Adenosine metabolism and murine strain-specific IL-4-induced inflammation, emphysema, and fibrosis

Journal of Clinical Investigation

Volumn 116, Issue 5, 2006, Pages 1274-1283

  Ma, Bing ^a   Blackburn, Michael R ^b   Chun, Geun Lee ^a   Homer, Robert J ^a,c   Liu, Wei ^a   Flavell, Richard A ^a   Boyden, Lynn ^a   Lifton, Richard P ^a   Sun, Chun Xiao ^b   Young, Hays W ^b   Elias, Jack A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ADENOSINE DEAMINASE; ADENOSINE RECEPTOR; ALPHA 1 ANTITRYPSIN; CATHEPSIN; CYTOKINE; INTERLEUKIN 4; METALLOPROTEINASE; PEGADEMASE; STAT6 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMPHYSEMA; ENZYME ACTIVITY; HISTOLOGY; IN SITU HYBRIDIZATION; INFLAMMATION; METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; STATISTICAL ANALYSIS; TH1 CELL; TH2 CELL; WESTERN BLOTTING;

ADENOSINE; ANIMALS; EMPHYSEMA; FEMALE; FIBROSIS; INFLAMMATION; INTERLEUKIN-4; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PULMONARY ALVEOLI; RATS; SPECIES SPECIFICITY; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 33646407318     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI26372     Document Type: Article

References (66)

