NF-κB mediates mesenchymal transition, remodeling, and pulmonary fibrosis in response to chronic inflammation by viral RNA patterns

American Journal of Respiratory Cell and Molecular Biology

Volumn 56, Issue 4, 2017, Pages 506-520

  Tian, Bing ^a,b   Patrikeev, Igor ^b   Ochoa, Lorenzo ^b   Vargas, Gracie ^b   Belanger, Karry Anne K ^a   Litvinov, Julia ^a   Boldogh, Istvan ^a,b   Ameredes, Bill T ^a,b   Motamedi, Massoud ^b   Brasier, Allan R ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Airway reprogramming; Epithelial mesenchymal transition; Polyinosinic:polycytidylic acid; Tissue clearing; Toll like receptor 3

Indexed keywords

4 (2 AMINOETHYLAMINO) 1,8 DIMETHYLIMIDAZO[1,2 A]QUINOXALINE; FIBRONECTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR SNAIL; VIMENTIN; VIRUS RNA; ZINC FINGER PROTEIN; COLLAGEN; TLR3 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL EXPANSION; CHRONIC INFLAMMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LUNG FIBROSIS; LUNG PARENCHYMA; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; AIRWAY REMODELING; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; CHRONIC DISEASE; COMPLICATION; DIAGNOSTIC IMAGING; DRUG EFFECTS; EPITHELIUM CELL; LUNG; MESODERM; METABOLISM; NEUTROPHIL; PATHOLOGY; PATHOPHYSIOLOGY; PNEUMONIA;

AIRWAY REMODELING; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CHRONIC DISEASE; COLLAGEN; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; LUNG; MESODERM; MICE, INBRED C57BL; NEUTROPHILS; NF-KAPPA B; PNEUMONIA; POLY I-C; PULMONARY FIBROSIS; RNA, VIRAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; X-RAY MICROTOMOGRAPHY;

EID: 85017365754     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2016-0259OC     Document Type: Article

References (54)

