele, L. et al. TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa. J Immunol 185, 1177-1185 (2010).
24. Kinnebrew, M.A. et al. Interleukin 23 production by intestinal CD103(+) CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 36, 276-287 (2012).
25. Sierro, F, Dubois, B, Coste, A, Kaiserlian, D, Kraehenbuhl, J.P. & Sirard, J.C. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci USA 98, 13722-13727 (2001).
26. Gewirtz, A.T. et al. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107, 99-109 (2001).
27. Fritz, J.H., Le Bourhis, L, Magalhaes, J.G. & Philpott, D.J. Innate immune recognition at the epithelial barrier drives adaptive immunity: APCs take the back seat. Trends Immunol 29, 41-49 (2008).
28. Janot, L. et al. Radioresistant cells expressing TLR5 control the respiratory epithelium's innate immune responses to flagellin. Eur J Immunol 39, 1587-1596 (2009).
29. Eilebrecht, S, Pellay, F.X., Odenwalder, P, Brysbaert, G, Benecke, B.J. & Benecke, A. EBER2 RNA-induced transcriptome changes identify cellular processes likely targeted during Epstein Barr Virus infection. BMC Res Notes 1, 100 (2008).
30. Noth, S, Brysbaert, G, Pellay, F.X. & Benecke, A. High-sensitivity transcriptome data structure and implications for analysis and biologic interpretation. Genomics Proteomics Bioinformatics 4, 212-229 (2006).
31. Anderle, P. et al. Novel markers of the human follicle-associated epithelium identified by genomic profiling and microdissection. Gastroenterol 129, 321-327 (2005).
32. Mizel, S.B. & Bates, J.T. Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 185, 5677-5682 (2010).
33. Miao, E.A. et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107, 3076-3080 (2010).
34. Lopez-Boado, Y.S., Espinola, M, Bahr, S & Belaaouaj, A. Neutrophil serine proteinases cleave bacterial flagellin, abrogating its host responseinducing activity. J Immunol 172, 509-515 (2004).
35. Vonderviszt, F, Uedaira, H, Kidokoro, S & Namba, K. Structural organization of flagellin. J Mol Biol 214, 97-104 (1990).
36. Le Borgne,M. et al. Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8(+) T cell crosspriming in vivo. Immunity 24, 191-201 (2006).
37. Eckmann, L, Kagnoff, M.F. & Fierer, J. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61, 4569-4574 (1993).
38. McCormick, B.A., Colgan, S.P., Delp-Archer, C, Miller, S.I. & Madara, J.L. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123, 895-907 (1993).
39. Evans, S.E., Xu, Y, Tuvim,M.J. & Dickey, B.F. Inducible innate resistance of lung epithelium to infection. Annu Rev Physiol 72, 413-435 (2010).
40. Feuillet, V. et al. Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci USA 103, 12487-12492 (2006).
41. Hammad, H, Chieppa, M, Perros, F, Willart, M.A., Germain, R.N. & Lambrecht, B.N. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 15, 410-416 (2009).
42. Nenci, A. et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446, 557-561 (2007).
43. Didierlaurent, A. et al. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 205, 323-329 (2008).
44. Sato, A & Iwasaki, A. Induction of antiviral immunity requires Toll-like receptor signaling in both stromal and dendritic cell compartments. Proc Natl Acad Sci USA 101, 16274-16279 (2004).
45. Hou, B, Reizis, B & DeFranco, A.L. Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and-extrinsic mechanisms. Immunity 29, 272-282 (2008).
46. Lee, H.C. & Ziegler, S.F. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkappaB. Proc Natl Acad Sci USA 104, 914-919 (2007).
47. Shang, L. et al. Toll-like receptor signaling in small intestinal epithelium promotes B-cell recruitment and IgA production in lamina propria. Gastroenterol 135, 529-538 (2008).
48. Pichavant, M. et al. Asthmatic bronchial epithelium activated by the proteolytic allergen Der p 1 increases selective dendritic cell recruitment. J Allergy Clin Immunol 115, 771-778 (2005).
49. Greter, M. et al. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36, 1031-1046 (2012).
50. Nolte, M.A., Leibundgut-Landmann, S, Joffre, O & Reis e Sousa, C. Dendritic cell quiescence during systemic inflammation driven by LPS stimulation of radioresistant cells in vivo. J Exp Med 204, 1487-1501 (2007).
51. Murray, P.J. & Smale, S.T. Restraint of inflammatory signaling by interdependent strata of negative regulatory pathways. Nat Immunol 13, 916-924 (2012).
52. Boone, D.L. et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 5, 1052-1060 (2004).
53. Oshima, N. et al. A20 is an early responding negative regulator of Toll-like receptor 5 signalling in intestinal epithelial cells during inflammation. Clin Exp Immunol 159, 185-198 (2010).
54. Vereecke, L. et al. Enterocyte-specific A20 deficiency sensitizes to tumor necrosis factor-induced toxicity and experimental colitis. J Exp Med 207, 1513-1523 (2010).
55. Gilchrist, M. et al. Activating transcription factor 3 is a negative regulator of allergic pulmonary inflammation. J Exp Med 205, 2349-2357 (2008).
56. Taylor, G.A. et al. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445-454 (1996).
57. Shaykhiev, R, Behr, J & Bals, R. Microbial patterns signaling via Toll-like receptors 2 and 5 contribute to epithelial repair, growth and survival. PLoS One 3, e1393 (2008).
58. Burdelya, L.G. et al. An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 320, 226-230 (2008).
59. Munoz, N, Van Maele, L, Marques, J.M., Rial, A, Sirard, J.C. & Chabalgoity, J.A. Mucosal administration of flagellin protects mice from Streptococcus pneumoniae lung infection. Infect Immun 78, 4226-4233 (2010).