Resident CD11b(+)Ly6C(-) Lung Dendritic Cells Are Responsible for Allergic Airway Sensitization to House Dust Mite in Mice.

Mesnil, Claire; Sabatel, Catherine; Marichal, Thomas; Toussaint, Marie; Cataldo, Didier; Drion, Pierre; Lekeux, Pierre; Bureau, Fabrice; Desmet, Christophe

doi:10.1371/journal.pone.0053242

Article (Scientific journals)

Resident CD11b(+)Ly6C(-) Lung Dendritic Cells Are Responsible for Allergic Airway Sensitization to House Dust Mite in Mice.

Mesnil, Claire; Sabatel, Catherine; Marichal, Thomas et al.

2012 • In PLoS ONE, 7 (12), p. 53242

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/142864

DOI
10.1371/journal.pone.0053242

PubMed
23300898

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

MesnilC_PloS One_2012.pdf

Publisher postprint (2.2 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Abstract :

[en] Conventional dendritic cells (DCs) are considered to be the prime initiators of airway allergy. Yet, it remains unclear whether specific DC subsets are preferentially involved in allergic airway sensitization. Here, we systematically assessed the respective pro-allergic potential of individually sorted lung DC subsets isolated from house dust mite antigen (HDM)-treated donor mice, following transfer to naive recipients. Transfer of lung CD11c(+)CD11b(+) DCs, but not CD11c(+)CD11b(-)CD103(+) DCs, was sufficient to prime airway allergy. The CD11c(+)CD11b(+) DC subpopulation was composed of CD11c(+)CD11b(+)Ly6C(+) inflammatory monocyte-derived cells, whose numbers increase in the lungs following HDM exposure, and of CD11c(+)CD11b(+)Ly6C(-) DCs, which remain stable. Counterintuitively, only CD11c(+)CD11b(+)Ly6C(-) DCs, and not CD11c(+)CD11b(+)Ly6C(+) DCs, were able to convey antigen to the lymph nodes and induce adaptive T cell responses and subsequent airway allergy. Our results thus support that lung resident non-inflammatory CD11c(+)CD11b(+)Ly6C(-) DCs are the essential inducers of allergic airway sensitization to the common aeroallergen HDM in mice.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Mesnil, Claire ^✱; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie

Sabatel, Catherine ^✱; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire

Marichal, Thomas ; Université de Liège - ULiège > GIGA-Research

Toussaint, Marie ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire

Cataldo, Didier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.

Drion, Pierre ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R:Méth. expér.des anim. de labo et éth. en expér. anim.

Lekeux, Pierre ; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie

Bureau, Fabrice ^✱; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire

Desmet, Christophe ^✱; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Resident CD11b(+)Ly6C(-) Lung Dendritic Cells Are Responsible for Allergic Airway Sensitization to House Dust Mite in Mice.

Publication date :

2012

Journal title :

PLoS ONE

eISSN :

1932-6203

Publisher :

Public Library of Science, San Franscisco, United States - California

Volume :

Issue :

Pages :

e53242

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 14 February 2013

Statistics

Number of views

172 (24 by ULiège)

