The airway epithelium in asthma: Developmental issues that scar the airways for life?

Pulmonary Pharmacology and Therapeutics

Volumn 25, Issue 6, 2012, Pages 420-426

  Roth, Hollis M ^a   Wadsworth, Samuel J ^a   Kahn, Michael ^b   Knight, Darryl A ^a,c  

^a The James Hogg iCAPTURE Centre for Cardiovascular and Pulmonary Research   (Canada)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Airways; Asthma; Epithelium; Immune barrier; Lung; Lung disease; Pulmonary; Wnt catenin signaling

Indexed keywords

BETA CATENIN; CELL ADHESION MOLECULE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN;

AIRWAY; ALLERGY; ASTHMA; EPITHELIUM CELL; GENE CONTROL; HUMAN; NONHUMAN; ORGANOGENESIS; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFLAMMATION; REVIEW; TISSUE DIFFERENTIATION; TISSUE REPAIR;

ALLERGENS; ANIMALS; ASTHMA; HUMANS; HYPERSENSITIVITY; INFLAMMATION; INHALATION EXPOSURE; RESPIRATORY MUCOSA;

EID: 84870237215     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2012.09.004     Document Type: Review

References (86)

1. Anderson G.P. Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 2008, 372:1107-1119.
2. Grainge C.L., Lau L.C.K., Ward J.A., Dulay V., Lahiff G., Wilson S., et al. Effect of bronchoconstriction on airway remodeling in asthma. N Engl J Med 2011, 364:2006-2015.
3. Moffatt M.F., Kabesch M., Liang L., Dixon A.L., Strachan D., Heath S., et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 2007, 448:470-473.
4. DeWan AT, Triche EW, Xu X, Hsu LI, Zhao C, Belanger K, et al. PDE11A associations with asthma: results of a genome-wide association scan. J Allergy Clin Immunol;126:871-3 e9.
5. Moffatt M.F., Gut I.G., Demenais F., Strachan D.P., Bouzigon E., Heath S., et al. A large-scale, consortium-based genomewide association study of asthma. N Engl J Med 2010, 363:1211-1221.
6. Binia A., Khorasani N., Bhavsar P.K., Adcock I., Brightling C.E., Chung K.F., et al. Chromosome 17q21 SNP and severe asthma. J Hum Genet 2010, 56:97-98.
7. Li X., Howard T.D., Zheng S.L., Haselkorn T., Peters S.P., Meyers D.A., et al. Genome-wide association study of asthma identifies RAD50-IL13 and HLA-DR/DQ regions. J Allergy Clin Immunol 2010, 125:328-335. e11.
8. Mathias R.A., Grant A.V., Rafaels N., Hand T., Gao L., Vergara C., et al. A genome-wide association study on African-ancestry populations for asthma. J Allergy Clin Immunol 2010, 125:336-346. e4.
9. Sleiman P.M., Flory J., Imielinski M., Bradfield J.P., Annaiah K., Willis-Owen S.A., et al. Variants of DENND1B associated with asthma in children. N Engl J Med 2010, 362:36-44.
10. Wu H, Romieu I, Shi M, Hancock DB, Li H, Sienra-Monge JJ, et al. Evaluation of candidate genes in a genome-wide association study of childhood asthma in Mexicans. J Allergy Clin Immunol;125:321-7 e13.
11. Holgate S.T. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol Rev 2011, 242:205-219.
12. Ierodiakonou D., Postma D.S., Koppelman G.H., Boezen H.M., Gerritsen J., Ten Hacken N., et al. E-cadherin gene polymorphisms in asthma patients using inhaled corticosteroids. Eur Respir J 2011, 38:1044-1052.
13. Koppelman G.H., Meyers D.A., Howard T.D., Zheng S.L., Hawkins G.A., Ampleford E.J., et al. Identification of PCDH1 as a novel susceptibility gene for bronchial hyperresponsiveness. Am J Respir Crit Care Med 2009, 180:929-935.
