Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice

Journal of Experimental Medicine

Volumn 202, Issue 1, 2005, Pages 47-59

  Rangasamy, Tirumalai ^a   Guo, Jia ^c   Mitzner, Wayne A ^a   Roman, Jessica ^c   Singh, Anju ^a   Fryer, Allison D ^a   Yamamoto, Masayuki ^a,d   Kensler, Thomas W ^a,b   Tuder, Rubin M ^a,c   Georas, Steve N ^c   Biswal, Shyam ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

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

^d UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 4; OVALBUMIN; TRANSCRIPTION FACTOR NRF2;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPERPLASIA; CELL INFILTRATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; EOSINOPHIL; GENE DISRUPTION; HISTOPATHOLOGY; IMMUNOPATHOGENESIS; LUNG LAVAGE; MOUSE; MUCOUS CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; SPLEEN CELL; TH2 CELL;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; ASTHMA; BASE SEQUENCE; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOKINES, CC; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; LUNG; MALE; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OVALBUMIN; OXIDATION-REDUCTION; OXIDATIVE STRESS; TH2 CELLS; TRANS-ACTIVATORS;

EID: 22344438250     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20050538     Document Type: Article

References (55)

1. 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.
2. Renauld, J.C. 2001. New insights into the role of cytokines in asthma. J. Clin. Pathol. 54:577-589.
3. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17:255-281.
4. Andreadis, A.A., S.L. Hazen, S.A. Comhair, and S.C. Erzurum. 2003. Oxidative and nitrosative events in asthma. Free Radic. Biol. Med. 35:213-225.
5. Henricks, P.A., and F.P. Nijkamp. 2001. Reactive oxygen species as mediators in asthma. Pulm. Pharmacol. Ther. 14:409-420.
6. Sanders, S.P., J.L. Zweier, S.J. Harrison, M.A. Trush, S.J. Rembish, and M.C. Liu. 1995. Spontaneous oxygen radical production at sites of antigen challenge in allergic subjects. Am. J. Respir. Crit. Care Med. 151:1725-1733.
7. Drost, E.M., and W. MacNee. 2002. Potential role of IL-8, plateletactivating factor and TNF-alpha in the sequestration of neutrophils in the lung: effects on neutrophil deformability, adhesion receptor expression, and chemotaxis. Eur. J. Immunol. 32:393-403.
8. Thomas, P.S. 2001. Tumour necrosis factor-alpha: the role of this multifunctional cytokine in asthma. Immunol. Cell Biol. 79:132-140.
9. Rojas-Ramos, E., A.F. Avalos, L. Perez-Fernandez, F. Cuevas-Schacht, E. Valencia-Maqueda, and L.M. Teran. 2003. Role of the chemokines RANTES, monocyte chemotactic proteins-3 and -4, and eotaxins-1 and -2 in childhood asthma. Eur. Respir. J. 22:310-316.
10. Nijkamp, F.P., and P.A. Henricks. 1990. Receptors in airway disease. Beta-adrenoceptors in lung inflammation. Am. Rev. Respir. Dis. 141:S145-S150.
11. Katsumata, U., M. Miura, M. Ichinose, K. Kimura, T. Takahashi, H. Inoue, and T. Takishima. 1990. Oxygen radicals produce airway constriction and hyperresponsiveness in anesthetized cats. Am. Rev. Respir. Dis. 141:1158-1161.
12. Ashutosh, K. 2000. Nitric oxide and asthma: a review. Curr. Opin. Pulm. Med. 6:21-25.
13. Adam, L., M. Bouvier, and T.L. Jones. 1999. Nitric oxide modulates beta(2)-adrenergic receptor palmitoylation and signaling. J. Biol. Chem. 274:26337-26343.
14. Sadeghi-Hashjin, G., G. Folkerts, P.A. Henricks, A.K. Verheyen, H.J. van der Linde, I. van Ark, A. Coene, and F.P. Nijkamp. 1996. Peroxynitrite induces airway hyperresponsiveness in guinea pigs in vitro and in vivo. Am. J. Respir. Crit. Care Med. 153:1697-1701.
15. Potoka, D.A., J.S. Upperman, X.R. Zhang, J.R. Kaplan, S.J. Corey, A. Grishin, R. Zamora, and H.R. Ford. 2003. Peroxynitrite inhibits en-terocyte proliferation and modulates Src kinase activity in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 285:G861-G869.
