Bronchial epithelium in children: A key player in asthma

European Respiratory Review

Volumn 25, Issue 140, 2016, Pages 158-169

  Carsin, Ania ^a,b   Mazenq, Julie ^a,b   Ilstad, Alexandra ^b   Dubus, Jean Christophe ^c   Chanez, Pascal ^b,d   Gras, Delphine ^b  

^a TIMONE HOSPITAL   (France)

^b INSERM   (France)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d HÔPITAL NORD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEFENSIN; LYSOZYME; OMALIZUMAB; AUTACOID; CYTOKINE;

ALLERGIC ASTHMA; ASTHMA; AUTOPSY; BASEMENT MEMBRANE; BRONCHUS BIOPSY; BRONCHUS MUCOSA; CELL CULTURE; CELL JUNCTION; CHEMOTAXIS; DRUG EFFICACY; DRUG TARGETING; EPITHELIUM CELL; HOST RESISTANCE; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; INTERMETHOD COMPARISON; LUNG DEVELOPMENT; LUNG LAVAGE; NASAL BIOPSY; NONHUMAN; REVIEW; AIRWAY REMODELING; ANIMAL; BRONCHUS; DISEASE MODEL; IMMUNOLOGY; METABOLISM; ONSET AGE; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; RESPIRATORY MUCOSA; RISK FACTOR; SIGNAL TRANSDUCTION;

AGE OF ONSET; AIRWAY REMODELING; ANIMALS; ASTHMA; BRONCHI; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; PHENOTYPE; RESPIRATORY MUCOSA; RISK FACTORS; SIGNAL TRANSDUCTION;

EID: 84971554734     PISSN: 09059180     EISSN: 16000617     Source Type: Journal    
DOI: 10.1183/16000617.0101-2015     Document Type: Review

References (76)

