NF-kappaB signaling in chronic inflammatory airway disease

Biomolecules

Volumn 5, Issue 3, 2015, Pages 1266-1283

  Schuliga, Michael ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Airway smooth muscle; Allergic asthma; Alveolar macrophages; Cigarette smoke; Emphysema; Eosinophils; Epithelium; Histone deacetylase; Phosphoinositide 3 kinase delta (PI3K ); Sirtuins

Indexed keywords

2 (6 AMINO 9 PURINYLMETHYL) 5 METHYL 3 (2 METHYLPHENYL) 3H QUINAZOLIN 4 ONE; ALLERGEN; ANTHRAQUINONE DERIVATIVE; CYTOKINE; DEHYDROXYMETHYLEPOXYQUINOMICIN; FLUTICASONE; FORMOTEROL; GLUCOCORTICOID RECEPTOR; I KAPPA B KINASE; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN E; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NORTRIPTYLINE; SOLITHROMYCIN; THEOPHYLLINE; GLUCOCORTICOID;

AIRWAY REMODELING; AIRWAY SMOOTH MUSCLE CELL; ASTHMA; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHRONIC OBSTRUCTIVE LUNG DISEASE; DISEASE MODEL; ENZYME ACTIVITY; EOSINOPHIL; EPITHELIUM CELL; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; INFLAMMATORY CELL; INTRACELLULAR SIGNALING; LUNG ALVEOLUS MACROPHAGE; LYMPHOCYTE; MAST CELL DEGRANULATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; RESPIRATORY TRACT INFLAMMATION; REVIEW; SIGNAL TRANSDUCTION; SMOKING; TRANSACTIVATION; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY SYSTEM;

ASTHMA; GLUCOCORTICOIDS; HUMANS; MOLECULAR TARGETED THERAPY; NF-KAPPA B; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY SYSTEM; SIGNAL TRANSDUCTION;

EID: 85012060126     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom5031266     Document Type: Review

References (118)

1. WHO. Global Surveillance, Prevention and Control of Chronic Respiratory Diseases: A Comprehensive Approach; WHO: Geneva, Switzerland, 2007; p. 155.
2. Decramer, M.; Janssens, W.; Miravitlles, M. Chronic obstructive pulmonary disease. Lancet 2012, 379, 1341-1351
3. Ambrosino, N.; Paggiaro, P. The management of asthma and chronic obstructive pulmonary disease: Current status and future perspectives. Expert Rev. Respir. Med. 2012, 6, 117-127.
4. Tetley, T.D. Inflammatory cells and chronic obstructive pulmonary disease. Curr. Drug Targets Inflamm. Allergy 2005, 4, 607-618.
5. Tubby, C.; Harrison, T.; Todd, I.; Fairclough, L. Immunological basis of reversible and fixed airways disease. Clin. Sci. 2011, 121, 285-296.
6. Papiris, S.A.; Kollintza, A.; Karatza, M.; Manali, E.D.; Sotiropoulou, C.; Milic-Emili, J.; Roussos, C.; Daniil, Z. CD8+ T lymphocytes in bronchoalveolar lavage in idiopathic pulmonary fibrosis. J. Inflamm. 2007, doi:10.1186/1476-9255-4-14.
7. Durham, A.; Adcock, I.M.; Tliba, O. Steroid resistance in severe asthma: Current mechanisms and future treatment. Curr. Pharm. Des. 2011, 17, 674-684.
8. Salter, M.; Biggadike, K.; Matthews, J.L.; West, M.R.; Haase, M.V.; Farrow, S.N.; Uings, I.J.; Gray, D.W. Pharmacological properties of the enhanced-affinity glucocorticoid fluticasone furoate in vitro and in an in vivo model of respiratory inflammatory disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293, L660-L667.
9. Ghosh, S.; May, M.J.; Kopp, E.B. NF-κB and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 1998, 16, 225-260.
10. Hinz, M.; Scheidereit, C. The IkB kinase complex in NF-κB regulation and beyond. EMBO Rep. 2014, 15, 46-61.
11. Koziol-White, C.J.; Panettieri, R.A. Airway smooth muscle and immunomodulation in acute exacerbations of airway disease. Immunol. Rev. 2011, 242, 178-185.
12. Ward, J.E.; Harris, T.; Bamford, T.; Mast, A.; Pain, M.C.; Robertson, C.; Smallwood, D.; Tran, T.; Wilson, J.; Stewart, A.G. Proliferation is not increased in airway myofibroblasts isolated from asthmatics. Eur. Respir. J. 2008, 32, 362-371.
13. Flavell, S.J.; Hou, T.Z.; Lax, S.; Filer, A.D.; Salmon, M.; Buckley, C.D. Fibroblasts as novel therapeutic targets in chronic inflammation. Br. J. Pharmacol. 2008, 153, S241-S246.
