Elf3 regulates allergic airway inflammation by controlling dendritic cell-driven T cell differentiation

Journal of Immunology

Volumn 187, Issue 9, 2011, Pages 4639-4653

  Kushwah, Rahul ^a,b,d   Oliver, Jordan R ^a,b   Wu, Jing ^a   Chang, Zhijie ^c   Hu, Jim ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Tsinghua University   (China)

^d MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INITIATION FACTOR 3; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 25; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; THYMIC STROMAL LYMPHOPOIETIN; TRANSCRIPTION FACTOR GATA 3;

ALLERGIC PNEUMONITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC ANALYSIS; GENETIC LINKAGE; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INFLAMMATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL;

ADMINISTRATION, INTRANASAL; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; DNA-BINDING PROTEINS; INFLAMMATION; INTERLEUKIN-12; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVALBUMIN; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTE SUBSETS; TH1 CELLS; TH2 CELLS; TRANSCRIPTION FACTORS;

EID: 80555154846     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101967     Document Type: Article

References (68)

1. Ng, A. Y., P. Waring, S. Ristevski, C. Wang, T. Wilson, M. Pritchard, P. Hertzog, and I. Kola. 2002. Inactivation of the transcription factor Elf3 in mice results in dysmorphogenesis and altered differentiation of intestinal epithelium. Gastroenterology 122: 1455-1466. (Pubitemid 34465186)
2. Friedman, A. D. 1996. Regulation of immature myeloid cell differentiation by PEBP2/CBF, Myb, C/EBP and Ets family members. Curr. Top. Microbiol. Immunol. 211: 149-157. (Pubitemid 26019275)
3. Moisan, J., R. Grenningloh, E. Bettelli, M. Oukka, and I. C. Ho. 2007. Ets-1 is a negative regulator of Th17 differentiation. J. Exp. Med. 204: 2825-2835. (Pubitemid 350179553)
4. Schotte, R., M. C. Rissoan, N. Bendriss-Vermare, J. M. Bridon, T. Duhen, K. Weijer, F. Brière, and H. Spits. 2003. The transcription factor Spi-B is expressed in plasmacytoid DC precursors and inhibits T-, B-, and NK-cell development. Blood 101: 1015-1023. (Pubitemid 36139374)
5. Nagasawa, M., H. Schmidlin, M. G. Hazekamp, R. Schotte, and B. Blom. 2008. Development of human plasmacytoid dendritic cells depends on the combined action of the basic helix-loop-helix factor E2-2 and the Ets factor Spi-B. Eur. J. Immunol. 38: 2389-2400.
6. Guerriero, A., P. B. Langmuir, L. M. Spain, and E. W. Scott. 2000. PU.1 is required for myeloid-derived but not lymphoid-derived dendritic cells. Blood 95: 879-885. (Pubitemid 30062709)
7. Laiosa, C. V., M. Stadtfeld, H. Xie, L. de Andres-Aguayo, and T. Graf. 2006. Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU.1 transcription factors. Immunity 25: 731-744. (Pubitemid 46107288)
8. Appel, S., A. Bringmann, F. Grünebach, M. M. Weck, J. Bauer, and P. Brossart. 2006. Epithelial-specific transcription factor ESE-3 is involved in the development of monocyte-derived DCs. Blood 107: 3265-3270.
9. Silverman, E. S., R. M. Baron, L. J. Palmer, L. Le, A. Hallock, V. Subramaniam, R. J. Riese, M. D. McKenna, X. Gu, T. A. Libermann, et al. 2002. Constitutive and cytokine-induced expression of the ETS transcription factor ESE-3 in the lung. Am. J. Respir. Cell Mol. Biol. 27: 697-704. (Pubitemid 35381178)
10. Brooks-Wilson, A. R., A. Buchler, L. Cardon, A. H. Carey, M. Galvin, A. Miller, and M. North, inventors; AxyS Pharmaceuticals, assignee. 2000 July 11. Asthma related genes. United States patent US 6,087,485.
11. Grall, F., X. Gu, L. Tan, J. Y. Cho, M. S. Inan, A. R. Pettit, U. Thamrongsak, B. K. Choy, C. Manning, Y. Akbarali, et al. 2003. Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1. Arthritis Rheum. 48: 1249-1260. (Pubitemid 36554524)