14. Spergel JM. From atopic dermatitis to asthma: the atopic march. Ann Allergy Asthma Immunol;105:99-106; quiz 7-9, 17.
15. Hudson T.J. Skin barrier function and allergic risk. Nat Genet 2006, 38:399-400.
16. Walley A.J., Chavanas S., Moffatt M.F., Esnouf R.M., Ubhi B., Lawrence R., et al. Gene polymorphism in Netherton and common atopic disease. Nat Genet 2001, 29:175-178.
17. O'Regan G.M., Sandilands A., McLean W.H., Irvine A.D. Filaggrin in atopic dermatitis. J Allergy Clin Immunol 2009, 124:R2-R6.
18. Barbato A., Turato G., Baraldo S., Bazzan E., Calabrese F., Panizzolo C., et al. Epithelial damage and angiogenesis in the airways of children with asthma. Am J Respir Crit Care Med 2006, 174:975-981.
19. de Boer W.I., Sharma H.S., Baelemans S.M., Hoogsteden H.C., Lambrecht B.N., Braunstahl G.J. Altered expression of epithelial junctional proteins in atopic asthma: possible role in inflammation. Can J Physiol Pharmacol 2008, 86:105-112.
20. Hackett T.-L., Singhera G.K., Shaheen F., Hayden P., Jackson G.R., Hegele R.G., et al. Intrinsic phenotypic differences of asthmatic epithelium and its inflammatory responses to RSV and air pollution. Am J Respir Cell Mol Biol 2011, 45:1090-1100.
21. Brauer M., Hoek G., Smit H.A., de Jongste J.C., Gerritsen J., Postma D.S., et al. Air pollution and development of asthma, allergy and infections in a birth cohort. Eur Respir J 2007, 29:879-888.
22. Morgenstern V., Zutavern A., Cyrys J., Brockow I., Koletzko S., Kramer U., et al. Atopic diseases, allergic sensitization, and exposure to traffic-related air pollution in children. Am J Respir Crit Care Med 2008, 177:1331-1337.
23. Bizzintino J., Lee W.M., Laing I.A., Vang F., Pappas T., Zhang G., et al. Association between human rhinovirus C and severity of acute asthma in children. Eur Respir J 2011, 37:1037-1042.
24. Gern J.E. Rhinovirus and the initiation of asthma. Curr Opin Allergy Clin Immunol 2009, 9:73-78.
25. Sigurs N., Bjarnason R., Sigurbergsson F., Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med 2000, 161:1501-1507.
26. Hirota J.A., Hackett T.-L., Inman M.D., Knight D.A. Modeling asthma in mice: what have we learned about the airway epithelium?. Am J Respir Cell Mol Biol 2011, 44:431-438.
27. Bates J.H., Wagers S.S., Norton R.J., Rinaldi L.M., Irvin C.G. Exaggerated airway narrowing in mice treated with intratracheal cationic protein. J Appl Physiol 2006, 100:500-506.
28. Turi GJ, Ellis R, Wattie JN, Labiris NR, Inman MD. The effects of inhaled house dust mite on airway barrier function and sensitivity to inhaled methacholine in mice. Am J Physiol Lung Cell Mol Physiol;300:L185-90.
29. Allen G.B., Leclair T.R., von Reyn J., Larrabee Y.C., Cloutier M.E., Irvin C.G., et al. Acid aspiration-induced airways hyperresponsiveness in mice. J Appl Physiol 2009, 107:1763-1770.
30. Bates J.H., Cojocaru A., Haverkamp H.C., Rinaldi L.M., Irvin C.G. The synergistic interactions of allergic lung inflammation and intratracheal cationic protein. Am J Respir Crit Care Med 2008, 177:261-268.
31. Xing Y., Li C., Li A., Sridurongrit S., Tiozzo C., Bellusci S., et al. Signaling via Alk5 controls the ontogeny of lung Clara cells. Development 2010, 137:825-833.
32. Rawlins E.L. The building blocks of mammalian lung development. Dev Dyn 2011, 240:463-476.
