Steroid-resistant neutrophilic inflammation in a mouse model of an acute exacerbation of asthma

American Journal of Respiratory Cell and Molecular Biology

Volumn 39, Issue 5, 2008, Pages 543-550

  Ito, Kazuhiro ^a   Herbert, Cristan ^b   Siegle, Jessica S ^b   Vuppusetty, Chaitanya ^a   Hansbro, Nicole ^d   Thomas, Paul S ^c   Foster, Paul S ^d,e   Barnes, Peter J ^a   Kumar, Rakesh K ^b  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF NEWCASTLE   (Australia)

^e Biology and Environment   (Australia)

Author keywords

Airway inflammation; Cytokines; Dexamethasone; Histone deacetylase 2

Indexed keywords

CHEMOATTRACTANT; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYTOKINE; DEXAMETHASONE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HISTONE ACETYL TRANSFERASE; HISTONE DEACETYLASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; METHACHOLINE; OVALBUMIN; TRANSFERASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; MESSENGER RNA; STEROID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; DISEASE EXACERBATION; DRUG MECHANISM; ENZYME ACTIVITY; EOSINOPHIL; FEMALE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATORY CELL; LIPID PEROXIDATION; MOUSE; NEUTROPHIL; NITRATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; T LYMPHOCYTE; ACUTE DISEASE; ANIMAL; BAGG ALBINO MOUSE; CELL NUCLEUS; DISEASE MODEL; DRUG EFFECT; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY;

MUS;

ACUTE DISEASE; ANIMALS; ASTHMA; BIOLOGICAL MARKERS; CELL NUCLEUS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; INFLAMMATION; MICE; MICE, INBRED BALB C; NEUTROPHILS; NF-KAPPA B; OXIDATIVE STRESS; RNA, MESSENGER; STEROIDS;

EID: 55249088124     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2008-0028OC     Document Type: Article

References (42)

1. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola A. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745.
2. Gibson PG, Simpson JL, Saltos N. Heterogeneity of airway inflammation in persistent asthma: evidence of neutrophilic inflammation and increased sputum interleukin-8. Chest 2001;119:1329-1336.
3. Green RH, Brightling CE, Woltmann G, Parker D, Wardlaw AJ, Pavord ID. Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax 2002;57:875-879.
4. Lamblin C, Gosset P, Tillie-Leblond I, Saulnier F, Marquette CH, Wallaert B, Tonnel AB. Bronchial neutrophilia in patients with noninfectious status asthmaticus. Am J Respir Crit Care Med 1998;157:394-402.
5. Fahy JV, Kim KW, Liu J, Boushey HA. Prominent neutrophilic inflammation in sputum from subjects with asthma exacerbation. J Allergy Clin Immunol 1995;95:843-852.
6. Wark PA, Johnston SL, Moric I, Simpson JL, Hensley MJ, Gibson PG. Neutrophil degranulation and cell lysis is associated with clinical severity in virus-induced asthma. Eur Respir J 2002;19:68-75.
7. Wenzel SE, Schwartz LB, Langmack EL, Halliday JL, Trudeau JB, Gibbs RL, Chu HW. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med 1999;160:1001-1008.
8. in't Veen JC, Smits HH, Hiemstra PS, Zwinderman AE, Sterk PJ, Bel EH. Lung function and sputum characteristics of patients with severe asthma during an induced exacerbation by double-blind steroid withdrawal. Am J Respir Crit Care Med 1999;160:93-99.
9. Barnes PJ. Transcription factors in airway diseases. Lab Invest 2006;86:867-872.
10. Ito K, Yamamura S, Essilfie-Quaye S, Cosio B, Ito M, Barnes PJ, Adcock IM. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. J Exp Med 2006;203:7-13.
11. Ito K, Caramori G, Lim S, Oates T, Chung KF, Barnes PJ, Adcock IM. Expression and activity of histone deacetylases in human asthmatic airways. Am J Respir Crit Care Med 2002;166:392-396.
12. Hew M, Bhavsar P, Torrego A, Meah S, Khorasani N, Barnes PJ, Adcock I, Chung KF. Relative corticosteroid insensitivity of peripheral blood mononuclear cells in severe asthma. Am J Respir Crit Care Med 2006;174:134-141.
13. Ito K, Ito M, Elliott WM, Cosio B, Caramori G, Kon OM, Barczyk A, Hayashi S, Adcock IM, Hogg JC, et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 2005;352:1967-1976.
14. Barnes PJ. New molecular targets for the treatment of neutrophilic diseases. J Allergy Clin Immunol 2007;119:1055-1062. (quiz 1063-1054).
15. Temelkovski J, Hogan SP, Shepherd DP, Foster PS, Kumar RK. An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolised allergen. Thorax 1998;53:849-856.
16. Siegle JS, Hansbro N, Herbert C, Yang M, Foster PS, Kumar RK. Airway hyperreactivity in exacerbation of chronic asthma is independent of eosinophilic inflammation. Am J Respir Cell Mol Biol 2006;35:565-570.
17. Ameredes BT. Cardiac activity during airway resistance alterations with intravenous and inhaled methacholine. Respir Physiolo Neurobiol 2004;139:281-292.
18. Korsgren M, Erjefalt JS, Korsgren O, Sundler F, Persson CGA. Allergic eosinophil-rich inflammation develops in lungs and airways of B cell-deficient mice. J Exp Med 1997;185:885-892.
19. Kumar RK. Quantitative immunohistologic assessment of lymphocyte populations in the pulmonary inflammatory response to intratracheal silica. Am J Pathol 1989;135:605-614.
20. Baggiolini M, Loetscher P, Moser B. Interleukin-8 and the chemokine family. Int J Immunopharmacol 1995;17:103-108.
21. Puddicombe SM, Torres-Lozano C, Richter A, Bucchieri F, Lordan JL, Howarth PH, Vrugt B, Albers R, Djukanovic R, Holgate ST, et al. Increased expression of p21(waf) cyclin-dependent kinase inhibitor in asthmatic bronchial epithelium. Am J Respir Cell Mol Biol 2003;28:61-68.
22. Grissell TV, Powell H, Shafren DR, Boyle MJ, Hensley MJ, Jones PD, Whitehead BF, Gibson PG. Interleukin-10 gene expression in acute virus-induced asthma. Am J Respir Crit Care Med 2005;172:433-439.
23. Green RM, Custovic A, Sanderson G, Hunter J, Johnston SL, Woodcock A. Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study. BMJ 2002;324:763.
24. Proud D, Chow CW. Role of viral infections in asthma and chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2006;35:513-518.
25. Bentley AM, Hamid Q, Robinson DS, Schotman E, Meng Q, Assoufi B, Kay AB, Durham SR. Prednisolone treatment in asthma: reduction in the numbers of eosinophils, T cells, tryptase-only positive mast cells, and modulation of IL-4, IL-5, and interferon-gamma cytokine gene expression within the bronchial mucosa. Am J Respir Crit Care Med 1996;153:551-556.
26. Nguyen LT, Lim S, Oates T, Chung KF. Increase in airway neutrophils after oral but not inhaled corticosteroid therapy in mild asthma. Respir Med 2005;99:200-207.
27. Selby C, MacNee W. Factors affecting neutrophil transit during acute pulmonary inflammation: Minireview. Exp Lung Res 1993;19:407-428.
28. Reutershan J, Ley K. Bench-to-bedside review: acute respiratory distress syndrome - how neutrophils migrate into the lung. Crit Care 2004;8:453-461.
29. Yoshida K, Kondo R, Wang Q, Doerschuk CM. Neutrophil cytoskeletal rearrangements during capillary sequestration in bacterial pneumonia in rats. Am J Respir Crit Care Med 2006;174:689-698.
30. Cox G. Glucocorticoid treatment inhibits apoptosis in human neutrophils: separation of survival and activation outcomes. J Immunol 1995;154:4719-4725.
31. Meagher LC, Cousin JM, Seckl JR, Haslett C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J Immunol 1996;156:4422-4428.
32. Ito K, Hanazawa T, Tomita K, Barnes PJ, Adcock IM. Oxidative stress reduces histone deacetylase 2 activity and enhances IL-8 gene expression: role of tyrosine nitration. Biochem Biophys Res Commun 2004;315:240-245.
33. Rajendrasozhan S, Yang SR, Edirisinghe I, Yao H, Adenuga D, Rahman I. Deacetylases and NF-kappaB in redox regulation of cigarette smoke-induced lung inflammation: epigenetics in pathogenesis of COPD. Antioxid Redox Signal 2008;10:799-811.
34. Wood LG, Garg ML, Simpson JL, Mori TA, Croft KD, Wark PA, Gibson PG. Induced sputum 8-isoprostane concentrations in inflammatory airway diseases. Am J Respir Crit Care Med 2005;171:426-430.
35. Cha HH, Cram EJ, Wang EC, Huang AJ, Kasler HG, Firestone GL. Glucocorticoids stimulate p21 gene expression by targeting multiple transcriptional elements within a steroid responsive region of the p21waf1/cip1 promoter in rat hepatoma cells. J Biol Chem 1998;273:1998-2007.
36. Wagers S, Lundblad LK, Ekman M, Irvin CG, Bates JH. The allergic mouse model of asthma: normal smooth muscle in an abnormal lung? J Appl Physiol 2004;96:2019-2027.
37. Wagers SS, Norton RJ, Rinaldi LM, Bates JH, Sobel BE, Irvin CG. Extravascular fibrin, plasminogen activator, plasminogen activator inhibitors, and airway hyperresponsiveness. J Clin Invest 2004;114:104-111.
38. Thomas PS, Yates DH, Barnes PJ. Tumor necrosis factor-alpha increases airway responsiveness and sputum neutrophilia in normal human subjects. Am J Respir Crit Care Med 1995;152:76-80.
39. Berry MA, Hargadon B, Shelley M, Parker D, Shaw DE, Green RH, Bradding P, Brightling CE, Wardlaw AJ, Pavord ID. Evidence of a role of tumor necrosis factor alpha in refractory asthma. N Engl J Med 2006;354:697-708.
40. Erin EM, Leaker BR, Nicholson GC, Tan AJ, Green LM, Neighbour H, Zacharasiewicz AS, Turner J, Barnathan ES, Kon OM, et al. The effects of a monoclonal antibody directed against tumor necrosis factor-alpha in asthma. Am J Respir Crit Care Med 2006;174:753-762.
41. Ito K, Lim S, Caramori G, Cosio B, Chung KF, Adcock IM, Barnes PJ. A molecular mechanism of action of theophylline: induction of histone deacetylase activity to decrease inflammatory gene expression. Proc Natl Acad Sci USA 2002;99:8921-8926.
42. Maneechotesuwan K, Essilfie-Quaye S, Meah S, Kelly C, Kharitonov SA, Adcock IM, Barnes PJ. Formoterol attenuates neutrophilic airway inflammation in asthma. Chest 2005;128:1936-1942.