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Volume 53, Issue 8

-induced acute lung injury in the setting of hyperoxia: protective role of tumour necrosis factor-α Free

Abstract

Among the main characteristics of pneumonia are acute lung injury and severe hypoxemia. Although high oxygen supplementation is a valuable supportive therapy in these patients, oxygen itself is known to be a risk factor for acute lung injury. The effects of hyperoxia on lung injury of mice with pneumonia were examined. Hyperoxia treatment reduced survival of the infected mice in an oxygen concentration- and exposure time-dependent manner. The enhanced lethality was associated with an increase in total lung weight and apoptosis markers, but not with bacterial burden in the lungs. Hyperoxia decreased the levels of the antioxidant glutathione (GSH) in infected lungs. Exogenous tumour necrosis factor-α (TNF-α) improved the survival of infected mice kept under hyperoxia. TNF-α effects were associated with restoration of total lung weight and histone DNA and GSH levels on day 2, whereas the lung bacterial burden did not differ significantly. Moreover, upregulation of GSH by TNF-α was observed in the lungs of mice without infection. These results demonstrate that hyperoxia exacerbates pneumonia. The data suggest that TNF-α may be a potential therapeutic candidate for these individuals, not only through modulating host antibacterial systems, but also by mediating induction of the antioxidant GSH.

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2004-08-01
2024-04-20
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References

