IL-6 activated integrated BATF/IRF4 functions in lymphocytes are T-bet-independent and reversed by subcutaneous immunotherapy

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Koch, Sonja ^a   Mousset, Stephanie ^a   Graser, Anna ^a   Reppert, Sarah ^a   Übel, Caroline ^a   Reinhardt, Cornelia ^b   Zimmermann, Theodor ^b   Rieker, Ralf ^b   Lehr, Hans A ^c   Finotto, Susetta ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; BATF PROTEIN, MOUSE; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR 4; INTERFERON REGULATORY FACTOR-4; INTERLEUKIN 21 RECEPTOR; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MESSENGER RNA; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR;

ANIMAL; ARTICLE; ASTHMA; B LYMPHOCYTE; CHILD; FEMALE; GENETICS; HUMAN; HYPERSENSITIVITY; IMMUNOLOGY; IMMUNOTHERAPY; LUNG; MALE; METABOLISM; METHODOLOGY; MOUSE; PRESCHOOL CHILD; TH17 CELL; TH2 CELL; PROCEDURES;

ANIMALS; ANTIBODIES; ASTHMA; B-LYMPHOCYTES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; HYPERSENSITIVITY; IMMUNOTHERAPY; INTERFERON REGULATORY FACTORS; INTERLEUKIN-6; LUNG; MALE; MICE; RECEPTORS, INTERLEUKIN-21; RECEPTORS, INTERLEUKIN-6; RNA, MESSENGER; T-BOX DOMAIN PROTEINS; TH17 CELLS; TH2 CELLS; TRANSCRIPTION FACTORS;

EID: 84877752694     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep01754     Document Type: Article

References (47)