1. Global Initiative for Asthma. 2015 GINA Report, Global Strategy for Asthma Management and Prevention. www. ginasthma.org/ Date last accessed: August 11, 2015.
2. Holgate ST. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol Rev 2011; 242: 205-219.
3. Benayoun L, Druilhe A, Dombret M-C, et al. Airway structural alterations selectively associated with severe asthma. Am J Respir Crit Care Med 2003; 167: 1360-1368.
4. Covar RA, Spahn JD, Murphy JR, et al. Progression of asthma measured by lung function in the childhood asthma management program. Am J Respir Crit Care Med 2004; 170: 234-241.
5. Hallstrand TS, Hackett TL, Altemeier WA, et al. Airway epithelial regulation of pulmonary immune homeostasis and inflammation. Clin Immunol 2014; 151: 1-15.
6. Hirota JA, Hackett T-L, Inman MD, et al. Modeling asthma in mice: what have we learned about the airway epithelium? Am J Respir Cell Mol Biol 2011; 44: 431-438.
7. Kumar RK, Foster PS. Are mouse models of asthma appropriate for investigating the pathogenesis of airway hyper-responsiveness?. Front Physiol 2012; 3: 312.
8. Plopper CG, Hyde DM. The non-human primate as a model for studying COPD and asthma. Pulm Pharmacol Ther 2008; 21: 755-766.
9. Bullone M, Lavoie J-P. Asthma “of horses and men” - how can equine heaves help us better understand human asthma immunopathology and its functional consequences? Mol Immunol 2015; 66: 97-105.
10. Hackett T-L, Singhera GK, Shaheen F, et al. Intrinsic phenotypic differences of asthmatic epithelium and its inflammatory responses to respiratory syncytial virus and air pollution. Am J Respir Cell Mol Biol 2011; 45: 1090-1100.
11. McNamara PS, Kicic A, Sutanto EN, et al. Comparison of techniques for obtaining lower airway epithelial cells from children. Eur Respir J 2008; 32: 763-768.
12. Hackett T-L, Shaheen F, Johnson A, et al. Characterization of side population cells from human airway epithelium. Stem Cells 2008; 26: 2576-2585.
13. Hackett T-L, Warner SM, Stefanowicz D, et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-β1. Am J Respir Crit Care Med 2009; 180: 122-133.
14. Lopez-Guisa JM, Powers C, File D, et al. Airway epithelial cells from asthmatic children differentially express proremodeling factors. J Allergy Clin Immunol 2012; 129: 990-997.
15. Kicic A, Sutanto EN, Stevens PT, et al. Intrinsic biochemical and functional differences in bronchial epithelial cells of children with asthma. Am J Respir Crit Care Med 2006; 174: 1110-1118.
16. Kicic A, Hallstrand TS, Sutanto EN, et al. Decreased fibronectin production significantly contributes to dysregulated repair of asthmatic epithelium. Am J Respir Crit Care Med 2010; 181: 889-898.
17. Thavagnanam S, Parker JC, McBrien ME, et al. Effects of IL-13 on mucociliary differentiation of pediatric asthmatic bronchial epithelial cells. Pediatr Res 2011; 69: 95-100.
18. Tillie-Leblond I, de Blic J, Jaubert F, et al. Airway remodeling is correlated with obstruction in children with severe asthma. Allergy 2008; 63: 533-541.
19. Sakiyama J-I, Yamagishi A, Kuroiwa A. Tbx4-Fgf10 system controls lung bud formation during chicken embryonic development. Development 2003; 130: 1225-1234.
20. Martin N, Ruddick A, Arthur GK, et al. Primary human airway epithelial cell-dependent inhibition of human lung mast cell degranulation. PLoS One 2012; 7: e43545.
21. Reeves SR, Kolstad T, Lien T-Y, et al. Fibroblast-myofibroblast transition is differentially regulated by bronchial epithelial cells from asthmatic children. Respir Res 2015; 16: 21.
22. Kasper JY, Hermanns MI, Unger RE, et al. A responsive human triple-culture model of the air-blood barrier: incorporation of different macrophage phenotypes. J Tissue Eng Regen Med 2015 [in press; DOI: 10.1002/term.2032].
23. McDougall CM, Blaylock MG, Douglas JG, et al. Nasal epithelial cells as surrogates for bronchial epithelial cells in airway inflammation studies. Am J Respir Cell Mol Biol 2008; 39: 560-568.
24. Pringle EJ, Richardson HB, Miller D, et al. Nasal and bronchial airway epithelial cell mediator release in children. Pediatr Pulmonol 2012; 47: 1215-1225.
25. Warburton D, El-Hashash A, Carraro G, et al. Lung organogenesis. Curr Top Dev Biol 2010; 90: 73-158.