14. Li, M.; Riddle, S.R.; Frid, M.G.; el Kasmi, K.C.; McKinsey, T.A.; Sokol, R.J.; Strassheim, D.; Meyrick, B.; Yeager, M.E.; Flockton, A.R., et al. Emergence of fibroblasts with a proinflammatory epigenetically altered phenotype in severe hypoxic pulmonary hypertension. J. Immunol. 2011, 157, 2711-2722.
15. Edwards, M.R.; Bartlett, N.W.; Clarke, D.; Birrell, M.; Belvisi, M.; Johnston, S.L. Targeting the NF-κB pathway in asthma and chronic obstructive pulmonary disease. Pharmacol. Ther. 2009, 121, 1-13.
16. Rajendrasozhan, S.; Yang, S.R.; Edirisinghe, I.; Yao, H.; Adenuga, D.; Rahman, I. Deacetylases and NF-κB in redox regulation of cigarette smoke-induced lung inflammation: Epigenetics in pathogenesis of COPD. Antioxid. Redox Signal. 2008, 10, 799-811.
17. Barnes, P.J. Anti-inflammatory actions of glucocorticoids: Molecular mechanisms. Clin. Sci. 1998, 94, 557-572.
18. Kagoshima, M.; Ito, K.; Cosio, B.; Adcock, I.M. Glucocorticoid suppression of nuclear factor-KB: A role for histone modifications. Biochem. Soc. Trans. 2003, 31, 60-65.
19. Adcock, I.M.; Ito, K.; Barnes, P.J. Histone deacetylation: An important mechanism in inflammatory lung diseases. COPD 2005, 2, 445-455.
20. To, T.; Stanojevic, S.; Moores, G.; Gershon, A.S.; Bateman, E.D.; Cruz, A.A.; Boulet, L.P. Global asthma prevalence in adults: Findings from the cross-sectional world health survey. BMC Public Health 2012, doi:10.1186/1471-2458-12-204.
21. Buist, A.S.; McBurnie, M.A.; Vollmer, W.M.; Gillespie, S.; Burney, P.; Mannino, D.M.; Menezes, A.M.; Sullivan, S.D.; Lee, T.A.; Weiss, K.B., et al. International variation in the prevalence of COPD (the BOLD Study): A population-based prevalence study. Lancet 2007, 370, 741-750.
22. Brusselle, G.; Bracke, K. Targeting immune pathways for therapy in asthma and chronic obstructive pulmonary disease. Ann. Am. Thorac. Soc. 2014, 11, S322-S328.
23. Hart, L.A.; Krishnan, V.L.; Adcock, I.M.; Barnes, P.J.; Chung, K.F. Activation and localization of transcription factor, nuclear factor-KB, in asthma. Am. J. Respir. Crit. Care Med. 1998, 155, 1585-1592.
24. Gagliardo, R.; Chanez, P.; Mathieu, M.; Bruno, A.; Costanzo, G.; Gougat, C.; Vachier, I.; Bousquet, J.; Bonsignore, G.; Vignola, A.M. Persistent activation of nuclear factor-KB signaling pathway in severe uncontrolled asthma. Am. J. Respir. Crit. Care Med. 2003, 168, 1190-1198.
25. Tully, J.E.; Hoffman, S.M.; Lahue, K.G.; Nolin, J.D.; Anathy, V.; Lundblad, L.K.; Daphtary, N.; Aliyeva, M.; Black, K.E.; Dixon, A.E., et al. Epithelial NF-κB orchestrates house dust mite-induced airway inflammation, hyperresponsiveness, and fibrotic remodeling. J. Immunol. 2013, 191, 5811-5821.
26. Poynter, M.E.; Cloots, R.; van Woerkom, T.; Butnor, K.J.; Vacek, P.; Taatjes, D.J.; Irvin, C.G.; Janssen-Heininger, Y.M. NF-κB activation in airways modulates allergic inflammation but not hyperresponsiveness. J. Immunol. 2004, 173, 7003-7009.
27. Poynter, M.E.; Irvin, C.G.; Janssen-Heininger, Y.M. Rapid activation of nuclear factor-KB in airway epithelium in a murine model of allergic airway inflammation. Am. J. Pathol. 2002, 160, 1325-1334.
28. Poynter, M.E.; Irvin, C.G.; Janssen-Heininger, Y.M. A prominent role for airway epithelial NF-κB activation in lipopolysaccharide-induced airway inflammation. J. Immunol. 2003, 170, 6257-6265.
29. Quinton, L.J.; Jones, M.R.; Simms, B.T.; Kogan, M.S.; Robson, B.E.; Skerrett, S.J.; Mizgerd, J.P. Functions and regulation of NF-κB RelA during pneumococcal pneumonia. J. Immunol. 2007, 178, 1896-1903.
