IL-13 receptor α2 selectively inhibits IL-13-induced responses in the murine lung

Journal of Immunology

Volumn 180, Issue 1, 2008, Pages 522-529

  Zheng, Tao ^a,d   Liu, Wei ^b   Oh, Sun Young ^a   Zhu, Zhou ^a   Hu, Buqu ^b   Homer, Robert J ^b   Cohn, Lauren ^b   Grusby, Michael J ^c   Elias, Jack A ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 4; MUCIN; OVALBUMIN; PROTEINASE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GENE DISRUPTION; GENE LOCUS; IMMUNE RESPONSE; INFLAMMATION; LUNG FIBROSIS; LUNG MODEL; METAPLASIA; MOUSE; NONHUMAN; NULL ALLELE; PHENOTYPE; PHYSIOLOGY; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; RESPIRATORY EPITHELIUM; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; DRUG EFFECT; DRUG POTENTIATION; FIBROSIS; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MOUSE MUTANT; MUCUS; PATHOLOGY;

ANIMALS; FIBROSIS; INTERLEUKIN-13; INTERLEUKIN-13 RECEPTOR ALPHA2 SUBUNIT; INTERLEUKIN-4; LUNG; METAPLASIA; MICE; MICE, MUTANT STRAINS; MUCUS; OVALBUMIN; PNEUMONIA;

EID: 40449124503     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.1.522     Document Type: Article

References (61)