26. Morrisey EE, Hogan BLM. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 2010; 18: 8-23.
27. Carraro G, El-Hashash A, Guidolin D, et al. miR-17 family of microRNAs controls FGF10-mediated embryonic lung epithelial branching morphogenesis through MAPK14 and STAT3 regulation of E-Cadherin distribution. Dev Biol 2009; 333: 238-250.
28. Marcet B, Chevalier B, Luxardi G, et al. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol 2011; 13: 693-699.
29. Gilliland FD, Li YF, Peters JM. Effects of maternal smoking during pregnancy and environmental tobacco smoke on asthma and wheezing in children. Am J Respir Crit Care Med 2001; 163: 429-436.
30. Fu XW, Wood K, Spindel ER. Prenatal nicotine exposure increases GABA signaling and mucin expression in airway epithelium. Am J Respir Cell Mol Biol 2011; 44: 222-229.
31. Barbato A, Turato G, Baraldo S, et al. Epithelial damage and angiogenesis in the airways of children with asthma. Am J Respir Crit Care Med 2006; 174: 975-981.
32. Milanese M, Crimi E, Scordamaglia A, et al. On the functional consequences of bronchial basement membrane thickening. J Appl Physiol (1985) 2001; 91: 1035-1040.
33. Bourdin A, Kleis S, Chakra M, et al. Limited short-term steroid responsiveness is associated with thickening of bronchial basement membrane in severe asthma. Chest 2012; 141: 1504-1511.
34. Barbato A, Turato G, Baraldo S, et al. Airway inflammation in childhood asthma. Am J Respir Crit Care Med 2003; 168: 798-803.
35. Bossley CJ, Fleming L, Gupta A, et al. Pediatric severe asthma is characterized by eosinophilia and remodeling without T(H)2 cytokines. J Allergy Clin Immunol 2012; 129: 974-982.
36. Parker JC, Thavagnanam S, Skibinski G, et al. Chronic IL9 and IL-13 exposure leads to an altered differentiation of ciliated cells in a well-differentiated paediatric bronchial epithelial cell model. PLoS One 2013; 8: e61023.
37. Lex C, Ferreira F, Zacharasiewicz A, et al. Airway eosinophilia in children with severe asthma: predictive values of noninvasive tests. Am J Respir Crit Care Med 2006; 174: 1286-1291.
38. Cokuğraş H, Akçakaya N, Seçkin İ, et al. Ultrastructural examination of bronchial biopsy specimens from children with moderate asthma. Thorax 2001; 56: 25-29.
39. Payne DN, Adcock IM, Wilson NM, et al. Relationship between exhaled nitric oxide and mucosal eosinophilic inflammation in children with difficult asthma, after treatment with oral prednisolone. Am J Respir Crit Care Med 2001; 164: 1376-1381.
40. de Blic J, Tillie-Leblond I, Tonnel AB, et al. Difficult asthma in children: an analysis of airway inflammation. J Allergy Clin Immunol 2004; 113: 94-100.
41. Bousquet J, Chanez P, Lacoste JY, et al. Eosinophilic inflammation in asthma. N Engl J Med 1990; 323: 1033-1039.
42. Parker J, Sarlang S, Thavagnanam S, et al. A 3-D well-differentiated model of pediatric bronchial epithelium demonstrates unstimulated morphological differences between asthmatic and nonasthmatic cells. Pediatr Res 2010; 67: 17-22.
43. Xiao C, Puddicombe SM, Field S, et al. Defective epithelial barrier function in asthma. J Allergy Clin Immunol 2011; 128: 549-556.
44. de Boer WI, Sharma HS, Baelemans SMI, et al. Altered expression of epithelial junctional proteins in atopic asthma: possible role in inflammation. Can J Physiol Pharmacol 2008; 86: 105-112.
45. Post S, Nawijn MC, Jonker MR, et al. House dust mite-induced calcium signaling instigates epithelial barrier dysfunction and CCL20 production. Allergy 2013; 68: 1117-1125.
46. Blume C, Swindle EJ, Dennison P, et al. Barrier responses of human bronchial epithelial cells to grass pollen exposure. Eur Respir J 2013; 42: 87-97.
47. Stevens PT, Kicic A, Sutanto EN, et al. Dysregulated repair in asthmatic paediatric airway epithelial cells: the role of plasminogen activator inhibitor-1. Clin Exp Allergy 2008; 38: 1901-1910.
48. Lezmi G, Gosset P, Deschildre A, et al. Airway remodeling in preschool children with severe recurrent wheeze. Am J Respir Crit Care Med 2015; 192: 164-171.
49. van Mastrigt E, Vanlaeken L, Heida F, et al. The clinical utility of reticular basement membrane thickness measurements in asthmatic children. J Asthma 2015; 52: 926-930.
