Cigarette Smoke Induced Airway Inflammation Is Independent of NF-κB Signalling

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Rastrick, Joseph M D ^a   Stevenson, Christopher S ^a,b   Eltom, Suffwan ^a   Grace, Megan ^a   Davies, Meirion ^a   Kilty, Iain ^c   Evans, Steven M ^c   Pasparakis, Manolis ^d   Catley, Matthew C ^e   Lawrence, Toby ^f   Adcock, Ian M ^g   Belvisi, Maria G ^a   Birrell, Mark A ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b HOFFMANN LA ROCHE INC   (United States)

^c PFIZER INC   (United States)

^d UNIVERSITY OF COLOGNE   (Germany)

^e ASTRAZENECA R AND D   (Sweden)

^f CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE 2 INHIBITOR; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; UNCLASSIFIED DRUG; 2-((AMINOCARBONYL)AMINO)-5-(4-FLUOROPHENYL)-3-THIOPHENECARBOXAMIDE; AMIDE; I KAPPA B KINASE; IKBKB PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; SMOKE; THIOPHENE DERIVATIVE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; EXPOSURE; HUMAN; HUMAN TISSUE; LUNG PARENCHYMA; LYMPHOCYTE COUNT; MACROPHAGE; MALE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; RESPIRATORY TRACT INFLAMMATION; SIGNAL TRANSDUCTION; SMOKING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CHEMISTRY; DISEASE MODEL; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY TRACT DISEASES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKE; TIME; TOBACCO; TOXICITY;

ANIMALIA; MUS;

AMIDES; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; I-KAPPA B KINASE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY TRACT DISEASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOKE; SMOKING; THIOPHENES; TIME FACTORS; TOBACCO; TRANSCRIPTION FACTOR RELA;

EID: 84872777798     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054128     Document Type: Article

References (50)