1. Akinbami LJ, Moorman JE, Bailey C, Zahran HS, King M, Johnson CA, Liu X. Trends in asthma prevalence, health care use, and mortality in the United States, 2001-2010. NCHS Data Brief 2012;(94):1-8.
2. Al-Muhsen S, Johnson JR, Hamid Q. Remodeling in asthma. J Allergy Clin Immunol 2011;128:451-462; quiz 463-454.
3. Wedzicha JA. Role of viruses in exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2004;1:115-120.
4. Harris WT, Kelly DR, Zhou Y, Wang D, MacEwen M, Hagood JS, Clancy JP, Ambalavanan N, Sorscher EJ. Myofibroblast differentiation and enhanced TGF-B signaling in cystic fibrosis lung disease. PLoS One 2013;8:e70196.
5. PLoS One 8
6. Fedorov IA, Wilson SJ, Davies DE, Holgate ST. Epithelial stress and structural remodelling in childhood asthma. Thorax 2005;60: 389-394.
7. Noble PW, Barkauskas CE, Jiang D. Pulmonary fibrosis: patterns and perpetrators. J Clin Invest 2012;122:2756-2762.
8. Holgate ST, Holloway J, Wilson S, Bucchieri F, Puddicombe S, Davies DE. Epithelial-mesenchymal communication in the pathogenesis of chronic asthma. Proc Am Thorac Soc 2004;1:93-98.
9. Aysola RS, Hoffman EA, Gierada D,Wenzel S, Cook-Granroth J, Tarsi J, Zheng J, Schechtman KB, Ramkumar TP, Cochran R, et al. Airway remodeling measured by multidetector CT is increased in severe asthma and correlates with pathology. Chest 2008;134: 1183-1191.
10. Ijaz T, Pazdrak K, Kalita M, Konig R, Choudhary S, Tian B, Boldogh I, Brasier AR. Systems biology approaches to understanding epithelial mesenchymal transition (EMT) in mucosal remodeling and signaling in asthma. World Allergy Organ J 2014;7:13.
11. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J, Pietras K, Virtanen I, Philipson L, Leopold PL, et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 2009;11:943-950.
12. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-1428.
13. Knight DA, Holgate ST. The airway epithelium: structural and functional properties in health and disease. Respirology 2003;8:432-446.
14. Kalita M, Tian B, Gao B, Choudhary S, Wood TG, Carmical JR, Boldogh I, Mitra S, Minna JD, Brasier AR. Systems approaches to modeling chronic mucosal inflammation. BioMed Res Int 2013;2013: 505864.
15. Wang Q, Wang Y, Zhang Y, Zhang Y, Xiao W. The role of uPAR in epithelial-mesenchymal transition in small airway epithelium of patients with chronic obstructive pulmonary disease. Respir Res 2013;14:67.
16. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745.
17. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 2004;350:2645-2653.
18. Johnston SL. Innate immunity in the pathogenesis of virus-induced asthma exacerbations. Proc Am Thorac Soc 2007;4:267-270.
19. Matsumoto K, Inoue H. Viral infections in asthma and COPD. Respir Investig 2014;52:92-100.
20. O'Byrne PM, Pedersen S, Lamm CJ, Tan WC, Busse WW; START Investigators Group. Severe exacerbations and decline in lung function in asthma. Am J Respir Crit Care Med 2009;179:19-24.
21. Bertolusso R, Tian B, Zhao Y, Vergara L, Sabree A, Iwanaszko M, Lipniacki T, Brasier AR, Kimmel M. 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:e93396.
22. Tian B, Li X, Kalita M, Widen SG, Yang J, Bhavnani SK, Dang B, Kudlicki A, Sinha M, Kong F, et al. Analysis of the TGFb-induced program in primary airway epithelial cells shows essential role of NF-kB/RelA signaling network in type II epithelial mesenchymal transition. BMC Genomics 2015;16:529.
23. Stowell NC, Seideman J, Raymond HA, Smalley KA, Lamb RJ, Egenolf DD, Bugelski PJ, Murray LA, Marsters PA, Bunting RA, et al. Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice. Respir Res 2009;10:43.
24. Ramirez RD, Sheridan S, Girard L, Sato M, Kim Y, Pollack J, Peyton M, Zou Y, Kurie JM, Dimaio JM, et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 2004;64:9027-9034.
25. Tian B, Yang J, Zhao Y, Ivanciuc T, Sun H, Garofalo RP, Brasier AR. Bromodomain containing 4 (BRD4) couples NFkB/RelA with airway inflammation and the IRF-RIG-I amplification loop in respiratory syncytial virus infection. J Virol. [online ahead of print] 11 Jan 2017; DOI: 10.1128/JVI.00007-17.
26. Vaughan MB, Ramirez RD, Wright WE, Minna JD, Shay JW. A threedimensional model of differentiation of immortalized human bronchial epithelial cells. Differentiation 2006;74:141-148.
27. Delgado O, Kaisani AA, Spinola M, Xie XJ, Batten KG, Minna JD, Wright WE, Shay JW. Multipotent capacity of immortalized human bronchial epithelial cells. PLoS One 2011;6:e22023.
28. Kaisani A, Delgado O, Fasciani G, Kim SB, Wright WE, Minna JD, Shay JW. Branching morphogenesis of immortalized human bronchial epithelial cells in three-dimensional culture. Differentiation 2014;87: 119-126.