30. Donovan, C.E.; Mark, D.A.; He, H.Z.; Liou, H.C.; Kobzik, L.; Wang, Y.; de Sanctis, G.T.; Perkins, D.L.; Finn, P.W. NF-ΚB/Rel transcription factors: c-Rel Promotes airway hyperresponsiveness and allergic pulmonary inflammation. J. Immunol. 1999, 163, 6827-3683.
31. Li, X.; Chen, Q.; Chu, C.; You, H.; Jin, M.; Zhao, X.; Zhu, X.; Zhou, W.; Ji, W. Ovalbumin-induced experimental allergic asthma is Toll-like receptor 2 dependent. Allergy Asthma Proc. 2014, 35, e15-e20.
32. Lam, D.; Ng, N.; Lee, S.; Batzer, G.; Horner, A.A. Airway house dust extract exposures modify allergen-induced airway hypersensitivity responses by TLR4-dependent and independent pathways. J. Immunol. 2008, 151, 2925-2932.
33. Wilson, S.J.; Wallin, A.; Della-Cioppa, G.; Sandstrom, T.; Holgate, S.T. Effects of budesonide and formoterol on NF-κB, adhesion molecules, and cytokines in asthma. Am. J. Respir. Crit. Care Med. 2001, 164, 1047-1052.
34. Hancox, R.J.; Stevens, D.A.; Adcock, I.M.; Barnes, P.J.; Taylor, D.R. Effects of inhaled beta agonist and corticosteroid treatment on nuclear transcription factors in bronchial mucosa in asthma. Thorax 1999, 54, 488-492.
35. Hart, L.; Lim, S.; Adcock, I.; Barnes, P.J.; Chung, K.F. Effects of inhaled corticosteroid therapy on expression and DNA-binding activity of nuclear factor kappaB in asthma. Am. J. Respir. Crit. Care Med. 2000, 161, 224-231.
36. Di Stefano, A.; Caramori, G.; Oates, T.; Capelli, A.; Lusuardi, M.; Gnemmi, I.; Ioli, F.; Chung, K.F.; Donner, C.F.; Barnes, P.J., et al. Increased expression of nuclear factor-KB in bronchial biopsies from smokers and patients with COPD. Eur. Respir. J. 2002, 20, 556-563.
37. Caramori, G.; Romagnoli, M.; Casolari, P.; Bellettato, C.; Casoni, G.; Boschetto, P.; Chung, K.F.; Barnes, P.J.; Adcock, I.M.; Ciaccia, A., et al. Nuclear localisation of p65 in sputum macrophages but not in sputum neutrophils during COPD exacerbations. Thorax 2003, 55, 348-351.
38. Szulakowski, P.; Crowther, A.J.; Jimenez, L.A.; Donaldson, K.; Mayer, R.; Leonard, T.B.; MacNee, W.; Drost, E.M. The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2006, 174, 41-50.
39. Gagliardo, R.; Chanez, P.; Profita, M.; Bonanno, A.; Albano, G.D.; Montalbano, A.M.; Pompeo, F.; Gagliardo, C.; Merendino, A.M.; Gjomarkaj, M. IkB kinase-driven nuclear factor-KB activation in patients with asthma and chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 2011, 128, 635.e2-645.e2.
40. Brown, V.; Elborn, J.S.; Bradley, J.; Ennis, M. Dysregulated apoptosis and NFkB expression in COPD subjects. Respir. Res. 2009, doi:10.1186/1465-9921-10-24.
41. Yang, S.R.; Yao, H.; Rajendrasozhan, S.; Chung, S.; Edirisinghe, I.; Valvo, S.; Fromm, G.; McCabe, M.J., Jr.; Sime, P.J.; Phipps, R.P., et al. RelB is differentially regulated by IkB Kinase-a in B cells and mouse lung by cigarette smoke. Am. J. Respir. Cell Mol. Biol. 2009, 40, 147-158.
42. Li, Y.T.; He, B.; Wang, Y.Z.; Wang, J. Effects of intratracheal administration of nuclear factor-KB decoy oligodeoxynucleotides on long-term cigarette smoke-induced lung inflammation and pathology in mice. Respir. Res. 2009, doi:10.1186/1465-9921-10-79.
43. Rajendrasozhan, S.; Hwang, J.W.; Yao, H.; Kishore, N.; Rahman, I. Anti-inflammatory effect of a selective IkB kinase-beta inhibitor in rat lung in response to LPS and cigarette smoke. Pulm. Pharmacol. Ther. 2010, 23, 172-181.
