Interferon response factor-3 promotes the pro-Th2 activity of mouse lung CD11b+ conventional dendritic cells in response to house dust mite allergens

Janss, T.; Mesnil, C.; Pirottin, Dimitri; Lemaitre, P.; Marichal, Thomas; Bureau, Fabrice; Desmet, Christophe

doi:10.1002/eji.201646513

Article (Scientific journals)

Interferon response factor-3 promotes the pro-Th2 activity of mouse lung CD11b+ conventional dendritic cells in response to house dust mite allergens

Janss, T.; Mesnil, C.; Pirottin, Dimitri et al.

2016 • In European Journal of Immunology, 46 (11), p. 2614-2628

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/265051

DOI
10.1002/eji.201646513

PubMed
27546168

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Keywords :

Allergy; Dendritic cell; House dust mite; Interferon response factor 3; Th2; Transcription factor; CD11b antigen; Irf3 protein, mouse; Article; Dermatophagoides; Th2 cell; Administration, Intranasal; Allergens; Animals; Antigens, CD11b; Antigens, Dermatophagoides; Cell Differentiation; Dendritic Cells; Interferon Regulatory Factor-3; Lung; Mice; Mice, Knockout; Microarray Analysis; Phenotype; Th2 Cells; Transcription Factors

Abstract :

[en] Very few transcription factors have been identified that are required by antigen-presenting cells (APCs) to induce T helper type 2 (Th2) responses. Because lung CD11b+ conventional dendritic cells (CD11b+ cDCs) are responsible for priming Th2 responses in house-dust mite (HDM)-induced airway allergy, we used them as a model to identify transcriptional events regulating the pro-Th2 activity of cDCs. Transcriptomic profiling of lung CD11b+ cDCs exposed to HDM in vivo revealed first that HDM triggers an antiviral defence-like response, and second that the majority of HDM-induced transcriptional changes depend on the transcription factor Interferon Response Factor-3 (Irf3). Validating the functional relevance of these observations, Irf3-deficient CD11b+ cDCs displayed reduced pro-allergic activity. Indeed, Irf3-deficient CD11b+ cDCs induced less Th2, more regulatory T cell, and similar Th1 differentiation in naïve CD4+ T cells compared to their wild-type counterparts. The altered APC activity of Irf3 CD11b+ cDCs was associated with reduced expression of CD86 and was phenocopied by blocking CD86 activity in wild-type CD11b+ cDCs. Altogether, these results establish Irf3, known mostly for its role in antiviral responses, as a transcription factor involved in the induction of Th2 responses through the promotion of pro-Th2 costimulation in CD11b+ DCs. © 2016 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Janss, T.; Laboratory of Cellular and Molecular Immunology, GIGA-I3, GIGA-Research Center and Faculty of Veterinary Medicine, University of LiegeLiege, Belgium

Mesnil, C.; Laboratory of Cellular and Molecular Immunology, GIGA-I3, GIGA-Research Center and Faculty of Veterinary Medicine, University of LiegeLiege, Belgium

Pirottin, Dimitri ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Département des sciences fonctionnelles (DSF)

Lemaitre, P.; Laboratory of Cellular and Molecular Immunology, GIGA-I3, GIGA-Research Center and Faculty of Veterinary Medicine, University of LiegeLiege, Belgium

Marichal, Thomas ; Université de Liège - ULiège > Physiologie générale et des systèmes

Bureau, Fabrice ^✱; Université de Liège - ULiège > Vice-Recteur à la Recherche

Desmet, Christophe ^✱; Université de Liège - ULiège > GIGA I3 - Cellular and Molecular Immunology

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Interferon response factor-3 promotes the pro-Th2 activity of mouse lung CD11b+ conventional dendritic cells in response to house dust mite allergens

Publication date :

2016

Journal title :

European Journal of Immunology

ISSN :

0014-2980

eISSN :

1521-4141

Publisher :

John Wiley & Sons, United Kingdom

Volume :

Issue :

Pages :

