Therapeutic targets for inflammation-mediated airway remodeling in chronic lung disease

References

• Busse WW, Lemanske RF Asthma. New England Journal of Medicine. 2001;344:350–362.
   PubMed Web of Science ®Google Scholar
• Akinbami LJ, Moorman JE, Bailey C, et al. Trends in asthma prevalence, health care use, and mortality in the United States, 2001–2010. NCHS Data Brief. 2012(94):1–8
   PubMedGoogle Scholar
• Celli BR, MacNee W, Force AET Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. The European Respiratory Journal: Official Journal of the European Society for Clinical Respiratory Physiology. 2004;23(6):932–946.
   PubMed Web of Science ®Google Scholar
• Decramer M, Vestbo J Global strategy for the diagnosis, management, and prevention of COPD. http://www.goldcopd.com/uploads/users/files/GOLD_Report_2014_Oct30.pdf.
   Google Scholar
• Ferkol T, Schraufnagel D The global burden of respiratory disease. Annals of the American Thoracic Society. 2014;11(3):404–406.
   PubMedGoogle Scholar
• Jeffery PK Remodeling and inflammation of bronchi in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2004;1(3):176–183.
   PubMedGoogle Scholar
• Bui DS, Burgess JA, Lowe AJ, et al. Childhood lung function predicts adult chronic obstructive pulmonary disease and asthma-chronic obstructive pulmonary disease overlap syndrome. Am J Respir Crit Care Med. 2017;196(1):39–46.
   PubMed Web of Science ®Google Scholar
• Postma DS, Rabe KF The asthma-copd overlap syndrome. N Engl J Med. 2015;373(13):1241–1249.
   PubMed Web of Science ®Google Scholar
• Kim SR, Rhee YK. Overlap between asthma and copd: where the two diseases converge. Allergy, Asthma & Immunology Research. 2010;2(4):209–214.
   PubMed Web of Science ®Google Scholar
• Dougherty RH, Fahy JV Acute exacerbations of asthma: epidemiology, biology and the exacerbation-prone phenotype. Clinical and Experimental Allergy: Journal of the British Society for Allergy and Clinical Immunology. 2009;39(2):193–202.
   PubMed Web of Science ®Google Scholar
• Seemungal TA, Donaldson GC, Paul EA, et al. Effect of exacerbation on quality of life in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;157(5 Pt 1):1418–1422
   PubMed Web of Science ®Google Scholar
• Donaldson GC, Seemungal TA, Bhowmik A, et al. Relationship between exacerbation frequency and lung function decline in chronic obstructive pulmonary disease. Thorax. 2002;57(10):847–852.
   PubMed Web of Science ®Google Scholar
• Chapman KR, Bourbeau J, Rance L The burden of COPD in Canada: results from the confronting COPD survey. Respiratory Medicine. 2003;97 Suppl C:S23–31
   PubMed Web of Science ®Google Scholar
• Johnston NW, Sears MR Asthma exacerbations · 1: epidemiology. Thorax. 2006;61(8):722–728.
   PubMed Web of Science ®Google Scholar
• Rossi GA, Colin AA Infantile respiratory syncytial virus and human rhinovirus infections: respective role in inception and persistence of wheezing. European Respiratory Journal. 2015;45(3):774–789.
   PubMed Web of Science ®Google Scholar
• Donaldson GC, Seemungal TA, Patel IS, et al. Airway and systemic inflammation and decline in lung function in patients with COPD. Chest. 2005;128(4):1995–2004.
   PubMed Web of Science ®Google Scholar
• Mallia P, Contoli M, Caramori G, et al. Exacerbations of asthma and chronic obstructive pulmonary disease (COPD): focus on virus induced exacerbations. Curr Pharm Des. 2007;13(1):73–97.
   PubMed Web of Science ®Google Scholar
• Jackson DJ, Makrinioti H, Rana BM, et al.IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. Am J Respir Crit Care Med. 2014;190(12):1373–1382.