44. Rastrick, J.M.; Stevenson, C.S.; Eltom, S.; Grace, M.; Davies, M.; Kilty, I.; Evans, S.M.; Pasparakis, M.; Catley, M.C.; Lawrence, T., et al. Cigarette smoke induced airway inflammation is independent of NF-κB signalling. PLoS ONE 2013, 8, e54128.
45. Yao, H.; Edirisinghe, I.; Rajendrasozhan, S.; Yang, S.R.; Caito, S.; Adenuga, D.; Rahman, I. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294, L1174-L1186.
46. Das, J.; Chen, C.H.; Yang, L.; Cohn, L.; Ray, P.; Ray, A. A critical role for NF-κB in GATA3 expression and TH2 differentiation in allergic airway inflammation. Nat. Immunol. 2001, 2, 45-50.
47. Coward, W.R.; Sagara, H.; Wilson, S.J.; Holgate, S.T.; Church, M.K. Allergen activates peripheral blood eosinophil nuclear factor-KB to generate granulocyte macrophage-colony stimulating factor, tumour necrosis factor-a and interleukin-8. Clin. Exp. Allergy 2004, 34, 1071-1078.
48. Wong, C.K.; Wang, C.B.; Li, M.L.; Ip, W.K.; Tian, Y.P.; Lam, C.W. Induction of adhesion molecules upon the interaction between eosinophils and bronchial epithelial cells: Involvement of p38 MAPK and NF-κB. Int. Immunopharmacol. 2006, 6, 1859-1871.
49. Langereis, J.D.; Raaijmakers, H.A.; Ulfman, L.H.; Koenderman, L. Abrogation of NF-κB signaling in human neutrophils induces neutrophil survival through sustained p38-MAPK activation. J. Leukoc. Biol. 2010, 88, 655-664.
50. Murugan, V.; Peck, M.J. Signal transduction pathways linking the activation of alveolar macrophages with the recruitment of neutrophils to lungs in chronic obstructive pulmonary disease. Exp. Lung Res. 2009, 35, 439-485.
51. Yang, S.R.; Chida, A.S.; Bauter, M.R.; Shafiq, N.; Seweryniak, K.; Maggirwar, S.B.; Kilty, I.; Rahman, I. Cigarette smoke induces proinflammatory cytokine release by activation of NF-κB and posttranslational modifications of histone deacetylase in macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291, L46-L57.
52. Lee, H.C.; Ziegler, S.F. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkB. Proc. Natl. Acad. Sci. USA 2007, 104, 914-919.
53. Newton, R.; Holden, N.S.; Catley, M.C.; Oyelusi, W.; Leigh, R.; Proud, D.; Barnes, P.J. Repression of inflammatory gene expression in human pulmonary epithelial cells by small-molecule IkB kinase inhibitors. J. Pharmacol. Exp. Ther. 2007, 321, 734-742.
54. Shimizu, K.; Konno, S.; Ozaki, M.; Umezawa, K.; Yamashita, K.; Todo, S.; Nishimura, M. Dehydroxymethylepoxyquinomicin (DHMEQ), a novel NF-κB inhibitor, inhibits allergic inflammation and airway remodelling in murine models of asthma. Clin. Exp. Allergy 2012, 42, 1273-1281.
55. Cao, J.; Ren, G.; Gong, Y.; Dong, S.; Yin, Y.; Zhang, L. Bronchial epithelial cells release IL-6, CXCL1 and CXCL8 upon mast cell interaction. Cytokine 2011, 56, 823-831.
56. Redhu, N.S.; Saleh, A.; Halayko, A.J.; Ali, A.S.; Gounni, A.S. Essential role of NF-κB and AP-1 transcription factors in TNF-a-induced TSLP expression in human airway smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 300, L479-L485.
57. Tirumurugaan, K.G.; Kang, B.N.; Panettieri, R.A.; Foster, D.N.; Walseth, T.F.; Kannan, M.S. Regulation of the CD38 promoter in human airway smooth muscle cells by TNF-a and dexamethasone. Respir. Res. 2008, doi:10.1186/1465-9921-9-26.
58. Lee, C.W.; Lin, W.N.; Lin, C.C.; Luo, S.F.; Wang, J.S.; Pouyssegur, J.; Yang, C.M. Transcriptional regulation of VCAM-1 expression by tumor necrosis factor-alpha in human tracheal smooth muscle cells: Involvement of MAPKs, NF-κB, p300, and histone acetylation. J. Cell. Physiol. 2006, 207, 174-186.
59. Catley, M.C.; Sukkar, M.B.; Chung, K.F.; Jaffee, B.; Liao, S.M.; Coyle, A.J.; Haddad, El-B.; Barnes, P.J.; Newton, R. Validation of the anti-inflammatory properties of small-molecule IkB Kinase (IKK)-2 inhibitors by comparison with adenoviral-mediated delivery of dominant-negative IKK1 and IKK2 in human airways smooth muscle. Mol. Pharmacol. 2006, 70, 697-705.