2614-2628

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 16 November 2021

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Bibliography

Paul, W. E. and Zhu, J., How are T(H)2-type immune responses initiated and amplified? Nat Rev Immunol 2010. 10: 225–235.
Tjota, M. Y. and Sperling, A. I., Distinct dendritic cell subsets actively induce Th2 polarization. Curr Opin Immunol 2014. 31c: 44–50.
Phythian-Adams, A. T., Cook, P. C., Lundie, R. J., Jones, L. H., Smith, K. A., Barr, T. A., Hochweller et al., CD11c depletion severely disrupts Th2 induction and development in vivo. J Exp Med 2010. 207: 2089–2096.
Kitajima, M. and Ziegler, S. F., Cutting edge: identification of the thymic stromal lymphopoietin-responsive dendritic cell subset critical for initiation of type 2 contact hypersensitivity. J Immunol 2013. 191: 4903–4907.
van Rijt, L. S., Jung, S., Kleinjan, A., Vos, N., Willart, M., Duez, C., Hoogsteden et al., In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J Exp Med 2005. 201: 981–991.
Guilliams, M., Ginhoux, F., Jakubzick, C., Naik, S. H., Onai, N., Schraml, B. U., Segura, E. et al., Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 2014. 14: 571–578.
Schraml, B. U., van Blijswijk, J., Zelenay, S., Whitney, P. G., Filby, A., Acton, S. E., Rogers et al., Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 2013. 154: 843–858.
Hildner, K., Edelson, B. T., Purtha, W. E., Diamond, M., Matsushita, H., Kohyama, M., Calderon, B., Schraml, B. U. et al., Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008. 322: 1097–1100.
Edelson, B. T., Kc, W., Juang, R., Kohyama, M., Benoit, L. A., Klekotka, P. A., Moon, C., Albring, J. C. et al., Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 2010. 207: 823–836.
Suzuki, S., Honma, K., Matsuyama, T., Suzuki, K., Toriyama, K., Akitoyo, I., Yamamoto, K. et al., Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha- dendritic cell development. Proc Natl Acad Sci U S A 2004. 101: 8981–8986.
Gao, Y., Nish, S. A., Jiang, R., Hou, L., Licona-Limon, P., Weinstein, J. S., Zhao et al., Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 2013. 39: 722–732.
Schlitzer, A., McGovern, N., Teo, P., Zelante, T., Atarashi, K., Low, D., Ho, A. W. et al., IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 2013. 38: 970–983.
Vander Lugt, B., Khan, A. A., Hackney, J. A., Agrawal, S., Lesch, J., Zhou, M., Lee, W. P. et al., Transcriptional programming of dendritic cells for enhanced MHC class II antigen presentation. Nat Immunol 2014. 15: 161–167.
Briseno, C. G., Murphy, T. L. and Murphy, K. M., Complementary diversification of dendritic cells and innate lymphoid cells. Curr Opin Immunol 2014. 29: 69–78.
Mesnil, C., Sabatel, C. M., Marichal, T., Toussaint, M., Cataldo, D., Drion, P. V., Lekeux, P. et al., Resident CD11b(+)Ly6C(-) lung dendritic cells are responsible for allergic airway sensitization to house dust mite in mice. PLoS One 2012. 7: e53242.
Plantinga, M., Guilliams, M., Vanheerswynghels, M., Deswarte, K., Branco-Madeira, F., Toussaint, W., Vanhoutte, L. et al., Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 2013. 38: 322–335.
Bell, B. D., Kitajima, M., Larson, R. P., Stoklasek, T. A., Dang, K., Sakamoto, K., Wagner, K. U. et al., The transcription factor STAT5 is critical in dendritic cells for the development of TH2 but not TH1 responses. Nat Immunol 2013. 14: 364–371.
Zhou, Q., Ho, A. W., Schlitzer, A., Tang, Y., Wong, K. H., Wong, F. H., Chua, Y. L. et al., GM-CSF-licensed CD11b+ lung dendritic cells orchestrate Th2 immunity to Blomia tropicalis. J Immunol 2014. 193: 496–509.