1. Barnes PJ, (2007) Chronic Obstructive Pulmonary Disease: A Growing but Neglected Global Epidemic. PLoS Med. 4: 779-780.
2. World Health Organization (2008) World health statistics. Geneva. Available: http://www.who.int/whosis/whostat/2008/en/index.html.
3. Barnes PJ, Stockley RA, (2005) COPD: Current therapeutic interventions and future approaches. Eur Respir J. 25: 1084-1106.
4. Di Stefano A, Turato G, Maestrelli P, Mapp CE, Ruggieri MP, et al. (1996) Airflow limitation in chronic bronchitis is associated with T-lymphocyte and macrophage infiltration in bronchial mucosa. Am J Respir Crit Care Med. 153: 629-632.
5. Saetta M, Turato G, Facchini FM, Corbino L, Lucchini RE, et al. (1997) Inflammatory cells in the bronchial glands of smokers with chronic bronchitis. Am J Respir Crit Care Med. 156: 1633-1639.
6. Hogg JC, (2004) Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet. 364: 709-721.
7. Van der Strate BW, Postma DS, Brandsma CA, Melgert BN, Luinge MA, (2006) Cigarette smoke-induced emphysema: A role for the B cell? Am J Respir Crit Care Med. 173: 751-758.
8. Edwards MR, Bartlett NW, Clarke D, Birrell M, Belvisi M, et al. (2009) Targeting the NF-4444B pathway in asthma and chronic obstructive pulmonary disease. Pharmacol Ther. 121: 1-13.
9. Barnes PJ, Karin M, (1997) Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med. 336: 1066-1071.
10. Caramori G, Romagnoli P, Casolari P, Bellaettato, Casoni G, et al. (2003) Nuclear localisation of p65 in sputum macrophages but not in sputum neutrophils during COPD exacerbations. Thorax. 58: 348-351.
11. Di Stefano A, Caramori G, Oates T, Capelli A, Lusuardi M, et al. (2002) Increased expression of nuclear factor-κB in bronchial biopsies from smokers and patients with COPD. Eur Respir J. 20: 556-563.
12. Li Q, Van Antwerp D, Mercurio F, Lee K-F, Verma IM, (1999) Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science 284: 321-325.
13. Podolin PL, Callahan JF, Bolognese BJ, Li YH, Carlson K, et al. (2005) Attenuation of murine collagen-induced arthritis by a novel, potent and selective small molecule inhibitor of IκB kinase 2, TPCA-1, occurs via reduction of pro-inflammatory cytokines and antigen-induced T cell proliferation. J Pharmacol Exp Ther 312: 373-381.
14. Birrell MA, Hardaker E, Wong S, McCluskie K, Catley M, et al. (2005) Ikappa-B kinase-2 inhibitor blocks inflammation in human airway smooth muscle and a rat model of asthma. Am J Respir Crit Care Med. 172: 962-971.
15. Murata T, Shimada M, Sakakibara S, Yoshino T, Masuda T, et al. (2004) Synthesis and structure-activity relationships of novel IKK-beta inhibitors. Part 3: Orally active anti-inflammatory agents. Bioorg Med Chem Lett. 14: 4019-4022.
16. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F, (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem. 274: 10689-10692.
17. Birrell MA, Wong S, Hardaker EL, Catley MC, McCluskie K, et al. (2006) IkappaB kinase-2-independent and-dependent inflammation in airway disease models: relevance of IKK-2 inhibition to the clinic. Mol Pharmacol. 69: 1791-1800.
18. Perl AK, Wert SE, Nagy A, Lobe CG, Whitsett JA, (2002) Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc Natl Acad Sci U S A. 99: 10482-10487.
19. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I, (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8: 265-277.
20. Perl AK, Wert SE, Loudy DE, Shan Z, Blair PA, et al. (2005) Conditional recombination reveals distinct subsets of epithelial cells in trachea, bronchi, and alveoli. Am J Respir Cell Mol Biol. 33: 455-462.
21. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 118: 285-296.
22. Takahashi H, Ogata H, Nishigaki R, Broide DH, Karin M, (2010) Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta- and JNK1-dependent inflammation. Cancer Cell. 17: 89-97.
23. Eltom S, Stevenson CS, Rastrick J, Dale N, Raemdonck K, et al. (2011) P2X7 receptor and caspase 1 activation are central to airway inflammation observed after exposure to tobacco smoke. PLoS One. 6: e24097.
24. Yang SR, Valvo S, Yao H, Kode A, Rajendrasozhan S, et al. (2008) IKK alpha causes chromatin modification on pro-inflammatory genes by cigarette smoke in mouse lung. Am J Respir Cell Mol Biol. 38: 689-698.
25. Yao H, Edirisinghe I, Rajendrasozhan S, Yang SR, Caito S, et al. (2008) Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol. 294: L1174-1186.
26. Valenca SS, Castro P, Pimenta WA, Lanzetti M, Silva SV, et al. (2006) Light cigarette smoke-induced emphysema and NFkappaB activation in mouse lung. Int J Exp Pathol. 87: 373-381.
27. Vlahos R, Bozinovski S, Jones JE, Powell J, Gras J, et al. (2006) Differential protease, innate immunity, and NF-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. Am J Physiol Lung Cell Mol Physiol. 290: L931-945.