60. John, A.E.; Zhu, Y.M.; Brightling, C.E.; Pang, L.; Knox, A.J. Human airway smooth muscle cells from asthmatic individuals have CXCL8 hypersecretion due to increased NF-κB p65, C/EBP ß, and RNA polymerase II binding to the CXCL8 promoter. J. Immunol. 2009, 153, 4682-4692.
61. Alrashdan, Y.A.; Alkhouri, H.; Chen, E.; Lalor, D.J.; Poniris, M.; Henness, S.; Brightling, C.E.; Burgess, J.K.; Armour, C.L.; Ammit, A.J., et al. Asthmatic airway smooth muscle CXCL10 production: Mitogen-activated protein kinase JNK involvement. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 302, L1118-L1127.
62. Gras, D.; Chanez, P.; Vachier, I.; Petit, A.; Bourdin, A. Bronchial epithelium as a target for innovative treatments in asthma. Pharmacol. Ther. 2013, 140, 290-305.
63. Clarke, D.L.; Clifford, R.L.; Jindarat, S.; Proud, D.; Pang, L.; Belvisi, M.; Knox, A.J. TNFa and IFNy synergistically enhance transcriptional activation of CXCL10 in human airway smooth muscle cells via STAT-1, NF-κB, and the transcriptional coactivator CREB-binding protein. J. Biol. Chem. 2010,255, 29101-29110.
64. Pelaia, G.; Vatrella, A.; Busceti, M.T.; Gallelli, L.; Calabrese, C.; Terracciano, R.; Maselli, R. Cellular mechanisms underlying eosinophilic and neutrophilic airway inflammation in asthma. Mediat. Inflamm. 2015, doi:10.1155/2015/879783.
65. Brusselle, G.G.; Maes, T.; Bracke, K.R. Eosinophils in the spotlight: Eosinophilic airway inflammation in nonallergic asthma. Nat. Med. 2013, 19, 977-979.
66. Chien, J.W.; Lin, C.Y.; Yang, K.D.; Lin, C.H.; Kao, J.K.; Tsai, Y.G. Increased IL-17A secreting CD4+ T cells, serum IL-17 levels and exhaled nitric oxide are correlated with childhood asthma severity. Clin. Exp. Allergy 2013, 43, 1018-1026.
67. Chesne, J.; Braza, F.; Mahay, G.; Brouard, S.; Aronica, M.; Magnan, A. IL-17 in severe asthma. Where do we stand? Am. J. Respir. Crit. Care Med. 2014, 190, 1094-1101.
68. Fujisawa, T.; Chang, M.M.; Velichko, S.; Thai, P.; Hung, L.Y.; Huang, F.; Phuong, N.; Chen, Y.; Wu, R. NF-κB mediates IL-1ß- and IL-17A-induced MUC5B expression in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2011, 45, 246-252.
69. Dragon, S.; Hirst, S.J.; Lee, T.H.; Gounni, A.S. IL-17A mediates a selective gene expression profile in asthmatic human airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 2014, 50, 1053-1063.
70. Chang, Y.; Al-Alwan, L.; Risse, P.A.; Halayko, A.J.; Martin, J.G.; Baglole, C.J.; Eidelman, D.H.; Hamid, Q. Th17-associated cytokines promote human airway smooth muscle cell proliferation. FASEB J. 2012, 26, 5152-5160.
71. Kankaanranta, H.; Ilmarinen, P.; Zhang, X.; Adcock, I.M.; Lahti, A.; Barnes, P.J.; Giembycz, M.A.; Lindsay, M.A.; Moilanen, E. Tumour necrosis factor-a regulates human eosinophil apoptosis via ligation of TNF-receptor 1 and balance between NF-κB and AP-1. PLoS ONE 2014, 9, e90298.
72. Ordonez, C.L.; Shaughnessy, T.E.; Matthay, M.A.; Fahy, J.V. Increased neutrophil numbers and IL-8 levels in airway secretions in acute severe asthma: Clinical and biologic significance. Am. J. Respir. Crit. Care Med. 2000, 161, 1185-1190.
73. Nakagome, K.; Matsushita, S.; Nagata, M. Neutrophilic inflammation in severe asthma. Int. Arch. Allergy Immunol. 2012, 158, 96-102.
74. Pappas, K.; Papaioannou, A.I.; Kostikas, K.; Tzanakis, N. The role of macrophages in obstructive airways disease: Chronic obstructive pulmonary disease and asthma. Cytokine 2013, 64, 613-625.
75. Cundall, M.; Sun, Y.; Miranda, C.; Trudeau, J.B.; Barnes, S.; Wenzel, S.E. Neutrophil-derived matrix metalloproteinase-9 is increased in severe asthma and poorly inhibited by glucocorticoids. J. Allergy Clin. Immunol. 2003, 112, 1064-1071.