   PubMed Web of Science ®Google Scholar
• Jozwik A, Habibi MS, Paras A, Zhu J, GuvenelA, Dhariwal J, et al. RSV-specific airway resident memory CD8+ T cells and differential disease severity after experimental human infection. Nature Communications. 2015;6:10224.
   PubMed Web of Science ®Google Scholar
• Calhoun WJ, Haselkorn T, Miller DP, et al. Asthma exacerbations and lung function in patients with severe or difficult-to-treat asthma. The Journal of Allergy and Clinical Immunology. 2015;136(4):1125–1174
   PubMed Web of Science ®Google Scholar
• Grainge CL, Lau LCK, Ward JA, et al. Effect of bronchoconstriction on airway remodeling in asthma. New England Journal of Medicine. 2011;364(21):2006–2015.
   PubMed Web of Science ®Google Scholar
• Bergeron C, Tulic MK, Hamid Q Airway remodelling in asthma: from benchside to clinical practice. Canadian Respiratory Journal. 2010;17(4):e85–93.
   PubMed Web of Science ®Google Scholar
• Takizawa H Remodeling in small airways of asthma. Respiratory Medicine CME. 2008;1(2):69–74.
   Google Scholar
• Holgate ST, Holloway J, Wilson S, et al. Epithelial-mesenchymal communication in the pathogenesis of chronic asthma. Proc Am Thorac Soc. 2004;1(2):93–98.
   PubMedGoogle Scholar
• Prakash YS, Halayko AJ, Gosens R et al.An official American thoracic society research statement: current challenges facing research and therapeutic advances in airway remodeling. Am J Respir Crit Care Med. 2017;195(2):e4–e19.
   PubMed Web of Science ®Google Scholar
• Calhoun WJ, Dick EC, Schwartz LB, et al. A common cold virus, rhinovirus 16, potentiates airway inflammation after segmental antigen bronchoprovocation in allergic subjects. J Clin Invest. 1994;94(6):2200–2208.
   PubMed Web of Science ®Google Scholar
• Message SD, Laza-Stanca V, Mallia P, et al. Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production. Proc Natl Acad Sci USA. 2008;105(36):13562–13567.
   PubMed Web of Science ®Google Scholar
• Mallia P, Message SD, Gielen V, et al. Experimental rhinovirus infection as a human model of chronic obstructive pulmonary disease exacerbation. Am J Respir Crit Care Med. 2011;183(6):734–742.
   PubMed Web of Science ®Google Scholar
• Frew AJ, St-Pierre J, Teran LM, et al. Cellular and mediator responses twenty-four hours after local endobronchial allergen challenge of asthmatic airways. Journal of Allergy and Clinical Immunology. 1996;98(1):133–143.
   PubMed Web of Science ®Google Scholar
• Whitsett JA, Alenghat T. Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat Immunol. 2015;16(1):27–35.
   PubMed Web of Science ®Google Scholar
• Akira S, Takeda K Toll-like receptor signaling. Nature Reviews Immunology. 2004;4(7):499–511.
   PubMed Web of Science ®Google Scholar
• Akira S, Uematsu S, Takeuchi O Pathogen recognition and innate immunity. Cell (Cambridge MA). 2006;124(4):783–801.
   PubMed Web of Science ®Google Scholar
• Liu P, Jamaluddin M, Li K, et al. Retinoic acid-inducible gene I mediates early antiviral response and toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. The Journal of Virology. 2007;81(3):1401–1411.
   PubMed Web of Science ®Google Scholar
• Alexopoulou L, Holt AC, Medzhitov R, et al. Recognition of double-stranded RNA and activation of NF-[kappa]B by toll-like receptor 3. Nature (London). 2001;413(6857):732–738.
   PubMed Web of Science ®Google Scholar
• Choudhary S, Boldogh I, Brasier AR Inside-out signaling pathways from nuclear reactive oxygen species control pulmonary innate immunity. Journal of Innate Immunity. 2016.
   PubMed Web of Science ®Google Scholar
• Hoffmann A, Baltimore D Circuitry of nuclear kappaB factor signaling. Immunological Review. 2006;210:171–186.