12. Wu, J., R. Duan, H. Cao, D. Field, C. M. Newnham, D. R. Koehler, N. Zamel, M. A. Pritchard, P. Hertzog, M. Post, et al. 2008. Regulation of epithelium-specific Ets-like factors ESE-1 and ESE-3 in airway epithelial cells: potential roles in airway inflammation. Cell Res. 18: 649-663. (Pubitemid 351793120)
13. Grall, F. T., W. C. Prall, W. Wei, X. Gu, J. Y. Cho, B. K. Choy, L. F. Zerbini, M. S. Inan, S. R. Goldring, E. M. Gravallese, et al. 2005. The Ets transcription factor ESE-1 mediates induction of the COX-2 gene by LPS in monocytes. FEBS J. 272: 1676-1687. (Pubitemid 40516218)
14. Zhan, Y., L. Yuan, M. Kondo, and P. Oettgen. 2010. The counter-regulatory effects of ESE-1 during angiotensin II-mediated vascular inflammation and remodeling. Am. J. Hypertens. 23: 1312-1317.
15. Cai, Z., Z. Shi, A. Sanchez, T. Zhang, M. Liu, J. Yang, F. Wang, and D. Zhang. 2009. Transcriptional regulation of Tlr11 gene expression in epithelial cells. J. Biol. Chem. 284: 33088-33096.
16. Di Cesare, A., P. Di Meglio, and F. O. Nestle. 2008. A role for Th17 cells in the immunopathogenesis of atopic dermatitis? J. Invest. Dermatol. 128: 2569-2571.
17. Spergel, J. M. 2010. Epidemiology of atopic dermatitis and atopic march in children. Immunol. Allergy Clin. North Am. 30: 269-280.
18. Spergel, J. M. 2010. From atopic dermatitis to asthma: the atopic march. Ann. Allergy Asthma Immunol. 105:99-106; quiz 107-109, 117.
19. Koga, C., K. Kabashima, N. Shiraishi, M. Kobayashi, and Y. Tokura. 2008. Possible pathogenic role of Th17 cells for atopic dermatitis. J. Invest. Dermatol. 128: 2625-2630.
20. Dong, C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8: 337-348. (Pubitemid 351595217)
21. Spergel, J. M., E. Mizoguchi, J. P. Brewer, T. R. Martin, A. K. Bhan, and R. S. Geha. 1998. Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice. J. Clin. Invest. 101: 1614-1622. (Pubitemid 28198490)
22. He, R., M. K. Oyoshi, H. Jin, and R. S. Geha. 2007. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc. Natl. Acad. Sci. USA 104: 15817-15822. (Pubitemid 350035382)
23. He, R., H. Y. Kim, J. Yoon, M. K. Oyoshi, A. MacGinnitie, S. Goya, E. J. Freyschmidt, P. Bryce, A. N. McKenzie, D. T. Umetsu, H. C. Oettgen, and R. S. Geha. 2009. Exaggerated IL-17 response to epicutaneous sensitization mediates airway inflammation in the absence of IL-4 and IL-13. J. Allergy Clin. Immunol. 124:761-770.e1.
24. Ma, W., P. J. Bryce, A. A. Humbles, D. Laouini, A. Yalcindag, H. Alenius, D. S. Friend, H. C. Oettgen, C. Gerard, and R. S. Geha. 2002. CCR3 is essential for skin eosinophilia and airway hyperresponsiveness in a murine model of allergic skin inflammation. J. Clin. Invest. 109: 621-628. (Pubitemid 34204841)
25. Piggott, D. A., S. C. Eisenbarth, L. Xu, S. L. Constant, J. W. Huleatt, C. A. Herrick, and K. Bottomly. 2005. MyD88-dependent induction of allergic Th2 responses to intranasal antigen. J. Clin. Invest. 115: 459-467. (Pubitemid 40385488)
26. Kushwah, R., H. Cao, and J. Hu. 2008. Characterization of pulmonary T cell response to helper-dependent adenoviral vectors following intranasal delivery. J. Immunol. 180: 4098-4108.
27. Lambrecht, B. N., M. De Veerman, A. J. Coyle, J. C. Gutierrez-Ramos, K. Thielemans, and R. A. Pauwels. 2000. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J. Clin. Invest. 106: 551-559. (Pubitemid 30666388)
28. Cohn, L., R. J. Homer, A. Marinov, J. Rankin, and K. Bottomly. 1997. Induction of airway mucus production By T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J. Exp. Med. 186: 1737-1747. (Pubitemid 27506286)
29. Liew, F. Y. 2002. T(H)1 and T(H)2 cells: a historical perspective. Nat. Rev. Immunol. 2: 55-60. (Pubitemid 37328776)
30. Swamy, M., C. Jamora, W. Havran, and A. Hayday. 2010. Epithelial decision makers: in search of the 'epimmunome'. Nat. Immunol. 11: 656-665.
