Modeling asthma in mice: What have we learned about the airway epithelium?

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 4, 2011, Pages 431-438

  Hirota, Jeremy A ^a,b   Hackett, Tillie Louise ^a,b   Inman, Mark D ^c   Knight, Darryl A ^a,b  

^a ST PAUL S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c ST JOSEPH S HOSPITAL   (Canada)

Author keywords

Damage; Inflammation; Permeability; Repair

Indexed keywords

ALLERGEN; CIGARETTE SMOKE; CORTICOSTEROID; EOTAXIN 2; EPIDERMAL GROWTH FACTOR RECEPTOR; HOUSE DUST ALLERGEN; INTERLEUKIN 5; NAPHTHALENE; PENTETATE TECHNETIUM TC 99M; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA1;

ADAPTIVE IMMUNITY; ALLERGIC ASTHMA; APOPTOSIS; ASTHMA; CELL PROLIFERATION; CELL ULTRASTRUCTURE; CORTICOSTEROID THERAPY; DERMATOPHAGOIDES; DISEASE MODEL; ELECTRON MICROSCOPY; ENVIRONMENTAL EXPOSURE; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INNATE IMMUNITY; LUNG LAVAGE; MOLECULAR BIOLOGY; NONHUMAN; OXIDATIVE STRESS; RESPIRATORY EPITHELIUM; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; STRUCTURE ANALYSIS; TH2 CELL; TRANSGENIC MOUSE;

ANIMALS; ASTHMA; DISEASE MODELS, ANIMAL; MICE; RESPIRATORY MUCOSA;

MUS;

EID: 79953738314     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0146TR     Document Type: Review

References (85)