   PubMed Web of Science ®Google Scholar
• Bertolusso R, Tian B, Zhao Y, et al. Dynamic cross talk model of the epithelial innate immune response to double-stranded RNA stimulation: coordinated dynamics emerging from cell-level noise. PLoS ONE. 2014;9(4):e93396.
   PubMed Web of Science ®Google Scholar
• Czerkies M, Korwek Z, Prus W, et al.Cell fate in antiviral response arises in the crosstalk of IRF, NF-kappaB and JAK/STAT pathways. Nature Communications. 2018;9(1):493.
   Google Scholar
• Brasier AR, Tian B, Jamaluddin M, Kalita MK, Garofalo RP, and Lu M. RelA Ser276 phosphorylation-coupled Lys310 acetylation controls transcriptional elongation of inflammatory cytokines in respiratory syncytial virus infection. J Virol. 2011;85(22):11752–11769.
   PubMed Web of Science ®Google Scholar
• Tian B, Zhang Y, Luxon BA, et al. Identification of NF-kappaB-dependent gene networks in respiratory syncytial virus-infected cells. J Virol. 2002;76(13):6800–6814.
   PubMed Web of Science ®Google Scholar
• Tian B, Yang J, Zhao Y, et al. Bromodomain containing 4 (BRD4) couples NFκB/RelA with airway inflammation and the IRF-RIG-I amplification loop in respiratory syncytial virus infection Journal of Virology. 2017;91 doi: 10.1128/JVI.00007-17
   Web of Science ®Google Scholar
• Tian B, Zhao Y, Kalita M, et al.CDK9-dependent transcriptional elongation in the innate interferon-stimulated gene response to respiratory syncytial virus infection in airway epithelial cells. J Virol. 2013;87(12):7075–7092.
   PubMed Web of Science ®Google Scholar
• Fang L, Choudhary S, Tian B, et al. Ataxia telangiectasia mutated kinase mediates NF-kappaB serine 276 phosphorylation and interferon expression via the IRF7-RIG-I amplification loop in paramyxovirus infection. J Virol. 2015;89(5):2628–2642.
   PubMed Web of Science ®Google Scholar
• Holt PG, Strickland DH, Wikstrom ME, et al. Regulation of immunological homeostasis in the respiratory tract. Nature Reviews Immunology. 2008;8(2):142–152.
   PubMed Web of Science ®Google Scholar
• Boldogh I, Basci A, Choudhary B, et al. ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation. Journal of Clinical Investigation. 2005;115(8):2169–2179.
   PubMed Web of Science ®Google Scholar
• Rezaee F Polyinosinic: polycytidylic acid induces protein kinase d-dependent disassembly of apical junctions and barrier dysfunction in airway epithelial cells. The Journal of Allergy and Clinical Immunology. 2011;128:1216–1224.
   PubMed Web of Science ®Google Scholar
• Liesman RM, Buchholz UJ, Luongo CL, et al. RSV-encoded NS2 promotes epithelial cell shedding and distal airway obstruction. The Journal of Clinical Investigation. 2014;124(5):2219–2233.
   PubMed Web of Science ®Google Scholar
• Lambrecht BN, Hammad H The airway epithelium in asthma. Nat Med. 2012;18(5):684–692.
   PubMed Web of Science ®Google Scholar
• Xiao C, Puddicombe SM, Field S, et al. Defective epithelial barrier function in asthma. The Journal of Allergy and Clinical Immunology. 2011;128(3): 549–56, 1–12
   PubMed Web of Science ®Google Scholar
• Hosoki K, Redding D, Itazawa T, et al. Innate mechanism of pollen- and cat dander-induced oxidative stress and DNA damage in the airways. The Journal of Allergy and Clinical Immunology. 2017.
   PubMed Web of Science ®Google Scholar
• Peebles RS, Graham BS Pathogenesis of respiratory syncytial virus infection in the murine model. Proceedings of the American Thoracic Society. 2005;2(2):110–115.
   PubMedGoogle Scholar
• Crystal RG, Randell SH, Engelhardt JF, et al. Airway epithelial cells. Proceedings of the American Thoracic Society. 2008;5(7):772–777.