50. Hoňková L, Uhlík J, Beránková K, et al. Epithelial basement membrane thickening is related to TGF-Beta 1 expression in children with chronic respiratory diseases. Pediatr Allergy Immunol 2014; 25: 593-599.
51. Payne DNR, Rogers AV, Adelroth E, et al. Early thickening of the reticular basement membrane in children with difficult asthma. Am J Respir Crit Care Med 2003; 167: 78-82.
52. Fahy JV, Dickey BF. Airway mucus function and dysfunction. N Engl J Med 2010; 363: 2233-2247.
53. Evans CM, Kim K, Tuvim MJ, et al. Mucus hypersecretion in asthma: causes and effects. Curr Opin Pulm Med 2009; 15: 4-11.
54. Biragyn A, Ruffini PA, Leifer CA, et al. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 2002; 298: 1025-1029.
55. Vareille M, Kieninger E, Edwards MR, et al. The airway epithelium: soldier in the fight against respiratory viruses. Clin Microbiol Rev 2011; 24: 210-229.
56. Travis SM, Conway BA, Zabner J, et al. Activity of abundant antimicrobials of the human airway. Am J Respir Cell Mol Biol 1999; 20: 872-879.
57. Parker D, Prince A. Innate immunity in the respiratory epithelium. Am J Respir Cell Mol Biol 2011; 45: 189-201.
58. Proud D. The role of defensins in virus-induced asthma. Curr Allergy Asthma Rep 2006; 6: 81-85.
59. Zebrak J, Herman T, Werys R, et al. Proteins in bronchial secretion of children with chronic pulmonary diseases. II. Relation to bronchoscopic and bronchographic examination. Scand J Respir Dis 1979; 60: 69-75.
60. Duits LA, Nibbering PH, van Strijen E, et al. Rhinovirus increases human β-defensin-2 and -3 mRNA expression in cultured bronchial epithelial cells. FEMS Immunol Med Microbiol 2003; 38: 59-64.
61. Jackson DJ, Johnston SL. The role of viruses in acute exacerbations of asthma. J Allergy Clin Immunol 2010; 125: 1178-1187.
62. Holgate ST, Davies DE, Lackie PM, et al. Epithelial-mesenchymal interactions in the pathogenesis of asthma. J Allergy Clin Immunol 2000; 105: 193-204.
63. Lambrecht BN, Hammad H. The airway epithelium in asthma. Nat Med 2012; 18: 684-692.
64. Kzuhara K, Conway SJ, Moore BB, et al. Roles of periostin in respiratory disorders. Am J Respir Crit Care Med 2016; 193: 949-956.
65. Chiappori A, De Ferrari L, Folli C, et al. Biomarkers and severe asthma: a critical appraisal. Clin Mol Allergy 2015; 13: 20.
66. Da la Fuente M, MacDonald TT, Hermoso MA. The IL-33/ST2 axis: role in health and disease. Cytokine Growth Factor Rev 2015; 26: 615-623.
67. Cheng D, Xue Z, Yi L, et al. Epithelial interleukin-25 is a key mediator in Th2-high, corticosteroid-responsive asthma. Am J Respir Crit Care Med 2014; 190: 639-648.
68. Uller L, Leino M, Bedke N, et al. Double-stranded RNA induces disproportionate expression of thymic stromal lymphopoietin versus interferon-beta in bronchial epithelial cells from donors with asthma. Thorax 2010; 65: 626-632.
69. Nino G, Huseni S, Perez GF, et al. Directional secretory response of double stranded RNA-induced thymic stromal lymphopoetin (TSLP) and CCL11/eotaxin-1 in human asthmatic airways. PLoS One 2014; 9: e115398.
70. Iwanaga K, Elliott MS, Vedal S, et al. Urban particulate matter induces pro-remodeling factors by airway epithelial cells from healthy and asthmatic children. Inhal Toxicol 2013; 25: 653-660.
71. Lee H-C, Headley MB, Loo Y-M, et al. Thymic stromal lymphopoietin is induced by respiratory syncytial virus-infected airway epithelial cells and promotes a type 2 response to infection. J Allergy Clin Immunol 2012; 130: 1187-1196.
72. Gras D, Chanez P, Vachier I, et al. Bronchial epithelium as a target for innovative treatments in asthma. Pharmacol Ther 2013; 140: 290-305.
73. Riccio AM, Dal Negro RW, Micheletto C, et al. Omalizumab modulates bronchial reticular basement membrane thickness and eosinophil infiltration in severe persistent allergic asthma patients. Int J Immunopathol Pharmacol 2012; 25: 475-484.
74. Huang Y-C, Leyko B, Frieri M. Effects of omalizumab and budesonide on markers of inflammation in human bronchial epithelial cells. Ann Allergy Asthma Immunol 2005; 95: 443-451.
75. Flood-Page P, Menzies-Gow A, Phipps S, et al. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest 2003; 112: 1029-1036.
76. Traub S, Nikonova A, Carruthers A, et al. An anti-human ICAM-1 antibody inhibits rhinovirus-induced exacerbations of lung inflammation. PLoS Pathog 2013; 9: e1003520.