29. Tian B, Zhao Y, Sun H, Zhang Y, Yang J, Brasier AR. BRD4 mediates NFkB-dependent epithelial-mesenchymal transition and pulmonary fibrosis via transcriptional elongation. Am J Physiol Lung Cell Mol Physiol 2016;311:L1183-L1201.
30. Wu Y, Deng J, Rychahou PG, Qiu S, Evers BM, Zhou BP. Stabilization of snail by NF-kB is required for inflammation-induced cell migration and invasion. Cancer Cell 2009;15: 416-428.
31. Hackett TL, Warner SM, Stefanowicz D, Shaheen F, Pechkovsky DV, Murray LA, Argentieri R, Kicic A, Stick SM, Bai TR, et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-b1. Am J Respir Crit Care Med 2009;180:122-133.
32. Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S, Chignard M, Si-Tahar M. Involvement of Toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J Biol Chem 2005;280:5571-5580.
33. Hubner RH, Gitter W, El Mokhtari NE, Mathiak M, Both M, Bolte H, Freitag-Wolf S, Bewig B. Standardized quantification of pulmonary fibrosis in histological samples. Biotechniques 2008;44:507-511, 514-517.
34. Moeller A, Ask K, Warburton D, Gauldie J, Kolb M. The bleomycin animal model: A useful tool to investigate treatment options for idiopathic pulmonary fibrosis? Int J Biochem Cell Biol 2008;40: 362-382.
35. Evans MJ, Van Winkle LS, Fanucchi MV, Plopper CG. The attenuated fibroblast sheath of the respiratory tract epithelial-mesenchymal trophic unit. Am J Respir Cell Mol Biol 1999;21:655-657.
36. Holgate ST. Epithelial damage and response. Clin Exp Allergy 2000;30 (suppl 1):37-41.
37. Lambrecht BN, Hammad H. The airway epithelium in asthma. Nat Med 2012;18:684-692.
38. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci U S A 2006;103: 13180-13185.
39. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, Harris JR, Liang J, Noble PW, Hogan BL. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci U S A 2011;108:E1475-E1483.
40. Desai P, Yang J, Tian B, Sun H, Kalita M, Ju H, Paulucci-Holthauzen A, Zhao Y, Brasier AR, Sadygov RG. Mixed-effects model of epithelial-mesenchymal transition reveals rewiring of signaling networks. Cell Signal 2015;27:1413-1425.
41. Zhao Y, Tian B, Sadygov RG, Zhang Y, Brasier AR. Integrative proteomic analysis reveals reprograming tumor necrosis factor signaling in epithelial mesenchymal transition. J Proteomics 2016; 148:126-138.
42. Aguilera-Aguirre L, Hosoki K, Bacsi A, Radák Z, Sur S, HegdeML, Tian B, Saavedra-Molina A, Brasier AR, Ba X, et al. Whole transcriptome analysis reveals a role for OGG1-initiated DNA repair signaling in airway remodeling. Free Radic Biol Med 2015;89:20-33.
43. Choudhary S, Boldogh I, Brasier AR. Inside-out signaling pathways from nuclear reactive oxygen species control pulmonary innate immunity. J Innate Immun 2016;8:143-155.
44. Kinnier CV, Martinu T, Gowdy KM, Nugent JL, Kelly FL, Palmer SM. Innate immune activation by the viral PAMP poly I:C potentiates pulmonary graft-versus-host disease after allogeneic hematopoietic cell transplant. Transpl Immunol 2011;24:83-93.
45. Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: soldier in the fight against respiratory viruses. Clin Microbiol Rev 2011;24:210-229.
46. Lazo JS, Hoyt DG, Sebti SM, Pitt BR. Bleomycin: A pharmacologic tool in the study of the pathogenesis of interstitial pulmonary fibrosis. Pharmacol Ther 1990;47:347-358.
47. Izbicki G, Segel MJ, Christensen TG, Conner MW, Breuer R. Time course of bleomycin-induced lung fibrosis. Int J Exp Pathol 2002; 83:111-119.
48. Li XW, Wu YH, Li XH, Li D, Du J, Hu CP, Li YJ. Role of eukaryotic translation initiation factor 3a in bleomycin-induced pulmonary fibrosis. Eur J Pharmacol 2015;749:89-97.
49. Reinert T, Serodio da Rocha Baldotto C, Nunes FAP, Alves de Souza Scheliga A. Bleomycin-induced lung injury. J Cancer Res 2013;2013: 480608.
50. Johnston NW, Sears MR. Asthma exacerbations. 1: epidemiology. Thorax 2006;61:722-728.
51. Wilkinson TM, Donaldson GC, Johnston SL, Openshaw PJ, Wedzicha JA. Respiratory syncytial virus, airway inflammation, and FEV1 decline in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006;173:871-876.
52. van Ewijk BE, van der Zalm MM, Wolfs TFW, van der Ent CK. Viral respiratory infections in cystic fibrosis. J Cyst Fibros 2005;4:31-36.
53. Donaldson GC, Seemungal TA, Patel IS, Bhowmik A, Wilkinson TM, Hurst JR, Maccallum PK, Wedzicha JA. Airway and systemic inflammation and decline in lung function in patients with COPD. Chest 2005;128:1995-2004.
54. Barnes PJ, Celli BR. Systemic manifestations and comorbidities of COPD. Eur Respir J 2009;33:1165-1185.