76. Wang, C.B.; Wong, C.K.; Ip, W.K.; Li, M.L.; Tian, Y.P.; Lam, C.W. Induction of IL-6 in co-culture of bronchial epithelial cells and eosinophils is regulated by p38 MAPK and NF-κB. Allergy 2005, 60, 1378-1385.
77. Kang, J.H.; Hwang, S.M.; Chung, I.Y. S100A8, S100A9 and S100A12 activate airway epithelial cells to produce MUC5AC via extracellular signal-regulated kinase and nuclear factor-KB pathways. Immunology 2015, 144, 79-90.
78. James, A.L.; Wenzel, S. Clinical relevance of airway remodelling in airway diseases. Eur. Respir. J. 2007, 30, 134-155.
79. Amin, K.; Ludviksdottir, D.; Janson, C.; Nettelbladt, O.; Bjornsson, E.; Roomans, G.M.; Boman, G.; Seveus, L.; Venge, P. Inflammation and structural changes in the airways of patients with atopic and nonatopic asthma. BHR Group. Am. J. Respir. Crit. Care Med. 2000, 162, 2295-2301.
80. Gosselink, J.V.; Hayashi, S.; Elliott, W.M.; Xing, L.; Chan, B.; Yang, L.; Wright, C.; Sin, D.; Pare, P.D.; Pierce, J.A., et al. Differential expression of tissue repair genes in the pathogenesis of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2010, 181, 1329-1335.
81. Xia, Y.C.; Redhu, N.S.; Moir, L.M.; Koziol-White, C.; Ammit, A.J.; Al-Alwan, L.; Camoretti-Mercado, B.; Clifford, R.L. Pro-inflammatory and immunomodulatory functions of airway smooth muscle: Emerging concepts. Pulm. Pharmacol. Ther. 2013, 26, 64-74.
82. Tran, T.; Fernandes, D.J.; Schuliga, M.; Harris, T.; Landells, L.; Stewart, A.G. Stimulus-dependent glucocorticoid-resistance of GM-CSF production in human cultured airway smooth muscle. Br. J. Pharmacol. 2005, 145, 123-131.
83. Keenan, C.R.; Salem, S.; Fietz, E.R.; Gualano, R.C.; Stewart, A.G. Glucocorticoid-resistant asthma and novel anti-inflammatory drugs. Drug Discov. Today 2012, 17, 1031-1038.
84. Salem, S.; Harris, T.; Mok, J.S.; Li, M.Y.; Keenan, C.R.; Schuliga, M.J.; Stewart, A.G. Transforming growth factor-ß impairs glucocorticoid activity in the A549 lung adenocarcinoma cell line. Br. J. Pharmacol. 2012, 166, 2036-2048.
85. Langenbach, S.Y.; Wheaton, B.J.; Fernandes, D.J.; Jones, C.; Sutherland, T.E.; Wraith, B.C.; Harris, T.; Schuliga, M.J.; McLean, C.; Stewart, A.G. Resistance of fibrogenic responses to glucocorticoid and 2-methoxyestradiol in bleomycin-induced lung fibrosis in mice. Can. J. Physiol. Pharmacol. 2007, 85, 727-738.
86. Bonacci, J.V.; Schuliga, M.; Harris, T.; Stewart, A.G. Collagen impairs glucocorticoid actions in airway smooth muscle through integrin signalling. Br. J. Pharmacol. 2006, 149, 365-373.
87. Barnes, P.J. Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 2013, 131, 636-645
88. Adcock, I.M.; Cosio, B.; Tsaprouni, L.; Barnes, P.J.; Ito, K. Redox regulation of histone deacetylases and glucocorticoid-mediated inhibition of the inflammatory response. Antioxid. Redox Signal. 2005, 7, 144-152.
89. Kagoshima, M.; Wilcke, T.; Ito, K.; Tsaprouni, L.; Barnes, P.J.; Punchard, N.; Adcock, I.M. Glucocorticoid-mediated transrepression is regulated by histone acetylation and DNA methylation. Eur. J. Pharmacol. 2001, 429, 327-334.
90. Ito, K.; Yamamura, S.; Essilfie-Quaye, S.; Cosio, B.; Ito, M.; Barnes, P.J.; Adcock, I.M. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-κB suppression. J. Exp. Med. 2006, 203, 7-13.
91. Rajendrasozhan, S.; Yang, S.R.; Kinnula, V.L.; Rahman, I. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2008, 177, 861-870.
92. Chen, Y.; Wang, H.; Luo, G.; Dai, X. SIRT4 inhibits cigarette smoke extracts-induced mononuclear cell adhesion to human pulmonary microvascular endothelial cells via regulating NF-κB activity. Toxicol. Lett. 2014, 226, 320-327.
