Foxa2 programs Th2 cell-mediated innate immunity in the developing lung

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 6133-6141

  Chen, Gang ^a   Wan, Huajing ^c   Luo, Fengming ^d   Zhang, Liqian ^a   Xu, Yan ^a   Lewkowich, Ian ^b   Wills Karp, Marsha ^b   Whitsett, Jeffrey A ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c SICHUAN UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EOTAXIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; THYMUS AND ACTIVATION REGULATED CHEMOKINE; FOXA2 PROTEIN, MOUSE; MESSENGER RNA;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CLINICAL ASSESSMENT; GENE DELETION; GENE EXPRESSION; GOBLET CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LUNG DEVELOPMENT; METAPLASIA; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; TH2 CELL; ANIMAL; CELL SEPARATION; CYTOLOGY; DNA MICROARRAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INFLAMMATION; LUNG; METABOLISM; MUCOSAL IMMUNITY; RESPIRATORY TRACT MUCOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GOBLET CELLS; HEPATOCYTE NUCLEAR FACTOR 3-BETA; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LUNG; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TH2 CELLS;

EID: 77953442986     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000223     Document Type: Article

References (59)

1. Nelms, K., A. D. Keegan, J. Zamorano, J. J. Ryan, and W. E. Paul. 1999. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17: 701-738.
2. Fan, J., R. D. Ye, and A. B. Malik. 2001. Transcriptional mechanisms of acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 281: L1037-L1050.
3. Atherton, H. C., G. Jones, and H. Danahay. 2003. IL-13-induced changes in the goblet cell density of human bronchial epithelial cell cultures: MAP kinase and phosphatidylinositol 3-kinase regulation. Am. J. Physiol. Lung Cell. Mol. Physiol. 285: L730-L739.
4. Kanno, H., Y. Horikawa, R. R. Hodges, D. Zoukhri, M. A. Shatos, J. D. Rios, and D. A. Dartt. 2003. Cholinergic agonists transactivate EGFR and stimulate MAPK to induce goblet cell secretion. Am. J. Physiol. Cell Physiol. 284: C988-C998.
5. Hamid, Q., and M. Tulic. 2009. Immunobiology of asthma. Annu. Rev. Physiol. 71: 489-507.
6. Wills-Karp, M., and F. D. Finkelman. 2008. Untangling the complex web of IL-4- and IL-13-mediated signaling pathways. Sci. Signal. 1: pe55.
7. Hershey, G. K. 2003. IL-13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. 111: 677-690, quiz 691.
8. Tomkinson, A., C. Duez, G. Cieslewicz, J. C. Pratt, A. Joetham, M. C. Shanafelt, R. Gundel, and E. W. Gelfand. 2001. A murine IL-4 receptor antagonist that inhibits IL-4- and IL-13-induced responses prevents antigen-induced airway eosinophilia and airway hyperresponsiveness. J. Immunol. 166: 5792-5800.
9. Karras, J. G., J. R. Crosby, M. Guha, D. Tung, D. A. Miller, W. A. Gaarde, R. S. Geary, B. P. Monia, and S. A. Gregory. 2007. Anti-inflammatory activity of inhaled IL-4 receptor-alpha antisense oligonucleotide in mice. Am. J. Respir. Cell Mol. Biol. 36: 276-285.
10. Diamond, G., D. Legarda, and L. K. Ryan. 2000. The innate immune response of the respiratory epithelium. Immunol. Rev. 173: 27-38.
11. Kato, A., and R. P. Schleimer. 2007. Beyond inflammation: airway epithelial cells are at the interface of innate and adaptive immunity. Curr. Opin. Immunol. 19: 711-720.
12. 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.
13. Hammad, H., M. Chieppa, F. Perros, M. A. Willart, R. N. Germain, and B. N. Lambrecht. 2009. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 15: 410-416.
14. Wan, H., K. H. Kaestner, S. L. Ang, M. Ikegami, F. D. Finkelman, M. T. Stahlman, P. C. Fulkerson, M. E. Rothenberg, and J. A. Whitsett. 2004. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development 131: 953-964.
15. Zhen, G., S. W. Park, L. T. Nguyenvu, M. W. Rodriguez, R. Barbeau, A. C. Paquet, and D. J. Erle. 2007. IL-13 and epidermal growth factor receptor have critical but distinct roles in epithelial cell mucin production. Am. J. Respir. Cell Mol. Biol. 36: 244-253.