16. Zhang, P., Y.Z. Wang, E. Kagan, and J.C. Bonner. 2000. Peroxynitrite targets the epidermal growth factor receptor, Raf-1, and MEK independently to activate MAPK. J. Biol. Chem. 275:22479-22486.
17. Crapo, J.D. 2003. Redox active agents in inflammatory lung injury. Am. J. Respir. Crit. Care Med. 168:1027-1028.
18. Bowler, R.P., and J.D. Crapo. 2002. Oxidative stress in allergic respiratory diseases. J. Allergy Clin. Immunol. 110:349-356.
19. Kelly, F.J., I. Mudway, A. Blomberg, A. Frew, and T. Sandstrom. 1999. Altered lung antioxidant status in patients with mild asthma. Lancet. 354:482-483.
20. Rubin, R.N., L. Navon, and P.A. Cassano. 2004. Relationship of serum antioxidants to asthma prevalence in youth. Am. J. Respir. Crit. Care Med. 169:393-398.
21. Nguyen, T., P.J. Sherratt, and C.B. Pickett. 2003. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43:233-260.
22. Huber, M.A., A. Denk, R.U. Peter, L. Weber, N. Kraut, and T. Wirth. 2002. The IKK-2/Ikappa Balpha/NF-kappa B pathway plays a key role in the regulation of CCR3 and eotaxin-1 in fibroblasts. A critical link to dermatitis in Ikappa Balpha-deficient mice. J. Biol. Chem. 277:1268-1275.
23. Blesa, S., J. Cortijo, M. Mata, A. Serrano, D. Closa, F. Santangelo, J.M. Estrela, J. Suchankova, and E.J. Morcillo. 2003. Oral N-acetylcysteine attenuates the rat pulmonary inflammatory response to antigen. Eur. Respir. J. 21:394-400.
24. Chang, L.Y., M. Subramaniam, B.A. Yoder, B.J. Day, M.C. Ellison, M.E. Sunday, and J.D. Crapo. 2003. A catalytic antioxidant attenuates alveolar structural remodeling in bronchopulmonary dysplasia. Am. J. Respir. Crit. Care Med. 167:57-64.
25. Kloek, J., I. Van Ark, F. De Clerck, N. Bloksma, F.P. Nijkamp, and G. Folkerts. 2003. Modulation of airway hyperresponsiveness by thiols in a murine in vivo model of allergic asthma. Inflamm. Res. 52:126-131.
26. Zhu, M., and W.E. Fahl. 2001. Functional characterization of transcription regulators that interact with the electrophile response element. Biochem. Biophys. Res. Commun. 289:212-219.
27. Meister, A. 1991. Glutathione deficiency produced by inhibition of its synthesis, and its reversal: applications in research and therapy. Pharmacol. Ther. 51:155-194.
28. Rangasamy, T., C.Y. Cho, R.K. Thimmulappa, L. Zhen, S.S. Srisuma, T.W. Kensler, M. Yamamoto, I. Petrache, R.M. Tuder, and S. Biswal. 2004. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 114:1248-1259.
29. Mapp, C.E., A.A. Fryer, N. De Marzo, V. Pozzato, M. Padoan, P. Boschetto, R.C. Strange, A. Hemmingsen, and M.A. Spiteri. 2002. Glutathione S-transferase GSTP1 is a susceptibility gene for occupational asthma induced by isocyanates. J. Allergy Clin. Immunol. 109:867-872.
30. Otterbein, L.E., J.K. Kolls, L.L. Mantell, J.L. Cook, J. Alam, and A.M. Choi. 1999. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J. Clin. Invest. 103:1047-1054.
31. Otterbein, L.E., F.H. Bach, J. Alam, M. Soares, H. Tao Lu, M. Wysk, R.J. Davis, R.A. Flavell, and A.M. Choi. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6:422-428.
32. Oury, T.D., L.Y. Chang, S.L. Marklund, B.J. Day, and J.D. Crapo. 1994. Immunocytochemical localization of extracellular superoxide dismutase in human lung. Lab. Invest. 70:889-898.
33. Oury, T.D., B.J. Day, and J.D. Crapo. 1996. Extracellular superoxide dismutase in vessels and airways of humans and baboons. Free Radic. Biol. Med. 20:957-965.
34. Ikuta, N., S. Sugiyama, K. Takagi, T. Satake, and T. Ozawa. 1992. Implication of oxygen radicals on airway hyperresponsiveness after ovalbumin challenge in guinea pigs. Am. Rev. Respir. Dis. 145:561-565.
35. Fahy, J.V., J. Liu, H. Wong, and H.A. Boushey. 1993. Cellular and biochemical analysis of induced sputum from asthmatic and from healthy subjects. Am. Rev. Respir. Dis. 147:1126-1131.