Tussiwand, R., Everts, B., Grajales-Reyes, G. E., Kretzer, N. M., Iwata, A., Bagaitkar, J., Wu, X. et al., Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 2015. 42: 916–928.
Liang, H. E., Reinhardt, R. L., Bando, J. K., Sullivan, B. M., Ho, I. C. and Locksley, R. M., Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol 2012. 13: 58–66.
Stumbles, P. A., Thomas, J. A., Pimm, C. L., Lee, P. T., Venaille, T. J., Proksch, S. and Holt, P. G., Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J Exp Med 1998. 188: 2019–2031.
Zhu, J., Jankovic, D., Oler, A. J., Wei, G., Sharma, S., Hu, G., Guo, L. et al., The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 2012. 37: 660–673.
van Rijt, L. S., Vos, N., Willart, M., Kleinjan, A., Coyle, A. J., Hoogsteden, H. C. and Lambrecht, B. N., Essential role of dendritic cell CD80/CD86 costimulation in the induction, but not reactivation, of TH2 effector responses in a mouse model of asthma. J Allergy Clin Immunol 2004. 114: 166–173.
Chu, D. K., Llop-Guevara, A., Walker, T. D., Flader, K., Goncharova, S., Boudreau, J. E., Moore, C. L. et al., IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol 2013. 131: 187–200 e181-188.
Diehl, S. and Rincon, M., The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol 2002. 39: 531–536.
Laouini, D., Alenius, H., Bryce, P., Oettgen, H., Tsitsikov, E. and Geha, R. S., IL-10 is critical for Th2 responses in a murine model of allergic dermatitis. J Clin Invest 2003. 112: 1058–1066.
Molofsky, A. B., Savage, A. K. and Locksley, R. M., Interleukin-33 in tissue homeostasis, injury, and inflammation. Immunity 2015. 42: 1005–1019.
Dillon, S., Agrawal, A., Van Dyke, T., Landreth, G., McCauley, L., Koh, A., Maliszewski, C. et al., A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells. J Immunol 2004. 172: 4733–4743.
Gringhuis, S. I., Kaptein, T. M., Wevers, B. A., Mesman, A. W. and Geijtenbeek, T. B., Fucose-specific DC-SIGN signalling directs T helper cell type-2 responses via IKKepsilon- and CYLD-dependent Bcl3 activation. Nat Commun 2014. 5: 3898.
Williams, J. W., Tjota, M. Y., Clay, B. S., Vander Lugt, B., Bandukwala, H. S., Hrusch, C. L., Decker, D. C. et al., Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat Commun 2013. 4: 2990.
Marichal, T., Bedoret, D., Mesnil, C., Pichavant, M., Goriely, S., Trottein, F., Cataldo, D. et al., Interferon response factor 3 is essential for house dust mite-induced airway allergy. J Allergy Clin Immunol 2010. 126: 836–844 e813.
Jaffar, Z. H., Stanciu, L., Pandit, A., Lordan, J., Holgate, S. T. and Roberts, K., Essential role for both CD80 and CD86 costimulation, but not CD40 interactions, in allergen-induced Th2 cytokine production from asthmatic bronchial tissue: role for alphabeta, but not gammadelta, T cells. J Immunol 1999. 163: 6283–6291.
Larche, M., Till, S. J., Haselden, B. M., North, J., Barkans, J., Corrigan, C. J., Kay, A. B. et al., Costimulation through CD86 is involved in airway antigen-presenting cell and T cell responses to allergen in atopic asthmatics. J Immunol 1998. 161: 6375–6382.
Gautier, G., Humbert, M., Deauvieau, F., Scuiller, M., Hiscott, J., Bates, E. E., Trinchieri et al., A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 2005. 201: 1435–1446.
Le Bon, A., Etchart, N., Rossmann, C., Ashton, M., Hou, S., Gewert, D. et al., Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 2003. 4: 1009–1015.
Huber, J. P., Gonzales-van Horn, S. R., Roybal, K. T., Gill, M. A. and Farrar, J. D., IFN-alpha suppresses GATA3 transcription from a distal exon and promotes H3K27 trimethylation of the CNS-1 enhancer in human Th2 cells. J Immunol 2014. 192: 5687–5694.