Number of downloads

181 (5 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Locksley RM, (2010) Asthma and Allergic Inflammation. Cell 140: 777-783.
Lambrecht BN, Hammad H, (2009) Biology of lung dendritic cells at the origin of asthma. Immunity 31: 412-424.
Lambrecht BN, Hammad H, (2012) Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu Rev Immunol 30: 243-270.
Vermaelen KY, Carro-Muino I, Lambrecht BN, Pauwels RA, (2001) Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J Exp Med 193: 51-60.
Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA, et al. (2010) Inflammatory dendritic cells-not basophils-are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med 207: 2097-2111.
Sung S, Rose CE, Fu SM, (2001) Intratracheal priming with ovalbumin- and ovalbumin 323-339 peptide-pulsed dendritic cells induces airway hyperresponsiveness, lung eosinophilia, goblet cell hyperplasia, and inflammation. J Immunol 166: 1261-1271.
Lambrecht BN, De Veerman M, Coyle AJ, Gutierrez-Ramos JC, Thielemans K, et al. (2000) Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J Clin Invest 106: 551-559.
del Rio M-L, Rodriguez-Barbosa J-I, Kremmer E, Forster R, (2007) CD103- and CD103+ Bronchial Lymph Node Dendritic Cells Are Specialized in Presenting and Cross-Presenting Innocuous Antigen to CD4+ and CD8+ T Cells. J Immunol 178: 6861-6866.
Sung SS, Fu SM, Rose CE Jr, Gaskin F, Ju ST, et al. (2006) A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176: 2161-2172.
Raymond M, Rubio M, Fortin G, Shalaby KH, Hammad H, et al. (2009) Selective control of SIRP-α-positive airway dendritic cell trafficking through CD47 is critical for the development of TH2-mediated allergic inflammation. J Allergy Clin Immunol 124: 1333-1342.
Xu Y, Zhan Y, Lew AM, Naik SH, Kershaw MH, (2007) Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol 179: 7577-7584.
Greter M, Helft J, Chow A, Hashimoto D, Mortha A, et al. (2012) GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36: 1031-1046.
Nakano H, Free ME, Whitehead GS, Maruoka S, Wilson RH, et al. (2011) Pulmonary CD103(+) dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol 5: 53-65.
Tailor P, Tamura T, Morse HC, 3rd, Ozato K (2008) The BXH2 mutation in IRF8 differentially impairs dendritic cell subset development in the mouse. Blood 111: 1942-1945.
Turcotte K, Gauthier S, Tuite A, Mullick A, Malo D, et al. (2005) A mutation in the Icsbp1 gene causes susceptibility to infection and a chronic myeloid leukemia-like syndrome in BXH-2 mice. J Exp Med 201: 881-890.
Turcotte K, Gauthier S, Malo D, Tam M, Stevenson MM, et al. (2007) Icsbp1/IRF-8 is required for innate and adaptive immune responses against intracellular pathogens. J Immunol 179: 2467-2476.
van Rijt LS, Jung S, KleinJan A, Vos N, Willart M, et al. (2005) In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J Exp Med 201: 981-991.
GeurtsvanKessel CH, Willart MA, van Rijt LS, Muskens F, Kool M, et al. (2008) Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells. J Exp Med 205: 1621-1634.
Hebel K, Griewank K, Inamine A, Chang H-D, Müller-Hilke B, et al. (2006) Plasma cell differentiation in T-independent type 2 immune responses is independent of CD11chigh dendritic cells. Eur J Immunol 36: 2912-2919.
Tittel AP, Heuser C, Ohliger C, Llanto C, Yona S, et al. (2012) Functionally relevant neutrophilia in CD11c diphtheria toxin receptor transgenic mice. Nat Methods 9: 385-390.
Bedoret D, Wallemacq H, Marichal T, Desmet C, Quesada Calvo F, et al. (2009) Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J Clin Invest 119: 3723-3738.
Marichal T, Bedoret D, Mesnil C, Pichavant M, Goriely S, et al. (2010) Interferon response factor 3 is essential for house dust mite-induced airway allergy. J Allergy Clin Immunol 126: 836-844.
Cates EC, Fattouh R, Wattie J, Inman MD, Goncharova S, et al. (2004) Intranasal exposure of mice to house dust mite elicits allergic airway inflammation via a GM-CSF-mediated mechanism. J Immunol 173: 6384-6392.
Phipps S, Lam CE, Kaiko GE, Foo SY, Collison A, et al. (2009) Toll/IL-1 signaling is critical for house dust mite-specific helper T cell type 2 and type 17 responses. Am J Respir Crit Care Med 179: 883-893.
Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, et al. (2009) House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 15: 410-416.
Tan AM, Chen HC, Pochard P, Eisenbarth SC, Herrick CA, et al. (2010) TLR4 signaling in stromal cells is critical for the initiation of allergic Th2 responses to inhaled antigen. J Immunol 184: 3535-3544.
Robays LJ, Maes T, Lebecque S, Lira SA, Kuziel WA, et al. (2007) Chemokine receptor CCR2 but not CCR5 or CCR6 mediates the increase in pulmonary dendritic cells during allergic airway inflammation. J Immunol 178: 5305-5311.
Naik SH, Metcalf D, van Nieuwenhuijze A, Wicks I, Wu L, et al. (2006) Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7: 663-671.
Kool M, Soullie T, van Nimwegen M, Willart MA, Muskens F, et al. (2008) Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 205: 869-882.
Marichal T, Ohata K, Bedoret D, Mesnil C, Sabatel C, et al. (2011) DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 17: 996-1002.
Krishnamoorthy N, Oriss TB, Paglia M, Fei M, Yarlagadda M, et al. (2008) Activation of c-Kit in dendritic cells regulates T helper cell differentiation and allergic asthma. Nat Med 14: 565-573.
Lambrecht BN, Hammad H, (2010) The role of dendritic and epithelial cells as master regulators of allergic airway inflammation. Lancet 376: 835-843.
Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, et al. (2007) Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111.
GeurtsvanKessel CH, Lambrecht BN, (2008) Division of labor between dendritic cell subsets of the lung. Mucosal Immunol 1: 442-450.
Plantinga M, Hammad H, Lambrecht BN, (2010) Origin and functional specializations of DC subsets in the lung. Eur J Immunol 40: 2112-2118.
Beaty SR, Rose CE Jr, Sung SS, (2007) Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J Immunol 178: 1882-1895.
Medoff BD, Seung E, Hong S, Thomas SY, Sandall BP, et al. (2009) CD11b+ myeloid cells are the key mediators of Th2 cell homing into the airway in allergic inflammation. J Immunol 182: 623-635.
Julia V, Hessel EM, Malherbe L, Glaichenhaus N, O'Garra A, et al. (2002) A restricted subset of dendritic cells captures airborne antigens and remains able to activate specific T cells long after antigen exposure. Immunity 16: 271-283.
Thornton EE, Looney MR, Bose O, Sen D, Sheppard D, et al. (2012) Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J Exp Med 209: 1183-1199.
Ortiz-Stern A, Kanda A, Mionnet C, Cazareth J, Lazzari A, et al. (2011) Langerin+ dendritic cells are responsible for LPS-induced reactivation of allergen-specific Th2 responses in postasthmatic mice. Mucosal Immunol 4: 343-353.