93. Keenan, C.R.; Schuliga, M.J.; Stewart, A.G. Pro-inflammatory mediators increase levels of the noncoding RNA GAS5 in airway smooth muscle and epithelial cells. Can. J. Physiol. Pharmacol. 2015, 93, 203-206.
94. Eddleston, J.; Herschbach, J.; Wagelie-Steffen, A.L.; Christiansen, S.C.; Zuraw, B.L. The anti-inflammatory effect of glucocorticoids is mediated by glucocorticoid-induced leucine zipper in epithelial cells. J. Allergy Clin. Immunol. 2007, 119, 115-122.
95. Ayroldi, E.; Migliorati, G.; Bruscoli, S.; Marchetti, C.; Zollo, O.; Cannarile, L.; D'Adamio, F.; Riccardi, C. Modulation of T-cell activation by the glucocorticoid-induced leucine zipper factor via inhibition of nuclear factor kB. Blood 2001, 95, 743-753.
96. Che, W.; Manetsch, M.; Quante, T.; Rahman, M.M.; Patel, B.S.; Ge, Q.; Ammit, A.J. Sphingosine 1-phosphate induces MKP-1 expression via p38 MAPK- and CREB-mediated pathways in airway smooth muscle cells. Biochim. Biophys. Acta 2012, 1523, 1658-1665.
97. Manetsch, M.; Che, W.; Seidel, P.; Chen, Y.; Ammit, A.J. MKP-1: A negative feedback effector that represses MAPK-mediated pro-inflammatory signaling pathways and cytokine secretion in human airway smooth muscle cells. Cell Signal. 2012, 24, 907-913.
98. King, E.M.; Holden, N.S.; Gong, W.; Rider, C.F.; Newton, R. Inhibition of NF-ΚB-dependent transcription by MKP-1: Transcriptional repression by glucocorticoids occurring via p38 MAPK. J. Biol. Chem. 2009, 254, 26803-26815.
99. Ziegelbauer, K.; Gantner, F.; Lukacs, N.W.; Berlin, A.; Fuchikami, K.; Niki, T.; Sakai, K.; Inbe, H.; Takeshita, K.; Ishimori, M., et al. A selective novel low-molecular-weight inhibitor of IkB kinase-ß (IKK-ß) prevents pulmonary inflammation and shows broad anti-inflammatory activity. Br. J. Pharmacol. 2005, 145, 178-192.
100. Sugita, A.; Ogawa, H.; Azuma, M.; Muto, S.; Honjo, A.; Yanagawa, H.; Nishioka, Y.; Tani, K.; Itai, A.; Sone, S. Antiallergic and anti-inflammatory effects of a novel IkB kinase beta inhibitor, IMD-0354, in a mouse model of allergic inflammation. Int. Arch. Allergy Immunol. 2009, 145, 186-198.
101. Ogawa, H.; Azuma, M.; Muto, S.; Nishioka, Y.; Honjo, A.; Tezuka, T.; Uehara, H.; Izumi, K.; Itai, A.; Sone, S. IkB kinase beta inhibitor IMD-0354 suppresses airway remodelling in a Dermatophagoides pteronyssinus'-sensitized mouse model of chronic asthma. Clin. Exp. Allergy 2011, 41, 104-115.
102. Sommers, C.D.; Thompson, J.M.; Guzova, J.A.; Bonar, S.L.; Rader, R.K.; Mathialagan, S.; Venkatraman, N.; Holway, V.W.; Kahn, L.E.; Hu, G., et al. Novel tight-binding inhibitory factor-KB kinase (IKK-2) inhibitors demonstrate target-specific anti-inflammatory activities in cellular assays and following oral and local delivery in an in vivo model of airway inflammation. J. Pharmacol. Exp. Ther. 2009, 330, 377-388.
103. Kobayashi, Y.; Wada, H.; Rossios, C.; Takagi, D.; Charron, C.; Barnes, P.J.; Ito, K. A novel macrolide/fluoroketolide, solithromycin (CEM-101), reverses corticosteroid insensitivity via phosphoinositide 3-kinase pathway inhibition. Br. J. Pharmacol. 2013, 169, 1024-1034.
104. To, Y.; Ito, K.; Kizawa, Y.; Failla, M.; Ito, M.; Kusama, T.; Elliott, W.M.; Hogg, J.C.; Adcock, I.M.; Barnes, P.J. Targeting phosphoinositide-3-kinase-delta with theophylline reverses corticosteroid insensitivity in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2010, 152, 897-904.
105. Mercado, N.; To, Y.; Ito, K.; Barnes, P.J. Nortriptyline reverses corticosteroid insensitivity by inhibition of phosphoinositide-3-kinase-delta. J. Pharmacol. Exp. Ther. 2011, 337, 465-470.
