ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling in vivo

Journal of Clinical Investigation

Volumn 116, Issue 1, 2006, Pages 163-173

  Lee, Patty J ^a   Zhang, Xuchen ^a   Shan, Peiying ^a   Ma, Bing ^a   Chun, Geun Lee ^a   Homer, Robert J ^a   Zhu, Zhou ^b   Mercedes, Rincon ^c   Mossman, Brooke T ^d   Elias, Jack A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ALPHA 1 ANTITRYPSIN; CATHEPSIN B; CHEMOKINE; GELATINASE A; GELATINASE B; INTERLEUKIN 3; MACROPHAGE ELASTASE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 2; MATRIX METALLOPROTEINASE 14; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEINASE; RANTES; STAT6 PROTEIN; STRESS ACTIVATED PROTEIN KINASE 1; SYNAPTOPHYSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HYPOTHESIS; IN VIVO STUDY; LUNG ALVEOLUS; LUNG DISEASE; MOUSE; MUTATION; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STIMULATION; TISSUE REACTION;

ANIMALS; CHEMOKINES; INFLAMMATION; INTERLEUKIN-13; LUNG; MATRIX METALLOPROTEINASES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; STAT6 TRANSCRIPTION FACTOR;

EID: 31044435286     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI25711     Document Type: Article

References (42)