33. Cardoso W.V., Lu J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 2006, 133:1611-1624.
34. Warburton D., Schwarz M., Tefft D., Flores-Delgado G., Anderson K.D., Cardoso W.V. The molecular basis of lung morphogenesis. Mech Dev 2000, 92:55-81.
35. Cardoso W.V., Whitsett J.A. Resident cellular components of the lung: developmental aspects. Proc Am Thorac Soc 2008, 5:767-771.
36. Rock J.R., Hogan B.L. Epithelial progenitor cells in lung development, maintenance, repair, and disease. Annu Rev Cell Dev Biol 2011, 27:493-512.
37. Hackett T.L., Shaheen F., Johnson A., Wadsworth S., Pechkovsky D.V., Jacoby D.B., et al. Characterization of side population cells from human airway epithelium. Stem Cells 2008, 26:2576-2585.
38. Alvi A., Clayton H., Joshi C., Enver T., Ashworth A., Md Vivanco, et al. Functional and molecular characterisation of mammary side population cells. Breast Cancer Res 2003, 5:R1-R8.
39. Smith G.H., Chepko G. Mammary epithelial stem cells. Microsc Res Tech 2001, 52:190-203.
40. Bhattacharya S., Jackson J.D., Das A.V., Thoreson W.B., Kuszynski C., James J., et al. Direct identification and enrichment of retinal stem cells/progenitors by Hoechst dye efflux assay. Invest Ophthalmol Vis Sci 2003, 44:2764-2773.
41. Redvers R.P., Li A., Kaur P. Side population in adult murine epidermis exhibits phenotypic and functional characteristics of keratinocyte stem cells. Proc Natl Acad Sci 2006, 103:13168-13173.
42. Giangreco A., Arwert E.N., Rosewell I.R., Snyder J., Watt F.M., Stripp B.R. Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci 2009, 106:9286-9291.
43. Erjefalt J.S., Erjefalt I., Sundler F., Persson C.G.A. In vivo restitution of airway epithelium. Cell Tiss Res 1995, 281:305-316.
44. Erjefalt J.S., Korsgren M., Nilsson M.C., Sundler F., Persson C.G.A. Prompt epithelial damage and restitution processes in allergen challenged guinea pig trachea in vivo. Clin Exp Allergy 1997, 27:1458-1470.
45. Beers M.F., Morrisey E.E. The three R's of lung health and disease: repair, remodeling, and regeneration. J Clin Invest 2011, 121:2065-2073.
46. Heguy A., Harvey B.G., Leopold P.L., Dolgalev I., Raman T., Crystal R.G. Responses of the human airway epithelium transcriptome to in vivo injury. Physiol Genomics 2007, 29:139-148.
47. Kicic A., Sutanto E.N., Stevens P.T., Knight D.A., Stick S.M. Intrinsic biochemical and functional differences in bronchial epithelial cells of children with asthma. Am J Respir Crit Care Med 2006, 174:1110-1118.
48. Xiao C., Puddicombe S.M., Field S., Haywood J., Broughton-Head V., Puxeddu I., et al. Defective epithelial barrier function in asthma. J Allergy Clin Immunol 2011, 128:549-556. e1-12.
49. Hackett T.L., Warner S.M., Stefanowicz D., Shaheen F., Pechkovsky D.V., Murray L.A., et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-beta1. Am J Respir Crit Care Med 2009, 180:122-133.
50. Stevens P.T., Kicic A., Sutanto E.N., Knight D.A., Stick S.M. Dysregulated repair in asthmatic paediatric airway epithelial cells: the role of plasminogen activator inhibitor-1. Clin Exp Allergy 2008, 38:1901-1910.
51. Freishtat R.J., Watson A.M., Benton A.S., Iqbal S.F., Pillai D.K., Rose M.C., et al. Asthmatic airway epithelium is intrinsically inflammatory and mitotically dyssynchronous. Am J Respir Cell Mol Biol 2010, 44:863-869.