  1. Barazzone C., White C. W. 2000; Mechanisms of cell injury and death in hyperoxia: role of cytokines and Bcl-2 family proteins. Am J Respir Cell Mol Biol 22:517–519 [CrossRef]
     [Google Scholar]
  2. Barazzone C., Horowitz S., Donati Y. R., Rodriguez I., Piguet P. F. 1998; Oxygen toxicity in mouse lung: pathways to cell death. Am J Respir Cell Mol Biol 19:573–581 [CrossRef]
     [Google Scholar]
  3. Bernard G. R., Lucht W. D., Niedermeyer M. E., Snapper J. R., Ogletree M. L., Brigham K. L. 1984; Effect of N -acetylcysteine on the pulmonary response to endotoxin in the awake sheep and upon in vitro granulocyte function. J Clin Invest 73:1772–1784 [CrossRef]
     [Google Scholar]
  4. Brieland J. K., Remick D. G., Freeman P. T., Hurley M. C., Fantone J. C., Engleberg N. C. 1995; In vivo regulation of replicative Legionella pneumophila lung infection by endogenous tumor necrosis factor alpha and nitric oxide. Infect Immun 63:3253–3258
     [Google Scholar]
  5. Brieland J. K., Remick D. G., LeGendre M. L., Engleberg N. C., Fantone J. C. 1998; In vivo regulation of replicative Legionella pneumophila lung infection by endogenous interleukin-12. Infect Immun 66:65–69
     [Google Scholar]
  6. Brown L. A., Perez J. A., Harris F. L., Clark R. H. 1996; Glutathione supplements protect preterm rabbits from oxidative lung injury. Am J Physiol 270:L446–L451
     [Google Scholar]
  7. Cantin A. M., Hubbard R. C., Crystal R. G. 1989; Glutathione deficiency in the epithelial lining fluid of the lower respiratory tract in idiopathic pulmonary fibrosis. Am Rev Respir Dis 139:370–372 [CrossRef]
     [Google Scholar]
  8. Crapo J. D. 1986; Morphologic changes in pulmonary oxygen toxicity. Annu Rev Physiol 48:721–731 [CrossRef]
     [Google Scholar]
  9. Deneke S. M., Fanburg B. L. 1989; Regulation of cellular glutathione. Am J Physiol 257:L163–L173
     [Google Scholar]
  10. Jensen J. C., Pogrebniak H. W., Pass H. I., Buresh C., Merino M. J., Kauffman D., Venzon D., Langstein H. N., Norton J. A. 1992; Role of tumor necrosis factor in oxygen toxicity. J Appl Physiol 72:1902–1907
     [Google Scholar]
  11. Kazzaz J. A., Xu J., Palaia T. A., Mantell L., Fein A. M., Horowitz S. 1996; Cellular oxygen toxicity.Oxidant injury without apoptosis. J Biol Chem 271:15182–15186 [CrossRef]
     [Google Scholar]
  12. Klein T. W., Yamamoto Y., Brown H. K., Friedman H. 1991; Interferon-gamma induced resistance to Legionella pneumophila in susceptible A/J mouse macrophages. J Leukoc Biol 49:98–103
     [Google Scholar]
  13. Marston B. J., Lipman H. B., Breiman R. F. 1994; Surveillance for Legionnaires’ disease.Risk factors for morbidity and mortality. Arch Intern Med 154:2417–2422 [CrossRef]
     [Google Scholar]
  14. Muller A., Hacker J., Brand B. C. 1996; Evidence for apoptosis of human macrophage-like HL-60 cells by Legionella pneumophila infection. Infect Immun 64:4900–4906
     [Google Scholar]
  15. Newton C., McHugh S., Widen R., Nakachi N., Klein T., Friedman H. 2000; Induction of interleukin-4 (IL-4) by Legionella pneumophila infection in BALB/c mice and regulation of tumor necrosis factor alpha, IL-6, and IL-1β. Infect Immun 68:5234–5240 [CrossRef]
     [Google Scholar]
  16. Park D. R., Skerrett S. J. 1996; IL-10 enhances the growth of Legionella pneumophila in human mononuclear phagocytes and reverses the protective effect of IFN-gamma: differential responses of blood monocytes and alveolar macrophages. J Immunol 157:2528–2538
     [Google Scholar]
  17. Patterson C. E., Butler J. A., Byrne F. D., Rhodes M. L. 1985; Oxidant lung injury: intervention with sulfhydryl reagents. Lung 163:23–32 [CrossRef]
     [Google Scholar]
  18. Rahman I., Li X. Y., Donaldson K., Harrison D. J., MacNee W. 1995; Glutathione homeostasis in alveolar epithelial cells in vitro and lung in vivo under oxidative stress. Am J Physiol 269:L285–L292
     [Google Scholar]
  19. Rahman I., Antonicelli F., MacNee W. 1999; Molecular mechanism of the regulation of glutathione synthesis by tumor necrosis factor-α and dexamethasone in human alveolar epithelial cells. J Biol Chem 274:5088–5096 [CrossRef]
     [Google Scholar]
  20. Reed D. J. 1990; Glutathione: toxicological implications. Annu Rev Pharmacol Toxicol 30:603–631 [CrossRef]
     [Google Scholar]
  21. Skerrett S. J., Bagby G. J., Schmidt R. A., Nelson S. 1997; Antibody-mediated depletion of tumor necrosis factor-alpha impairs pulmonary host defenses to Legionella pneumophila . J Infect Dis 176:1019–1028 [CrossRef]
     [Google Scholar]
  22. Tateda K., Moore T. A., Deng J. C., Newstead M. W., Zeng X., Matsukawa A., Swanson M. S., Yamaguchi K., Standiford T. J. 2001; Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J Immunol 166:3355–3361 [CrossRef]
     [Google Scholar]
  23. Tateda K., Deng J. C., Moore T. A., Newstead M. W., Paine R. III, Kobayashi N., Yamaguchi K., Standiford T. J. 2003; Hyperoxia mediates acute lung injury and increased lethality in murine Legionella pneumonia: the role of apoptosis. J Immunol 170:4209–4216 [CrossRef]
     [Google Scholar]
  24. Tkatch L. S., Kusne S., Irish W. D., Krystofiak S., Wing E. 1998; Epidemiology of Legionella pneumonia and factors associated with Legionella -related mortality at a tertiary care center. Clin Infect Dis 27:1479–1486 [CrossRef]
     [Google Scholar]
  25. Tsan M. F., White J. E., Santana T. A., Lee C. Y. 1990a; Tracheal insufflation of tumor necrosis factor protects rats against oxygen toxicity. J Appl Physiol 68:1211–1219
     [Google Scholar]
  26. Tsan M. F., White J. E., Treanor C., Shaffer J. B. 1990b; Molecular basis for tumor necrosis factor-induced increase in pulmonary superoxide dismutase activities. Am J Physiol 259:L506–L512
     [Google Scholar]
  27. Tsan M. F., White J. E., Michelsen P. B., Wong G. H. 1995; Pulmonary O2 toxicity: role of endogenous tumor necrosis factor. Exp Lung Res 21:589–597 [CrossRef]
     [Google Scholar]
  28. Ward N. S., Waxman A. B., Homer R. J., Mantell L. L., Einarsson O., Du Y., Elias J. A. 2000; Interleukin-6-induced protection in hyperoxic acute lung injury. Am J Respir Cell Mol Biol 22:535–542 [CrossRef]
     [Google Scholar]
  29. Waxman A. B., Einarsson O., Seres T., Knickelbein R. G., Warshaw J. B., Johnston R., Homer R. J., Elias J. A. 1998; Targeted lung expression of interleukin-11 enhances murine tolerance of 100% oxygen and diminishes hyperoxia-induced DNA fragmentation. J Clin Invest 101:1970–1982 [CrossRef]
     [Google Scholar]
  30. Weber C. A., Duncan C. A., Lyons M. J., Jenkinson S. G. 1990; Depletion of tissue glutathione with diethyl maleate enhances hyperbaric oxygen toxicity. Am J Physiol 258:L308–L312
     [Google Scholar]
  31. White C. W., Ghezzi P. 1989; Protection against pulmonary oxygen toxicity by interleukin-1 and tumor necrosis factor: role of antioxidant enzymes and effect of cyclooxygenase inhibitors. Biotherapy 1:361–367 [CrossRef]
     [Google Scholar]
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Legionella-induced acute lung injury in the setting of hyperoxia: protective role of tumour necrosis factor-α
J. Med. Microbiol. 53, 727 (2004); https://doi.org/10.1099/jmm.0.45592-0
/content/journal/jmm/10.1099/jmm.0.45592-0
/content/journal/jmm/10.1099/jmm.0.45592-0
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