31. Soumelis, V., P. A. Reche, H. Kanzler, W. Yuan, G. Edward, B. Homey, M. Gilliet, S. Ho, S. Antonenko, A. Lauerma, et al. 2002. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat. Immunol. 3: 673-680. (Pubitemid 34752477)
32. Liu, Y. J., V. Soumelis, N. Watanabe, T. Ito, Y. H. Wang, Rde. W. Malefyt, M. Omori, B. Zhou, and S. F. Ziegler. 2007. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu. Rev. Immunol. 25: 193-219. (Pubitemid 46697907)
33. Paul, W. E., and J. Zhu. 2010. How are T(H)2-type immune responses initiated and amplified? Nat. Rev. Immunol. 10: 225-235.
34. Smit, J. J., B. D. Rudd, and N. W. Lukacs. 2006. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203: 1153-1159. (Pubitemid 43736586)
35. Hammad, H., and B. N. Lambrecht. 2008. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat. Rev. Immunol. 8: 193-204. (Pubitemid 351323293)
36. Plantinga, M., H. Hammad, and B. N. Lambrecht. 2010. Origin and functional specializations of DC subsets in the lung. Eur. J. Immunol. 40: 2112-2118.
37. Beaty, S. R., C. E. Rose, Jr., and S. S. Sung. 2007. Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 178: 1882-1895. (Pubitemid 46154661)
38. Oriss, T. B., M. Ostroukhova, C. Seguin-Devaux, B. Dixon-McCarthy, D. B. Stolz, S. C. Watkins, B. Pillemer, P. Ray, and A. Ray. 2005. Dynamics of dendritic cell phenotype and interactions with CD4+ T cells in airway inflammation and tolerance. J. Immunol. 174: 854-863. (Pubitemid 40094280)
39. Yoshinaga, S. K., J. S. Whoriskey, S. D. Khare, U. Sarmiento, J. Guo, T. Horan, G. Shih, M. Zhang, M. A. Coccia, T. Kohno, et al. 1999. T-cell co-stimulation through B7RP-1 and ICOS. Nature 402: 827-832. (Pubitemid 129638129)
40. Tafuri, A., A. Shahinian, F. Bladt, S. K. Yoshinaga, M. Jordana, A. Wakeham, L. M. Boucher, D. Bouchard, V. S. Chan, G. Duncan, et al. 2001. ICOS is essential for effective T-helper-cell responses. Nature 409: 105-109. (Pubitemid 32098634)
41. Imai, T., D. Chantry, C. J. Raport, C. L. Wood, M. Nishimura, R. Godiska, O. Yoshie, and P. W. Gray. 1998. Macrophage-derived chemokine is a functional ligand for the CC chemokine receptor 4. J. Biol. Chem. 273: 1764-1768. (Pubitemid 28133708)
42. Imai, T., M. Baba, M. Nishimura, M. Kakizaki, S. Takagi, and O. Yoshie. 1997. The T cell-directed CC chemokine TARC is a highly specific biological ligand for CC chemokine receptor 4. J. Biol. Chem. 272: 15036-15042. (Pubitemid 27251781)
43. Freeman, G. J., V. A. Boussiotis, A. Anumanthan, G. M. Bernstein, X. Y. Ke, P. D. Rennert, G. S. Gray, J. G. Gribben, and L. M. Nadler. 1995. 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 2: 523-532.
44. Fahlén-Yrlid, L., T. Gustafsson, J. Westlund, A. Holmberg, A. Strömbeck, M. Blomquist, G. G. MacPherson, J. Holmgren, and U. Yrlid. 2009. CD11c(high) dendritic cells are essential for activation of CD4+ T cells and generation of specific antibodies following mucosal immunization. J. Immunol. 183: 5032-5041.
45. Kool, M., T. Soullié, M. van Nimwegen, M. A. Willart, F. Muskens, S. Jung, H. C. Hoogsteden, H. Hammad, and B. N. Lambrecht. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 205: 869-882. (Pubitemid 351549884)
46. Jaffar, Z., M. E. Ferrini, L. A. Herritt, and K. Roberts. 2009. Cutting edge: lung mucosal Th17-mediated responses induce polymeric Ig receptor expression by the airway epithelium and elevate secretory IgA levels. J. Immunol. 182: 4507-4511.
47. Pelletier, M., L. Maggi, A. Micheletti, E. Lazzeri, N. Tamassia, C. Costantini, L. Cosmi, C. Lunardi, F. Annunziato, S. Romagnani, and M. A. Cassatella. 2010. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115: 335-343.
48. Rodgers, H. C., L. Pang, E. Holland, L. Corbett, S. Range, and A. J. Knox. 2002. Bradykinin increases IL-8 generation in airway epithelial cells via COX-2- derived prostanoids. Am. J. Physiol. Lung Cell. Mol. Physiol. 283: L612-L618.
49. Rincón, M., J. Anguita, T. Nakamura, E. Fikrig, and R. A. Flavell. 1997. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 185: 461-469. (Pubitemid 27078364)