1. Zhu, Z., R. J. Homer, Z. Wang, Q. Chen, G. P. Geba, J. Wang, Y. Zhang, and J. A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103: 779-788.
2. 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.
3. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17: 255-281.
4. Bochner, B. S., D. A. Klunk, S. A. Sterbinsky, R. L. Coffman, and R. P. Schleimer. 1995. IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J. Immunol. 154: 799-803.
5. Emson, C. L., S. E. Bell, A. Jones, W. Wisden, and A. N. McKenzie. 1998. Interleukin (IL)-4-independent induction of immunoglobulin (Ig)E, and perturbation of T cell development in transgenic mice expressing IL-13. J. Exp. Med. 188: 399-404.
6. Webb, D. C., A. N. McKenzie, A. M. Koskinen, M. Yang, J. Mattes, and P. S. Foster. 2000. Integrated signals between IL-13, IL-4, and IL-5 regulate airways hyperreactivity. J. Immunol. 165: 108-113.
7. Rankin, J. A., D. E. Picarella, G. P. Geba, U. A. Temann, B. Prasad, B. DiCosmo, A. Tarallo, B. Stripp, J. Whitsett, and R. A. Flavell. 1996. Phenotypic and physiologic characterization of transgenic mice expressing interleukin 4 in the lung: lymphocytic and eosinophilic inflammation without airway hyperreactivity. Proc. Natl. Acad. Sci. USA 93: 7821-7825.
8. Finkelman, F. D., T. A. Wynn, D. D. Donaldson, and J. F. Urban. 1999. The role of IL-13 in helminth-induced inflammation and protective immunity against nematode infections. Curr. Opin. Immunol. 11: 420-426.
9. Brusselle, G., J. Kips, G. Joos, H. Bluethmann, and R. Pauwels. 1995. Allergen-induced airway inflammation and bronchial responsiveness in wild-type and interleukin-4-deficient mice. Am. J. Respir. Cell Mol. Biol. 12: 254-259.
10. Coyle, A. J., G. Le Gros, C. Bertrand, S. Tsuyuki, C. H. Heusser, M. Kopf, and G. P. Anderson. 1995. Interleukin-4 is required for the induction of lung Th2 mucosal immunity. Am. J. Respir. Cell Mol. Biol. 13: 54-59.
11. Miloux, B., P. Laurent, O. Bonnin, J. Lupker, D. Caput, N. Vita, and P. Ferrara. 1997. Cloning of the human IL-13R α1 chain and reconstitution with the IL4Rα of a functional IL-4/IL-13 receptor complex. FEBS Lett. 401: 163-166.
12. Chomarat, P., and J. Banchereau. 1998. Interleukin-4 and interleukin-13: their similarities and discrepancies. Int. Rev. Immunol. 17: 1-52.
13. Oettgen, H. C., and R. S. Geha. 2001. IgE regulation and roles in asthma pathogenesis. J. Allergy Clin. Immunol. 107: 429-440.
14. Leonard, W. J., and J. X. Lin. 2000. Cytokine receptor signaling pathways. J. Allergy Clin. Immunol. 105: 877-888.
15. Donaldson, D. D., M. J. Whitters, L. J. Fitz, T. Y. Neben, H. Finnerty, S. L. Henderson, R. M. O'Hara, Jr., D. R. Beier, K. J. Turner, C. R. Wood, and M. Collins. 1998. The murine IL-13 receptor α 2: molecular cloning, characterization, and comparison with murine IL-13 receptor α 1. J. Immunol. 161: 2317-2324.
16. Zhang, J. G., D. J. Hilton, T. A. Willson, C. McFarlane, B. A. Roberts, R. L. Moritz, R. J. Simpson, W. S. Alexander, D. Metcalf, and N. A. Nicola. 1997. Identification, purification, and characterization of a soluble interleukin (IL)-13-binding protein: evidence that it is distinct from the cloned Il-13 receptor and Il-4 receptor α-chains. J. Biol. Chem. 272: 9474-9480.
17. Kawakami, K., J. Taguchi, T. Murata, and R. K. Puri. 2001. The interleukin-13 receptor α2 chain: an essential component for binding and internalization but not for interleukin-13-induced signal transduction through the STAT6 pathway. Blood 97: 2673-2679.
18. Daines, M. O., and G. K. Hershey. 2002. A novel mechanism by which interferon-γ can regulate interleukin (IL)-13 responses: evidence for intracellular stores of IL-13 receptor α-2 and their rapid mobilization by interferon-γ. J. Biol. Chem. 277: 10387-10393.
19. Chiaramonte, M. G., M. Mentink-Kane, B. A. Jacobson, A. W. Cheever, M. J. Whitters, M. E. Goad, A. Wong, M. Collins, D. D. Donaldson, M. J. Grusby, and T. A. Wynn. 2003. Regulation and function of the interleukin 13 receptor α 2 during a T helper cell type 2-dominant immune response. J. Exp. Med. 197: 687-701.