16. Wan, H., Y. Xu, M. Ikegami, M. T. Stahlman, K. H. Kaestner, S. L. Ang, and J. A. Whitsett. 2004. Foxa2 is required for transition to air breathing at birth. Proc. Natl. Acad. Sci. USA 101: 14449-14454.
17. Park, K. S., T. R. Korfhagen, M. D. Bruno, J. A. Kitzmiller, H. Wan, S. E. Wert, G. K. Khurana Hershey, G. Chen, and J. A. Whitsett. 2007. SPDEF regulates goblet cell hyperplasia in the airway epithelium. J. Clin. Invest. 117: 978-988.
18. Chen, G., T. R. Korfhagen, Y. Xu, J. Kitzmiller, S. E. Wert, Y. Maeda, A. Gregorieff, H. Clevers, and J. A. Whitsett. 2009. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J. Clin. Invest. 119: 2914-2924.
19. Tompkins, D. H., V. Besnard, A. W. Lange, S. E. Wert, A. R. Keiser, A. N. Smith, R. Lang, and J. A. Whitsett. 2009. Sox2 is required for maintenance and differentiation of bronchiolar Clara, ciliated, and goblet cells. PLoS One 4: e8248.
20. Perl, A. K., L. Zhang, and J. A. Whitsett. 2009. Conditional expression of genes in the respiratory epithelium in transgenic mice: cautionary notes and toward building a better mouse trap. Am. J. Respir. Cell Mol. Biol. 40: 1-3.
21. Waclaw, R. R., B. Wang, Z. Pei, L. A. Ehrman, and K. Campbell. 2009. Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 63: 451-465.
22. Reed, J. A., M. Ikegami, L. Robb, C. G. Begley, G. Ross, and J. A. Whitsett. 2000. Distinct changes in pulmonary surfactant homeostasis in common beta-chain- and GM-CSF-deficient mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 278: L1164-L1171.
23. Iwakura, Y., S. Nakae, S. Saijo, and H. Ishigame. 2008. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol. Rev. 226: 57-79.
24. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517.
25. Chatila, T. A. 2004. Interleukin-4 receptor signaling pathways in asthma pathogenesis. Trends Mol. Med. 10: 493-499.
26. Kotowicz, K., R. E. Callard, K. Friedrich, D. J. Matthews, and N. Klein. 1996. Biological activity of IL-4 and IL-13 on human endothelial cells: functional evidence that both cytokines act through the same receptor. Int. Immunol. 8: 1915-1925.
27. Schnyder, B., S. Lugli, N. Feng, H. Etter, R. A. Lutz, B. Ryffel, K. Sugamura, H. Wunderli-Allenspach, and R. Moser. 1996. Interleukin-4 (IL-4) and IL-13 bind to a shared heterodimeric complex on endothelial cells mediating vascular cell adhesion molecule-1 induction in the absence of the common gamma chain. Blood 87: 4286-4295.
28. Yang, M., S. P. Hogan, P. J. Henry, K. I. Matthaei, A. N. McKenzie, I. G. Young, M. E. Rothenberg, and P. S. Foster. 2001. Interleukin-13 mediates airways hyperreactivity through the IL-4 receptor-alpha chain and STAT-6 independently of IL-5 and eotaxin. Am. J. Respir. Cell Mol. Biol. 25: 522-530.
29. 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.
30. Livraghi, A., B. R. Grubb, E. J. Hudson, K. J. Wilkinson, J. K. Sheehan, M. A. Mall, W. K. O'Neal, R. C. Boucher, and S. H. Randell. 2009. Airway and lung pathology due to mucosal surface dehydration in beta-epithelial Na+ channel-overexpressing mice: role of TNF-alpha and IL-4Ralpha signaling, influence of neonatal development, and limited efficacy of glucocorticoid treatment. J. Immunol. 182: 4357-4367.
31. Lambrecht, B. N., and H. Hammad. 2003. Taking our breath away: dendritic cells in the pathogenesis of asthma. Nat. Rev. Immunol. 3: 994-1003.
32. 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.
33. de Heer, H. J., H. Hammad, T. Soullié, D. Hijdra, N. Vos, M. A. Willart, H. C. Hoogsteden, and B. N. Lambrecht. 2004. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200: 89-98.
34. 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.
35. Ito, T., Y. H. Wang, O. Duramad, T. Hori, G. J. Delespesse, N. Watanabe, F. X. Qin, Z. Yao, W. Cao, and Y. J. Liu. 2005. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202: 1213-1223.
36. Dieu-Nosjean, M. C., C. Massacrier, B. Homey, B. Vanbervliet, J. J. Pin, A. Vicari, S. Lebecque, C. Dezutter-Dambuyant, D. Schmitt, A. Zlotnik, and C. Caux. 2000. Macrophage inflammatory protein 3alpha is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 192: 705-718.
37. Izadpanah, A., M. B. Dwinell, L. Eckmann, N. M. Varki, and M. F. Kagnoff. 2001. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G710-G719.