Al-Garawi, A., Fattouh, R., Botelho, F., Walker, T. D., Goncharova, S., Moore, C. L., Mori, M. et al., Influenza A facilitates sensitization to house dust mite in infant mice leading to an asthma phenotype in adulthood. Mucosal Immunol 2011. 4: 682–694.
Siegle, J. S., Hansbro, N., Herbert, C., Rosenberg, H. F., Domachowske, J. B., Asquith, K. L., Foster, P. S. et al., Early-life viral infection and allergen exposure interact to induce an asthmatic phenotype in mice. Respir Res 2010. 11: 14.
Ozato, K., Tailor, P. and Kubota, T., The interferon regulatory factor family in host defense: mechanism of action. J Biol Chem 2007. 282: 20065–20069.
Desmet, C. J. and Ishii, K. J., Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol 2012. 12: 479–491.
Hammad, H., Chieppa, M., Perros, F., Willart, M. A., Germain, R. N. and Lambrecht, B. N., House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 2009. 15: 410–416.
McAlees, J. W., Whitehead, G. S., Harley, I. T., Cappelletti, M., Rewerts, C. L., Holdcroft, A. M., Divanovic, S. et al., Distinct Tlr4-expressing cell compartments control neutrophilic and eosinophilic airway inflammation. Mucosal Immunol 2015. 8: 863–873.
Roers, A., Hiller, B. and Hornung, V., Recognition of endogenous nucleic acids by the innate immune system. Immunity 2016. 44: 739–754.
Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W. and Selbach, M., Global quantification of mammalian gene expression control. Nature 2011. 473: 337–342.
Cabezas-Wallscheid, N., Klimmeck, D., Hansson, J., Lipka, D. B., Reyes, A., Wang, Q., Weichenhan, D. et al., Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis. Cell Stem Cell 2014. 15: 507–522.
Freeman, G. J., Boussiotis, V. A., Anumanthan, A., Bernstein, G. M., Ke, X. Y., Rennert, P. D., Gray, G. S. et al., B7-1 and B7-2 do not deliver identical costimulatory signals, since B7-2 but not B7-1 preferentially costimulates the initial production of IL-4. Immunity 1995. 2: 523–532.
Jackson, D. J., Gern, J. E. and Lemanske, R. F., Jr., The contributions of allergic sensitization and respiratory pathogens to asthma inception. J Allergy Clin Immunol 2016. 137: 659–665.
Sato, M., Suemori, H., Hata, N., Asagiri, M., Ogasawara, K., Nakao, K., Nakaya, T. et al., Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000. 13: 539–548.
Huber, W., Carey, V. J., Gentleman, R., Anders, S., Carlson, M., Carvalho, B. S., Bravo, H. C. et al., Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods 2015. 12: 115–121.
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W. and Smyth, G. K., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 2015. 43: e47.
Carvalho, B. S. and Irizarry, R. A., A framework for oligonucleotide microarray preprocessing. Bioinformatics 2010. 26: 2363–2367.
Stacklies, W., Redestig, H., Scholz, M., Walther, D. and Selbig, J., pcaMethods–a bioconductor package providing PCA methods for incomplete data. Bioinformatics 2007. 23: 1164–1167.
Mi, H., Poudel, S., Muruganujan, A., Casagrande, J. T. and Thomas, P. D., PANTHER version 10: expanded protein families and functions, and analysis tools. Nucleic Acids Res 2016. 44: D336–D342.
Paulissen, G., Rocks, N., Gueders, M. M., Bedoret, D., Crahay, C., Quesada-Calvo, F. et al., ADAM-8, a metalloproteinase, drives acute allergen-induced airway inflammation. Eur J Immunol 2011. 41: 380–391.
R Core Team. R: A language and Environment for Statistical Computing, https://R-projetcr.org 2016.
Bates, D., Mächler, M., Bolker, B. and Walker, S., Fitting linear mixed-effects models using lme4; 2014. Preprint. Available 2015.