1. Dunnill MS, Massarella GR, Anderson JA. A comparison of the quantitative anatomy of the bronchi in normal subjects, in status asthmaticus, in chronic bronchitis, and in emphysema. Thorax 1969; 24:176-179.
2. Naylor B. The shedding of the mucosa of the bronchial tree in asthma. Thorax 1962;17:69-72.
3. Tesfaigzi Y. Regulation of mucous cell metaplasia in bronchial asthma. Curr Mol Med 2008;8:408-415.
4. Ebina M, Yaegashi H, Chiba R, Takahashi T, Motomiya M, Tanemura M. Hyperreactive site in the airway tree of asthmatic patients revealed by thickening of bronchial muscles: a morphometric study. Am Rev Respir Dis 1990;141:1327-1332. (Pubitemid 20172591)
5. Jeffery PK, Wardlaw AJ, Nelson FC, Collins JV, Kay AB. Bronchial biopsies in asthma: an ultrastructural, quantitative study and correlation with hyperreactivity. Am Rev Respir Dis 1989;140:1745-1753. (Pubitemid 20041063)
6. Knight DA, Holgate ST. The airway epithelium: structural and functional properties in health and disease. Respirology 2003;8:432-446. (Pubitemid 38009637)
7. Laitinen LA, Heino M, Laitinen A, Kava T, Haahtela T. Damage of the airway epithelium and bronchial reactivity in patients with asthma. Am Rev Respir Dis 1985;131:599-606. (Pubitemid 15086749)
8. 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 asthmatic patients by TGF-1. Am J Respir Crit Care Med 2009; 180(2):122-133.
9. de Boer WI, Sharma HS, Baelemans SM, Hoogsteden HC, Lambrecht BN, Braunstahl GJ. Altered expression of epithelial junctional proteins in atopic asthma: possible role in inflammation. Can J Physiol Pharmacol 2008;86:105-112. (Pubitemid 351536459)
10. Trautmann A, Kruger K, Akdis M, Muller-Wening D, Akkaya A, Brocker EB, Blaser K, Akdis CA. Apoptosis and loss of adhesion of bronchial epithelial cells in asthma. Int Arch Allergy Immunol 2005;138:142-150. (Pubitemid 41540671)
11. Bhure UN, Bhure SU, Bhatt BM, Mistry S, Pednekar SJ, Chari VV, Desai SA, Joshi JM, Paidhungat AJ. Lung epithelial permeability and inhaled furosemide: added dimensions in asthmatics. Ann Nucl Med 2009;23:549-557.
12. Kicic A, Sutanto EN, Stevens PT, Knight DA, Stick SM. Intrinsic biochemical and functional differences in bronchial epithelial cells of children with asthma. Am J Respir Crit Care Med 2006;174:1110-1118. (Pubitemid 44772081)
13. Stevens PT, Kicic A, Sutanto EN, Knight DA, Stick SM. Dysregulated repair in asthmatic paediatric airway epithelial cells: the role of plasminogen activator inhibitor-1. Clin Exp Allergy 2008;38:1901-1910.
14. Puddicombe SM, Polosa R, Richter A, Krishna MT, Howarth PH, Holgate ST, Davies DE. Involvement of the epidermal growth factor receptor in epithelial repair in asthma. FASEB J 2000;14:1362-1374. (Pubitemid 30439745)
15. Dunsmore SE, Saarialho-Kere UK, Roby JD, Wilson CL, Matrisian LM, Welgus HG, Parks WC. Matrilysin expression and function in airway epithelium. J Clin Invest 1998;102:1321-1331. (Pubitemid 28467560)
16. Gomperts BN, Belperio JA, Fishbein MC, Keane MP, Burdick MD, Strieter RM. Keratinocyte growth factor improves repair in the injured tracheal epithelium. Am J Respir Cell Mol Biol 2007;37:48-56. (Pubitemid 46999536)
17. Kato A, Schleimer RP. Beyond inflammation: Airway epithelial cells are at the interface of innate and adaptive immunity. Curr Opin Immunol 2007;19:711-720. (Pubitemid 350236807)
18. Holgate ST. The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol 2007;28:248-251. (Pubitemid 46810353)
19. Holgate ST. Epithelium dysfunction in asthma. J Allergy Clin Immunol 2007;120:1233-1244; quiz 1245-1236.
20. Hammad H, Lambrecht BN. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol 2008;8: 193-204. (Pubitemid 351323293)
21. Ying S, O'Connor B, Ratoff J, Meng Q, Mallett K, Cousins D, Robinson D, Zhang G, Zhao J, Lee TH, et al. Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J Immunol 2005; 174:8183-8190. (Pubitemid 40806330)
22. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005;23: 479-490. (Pubitemid 41587888)
23. Shannon J, Ernst P, Yamauchi Y, Olivenstein R, Lemiere C, Foley S, Cicora L, Ludwig M, Hamid Q, Martin JG. Differences in airway cytokine profile in severe asthma compared to moderate asthma. Chest 2008;133:420-426.