   PubMedGoogle Scholar
• Zhao Y, Jamaluddin M, Zhang Y, et al. Systematic analysis of cell-type differences in the epithelial secretome reveals insights into the pathogenesis of respiratory syncytial virus-induced lower respiratory tract infections. Journal of Immunology (Baltimore, MD: 1950). 2017;198(8):3345–3364.
   PubMed Web of Science ®Google Scholar
• Olszewska-Pazdrak B, Casola A, Saito T, et al. Cell-specific expression of RANTES, MCP-1, and MIP-1alpha by lower airway epithelial cells and eosinophils infected with respiratory syncytial virus. J Virol. 1998;72(6):4756–4764.
   PubMed Web of Science ®Google Scholar
• Rawlins EL, Okubo T, Xue Y, et al. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell. 2009;4(6):525–534.
   PubMed Web of Science ®Google Scholar
• **. Tian B, Yang J, Zhao Y, Ivanciuc T, Sun H, Wakamiya M, et al. Central role of the NF-kappaB pathway in the Scgb1a1-expressing epithelium in mediating respiratory syncytial virus-induced airway inflammation. J Virol. 2018;92(11).
   Web of Science ®Google Scholar
• Tian B, Liu Z, Yang J, et al., Selective antagonists of the bronchiolar epithelial NF-kappaB-bromodomain-containing protein 4 pathway in viral-induced airway inflammation. Cell Rep. 2018;23(4):1138–1151.
   PubMed Web of Science ®Google Scholar
• Stowell NC, Seideman J, Raymond HA, et al. Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice. Respir Res. 2009;10:43.
   PubMed Web of Science ®Google Scholar
• Harris P, Sridhar S, Peng R, et al. Double-stranded RNA induces molecular and inflammatory signatures that are directly relevant to COPD. Mucosal Immunology. 2013;6(3):474–484.
   PubMed Web of Science ®Google Scholar
• Tully JE, Hoffman SM, Lahue KG, et al. Epithelial NF-κB orchestrates house dust mite-induced airway inflammation, Hyperresponsiveness, and Fibrotic Remodeling. The Journal of Immunology. 2013.
   Google Scholar
• Bezemer GF, Sagar S, van Bergenhenegouwen J, et al. Dual role of Toll-like receptors in asthma and chronic obstructive pulmonary disease. Pharmacol Rev. 2012;64(2):337–358.
   PubMed Web of Science ®Google Scholar
• Tian B, Zhao Y, Sun H, et al.4 Mediates NFkB-dependent epithelial-mesenchymal transition and pulmonary fibrosis via transcriptional elongation. The American Journal of Physiology -Lung Cellular and Molecular Physiology 2016;311(6):L1183–L201.
   PubMed Web of Science ®Google Scholar
• Holgate ST, Lackie PM, Davies DE, et al. The bronchial epithelium as a key regulator of airway inflammation and remodelling in asthma. Clinical & Experimental Allergy. 1999;29:90–95.
   PubMed Web of Science ®Google Scholar
• Sisson TH, Mendez M, Choi K, et al. Targeted injury of type II alveolar epithelial cells induces pulmonary fibrosis. Am J Respir Crit Care Med. 2010;181(3):254–263.
   PubMed Web of Science ®Google Scholar
• Schiller HB, Fernandez IE, Burgstaller G, et al. Time- and compartment-resolved proteome profiling of the extracellular niche in lung injury and repair. Mol Syst Biol. 2015;11(7):819.
   PubMed Web of Science ®Google Scholar
• Tian B, Widen SG, Yang J, et al. NFκB is a master transcription factor mediating partial-to fully committed epithelial-mesenchymal transition. Journal of Biological Chemistry. 2018;in press.
   Google Scholar
• Kalluri R, Weinberg RA The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1420–1428.
   PubMed Web of Science ®Google Scholar
• Tian B, Li X, Kalita M, et al. Analysis of the TGFbeta-induced program in primary airway epithelial cells shows essential role of NF-kappaB/RelA signaling network in type II epithelial mesenchymal transition. BMC Genomics. 2015;16(1):529.