52. Kicic A., Hallstrand T.S., Sutanto E.N., Stevens P.T., Kobor M.S., Taplin C., et al. Decreased fibronectin production significantly contributes to dysregulated repair of asthmatic epithelium. Am J Respir Crit Care Med 2010, 181:889-898.
53. Puddicombe S.M., Torres-Lozano C., Richter A., Bucchieri F., Lordan J.L., Howarth P.H., et al. Increased expression of p21(waf) cyclin-dependent kinase inhibitor in asthmatic bronchial epithelium. Am J Respir Cell Mol Biol 2003, 28:61-68.
54. Holgate S.T. The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol 2007, 28:248-251.
55. Holgate S.T., Davies D.E., Powell R.M., Howarth P.H., Haitchi H.M., Holloway J.W. Local genetic and environmental factors in asthma disease pathogenesis: chronicity and persistence mechanisms. Eur Respir J 2007, 29:793-803.
56. Sampath D., Castro M., Look D.C., Holtzman M.J. Constitutive activation of an epithelial signal transducer and activator of transcription (STAT) pathway in asthma. J Clin Invest 1999, 103:1353-1361.
57. Knight D.A., Stick S.M., Hackett T.L. Defective function at the epithelial junction: a novel therapeutic frontier in asthma?. J Allergy Clin Immunol 2011, 128:557-558.
58. Wark P.A., Johnston S.L., Bucchieri F., Powell R., Puddicombe S., Laza-Stanca V., et al. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med 2005, 201:937-947.
59. Cakebread J.A., Xu Y., Grainge C., Kehagia V., Howarth P.H., Holgate S.T., et al. Exogenous IFN-beta has antiviral and anti-inflammatory properties in primary bronchial epithelial cells from asthmatic subjects exposed to rhinovirus. J Allergy Clin Immunol 2011, 127:1148-1154. e9.
60. Contoli M., Message S.D., Laza-Stanca V., Edwards M.R., Wark P.A., Bartlett N.W., et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med 2006, 12:1023-1026.
61. Romano R.A., Smalley K., Liu S., Sinha S. Abnormal hair follicle development and altered cell fate of follicular keratinocytes in transgenic mice expressing DeltaNp63alpha. Development 2010, 137:1431-1439.
62. Heijink I.H., Postma D.S., Noordhoek J.A., Broekema M., Kapus A. House dust mite-promoted epithelial-to-mesenchymal transition in human bronchial epithelium. Am J Respir Cell Mol Biol 2010, 42:69-79.
63. Kaarteenaho R., Lappi-Blanco E., Lehtonen S. Epithelial N-cadherin and nuclear beta-catenin are up-regulated during early development of human lung. BMC Dev Biol 2010, 10:113.
64. Schmidt-Ott K.M., Barasch J. WNT/beta-catenin signaling in nephron progenitors and their epithelial progeny. Kidney Int 2008, 74:1004-1008.
65. Hashimoto S., Chen H., Que J., Brockway B.L., Drake J.A., Snyder J.C., et al. Beta-catenin-SOX2 signaling regulates the fate of developing airway epithelium. J Cell Sci 2012, 125:932-942.
66. Brechbuhl H.M., Ghosh M., Smith M.K., Smith R.W., Li B., Hicks D.A., et al. Beta-catenin dosage is a critical determinant of tracheal basal cell fate determination. Am J Pathol 2011, 179:367-379.
67. Smith M.K., Koch P.J., Reynolds S.D. Direct and indirect roles for beta-catenin in facultative basal progenitor cell differentiation. Am J Physiol Lung Cell Mol Physiol 2012, 302:L580-L594.
68. Driskell R.R., Goodheart M., Neff T., Liu X., Luo M., Moothart C., et al. Wnt3a regulates Lef-1 expression during airway submucosal gland morphogenesis. Dev Biol 2007, 305:90-102.