24. Sekiya T, Miyamasu M, Imanishi M, Yamada H, Nakajima T, Yamaguchi M, Fujisawa T, Pawankar R, Sano Y, Ohta K, et al. Inducible expression of a Th2-type CC chemokine thymus- and activation-regulated chemokine by human bronchial epithelial cells. J Immunol 2000;165:2205-2213. (Pubitemid 30648752)
25. Zhou B, Comeau MR, De Smedt T, Liggitt HD, Dahl ME, Lewis DB, Gyarmati D, Aye T, Campbell DJ, Ziegler SF. Thymic stromal lymphopoietin as a key initiator of allergic airway inflammation in mice. Nat Immunol 2005;6:1047-1053. (Pubitemid 41486190)
26. Zemke AC, Snyder JC, Brockway BL, Drake JA, Reynolds SD, Kaminski N, Stripp BR. Molecular staging of epithelial maturation using secretory cell-specific genes as markers. Am J Respir Cell Mol Biol 2009;40:340-348.
27. Tillie-Leblond I, Gosset P, Le Berre R, Janin A, Prangere T, Tonnel AB, Guery BP. Keratinocyte growth factor improves alterations of lung permeability and bronchial epithelium in allergic rats. Eur Respir J 2007;30:31-39. (Pubitemid 47074003)
28. 3-induced epithelial damage and proliferation in nasal and bronchial airways of mice. J Appl Physiol 1996;80:1322-1330.
29. Royston BD, Webster NR, Nunn JF. Time course of changes in lung permeability and edema in the rat exposed to 100% oxygen. J Appl Physiol 1990;69:1532-1537. (Pubitemid 20361278)
30. Boucher RC, Ranga V, Pare PD, Inoue S, Moroz LA, Hogg JC. Effect of histamine and methacholine on guinea pig tracheal permeability to HRP. J Appl Physiol 1978;45:939-948. (Pubitemid 9189750)
31. Koohsari H, Tamaoka M, Campbell HR, Martin JG. The role of gamma delta T cells in airway epithelial injury and bronchial responsiveness after chlorine gas exposure in mice. Respir Res 2007;8:21.
32. Barazzone C, Horowitz S, Donati YR, Rodriguez I, Piguet PF. Oxygen toxicity in mouse lung: pathways to cell death. Am J Respir Cell Mol Biol 1998;19:573-581. (Pubitemid 128354238)
33. Erjefalt JS, Erjefalt I, Sundler F, Persson CG. In vivo restitution of airway epithelium. Cell Tissue Res 1995;281:305-316.
34. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV. Epithelial cell cycle arrest in g2/m mediates kidney fibrosis after injury. Nat Med 2010;16:535-543.
35. Bates JH, Rincon M, Irvin CG. Animal models of asthma. Am J Physiol Lung Cell Mol Physiol 2009;297:L401-L410.
36. Curran DR, Cohn L. Advances in mucous cell metaplasia: a plug for mucus as a therapeutic focus in chronic airway disease. Am J Respir Cell Mol Biol 2010;42:268-275.
37. Dorscheid DR, Low E, Conforti A, Shifrin S, Sperling AI, White SR. Corticosteroid-induced apoptosis in mouse airway epithelium: effect in normal airways and after allergen-induced airway inflammation. J Allergy Clin Immunol 2003;111:360-366. (Pubitemid 36228558)
38. Leigh R, Ellis R, Wattie J, Southam DS, De Hoogh M, Gauldie J, O'Byrne PM, Inman MD. Dysfunction and remodeling of the mouse airway persist after resolution of acute allergen-induced airway inflammation. Am J Respir Cell Mol Biol 2002;27:526-535. (Pubitemid 35301806)
39. Kelly MM, Leigh R, Bonniaud P, Ellis R, Wattie J, Smith MJ, Martin G, Panju M, Inman MD, Gauldie J. Epithelial expression of profibrotic mediators in a model of allergen-induced airway remodeling. Am J Respir Cell Mol Biol 2005;32:99-107. (Pubitemid 40189691)
40. Bates JH, Cojocaru A, Haverkamp HC, Rinaldi LM, Irvin CG. The synergistic interactions of allergic lung inflammation and intratracheal cationic protein. Am J Respir Crit Care Med 2008;177:261-268. (Pubitemid 351198368)
41. Bates JH, Wagers SS, Norton RJ, Rinaldi LM, Irvin CG. Exaggerated airway narrowing in mice treated with intratracheal cationic protein. J Appl Physiol 2006;100:500-506. (Pubitemid 43671600)
42. Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, Malefyt Rde W, Omori M, Zhou B, Ziegler SF. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu Rev Immunol 2007;25:193-219. (Pubitemid 46697907)
43. Weckmann M, Collison A, Simpson JL, Kopp MV, Wark PA, Smyth MJ, Yagita H, Matthaei KI, Hansbro N, Whitehead B, et al. Critical link between trail and CCL20 for the activation of Th2 cells and the expression of allergic airway disease. Nat Med 2007;13:1308-1315. (Pubitemid 350073595)
44. Plopper CG, Suverkropp C, Morin D, Nishio S, Buckpitt A. Relationship of cytochrome p-450 activity to clara cell cytotoxicity. I. Histopathologic comparison of the respiratory tract of mice, rats and hamsters after parenteral administration of naphthalene. J Pharmacol Exp Ther 1992;261:353-363.