   PubMedGoogle Scholar
• Tian B, Patrikeev I, Ochoa L, et al.NF-kappab mediates mesenchymal transition, remodeling, and pulmonary fibrosis in response to chronic inflammation by viral RNA patterns. Am J Respir Cell Mol Biol. 2017;56(4):506–520.
   PubMed Web of Science ®Google Scholar
• Devaiah BN, Lewis BA, Cherman N, et al.BRD4 is an atypical kinase that phosphorylates serine2 of the RNA polymerase II carboxy-terminal domain. Proc Natl Acad Sci USA. 2012;109(18):6927–6932.
   PubMed Web of Science ®Google Scholar
• Devaiah BN, Case-Borden C, Gegonne A, et al.BRD4 is a histone acetyltransferase that evicts nucleosomes from chromatin. Nat Struct Mol Biol. 2016;23(6):540–548.
   PubMed Web of Science ®Google Scholar
• Brown JD, Lin CY, Duan Q, et al.NF-kappaB directs dynamic super enhancer formation in inflammation and atherogenesis. Mol Cell. 2014;56(2):219–231.
   PubMed Web of Science ®Google Scholar
• Tian B, Liu Z, Litvinov J, et al. Efficacy of novel highly specific bromodomain-containing protein 4 inhibitors in innate inflammation-driven airway remodeling. Am J Respir Cell Mol Biol. 2018.
   Google Scholar
• Karvonen HM, Lehtonen ST, Harju T, et al. Myofibroblast expression in airways and alveoli is affected by smoking and COPD. Respiratory Research. 2013;14(1):84.
   PubMedGoogle Scholar
• Kim KK, Kugler MC, Wolters PJ, et al. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA. 2006;103(35):13180–13185.
   PubMed Web of Science ®Google Scholar
• Phillips RJ, Burdick MD, Hong K, et al. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest. 2004;114(3):438–446.
   PubMed Web of Science ®Google Scholar
• Carroll NG, Perry S, Karkhanis A, et al. The airway longitudinal elastic fiber network and mucosal folding in patients with asthma. Am J Respir Crit Care Med. 2000;161(1):244–248.
   PubMed Web of Science ®Google Scholar
• Dube J, Chakir J, Laviolette M, et al. In vitro procollagen synthesis and proliferative phenotype of bronchial fibroblasts from normal and asthmatic subjects. Lab Invest. 1998;78(3):297–307.
   PubMed Web of Science ®Google Scholar
• Thannickal VJ Mechanisms of pulmonary fibrosis: role of activated myofibroblasts and NADPH oxidase. Fibrogenesis & Tissue Repair. 2012;5(1):S23.
   PubMedGoogle Scholar
• Royce SG, Tan L, Koek AA, et al. Effect of extracellular matrix composition on airway epithelial cell and fibroblast structure: implications for airway remodeling in asthma. Annals of Allergy, Asthma & Immunology: Official Publication of the American College of Allergy, Asthma, & Immunology. 2009;102(3):238–246.
   PubMed Web of Science ®Google Scholar
• Tian B, Hosoki K, Liu Z, et al. Mucosal bromodomain-containing protein 4 (brd4) regulates aeroallergen-induced airway remodeling and sensitization Journal Allergy and Clinical Immunology. 2019;in press.
   Google Scholar
• Zhang Y, Sun H, Zhang J, et al. Quantitative assessment of the effects of trypsin digestion methods on affinity purification-mass spectrometry-based protein-protein interaction analysis. J Proteome Res. 2017;16(8):3068–3082.
   PubMed Web of Science ®Google Scholar
• Liu Z, Wang P, Chen H, et al. Drug discovery targeting bromodomain-containing protein 4. J Med Chem. 2017;60(11):4533–4558.
   PubMed Web of Science ®Google Scholar
• Liu Z, Tian B, Chen H, et al. Discovery of potent and selective BRD4 inhibitors capable of blocking TLR3-induced acute airway inflammation. European Journal of Medicinal Chemistry. 2018;151:450–461
   PubMed Web of Science ®Google Scholar