50. Diehl, S., and M. Rincón. 2002. The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39: 531-536. (Pubitemid 35341492)
51. Wang, J., R. J. Homer, Q. Chen, and J. A. Elias. 2000. Endogenous and exogenous IL-6 inhibit aeroallergen-induced Th2 inflammation. J. Immunol. 165: 4051-4061. (Pubitemid 32063095)
52. Huang, C. H., E. X. Loo, I. C. Kuo, G. H. Soh, D. L. Goh, B. W. Lee, and K. Y. Chua. 2011. Airway inflammation and IgE production induced by dust mite allergen-specific memory/effector Th2 cell line can be effectively attenuated by IL-35. J. Immunol. 187: 462-471.
53. Cohn, L., L. Whittaker, N. Niu, and R. J. Homer. 2002. Cytokine regulation of mucus production in a model of allergic asthma. Novartis Found. Symp. 248: 201-213; discussion 213-220, 277-282.
54. Kuperman, D. A., X. Huang, L. Nguyenvu, C. Hölscher, F. Brombacher, and D. J. Erle. 2005. IL-4 receptor signaling in Clara cells is required for allergeninduced mucus production. J. Immunol. 175: 3746-3752. (Pubitemid 41292034)
55. Liew, F. Y., N. I. Pitman, and I. B. McInnes. 2010. Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat. Rev. Immunol. 10: 103-110.
56. Kurowska-Stolarska, M., P. Kewin, G. Murphy, R. C. Russo, B. Stolarski, C. C. Garcia, M. Komai-Koma, N. Pitman, Y. Li, W. Niedbala, et al. 2008. IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. [Published erratum appears in 2008 J. Immunol. 181: 8170.] J. Immunol. 181: 4780-4790.
57. Muthuswamy, R., J. Mueller-Berghaus, U. Haberkorn, T. A. Reinhart, D. Schadendorf, and P. Kalinski. 2010. PGE(2) transiently enhances DC expression of CCR7 but inhibits the ability of DCs to produce CCL19 and attract naive T cells. Blood 116: 1454-1459.
58. Vermaelen, K., and R. Pauwels. 2003. Accelerated airway dendritic cell maturation, trafficking, and elimination in a mouse model of asthma. Am. J. Respir. Cell Mol. Biol. 29: 405-409. (Pubitemid 37094000)
59. Wirnsberger, G., D. Hebenstreit, G. Posselt, J. Horejs-Hoeck, and A. Duschl. 2006. IL-4 induces expression of TARC/CCL17 via two STAT6 binding sites. Eur. J. Immunol. 36: 1882-1891. (Pubitemid 44089054)
60. Watanabe, M., T. Satoh, Y. Yamamoto, Y. Kanai, H. Karasuyama, and H. Yokozeki. 2008. Overproduction of IgE induces macrophage-derived chemokine (CCL22) secretion from basophils. J. Immunol. 181: 5653-5659.
61. Inaba, K., G. Schuler, M. D. Witmer, J. Valinksy, B. Atassi, and R. M. Steinman. 1986. Immunologic properties of purified epidermal Langerhans cells. Distinct requirements for stimulation of unprimed and sensitized T lymphocytes. J. Exp. Med. 164: 605-613. (Pubitemid 16050704)
62. Schuler, G., and R. M. Steinman. 1985. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161: 526-546. (Pubitemid 15142803)
63. Kaplan, M. H., Y. L. Sun, T. Hoey, and M. J. Grusby. 1996. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382: 174-177. (Pubitemid 26242885)
64. Manetti, R., P. Parronchi, M. G. Giudizi, M. P. Piccinni, E. Maggi, G. Trinchieri, and S. Romagnani. 1993. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 177: 1199-1204. (Pubitemid 23097410)
65. Gavett, S. H., D. J. O'Hearn, X. Li, S. K. Huang, F. D. Finkelman, and M. Wills- Karp. 1995. Interleukin 12 inhibits antigen-induced airway hyperresponsiveness, inflammation, and Th2 cytokine expression in mice. J. Exp. Med. 182: 1527-1536.
66. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
67. Usui, T., R. Nishikomori, A. Kitani, and W. Strober. 2003. GATA-3 suppresses Th1 development by downregulation of Stat4 and not through effects on IL-12Rbeta2 chain or T-bet. Immunity 18: 415-428. (Pubitemid 36351520)
68. McGeachy, M. J., K. S. Bak-Jensen, Y. Chen, C. M. Tato, W. Blumenschein, T. McClanahan, and D. J. Cua. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397. (Pubitemid 350138974)