45. Van Winkle LS, Brown CD, Shimizu JA, Gunderson AD, Evans MJ, Plopper CG. Impaired recovery from naphthalene-induced bronchiolar epithelial injury in mice exposed to aged and diluted sidestream cigarette smoke. Toxicol Lett 2004;154:1-9. (Pubitemid 39314583)
46. Snyder JC, Zemke AC, Stripp BR. Reparative capacity of airway epithelium impacts deposition and remodeling of extracellular matrix. Am J Respir Cell Mol Biol 2009;40:633-642.
47. Jorres R, Nowak D, Magnussen H. The effect of ozone exposure on allergen responsiveness in subjects with asthma or rhinitis. Am J Respir Crit Care Med 1996;153:56-64. (Pubitemid 26026827)
48. Martin JG, Campbell HR, Iijima H, Gautrin D, Malo JL, Eidelman DH, Hamid Q, Maghni K. Chlorine-induced injury to the airways in mice. Am J Respir Crit Care Med 2003;168:568-574. (Pubitemid 37088600)
49. Tuck SA, Ramos-Barbon D, Campbell H, McGovern T, Karmouty-Quintana H, Martin JG. Time course of airway remodelling after an acute chlorine gas exposure in mice. Respir Res 2008;9:61.
50. Reynolds SD, Hong KU, Giangreco A, Mango GW, Guron C, Morimoto Y, Stripp BR. Conditional Clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells. Am J Physiol Lung Cell Mol Physiol 2000;278:L1256-L1263. (Pubitemid 30439250)
51. Erjefalt JS, Erjefalt I, Sundler F, Persson CG. Microcirculation-derived factors in airway epithelial repair in vivo. Microvasc Res 1994;48: 161-178. (Pubitemid 24315712)
52. Malavia NK, Raub CB, Mahon SB, Brenner M, Panettieri RA Jr, George SC. Airway epithelium stimulates smooth muscle proliferation. Am J Respir Cell Mol Biol 2009;41:297-304.
53. Kato A, Truong-Tran AQ, Scott AL, Matsumoto K, Schleimer RP. Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism. J Immunol 2006;177:7164-7172. (Pubitemid 44715085)
54. Hollingsworth JW, Free ME, Li Z, Andrews LN, Nakano H, Cook DN. Ozone activates pulmonary dendritic cells and promotes allergic sensitization through a Toll-like receptor 4-dependent mechanism. J Allergy Clin Immunol 2010;125:1167-1170.
55. Sykes A, Johnston SL. Etiology of asthma exacerbations. J Allergy Clin Immunol 2008;122:685-688.
56. Schwarze J, Cieslewicz G, Joetham A, Ikemura T, Makela MJ, Dakhama A, Shultz LD, Lamers MC, Gelfand EW. Critical roles for interleukin-4 and interleukin-5 during respiratory syncytial virus infection in the development of airway hyperresponsiveness after airway sensitization. Am J Respir Crit Care Med 2000;162:380-386. (Pubitemid 30647170)
57. Bartlett NW, Walton RP, Edwards MR, Aniscenko J, Caramori G, Zhu J, Glanville N, Choy KJ, Jourdan P, Burnet J, et al. Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat Med 2008;14:199-204. (Pubitemid 351214556)
58. Newcomb DC, Sajjan US, Nagarkar DR, Wang Q, Nanua S, Zhou Y, McHenry CL, Hennrick KT, Tsai WC, Bentley JK, et al. Human rhinovirus 1B exposure induces phosphatidylinositol 3-kinase-dependent airway inflammation in mice. Am J Respir Crit CareMed 2008;177:1111-1121. (Pubitemid 351717570)
59. Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 2008;178:1271-1281.
60. Phillips JR, Tripp TJ, Regelmann WE, Schlievert PM, Wangensteen OD. Staphylococcal alpha-toxin causes increased tracheal epithelial permeability. Pediatr Pulmonol 2006;41:1146-1152. (Pubitemid 44893867)
61. Hogan SP, Rosenberg HF, Moqbel R, Phipps S, Foster PS, Lacy P, Kay AB, Rothenberg ME. Eosinophils: biological properties and role in health and disease. Clin Exp Allergy 2008;38:709-750. (Pubitemid 351550670)
62. Ochkur SI, Jacobsen EA, Protheroe CA, Biechele TL, Pero RS, McGarry MP, Wang H, O'Neill KR, Colbert DC, Colby TV, et al. Coexpression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J Immunol 2007;178:7879-7889. (Pubitemid 46898060)
63. Wan H, Winton HL, Soeller C, Taylor GW, Gruenert DC, Thompson PJ, Cannell MB, Stewart GA, Garrod DR, Robinson C. The transmembrane protein occludin of epithelial tight junctions is a functional target for serine peptidases from faecal pellets of dermatophagoides pteronyssinus. Clin Exp Allergy 2001;31:279-294. (Pubitemid 32231861)
64. Wan H, Winton HL, Soeller C, Tovey ER, Gruenert DC, Thompson PJ, Stewart GA, Taylor GW, Garrod DR, Cannell MB, et al. Der p 1 facilitates transepithelial allergen delivery by disruption of tight junctions. J Clin Invest 1999;104:123-133.