1. Hamilton, B.A., and Frankel, W.N. 2001. Of mice and genome sequence. Cell. 107:13-16.
2. Anderson, C.F., Mendez, S., and Sacks, D.L. 2005. Non-healing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice. J. Immunol. 174:2934-2941.
3. Barth, R.K., Hanchett, L.A., and Baecher-Allan, C.M. 2002. Mapping susceptibility genes for the induction of pulmonary fibrosis in mice. Chest. 121:21S.
4. Bix, M., Wang, Z.E., Thiel, B., Schork, N.J., and Locksley, R.M. 1998. Genetic regulation of commitment to interleukin 4 production by a CD4(+) T cell-intrinsic mechanism. J. Exp. Med. 188:2289-2299.
5. Bonniaud, P., et al. 2004. Connective tissue growth factor is crucial to inducing a profibrotic environment in "fibrosis-resistant" BALB/c mouse lungs. Am. J. Respir. Cell Mol. Biol. 31:510-516.
6. De Sanctis, G.T., et al. 1995. Quantitative locus analysis of airway hyperresponsiveness in A/J and C57BL/6J mice. Nat. Genet. 11:150-154.
7. Duguet, A., et al. 2000. Bronchial responsiveness among inbred mouse strains. Role of airway smooth-muscle shortening velocity. Am. J. Respir. Crit. Care Med. 161:839-848.
8. Guerassimov, A., et al. 2004. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am. J. Respir. Crit. Care Med. 170:974-980.
9. Haston, C.K., Corey, M., and Tsui, L.C. 2002. Mapping of genetic factors influencing the weight of cystic fibrosis knockout mice. Mamm. Genome. 13:614-618.
10. Haston, C.K., and Travis, E.L. 1997. Murine susceptibility to radiation-induced pulmonary fibrosis is influenced by a genetic factor implicated in susceptibility to bleomycin-induced pulmonary fibrosis. Cancer Res. 57:5286-5291.
11. Haston, C.K., et al. 2002. Universal and radiation-specific loci influence murine susceptibility to radiation-induced pulmonary fibrosis. Cancer Res. 62:3782-3788.
12. Charles, P.C., Weber, K.S., Cipriani, B., and Brosnan, C.F. 1999. Cytokine, chemokine and chemokine receptor mRNA expression in different strains of normal mice: implications for establishment of a Th1/Th2 bias. J. Neuroimmunol. 100:64-73.
13. Fan, T., Yang, M., Halayko, A., Mohapatra, S.S., and Stephens, N.L. 1997. Airway responsiveness in two inbred strains of mouse disparate in IgE and IL-4 production. Am. J. Respir. Cell Mol. Biol. 17:156-163.
14. Takeda, K., Haczku, A., Lee, J.J., Irvin, C.G., and Gelfand, E.W. 2001. Strain dependence of airway hyperresponsiveness reflects differences in eosinophil localization in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 281:L394-L402.
15. Takeshita, K., Yamasaki, T., Akira, S., Gantner, F., and Bacon, K.B. 2004. Essential role of MHC IIindependent CD4+ T cells, IL-4 and STAT6 in contact hypersensitivity induced by fluorescein isothiocyanate in the mouse. Int. Immunol. 16:685-695.
16. Zhang, Y., et al. 1997. Influence of the route of allergen administration and genetic background on the murine allergic pulmonary response. Am. J. Respir. Crit. Care Med. 155:661-669.
17. Snapper, C.M., and Paul, W.E. 1987. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 236:944-947.
18. Rankin, J.A., et al. 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. U. S. A. 93:7821-7825.
19. Voehringer, D., Shinkai, K., and Locksley, R.M. 2004. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity. 20:267-277.
20. Richter, A., et al. 2001. The contribution of interleukin (IL)-4 and IL-13 to the epithelial-mesenchymal trophic unit in asthma. Am. J. Respir. Cell Mol. Biol. 25:385-391.
21. Jain-Vora, S., Wert, S.E., Temann, U.A., Rankin, J.A., and Whitsett, J.A. 1997. Interleukin-4 alters epithelial cell differentiation and surfactant homeostasis in the postnatal mouse lung. Am. J. Respir. Cell Mol. Biol. 17:541-551.
22. Leigh, R., et al. 2004. Type 2 cytokines in the pathogenesis of sustained airway dysfunction and airway remodeling in mice. Am. J. Respir. Crit. Care Med. 169:860-867.
23. Saito, A., Okazaki, H., Sugawara, I., Yamamoto, K., and Takizawa, H. 2003. Potential action of IL-4 and IL-13 as fibrogenic factors on lung fibroblasts in vitro. Int. Arch. Allergy Immunol. 132:168-176.
24. Shimizu, K., Shichiri, M., Libby, P., Lee, R.T., and Mitchell, R.N. 2004. Th2-predominant inflammation and blockade of IFN-γ signaling induce aneurysms in allografted aortas. J. Clin. Invest. 114:300-308. doi:10.1172/JCI200419855.
25. Leonardi, A., et al. 2003. Effects of Th2 cytokines on expression of collagen, MMP-1, and TIMP-1 in conjunctival fibroblasts. Invest. Ophthalmol. Vis. Sci. 44:183-189.
26. Wynn, T.A. 2004. Fibrotic disease and the Th1/Th2 paradigm. Nat. Rev. Immunol. 4:583-594.
27. Zhu, Z., et al. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities and eotaxin production. J. Clin. Invest. 103:779-788.
28. Elias, J.A., et al. 2003. New insights into the pathogenesis of asthma. J. Clin. Invest. 111:291-297. doi:10.1172/JCI200419855.
29. Wills-Karp, M., and Chiaramonte, M. 2003. Interleukin-13 in asthma. Curr. Opin. Pulm. Med. 9:21-27.
30. Burri, P.H. 1997. Structural aspects of prenatal and postnatal development and growth of the lung. In Lung growth and development. J.A. McDonald, editor. Marcel Dekker Inc. New York, New York, USA. 1-35.
31. Ray, P., et al. 1997. Regulated overexpression of interleukin-11 in the lung: use to dissociate development-dependent and -independent phenotypes. J. Clin. Invest. 100:2501-2511.
32. Zheng, T., et al. 2000. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase-and cathepsin-dependent emphysema. J. Clin. Invest. 106:1081-1093.
33. Lee, C.G., et al. 2002. Transgenic overexpression of interleukin (IL)-10 in the lung causes mucus metaplasia, tissue inflammation, and airway remodeling via IL-13-dependent and -independent pathways. J. Biol. Chem. 277:35466-35474.