20. Wood, N., M. J. Whitters, B. A. Jacobson, J. Witek, J. P. Sypek, M. Kasaian, M. J. Eppihimer, M. Unger, T. Tanaka, S. J. Goldman, et al. 2003. Enhanced interleukin (IL)-13 responses in mice lacking IL-13 receptor α 2. J. Exp. Med. 197: 703-709.
21. Zhao, Y., D. He, J. Zhao, L. Wang, A. R. Leff, E. W. Spannhake, S. Georas, and V. Natarajan. 2007. Lysophosphatidic acid induces interleukin-13 (IL-13) receptor α2 expression and inhibits IL-13 signaling in primary human bronchial epithelial cells. J. Biol. Chem. 282: 10172-10179.
22. Fichtner-Feigl, S., W. Strober, K. Kawakami, R. K. Puri, and A. Kitani. 2006. IL-13 signaling through the IL-13α2 receptor is involved in induction of TGF-β1 production and fibrosis. Nat. Med. 12: 99-106.
23. Zheng, T., Z. Zhu, W. Liu, C. G. Lee, Q. Chen, R. J. Homer, and J. A. Elias. 2003. Cytokine regulation of IL-13Rα2 and IL-13Rα1 in vivo and in vitro. J. Allergy Clin. Immunol. 111: 720-728.
24. Rahaman, S. O., P. Sharma, P. C. Harbor, M. J. Aman, M. A. Vogelbaum, and S. J. Haque. 2002. IL-13Rα2, a decoy receptor for IL-13 acts as an inhibitor of IL-4-dependent signal transduction in glioblastoma cells. Cancer Res. 62: 1103-1109.
25. Zheng, T., Z. Zhu, Z. Wang, R. J. Homer, B. Ma, R. J. Riese, Jr., H. A. Chapman, Jr., S. D. Shapiro, and J. A. Elias. 2000. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J. Clin. Invest. 106: 1081-1093.
26. 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.
27. Wang, Z., T. Zheng, Z. Zhu, R. J. Homer, R. J. Riese, H. A. Chapman, Jr., S. D. Shapiro, and J. A. Elias. 2000. Interferon γ induction of pulmonary emphysema in the adult murine lung. J. Exp. Med. 192: 1587-1600.
28. Lee, C. G., S. J. Cho, M. J. Kang, S. P. Chapoval, P. J. Lee, P. W. Noble, T. Yehualaeshet, B. Lu, R. A. Flavell, J. Milbrandt, et al. 2004. Early growth response gene 1-mediated apoptosis is essential for transforming growth factor β1-induced pulmonary fibrosis. J. Exp. Med. 200: 377-389.
29. Ma, B., W. Liu, R. J. Homer, P. J. Lee, A. J. Coyle, J. M. Lora, C. G. Lee, and J. A. Elias. 2006. Role of CCR5 in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 176: 4968-4978.
30. Zhu, Z., B. Ma, T. Zheng, R. J. Homer, C. G. Lee, I. F. Charo, P. Noble, and J. A. Elias. 2002. IL-13-induced chemokine responses in the lung: role of CCR2 in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 68: 2953-2962.
31. Ma, B., Z. Zhu, R. J. Homer, C. Gerard, R. Strieter, and J. A. Elias. 2004. The C10/CCL6 chemokine and CCR1 play critical roles in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 172: 1872-1881.
32. Lee, C. G., R. J. Homer, Z. Zhu, S. Lanone, X. Wang, V. Koteliansky, J. M. Shipley, P. Gotwals, P. Noble, Q. Chen, et al. 2001. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor β1. J. Exp. Med. 194: 809-821.
33. 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.
34. Grunig, G., M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley, and D. B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263.
35. Ma, B., M. R. Blackburn, C. G. Lee, R. J. Homer, W. Liu, R. A. Flavell, L. Boyden, R. P. Lifton, C. X. Sun, H. W. Young, and J. A. Elias. 2006. Adenosine metabolism and murine strain-specific IL-4-induced inflammation, emphysema, and fibrosis. J. Clin. Invest. 116: 1274-1283.
36. Jain-Vora, S., S. E. Wert, U. A. Temann, J. A. Rankin, and J. A. Whitsett. 1997. Interleukin-4 alters epithelial cell differentiation and surfactant homeostasis in the postnatal mouse lung. Am. J. Respir. Cell Mol. Biol. 17: 541-551.
37. Wills-Karp, M., and M. Chiaramonte. 2003. Interleukin-13 in asthma. Curr. Opin. Pulm. Med. 9: 21-27.
38. Wynn, T. A. 2004. Fibrotic disease and the TH1/TH2 paradigm. Nat. Rev. Immunol. 4: 583-594.
39. Elias, J. A., C. G. Lee, T. Zheng, B. Ma, R. J. Homer, and Z. Zhu. 2003. New insights into the pathogenesis of asthma. J. Clin. Invest. 111: 291-297.
40. Corry, D. B., and F. Kheradmand. 2002. Biology and therapeutic potential of the interleukin-4/interleukin-13 signaling pathway in asthma. Am. J. Respir. Med. 1: 185-193.
41. Belperio, J. A., M. Dy, M. D. Burdick, Y. Y. Xue, K. Li, J. A. Elias, and M. P. Keane. 2002. Interaction of IL-13 and C10 in the pathogenesis of bleomycin-induced pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 27: 419-427.