1. Holgate, S. T. & Polosa, R. Treatment strategies for allergy and asthma. Nat Rev Immunol 8, 218-230 (2008). (Pubitemid 351323290)
2. Akdis, C. A. Therapies for allergic inflammation: refining strategies to induce tolerance. Nat Med 18, 736-749 (2012).
3. Akdis, M. & Akdis, C. A. Therapeutic manipulation of immune tolerance in allergic disease. Nat Rev Drug Discov 8, 645-660 (2009).
4. Durham, S. R. et al. Long-term clinical efficacy in grass pollen-induced rhinoconjunctivitis after treatment with SQ-standardized grass allergy immunotherapy tablet. J Allergy Clin Immunol 125, 131-138 e131-137 (2010).
5. Fujita, H., Soyka, M. B., Akdis, M. & Akdis, C. A. Mechanisms of allergen-specific immunotherapy. Clin Transl Allergy 2, 2 (2012).
6. Xepapadaki, P. & Papadopoulos, N. G. Childhood asthma and infection: virus-induced exacerbations as determinants and modifiers. Eur Respir J 36, 438-445 (2010).
7. Dienz, O. & Rincon, M. The effects of IL-6onCD4 T cell responses.Clin Immunol 130, 27-33 (2009).
8. Bettelli, E. et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238 (2006).
9. He, R., Oyoshi, M. K., Jin, H. & Geha, R. S. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc Natl Acad Sci U S A 104, 15817-15822 (2007). (Pubitemid 350035382)
10. McKinley, L. et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 181, 4089-4097 (2008).
11. Wilson, R. H. et al. Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am J Respir Crit Care Med 180, 720-730 (2009).
12. Lazarevic, V. et al. T-bet represses T(H)17 differentiation by preventing Runx1-mediated activation of the gene encoding RORgammat. Nat Immunol 12, 96-104 (2011).
13. Durrant, D. M., Gaffen, S. L., Riesenfeld, E. P., Irvin, C. G. & Metzger, D. W. Development of allergen-induced airway inflammation in the absence of T-bet regulation is dependent on IL-17. J Immunol 183, 5293-5300 (2009).
14. Finotto, S. et al. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 295, 336-338 (2002). (Pubitemid 34074365)
15. Doganci, A. et al. The IL-6R alpha chain controls lung CD41CD251 Treg development and function during allergic airway inflammation in vivo. J Clin Invest 115, 313-325 (2005). (Pubitemid 40385473)
16. Finotto, S. et al. Local blockade of IL-6R signaling induces lung CD41 T cell apoptosis in a murine model of asthma via regulatory T cells. Int Immunol 19, 685-693 (2007). (Pubitemid 47073260)
17. Betz, B. C. et al. Batf coordinates multiple aspects of B and T cell function required for normal antibody responses. J Exp Med 207, 933-942 (2010).
18. Ise, W. et al. The transcription factor BATF controls the global regulators of class-switch recombination in both B cells and T cells. Nat Immunol 12, 536-543 (2011).
19. Martinez, G. J. & Dong, C. BATF: bringing (in) another Th17-regulating factor. J Mol Cell Biol 1, 66-68 (2009).
20. Schraml, B. U. et al. The AP-1 transcription factor Batf controls T(H)17 differentiation. Nature 460, 405-409 (2009).
21. Ciofani, M. et al. A validated regulatory network for th17 cell specification. Cell 151, 289-303 (2012).
22. Glasmacher, E. et al. A genomic regulatory element that directs assembly and function of immune-specific AP-1-IRF complexes. Science 338, 975-980 (2012).
23. Li, P. et al. BATF-JUN is critical for IRF4-mediated transcription in T cells. Nature (2012).
24. Munthe-Kaas, M. C. et al. T cell-specific T-box transcription factor haplotype is associated with allergic asthma in children. J Allergy Clin Immunol 121, 51-56 (2008).
25. Broide, D. H. et al. Cytokines in symptomatic asthma airways. J Allergy Clin Immunol 89, 958-967 (1992).
26. Marini, M., Vittori, E., Hollemborg, J. & Mattoli, S. Expression of the potent inflammatory cytokines, granulocyte-macrophage-colony-stimulating factor and interleukin-6 and interleukin-8, in bronchial epithelial cells of patients with asthma. J Allergy Clin Immunol 89, 1001-1009 (1992).
27. Yokoyama, A. et al. Circulating interleukin-6 levels in patients with bronchial asthma. Am J Respir Crit Care Med 151, 1354-1358 (1995).
28. Zhou, L. et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 8, 967-974 (2007). (Pubitemid 47300011)
29. Aujla, S. J. & Alcorn, J. F. T(H)17 cells in asthma and inflammation. Biochim Biophys Acta 1810, 1066-1079 (2011).
30. Ivanov, II, Zhou, L. & Littman, D. R. Transcriptional regulation of Th17 cell differentiation. Semin Immunol 19, 409-417 (2007). (Pubitemid 351274050)
31. Brustle, A. et al. The development of inflammatory T(H)-17 cells requires interferon-regulatory factor 4. Nat Immunol 8, 958-966 (2007). (Pubitemid 47300010)
32. Huber, M. et al. IRF4 is essential for IL-21-mediated induction, amplification, and stabilization of the Th17 phenotype. Proc Natl Acad Sci U S A 105, 20846-20851 (2008).
33. Staudt, V. et al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33, 192-202 (2010).
34. Huber, S. et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3 and Foxp31 regulatory CD41 T cells in an interleukin-10-dependent manner. Immunity 34, 554-565 (2011).
35. Xu, J. et al. c-Maf regulates IL-10 expression during Th17 polarization. J Immunol 182, 6226-6236 (2009).
36. Finotto, S. et al. Asthmatic changes in mice lacking T-bet are mediated by IL-13. Int Immunol 17, 993-1007 (2005). (Pubitemid 41158383)
37. Doganci, A. et al. IL-2 receptor beta-chain signaling controls immunosuppressive CD41 T cells in the draining lymph nodes and lung during allergic airway inflammation in vivo. J Immunol 181, 1917-1926 (2008).
38. Ellyard, J. I. & Vinuesa, C. G. A BATF-ling connection between B cells and follicular helper T cells. Nat Immunol 12, 519-520 (2011).
39. Yoshizaki, K. et al. Isolation and characterization of B cell differentiation factor (BCDF) secreted from a human B lymphoblastoid cell line. J Immunol 132, 2948-2954 (1984). (Pubitemid 14105681)
40. Hiramatsu, Y. et al. c-Maf activates the promoter and enhancer of the IL-21 gene, and TGF-beta inhibits c-Maf-induced IL-21 productionin CD41T cells. JLeukoc Biol 87, 703-712 (2010).
41. Yang, Y., Ochando, J., Yopp, A., Bromberg, J. S. & Ding, Y. IL-6 plays a unique role in initiating c-Maf expression during early stage of CD4 T cell activation. J Immunol 174, 2720-2729 (2005). (Pubitemid 40279687)
42. Neurath, M. F. & Finotto, S. IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev 22, 83-89 (2011).
43. Mudter, J. et al. IRF4 regulates IL-17A promoter activity and controls RORgammat-dependent Th17 colitis in vivo. Inflamm Bowel Dis 17, 1343-1358 (2011).
44. Spolski, R. & Leonard, W. J. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu Rev Immunol 26, 57-79 (2008). (Pubitemid 351600371)
45. Pesce, J. et al. The IL-21 receptor augments Th2 effector function and alternative macrophage activation. J Clin Invest 116, 2044-2055 (2006). (Pubitemid 44033328)
46. Taher, Y. A., van Esch, B. C., Hofman, G. A., Henricks, P. A. & van Oosterhout, A. J. 1alpha, 25-dihydroxyvitamin D3 potentiates the beneficial effects of allergen immunotherapy in a mouse model of allergic asthma: role for IL-10 and TGF-beta. J Immunol 180, 5211-5221 (2008).
47. Sauer, K. A., Scholtes, P., Karwot, R. & Finotto, S. Isolation of CD41 T cells from murine lungs: a method to analyze ongoing immune responses in the lung. Nat Protoc 1, 2870-2875 (2006).