28. Thatcher TH, Maggirwar SB, Baglole CJ, Lakatos HF, Gasiewicz TA, et al. (2007) Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-kappaB component RelB. Am J Pathol. 170: 855-864.
29. Li YT, He B, Wang YZ, Wang J, (2009) Effects of intratracheal administration of nuclear factor-kappaB decoy oligodeoxynucleotides on long-term cigarette smoke-induced lung inflammation and pathology in mice. Respir Res. 10: 79.
30. Rajendrasozhan S, Hwang JW, Yao H, Kishore N, Rahman I, (2010) Anti-inflammatory effect of a selective IkappaB kinase-beta inhibitor in rat lung in response to LPS and cigarette smoke. Pulm Pharmacol Ther. 23: 172-181.
31. Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, et al. (2004) Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol. 31: 633-642.
32. Lixuan Z, Jingcheng D, Wenqin Y, Jianhua H, Baojun L, et al. (2010) Baicalin attenuates inflammation by inhibiting NF-kappaB activation in cigarette smoke induced inflammatory models. Pulm Pharmacol Ther. 23: 411-419.
33. Rajendrasozhan S, Chung S, Sundar IK, Yao H, Rahman I, (2010) P50 Targeted disruption of NF-{kappa}B1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling. Am J Physiol Lung Cell Mol Physiol. 298: L197-209.
34. Li YT, He B, Wang YZ, Wang J, (2009) Effects of intratracheal administration of nuclear factor-kappaB decoy oligodeoxynucleotides on long-term cigarette smoke-induced lung inflammation and pathology in mice. Respir Res. 10: 79.
35. Tharappel JC, Cholewa J, Espandiari P, Spear BT, Gairola CG, et al. (2010) Effects of cigarette smoke on the activation of oxidative stress-related transcription factors in female A/J mouse lung. J Toxicol Environ Health A. 73: 1288-1297.
36. Gottipati KR, Poulsen H, Starcher B, (2008) Passive cigarette smoke exposure inhibits ultraviolet light B-induced skin tumors in SKH-1 hairless mice by blocking the nuclear factor kappa B signalling pathway. Exp Dermatol. 17: 780-787.
37. Zhong CY, Zhou YM, Pinkerton KE, (2008) NF-kappaB inhibition is involved in tobacco smoke-induced apoptosis in the lungs of rats. Toxicol Appl Pharmacol. 230: 150-158.
38. Zhong CY, Zhou YM, Joad JP, Pinkerton KE, (2006) Environmental tobacco smoke suppresses nuclear factor-kappaB signaling to increase apoptosis in infant monkey lungs. Am J Respir Crit Care Med. 174: 428-436.
39. Szulakowski P, Crowther AJL, Luis A, Jimenez LA, Donaldson K, et al. (2006) The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 174: 41-50.
40. Drost EM, Skwarski KM, Sauleda J, Soler N, Roca J, et al. (2004) Oxidative stress and airway inflammation in severe exacerbations of COPD. Thorax. 60: 293-300.
41. Beg AA, Baltimore D, (1996) An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 274: 782-784.
42. Greten FR, Arkan MC, Bollrath J, Hsu LC, Goode J, et al. (2007) NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell. 130: 918-931.
43. Fong CH, Bebien M, Didierlaurent A, Nebauer R, Hussell T, et al. (2008) An antiinflammatory role for IKKbeta through the inhibition of "classical" macrophage activation. J Exp Med. 205: 1269-1276.
44. Tudhope SJ, Catley MC, Fenwick PS, Russell RE, Rumsey WL, et al. (2007) The role of IkappaB kinase 2, but not activation of NF-kappaB, in the release of CXCR3 ligands from IFN-gamma-stimulated human bronchial epithelial cells. J Immunol. 179(9): 6237-45.
45. Jacque E, Tchenio T, Piton G, Romeo PH, Baud V, (2005) RelA repression of RelB activity induces selective gene activation downstream of TNF receptors. PNAS. 102(41): 14635-14640.
46. Lee SY, Miller M, Cho JY, Song DJ, et al. (2010) Inactivation of I kappaB-kinase-beta dependent genes in airway epithelium reduces tobacco smoke induced acute airway inflammation. Int Immunopharmacol. 10: 906-912.
47. Oliver KM, Garvey JF, Ng CT, Veale DJ, Fearon U, et al. (2009) Hypoxia activates NF-kappaB-dependent gene expression through the canonical signaling pathway. Antioxid Redox Signal. 11: 2057-2064.
48. Broide DH, Lawrence T, Doherty T, Cho JY, Miller M, et al. (2005) Allergen-induced peribronchial fibrosis and mucus production mediated by IkappaB kinase beta-dependent genes in airway epithelium. Proc Natl Acad Sci U S A. 102: 17723-17728.
49. Culpitt SV, Nightingale JA, Barnes PJ, (1999) Effect of high dose inhaled steroid on cells, cytokines and proteases in induced sputum in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 160: 1635-1639.
50. Keatings VM, Jatakanon A, Worsdall YM, Barnes PJ, (1997) Effects of inhaled and oral glucocorticoids on inflammatory indices in asthma and COPD. Am J Respir Crit Care Med. 155: 542-548.