1. Elias, J.A., Lee, C.G., Zheng, T., Shim, Y., and Zhu, Z. 2003. Interleukin-13 and leukotrienes: an intersection of pathogenetic schema. Am. J. Respir. Cell Mol. Biol. 28:401-404.
2. Wills-Karp, M., et al. 1998. Interleukin-13: central mediator of allergic asthma. Science. 282:2258-2261.
3. Grunig, G., et al. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science. 282:2261-2263.
4. 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.
5. 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.
6. Zhu, Z., et al. 2002. IL-13-induced chemokine responses in the lung: role of CCR2 in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 168:2953-2962.
7. Kuperman, D.A., et al. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8:885-889.
8. Blease, K., et al. 2000. Enhanced pulmonary allergic responses to Aspergillus in CCR2-/- mice. J. Immunol. 165:2603-2611.
9. Chiaramonte, M.G., Donaldson, D.D., Cheever, A.W., and Wynn, T.A. 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.
10. Hancock, A., Armstrong, L., Gama, R., and Millar, A. 1998. Production of interleukin 13 by alveolar macrophages from normal and fibrotic lung. Am. J. Respir. Cell Mol. Biol. 18:60-65.
11. Ohshima, K., et al. 2001. Interleukin-13 and interleukin-13 receptor in Hodgkin's disease: possible autocrine mechanism and involvement in fibrosis. Histopathology. 38:368-375.
12. Mattes, J., et al. 2001. IL-13 induces airways hyperreactivity independently of the IL-4R alpha chain in the allergic lung. J. Immunol. 167:1683-1692.
13. Yang, M., et al. 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.
14. Kuperman, D., Schofield, B., Wills-Karp, M., and Grusby, M.J. 1998. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyper-responsiveness and mucus production. J. Exp. Med. 187:939-948.
15. Blenis, J. 1993. Signal transduction via the MAP kinases: proceed at your own RSK. Proc. Natl. Acad. Sci. U. S. A. 90:5889-5892.
16. Davis, R.J. 1993. The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 268:14553-14556.
17. Davis, R.J. 1994. MAPKs: new JNK expands the group. Trends Biochem. Sci. 19:470-473.
18. Duan, W., Chan, J.H., Wong, C.H., Leung, B.P., and Wong, W.S. 2004. Anti-inflammatory effects of mitogen-activated protein kinase kinase inhibitor U0126 in an asthma mouse model. J. Immunol. 172:7053-7059.
19. Pahl, A., Zhang, M., Kuss, H., Szelenyi, I., and Brune, K. 2002. Regulation of IL-13 synthesis in human lymphocytes: implications for asthma therapy. Br. J. Pharmacol. 135:1915-1926.
20. David, M., Ford, D., Bertoglio, J., Maizel, A.L., and Pierre, J. 2001. Induction of the IL-13 receptor alpha2-chain by IL-4 and IL-13 in human keratinocytes: involvement of STAT6, ERK and p38 MAPK pathways. Oncogene. 20:6660-6668.
21. Hirst, S.J., Hallsworth, M.P., Peng, Q., and Lee, T.H. 2002. Selective induction of eotaxin release by interleukin-13 or interleukin-4 in human airway smooth muscle cells is synergistic with interleukin-1beta and is mediated by the interleukin-4 receptor alpha-chain. Am. J. Respir. Crit. Care Med. 165:1161-1171.
22. Laporte, J.C., et al. 2001. Direct effects of interleukin-13 on signaling pathways for physiological responses in cultured human airway smooth muscle cells. Am. J. Respir. Crit. Care Med. 164:141-148.
23. Moore, P.E., Church, T.L., Chism, D.D., Panettieri, R.A., Jr., and Shore, S.A. 2002. IL-13 and IL-4 cause eotaxin release in human airway smooth muscle cells: a role for ERK. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L847-L853.
24. Peng, Q., Matsuda, T., and Hirst, S.J. 2004. Signaling pathways regulating interleukin-13-stimulated chemokine release from airway smooth muscle. Am. J. Respir. Crit. Care Med. 169:596-603.
25. Xu, B., et al. 2003. Interleukin-13 induction of 15-lipoxygenase gene expression requires p38 mitogen-activated protein kinase-mediated serine 727 phosphorylation of Stat1 and Stat3. Mol. Cell. Biol. 23:3918-3928.
26. Ma, B., et al. 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.
27. Nelms, K., Keegan, A.D., Zamorano, J., Ryan, J.J., and Paul, W.E. 1999. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17:701-738.
28. 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.
29. Lanone, S., et al. 2002. Overlapping and enzymespecific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J. Clin. Invest. 110:463-474. doi:10.1172/JCI200214136.
30. Lee, C.G., et al. 2001. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta(1). J. Exp. Med. 194:809-821.
31. Mould, A.W., et al. 2000. The effect of IL-5 and eotaxin expression in the lung on eosinophil trafficking and degranulation and the induction of bronchial hyperreactivity. J. Immunol. 164:2142-2150.
32. Rothenberg, M.E., MacLean, J.A., Pearlman, E., Luster, A.D., and Leder, P. 1997. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J. Exp. Med. 185:785-790.
33. Rothenberg, M.E., et al. 1996. Eotaxin triggers eosinophil-selective chemotaxis and calcium flux via a distinct receptor and induces pulmonary eosinophilia in the presence of interleukin 5 in mice. Mol. Med. 2:334-348.
34. Oliveira, S.H., et al. 2002. Increased responsiveness of murine eosinophils to MIP-1beta (CCL4) and TCA-3 (CCL1) is mediated by their specific receptors, CCR5 and CCR8. J. Leukoc. Biol. 71:1019-1025.
35. Rot, A., et al. 1992. RANTES and macrophage inflammatory protein 1 alpha induce the migration and activation of normal human eosinophil granulocytes. J. Exp. Med. 176:1489-1495.
36. 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.
37. van der Pouw Kraan, T.C., et al. 2002. Chronic obstructive pulmonary disease is associated with the -1055 IL-13 promoter polymorphism. Genes Immun. 3:436-439.
38. Mercer, B.A., Kolesnikova, N., Sonett, J., and D'Armiento, J. 2004. ERK MAP kinase is upregulated in pulmonary emphysema and mediates MMP-1 induction by cigarette smoke. J. Biol. Chem. 279:17690-17696.
39. Alessandrini, A., Greulich, H., Huang, W., and Erikson, R.L. 1996. Mek1 phosphorylation site mutants activate Raf-1 in NIH 3T3 cells. J. Biol. Chem. 271:31612-31618.
40. Stripp, B.R., et al. 1992. cis-acting elements that confer lung epithelial cell expression of the CC10 gene. J. Biol. Chem. 267:14703-14712.
41. Zhang, X., et al. 2002. Mitogen-activated protein kinases regulate HO-1 gene transcription after ischemia-reperfusion lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L815-L829.
42. McGuckin, M.A., and Thornton, D.J. 2000. Detection and quantitation of mucins using chemical, lectin, and antibody methods. Methods Mol. Biol. 125:45-55.