42. Chiaramonte, M. G., D. D. Donaldson, A. W. Cheever, and T. A. Wynn. 1999. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Invest. 104: 777-785.
43. Hancock, A., L. Armstrong, R. Gama, and A. Millar. 1998. Production of interleukin 13 by alveolar macrophages from normal and fibrotic lung. Am. J. Respir. Cell Mol. Biol. 18: 60-65.
44. Hasegawa, M., M. Fujimoto, K. Kikuchi, and K. Takehara. 1997. Elevated serum levels of interleukin 4 (IL-4), IL-10, and IL-13 in patients with systemic sclerosis. J. Rheumatol. 24: 328-332.
45. Ohshima, K., M. Akaiwa, R. Umeshita, J. Suzumiya, K. Izuhara, and M. Kikuchi. 2001. Interleukin-13 and interleukin-13 receptor in Hodgkin's disease: possible autocrine mechanism and involvement in fibrosis. Histopathology 38: 368-375.
46. Van der Pouw Kraan, T. C., M. Kucukaycan, A. M. Bakker, J. M. Baggen, J. S. van der Zee, M. A. Dentener, E. F. Wouters, and C. L. Verweij. 2002. Chronic obstructive pulmonary disease is associated with the -1055 IL-13 promoter polymorphism. Genes Immun. 3: 436-439.
47. Wills-Karp, M. 2004. Interleukin-13 in asthma pathogenesis. Immunol. Rev. 202: 175-190.
48. Zhu, Z., C. G. Lee, T. Zheng, G. Chupp, J. Wang, R. J. Homer, P. W. Noble, Q. Hamid, and J. A. Elias. 2001. Airway inflammation and remodeling in asthma: lessons from interleukin 11 and interleukin 13 transgenic mice. Am. J. Respir. Crit. Care Med. 164: S67-S70.
49. Haque, S. J., P. Harbor, M. Tabrizi, T. Yi, and B. R. Williams. 1998. Protein-tyrosine phosphatase Shp-1 is a negative regulator of IL-4- and IL-13-dependent signal transduction. J. Biol. Chem. 273: 33893-33896.
50. Haque, S. J., P. C. Harbor, and B. R. Williams. 2000. Identification of critical residues required for suppressor of cytokine signaling-specific regulation of interleukin-4 signaling. J. Biol. Chem. 275: 26500-26506.
51. Mentink-Kane, M. M., A. W. Cheever, R. W. Thompson, D. M. Hari, N. B. Kabatereine, B. J. Vennervald, J. H. Ouma, J. K. Mwatha, F. M. Jones, D. D. Donaldson, et al. 2004. IL-13 receptor α 2 down-modulates granulomatous inflammation and prolongs host survival in schistosomiasis. Proc. Natl. Acad. Sci. USA 101: 586-590.
52. Gelb, A. F., and N. Zamel. 2000. Unsuspected pseudophysiologic emphysema in chronic persistent asthma. Am. J. Respir. Crit. Care Med. 162: 1778-1782.
53. Gelb, A. F., J. Licuanan, C. M. Shinar, and N. Zamel. 2002. Unsuspected loss of lung elastic recoil in chronic persistent asthma. Chest 121: 715-721.
54. Chetta, A., A. Foresi, M. Del Donno, G. Bertorelli, A. Pesci, and D. Olivieri. 1997. Airways remodeling is a distinctive feature of asthma and is related to severity of disease. Chest 111: 852-857.
55. Minshall, E. M., D. Y. Leung, R. J. Martin, Y. L. Song, L. Cameron, P. Ernst, and Q. Hamid. 1997. Eosinophil-associated TGF-β1 mRNA expression and airways fibrosis in bronchial asthma. Am. J. Respir. Cell Mol. Biol. 17: 326-333.
56. Kaviratne, M., M. Hesse, M. Leusink, A. W. Cheever, S. J. Davies, J. H. McKerrow, L. M. Wakefield, J. J. Letterio, and T. A. Wynn. 2004. IL-13 activates a mechanism of tissue fibrosis that is completely TGF-β independent. J. Immunol. 173: 4020-4029.
57. Chiaramonte, M. G., A. W. Cheever, J. D. Malley, D. D. Donaldson, and T. A. Wynn. 2001. Studies of murine schistosomiasis reveal interleukin-13 blockade as a treatment for established and progressive liver fibrosis. Hepatology 34: 273-282.
58. + T-cell response by a hepatitis B core particle-based HIV vaccine. Clin. Immunol. 112: 92-105.
59. Takeno, M., H. Yoshikawa, M. Kurokawa, Y. Takeba, J. I. Kashiwakura, M. Sakaguchi, H. Yasueda, and N. Suzuki. 2004. Th1-dominant shift of T cell cytokine production, and subsequent reduction of serum immunoglobulin E response by administration in vivo of plasmid expressing Txk/Rlk, a member of Tec family tyrosine kinases, in a mouse model. Clin. Exp. Allergy 34: 965-970.
60. Zurawski, G., and J. E. de Vries. 1994. Interleukin 13 elicits a subset of the activities of its close relative interleukin 4. Stem Cells 12: 169-174.
61. Hershey, G. K. 2003. IL-13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. 111: 677-691.