69. Filali M., Liu X., Cheng N., Abbott D., Leontiev V., Engelhardt J.F. Mechanisms of submucosal gland morphogenesis in the airway. Novartis Found Symp 2002, 248:38-45. discussion-50, 277-82.
70. Ritchie T.C., Zhou W., McKinstry E., Hosch M., Zhang Y., Nathke I., et al. Developmental expression of catenins and associated proteins during submucosal gland morphogenesis in the airway. Exp Lung Res 2001, 27:121-141.
71. Stripp B.R., Reynolds S.D. Maintenance and repair of the bronchiolar epithelium. Proc Am Thorac Soc 2008, 5:328-333.
72. Aplin A.E., Howe A., Alahari S.K., Juliani R.L. Signal transduction and signal modulation by cell adhesion receptors. The role of integrins, cadherins, immunoglobulin-cell adhesion molecules and selectins. Pharmacol Rev 1998, 50:197-263.
73. Tian X., Liu Z., Niu B., Zhang J., Tan T.K., Lee S.R., et al. E-cadherin/beta-catenin complex and the epithelial barrier. J Biomed Biotechnol 2011, 2011:567305.
74. Hart M.J., de los Santos R., Albert I.N., Rubinfeld B., Polakis P. Downregulation of beta-catenin by human axin and its association with the APC tumor suppressor, beta-catenin and GSK3 beta. Curr Biol 1998, 8:573-581.
75. Teo J-L, Kahn M. The Wnt signaling pathway in cellular proliferation and differentiation: a tale of two coactivators. Advanced Drug Delivery Reviews;62:1149-55.
76. Karamouzis M.V., Konstantinopoulos P.A., Papavassiliou A.G. Roles of CREB-binding protein (CBP)/p300 in respiratory epithelium tumorigenesis. Cell Res 2007, 17:324-332.
77. Ma H., Nguyen C., Lee K.S., Kahn M. Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene 2005, 24:3619-3631.
78. Miyabayashi T., Teo J.L., Yamamoto M., McMillan M., Nguyen C., Kahn M. Wnt/beta-catenin/CBP signaling maintains long-term murine embryonic stem cell pluripotency. Proc Natl Acad Sci U S A 2007, 104:5668-5673.
79. Konigshoff M., Eickelberg O. WNT signaling in lung disease: a failure or a regeneration signal?. Am J Respir Cell Mol Biol 2010, 42:21-31.
80. Zhao J., Kim K.A., Abo A. Tipping the balance: modulating the Wnt pathway for tissue repair. Trends Biotechnol 2009, 27:131-136.
81. Eguchi M., Nguyen C., Lee S.C., Kahn M. ICG-001, a novel small molecule regulator of TCF/beta-catenin transcription. Med Chem 2005, 1:467-472.
82. McMillan M., Kahn M. Investigating Wnt signaling: a chemogenomic safari. Drug Discov Today 2005, 10:1467-1474.
83. Henderson W.R., Chi E.Y., Ye X., Nguyen C., Tien Y.-T., Zhou B., et al. Inhibition of Wnt/B-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc Natl Acad Sci 2010, 107:14309-14314.
84. Hao S., He W., Li Y., Ding H., Hou Y., Nie J., et al. Targeted inhibition of B-catenin/CBP signaling ameliorates renal interstitial fibrosis. J Am Soc Nephrol 2011, 22:1642-1653.
85. Zemans R.L., Briones N., Campbell M., McClendon J., Young S.K., Suzuki T., et al. Neutrophil transmigration triggers repair of the lung epithelium via B-catenin signaling. Proc Natl Acad Sci 2011, 108:15990-15995.
86. Banerjee E.R., Laflamme M.A., Papayannopoulou T., Kahn M., Murry C.E., Henderson W.R. Human embryonic stem cells differentiated to lung lineage-specific cells ameliorate pulmonary fibrosis in a xenograft transplant mouse model. PLoS One 2012, 7. e33165.