38. Saenz, S. A., B. C. Taylor, and D. Artis. 2008. Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol. Rev. 226: 172-190.
39. Schmitz, J., A. Owyang, E. Oldham, Y. Song, E. Murphy, T. K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, et al. 2005. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23: 479-490.
40. Sekiya, T., M. Miyamasu, M. Imanishi, H. Yamada, T. Nakajima, M. Yamaguchi, T. Fujisawa, R. Pawankar, Y. Sano, K. Ohta, et al. 2000. Inducible expression of a Th2-type CC chemokine thymus- and activation-regulated chemokine by human bronchial epithelial cells. J. Immunol. 165: 2205-2213.
41. Berin, M. C., L. Eckmann, D. H. Broide, and M. F. Kagnoff. 2001. Regulated production of the T helper 2-type T-cell chemoattractant TARC by human bronchial epithelial cells in vitro and in human lung xenografts. Am. J. Respir. Cell Mol. Biol. 24: 382-389.
42. Imai, T., M. Nagira, S. Takagi, M. Kakizaki, M. Nishimura, J. Wang, P. W. Gray, K. Matsushima, and O. Yoshie. 1999. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int. Immunol. 11: 81-88.
43. Rawlins, E. L., and B. L. Hogan. 2006. Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133: 2455-2465.
44. Zimmermann, N., G. K. Hershey, P. S. Foster, and M. E. Rothenberg. 2003. Chemokines in asthma: cooperative interaction between chemokines and IL-13. J. Allergy Clin. Immunol. 111: 227-242, quiz 243.
45. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261.
46. Robays, L. J., T. Maes, S. Lebecque, S. A. Lira, W. A. Kuziel, G. G. Brusselle, G. F. Joos, and K. V. Vermaelen. 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.
47. Motojima, S., E. Frigas, D. A. Loegering, and G. J. Gleich. 1989. Toxicity of eosinophil cationic proteins for guinea pig tracheal epithelium in vitro. Am. Rev. Respir. Dis. 139: 801-805.
48. Zhu, Z., T. Zheng, R. J. Homer, Y. K. Kim, N. Y. Chen, L. Cohn, Q. Hamid, and J. A. Elias. 2004. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678-1682.
49. Homer, R. J., Z. Zhu, L. Cohn, C. G. Lee, W. I. White, S. Chen, and J. A. Elias. 2006. Differential expression of chitinases identify subsets of murine airway epithelial cells in allergic inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 291: L502-L511.
50. Hartl, D., C. H. He, B. Koller, C. A. Da Silva, R. Homer, C. G. Lee, and J. A. Elias. 2008. Acidic mammalian chitinase is secreted via an ADAM17/epidermal growth factor receptor-dependent pathway and stimulates chemokine production by pulmonary epithelial cells. J. Biol. Chem. 283: 33472-33482.
51. Diehl, S., and M. Rincón. 2002. The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39: 531-536.
52. Benwell, R. K., and D. R. Lee. 2010. Essential and synergistic roles of IL1 and IL6 in human Th17 differentiation directed by TLR ligand-activated dendritic cells. Clin Immunol 134: 178-187.
53. Li, Z., P. White, G. Tuteja, N. Rubins, S. Sackett, and K. H. Kaestner. 2009. Foxa1 and Foxa2 regulate bile duct development in mice. J. Clin. Invest. 119: 1537-1545.
54. Romagnani, S. 2002. Cytokines and chemoattractants in allergic inflammation. Mol. Immunol. 38: 881-885.
55. Takizawa, H. 2005. Bronchial epithelial cells in allergic reactions. Curr. Drug Targets Inflamm. Allergy 4: 305-311.
56. Lambrecht, B. N. 2005. Dendritic cells and the regulation of the allergic immune response. Allergy 60: 271-282.
57. Jahnsen, F. L., E. D. Moloney, T. Hogan, J. W. Upham, C. M. Burke, and P. G. Holt. 2001. Rapid dendritic cell recruitment to the bronchial mucosa of patients with atopic asthma in response to local allergen challenge. Thorax 56: 823-826.
58. Lewkowich, I. P., S. Lajoie, J. R. Clark, N. S. Herman, A. A. Sproles, and M. Wills-Karp. 2008. Allergen uptake, activation, and IL-23 production by pulmonary myeloid DCs drives airway hyperresponsiveness in asthma-susceptible mice. PLoS ONE 3: e3879.
59. Park, S. W., C. Verhaeghe, L. T. Nguyenvu, R. Barbeau, C. J. Eisley, Y. Nakagami, X. Huang, P. G.Woodruff, J. V. Fahy, and D. J. Erle. 2009. Distinct roles of FOXA2 and FOXA3 in allergic airway disease and asthma. Am. J. Respir. Crit. Care Med. 180: 603-610.