34. Temann, U.A., Ray, P., and Flavell, R.A. 2002. Pulmonary overexpression of IL-9 induces Th2 cytokine expression, leading to immune pathology. J. Clin. Invest. 109:29-39. doi:10.1172/JCI200213696.
35. Wang, Z., et al. 2000. Interferon gamma induction of pulmonary emphysema in the adult murine lung. J. Exp. Med. 192:1587-1600.
36. Kwak, Y.G., et al. 2003. Involvement of PTEN in airway hyperresponsiveness and inflammation in bronchial asthma. J. Clin. Invest. 111:1083-1092. doi:10.1172/JCI200316440.
37. Wang, J., Homer, R.J., Chen, Q., and Elias, J.A. 2000. Endogenous and exogenous IL-6 inhibit aeroallergen-induced Th2 inflammation. J. Immunol. 165:4051-4061.
38. Wang, J., et al. 2000. IL-11 selectively inhibits aeroallergen-induced pulmonary eosinophilia and Th2 cytokine production. J. Immunol. 165:2222-2231.
39. Shapiro, S.D. 2000. Animal models for COPD. Chest. 117:223S-227S.
40. Jeffery, P.K. 1999. Differences and similarities between chronic obstructive pulmonary disease and asthma. Clin. Exp. Allergy. 29:14-26.
41. Jeffery, P.K. 2001. Lymphocytes, chronic bronchitis and chronic obstructive pulmonary disease. Novartis Found. Symp. 234:149-168.
42. Bartalesi, B., et al. 2005. Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur. Respir. J. 25:15-22.
43. Zhang, N., et al. 1999. Effects of theophylline on plasma levels of interleukin-4, cyclic nucleotides and pulmonary functions in patients with chronic obstructive pulmonary disease. J. Tongji Med. Univ. 19:15-19.
44. Sutherland, E.R., and Cherniack, R.M. 2004. Management of chronic obstructive pulmonary disease. N. Engl. J. Med. 350:2689-2697.
45. Senior, R.M., and Shapiro, S.D. 1998. Chronic obstructive pulmonary disease: epidemiology, pathophysiology, and pathogenesis. In Fishman's pulmonary diseases and disorders. A.P. Fishman et al., editors. McGraw-Hill Inc. New York, New York, USA. 659-681.
46. Hashimoto, S., Gon, Y., Takeshita, I., Maruoka, S., and Horie, T. 2001. IL-4 and IL-13 induce myofibroblastic phenotype of human lung fibroblasts through c-Jun NH2-terminal kinase-dependent pathway. J. Allergy Clin. Immunol. 107:1001-1008.
47. Hashimoto-Uoshima, M., et al. 2002. Effects of interleukin-4 on proteoglycan accumulation in human gingival fibroblasts. J. Periodont. Res. 37:42-49.
48. Steinke, J.W., et al. 2004. Characterization of interleukin-4-stimulated nasal polyp fibroblasts. Am. J. Respir. Cell Mol. Biol. 30:212-219.
49. Kolb, M., et al. 2002. Differences in the fibrogenic response after transfer of active transforming growth factor-beta1 gene to lungs of "fibrosisprone" and "fibrosis-resistant" mouse strains. Am. J. Respir. Cell Mol. Biol. 27:141-150.
50. Belardinelli, L., Linden, J., and Berne, R.M. 1989. The cardiac effects of adenosine. Prog. Cardiovasc. Dis. 32:73-97.
51. Blackburn, M.R., et al. 2003. Adenosine mediates IL-13-induced inflammation and remodeling in the lung and interacts in an IL-13-adenosine amplification pathway. J. Clin. Invest. 112:332-344. doi:10.1172/JCI200316815.
52. Churchill, P.C. 1982. Renal effects of 2-chloroadenosine and their antagonism by aminophylline in anesthetized rats. J. Pharmacol. Exp. Ther. 222:319-323.
53. Fredholm, B.B., and Dunwiddie, T.V. 1988. How does adenosine inhibit transmitter release? Trends Pharmacol. Sci. 9:130-134.
54. Huang, S., Apasov, S., Koshiba, M., and Sitkovsky, M. 1997. Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood. 90:1600-1610.
55. Ohta, A., and Sitkovsky, M. 2001. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature. 414:916-920.
56. Tilley, S.L., Wagoner, V.A., Salvatore, C.A., Jacobson, M.A., and Koller, B.H. 2000. Adenosine and inosine increase cutaneous vasopermeability by activating A(3) receptors on mast cells. J. Clin. Invest. 105:361-367.
57. Driver, A.G., Kukoly, C.A., Ali, S., and Mustafa, S.J. 1993. Adenosine in bronchoalveolar lavage fluid in asthma. Am. Rev. Respir. Dis. 148:91-97.
58. Marquardt, D.L., Parker, C.W., and Sullivan, T.J. 1978. Potentiation of mast cell mediator release by adenosine. J. Immunol. 120:871-878.
59. Walker, B.A., et al. 1997. Adenosine A3 receptor expression and function in eosinophils. Am. J. Respir. Cell Mol. Biol. 16:531-537.
60. Cushley, M.J., Tattersfield, A.E., and Holgate, S.T. 1983. Inhaled adenosine and guanosine on airway resistance in normal and asthmatic subjects. Br. J. Clin. Pharmacol. 15:161-165.
61. Oosterhoff, Y., de Jong, J.W., Jansen, M.A., Koeter, G.H., and Postma, D.S. 1993. Airway responsiveness to adenosine 5′-monophosphate in chronic obstructive pulmonary disease is determined by smoking. Am. Rev. Respir. Dis. 147:553-558.
62. Blackburn, M.R., et al. 2000. Metabolic consequences of adenosine deaminase deficiency in mice are associated with defects in alveogenesis, pulmonary inflammation, and airway obstruction. J. Exp. Med. 192:159-170.
63. Zheng, T., et al. 2005. Role of cathepsin S-dependent epithelial cell apoptosis in IFN-gammainduced alveolar remodeling and pulmonary emphysema. J. Immunol. 174:8106-8115.
64. Lee, C.G., et al. 2004. Early growth response gene 1-mediated apoptosis is essential for transforming growth factor beta1-induced pulmonary fibrosis. J. Exp. Med. 200:377-389.
65. Lee, P.J., et al. 2006. ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling in vivo. J. Clin. Invest. 116:163-173. doi:10.1172/JCI25711.
66. Winston, J.H., Hanten, G.R., Overbeek, P.A., and Kellems, R.E. 1992. 5′ flanking sequences of the murine adenosine deaminase gene direct expression of a reporter gene to specific prenatal and postnatal tissues in transgenic mice. J. Biol. Chem. 267:13472-13479.