36. Slungaard, A., G.M. Vercellotti, G. Walker, R.D. Nelson, and H.S. Jacob. 1990. Tumor necrosis factor-α/cachectin stimulates eosinophil oxidant production and toxicity towards human endothelium. J. Exp. Med. 171:2025-2041.
37. Griffiths-Johnson, D.A., P.D. Collins, A.G. Rossi, P.J. Jose, and T.J. Williams. 1993. The chemokine, eotaxin, activates guinea-pig eosinophils in vitro and causes their accumulation into the lung in vivo. Biochem. Biophys. Res. Commun. 197:1167-1172.
38. Erlemann, K.R., J. Rokach, and W.S. Powell. 2004. Oxidative stress stimulates the synthesis of the eosinophil chemoattractant 5-oxo-6,8,11,14- eicosatetraenoic acid by inflammatory cells. J. Biol. Chem. 279:40376-40384.
39. Stamatiou, P., Q. Hamid, R. Taha, W. Yu, T.B. Issekutz, J. Rokach, S.P. Khanapure, and W.S. Powell. 1998. 5-oxo-ETE induces pulmonary eosinophilia in an integrin-dependent manner in Brown Norway rats. J. Clin. Invest. 102:2165-2172.
40. Truong-Tran, A.Q., D. Grosser, R.E. Ruffin, C. Murgia, and P.D. Zalewski. 2003. Apoptosis in the normal and inflamed airway epithelium: role of zinc in epithelial protection and procaspase-3 regulation. Biochem. Pharmacol. 66:1459-1468.
41. Laitinen, L.A., M. Heino, A. Laitinen, T. Kava, and T. Haahtela. 1985. Damage of the airway epithelium and bronchial reactivity in patients with asthma. Am. Rev. Respir. Dis. 131:599-606.
42. Frade, J.M., and T.M. Michaelidis. 1997. Origin of eukaryotic programmed cell death: a consequence of aerobic metabolism? Bioessays. 19:827-832.
43. Shim, J.J., K. Dabbagh, I.F. Ueki, T. Dao-Pick, P.R. Burgel, K. Takeyama, D.C. Tam, and J.A. Nadel. 2001. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils. Am. J. Physiol. Lung Cell. Mol. Physiol. 280:L134-L140.
44. Osebold, J.W., Y.C. Zee, and L.J. Gershwin. 1988. Enhancement of allergic lung sensitization in mice by ozone inhalation. Proc. Soc. Exp. Biol. Med. 188:259-264.
45. Neuhaus-Steinmetz, U., F. Uffhausen, U. Herz, and H. Renz. 2000. Priming of allergic immune responses by repeated ozone exposure in mice. Am. J. Respir. Cell Mol. Biol. 23:228-233.
46. Wedemeyer, J., M. Tsai, and S.J. Galli. 2000. Roles of mast cells and basophils in innate and acquired immunity. Curr. Opin. Immunol. 12:624-631.
47. Walter, D.M., J.J. McIntire, G. Berry, A.N. McKenzie, D.D. Donaldson, R.H. DeKruyff, and D.T. Umetsu. 2001. Critical role for IL-13 in the development of allergen-induced airway hyperreactivity. J. Immunol. 167:4668-4675.
48. Itoh, K., T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, et al. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236:313-322.
49. Ramos-Gomez, M., M.K. Kwak, P.M. Dolan, K. Itoh, M. Yamamoto, P. Talalay, and T.W. Kensler. 2001. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in Nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. USA. 98:3410-3415.
50. Saltini, C., A.J. Hance, V.J. Ferrans, F. Basset, P.B. Bitterman, and R.G. Crystal. 1984. Accurate quantification of cells recovered by bronchoalveolar lavage. Am. Rev. Respir. Dis. 130:650-658.
51. Steiger, D., J. Hotchkiss, L. Bajaj, J. Harkema, and C. Basbaum. 1995. Concurrent increases in the storage and release of mucin-like molecules by rat airway epithelial cells in response to bacterial endotoxin. Am. J. Respir. Cell Mol. Biol. 12:307-314.
52. Jiang, Z.Y., J.V. Hunt, and S.P. Wolff. 1992. Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal. Biochem. 202:384-389.
53. Oliver, C.N., B.W. Ahn, E.J. Moerman, S. Goldstein, and E.R. Stadtman. 1987. Age-related changes in oxidized proteins. J. Biol. Chem. 262:5488-5491.
54. Ewart, S., R. Levitt, and W. Mitzner. 1995. Respiratory system mechanics in mice measured by end-inflation occlusion. J. Appl. Physiol. 79:560-566.
55. Tirumalai, R., T. Rajesh Kumar, K.H. Mai, and S. Biswal. 2002. Acrolein causes transcriptional induction of phase II genes by activation of Nrf2 in human lung type II epithelial (A549) cells. Toxicol. Lett. 132: 27-36.