106. Rossios, C.; To, Y.; Osoata, G.; Ito, M.; Barnes, P.J.; Ito, K. Corticosteroid insensitivity is reversed by formoterol via phosphoinositide-3-kinase inhibition. Br. J. Pharmacol. 2012, 167, 775-786.
107. Kobayashi, Y.; Wada, H.; Rossios, C.; Takagi, D.; Higaki, M.; Mikura, S.; Goto, H.; Barnes, P.J.; Ito, K. A novel macrolide solithromycin exerts superior anti-inflammatory effect via NF-κB inhibition. J. Pharmacol. Exp. Ther. 2013, 345, 76-84.
108. Li, M.; Zhong, X.; He, Z.; Wen, M.; Li, J.; Peng, X.; Liu, G.; Deng, J.; Zhang, J.; Bai, J. Effect of erythromycin on cigarette-induced histone deacetylase protein expression and nuclear factor-KB activity in human macrophages in vitro. Int. Immunopharmacol. 2012, 12, 643-650.
109. Lee, K.S.; Park, S.J.; Kim, S.R.; Min, K.H.; Jin, S.M.; Puri, K.D.; Lee, Y.C. Phosphoinositide 3-kinase-delta inhibitor reduces vascular permeability in a murine model of asthma. J. Allergy Clin. Immunol. 2006, 115, 403-409.
110. De Souza Alves, C.C.; Collison, A.; Hatchwell, L.; Plank, M.; Morten, M.; Foster, P.S.; Johnston, S.L.; da Costa, C.F.; de Almeida, M.V.; Couto Teixeira, H., et al. Inhibiting AKT phosphorylation employing non-cytotoxic anthraquinones ameliorates TH2 mediated allergic airways disease and rhinovirus exacerbation. PLoS ONE 2013, 5, e79565.
111. Choi, Y.H.; Jin, G.Y.; Li, L.C.; Yan, G.H. Inhibition of protein kinase C delta attenuates allergic airway inflammation through suppression of PI3K/Akt/mTOR/HIF-1 alpha/VEGF pathway. PLoS ONE 2013, 5, e81773.
112. Kim, S.R.; Lee, K.S.; Park, S.J.; Min, K.H.; Choe, Y.H.; Moon, H.; Yoo, W.H.; Chae, H.J.; Han, M.K.; Lee, Y.C. Involvement of sirtuin 1 in airway inflammation and hyperresponsiveness of allergic airway disease. J. Allergy Clin. Immunol. 2010, 125, 449.e14-460.e14.
113. Chen, J.; Zhou, H.; Wang, J.; Zhang, B.; Liu, F.; Huang, J.; Li, J.; Lin, J.; Bai, J.; Liu, R. Therapeutic effects of resveratrol in a mouse model of HDM-induced allergic asthma. Int. Immunopharmacol. 2015, 25, 43-48.
114. Ichikawa, T.; Hayashi, R.; Suzuki, K.; Imanishi, S.; Kambara, K.; Okazawa, S.; Inomata, M.; Yamada, T.; Yamazaki, Y.; Koshimizu, Y., et al. Sirtuin 1 activator SRT1720 suppresses inflammation in an ovalbumin-induced mouse model of asthma. Respirology 2013, 15, 332-339.
115. Royce, S.G.; Dang, W.; Yuan, G.; Tran, J.; el Osta, A.; Karagiannis, T.C.; Tang, M.L. Resveratrol has protective effects against airway remodeling and airway hyperreactivity in a murine model of allergic airways disease. Pathobiol. Aging Age Relat. Dis. 2011, doi:10.3402/pba.v1i0.7134.
116. Lee, M.; Kim, S.; Kwon, O.K.; Oh, S.R.; Lee, H.K.; Ahn, K. Anti-inflammatory and anti-asthmatic effects of resveratrol, a polyphenolic stilbene, in a mouse model of allergic asthma. Int. Immunopharmacol. 2009, 9, 418-424.
117. Yao, H.; Chung, S.; Hwang, J.W.; Rajendrasozhan, S.; Sundar, I.K.; Dean, D.A.; McBurney, M.W.; Guarente, L.; Gu, W.; Ronty, M., et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J. Clin. Invest. 2012, 122, 2032-2045.
118. Yao, H.; Sundar, I.K.; Ahmad, T.; Lerner, C.; Gerloff, J.; Friedman, A.E.; Phipps, R.P.; Sime, P.J.; McBurney, M.W.; Guarente, L., et al. SIRT1 protects against cigarette smoke-induced lung oxidative stress via a FOXO3-dependent mechanism. Am. J. Physiol. Lung Cell. Mol. Physiol. 2014, 306, L816-L828.