65. Roschmann K, Farhat K, Konig P, Suck R, Ulmer AJ, Petersen A. Timothy grass pollen major allergen Phl p 1 activates respiratory epithelial cells by a non-protease mechanism. Clin Exp Allergy 2009; 39:1358-1369.
66. Sur S, Lam J, Bouchard P, Sigounas A, Holbert D, Metzger WJ. Immunomodulatory effects of IL-12 on allergic lung inflammation depend on timing of doses. J Immunol 1996;157:4173-4180. (Pubitemid 126449332)
67. Chambers L, Brown A, Pritchard DI, Sreedharan S, Brocklehurst K, Kalsheker NA. Enzymatically active papain preferentially induces an allergic response in mice. Biochem Biophys Res Commun 1998;253: 837-840.
68. McGlade JP, Gorman S, Lenzo JC, Tan JW, Watanabe T, Finlay-Jones JJ, Thomas WR, Hart PH. Effect of both ultraviolet B irradiation and histamine receptor function on allergic responses to an inhaled antigen. J Immunol 2007;178:2794-2802. (Pubitemid 46333157)
69. Ciencewicki J, Trivedi S, Kleeberger SR. Oxidants and the pathogenesis of lung diseases. J Allergy Clin Immunol 2008;122:456-468.
70. Hackett TL, Shaheen F, Johnson A, Wadsworth S, Pechkovsky DV, Jacoby DB, Kicic A, Stick SM, Knight DA. Characterization of side population cells from human airway epithelium. Stem Cells 2008;26: 2576-2585.
71. Daniely Y, Liao G, Dixon D, Linnoila RI, Lori A, Randell SH, Oren M, Jetten AM. Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am J Physiol Cell Physiol 2004;287:C171-C181. (Pubitemid 38780165)
72. Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, Xue Y, Randell SH, Hogan BL. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA 2009;106:12771-12775.
73. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. P63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999;398:708-713. (Pubitemid 29197649)
74. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, et al. P63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999;398:714-718. (Pubitemid 29197650)
75. Plopper CG, Mariassy AT, Hill LH. Ultrastructure of the nonciliated bronchiolar epithelial (Clara) cell of mammalian lung: I. A comparison of rabbit, guinea pig, rat, hamster, and mouse. Exp Lung Res 1980;1:139-154.
76. Pack RJ, Al Ugaily LH, Morris G. The cells of the tracheobronchial epithelium of the mouse: a quantitative light and electron microscope study. J Anat 1981;132:71-84. (Pubitemid 11210854)
77. Plopper CG, Mango GW, Hatch GE, Wong VJ, Toskala E, Reynolds SD, Tarkington BK, Stripp BR. Elevation of susceptibility to ozone-induced acute tracheobronchial injury in transgenic mice deficient in clara cell secretory protein. Toxicol Appl Pharmacol 2006;213:74-85.
78. Van Winkle LS, Evans MJ, Brown CD, Willits NH, Pinkerton KE, Plopper CG. Prior exposure to aged and diluted sidestream cigarette smoke impairs bronchiolar injury and repair. Toxicol Sci 2001; 60:152-164. (Pubitemid 32229835)
79. Van Winkle LS, Isaac JM, Plopper CG. Distribution of epidermal growth factor receptor and ligands during bronchiolar epithelial repair from naphthalene-induced Clara cell injury in the mouse. Am J Pathol 1997;151:443-459. (Pubitemid 27330064)
80. Cohen L, Xueping E, Tarsi J, Ramkumar T, Horiuchi TK, Cochran R, DeMartino S, Schechtman KB, Hussain I, Holtzman MJ, et al. Epithelial cell proliferation contributes to airway remodeling in severe asthma. Am J Respir Crit Care Med 2007;176:138-145. (Pubitemid 47057849)
81. Chimenti L, Morici G, Paterno A, Bonanno A, Siena L, Licciardi A, Veca M, Guccione W, Macaluso F, Bonsignore G, et al. Endurance training damages small airway epithelium in mice. Am J Respir Crit Care Med 2007;175:442-449. (Pubitemid 46354247)
82. Tormanen KR, Uller L, Persson CG, Erjefalt JS. Allergen exposure of mouse airways evokes remodeling of both bronchi and large pulmonary vessels. Am J Respir Crit Care Med 2005;171:19-25. (Pubitemid 40051690)
83. Reader JR, Tepper JS, Schelegle ES, Aldrich MC, Putney LF, Pfeiffer JW, Hyde DM. Pathogenesis of mucous cell metaplasia in a murine asthma model. Am J Pathol 2003;162:2069-2078. (Pubitemid 36613062)
84. Truong-Tran AQ, Ruffin RE, Foster PS, Koskinen AM, Coyle P, Philcox JC, Rofe AM, Zalewski PD. Altered zinc homeostasis and caspase-3 activity in murine allergic airway inflammation. Am J Respir Cell Mol Biol 2002;27:286-296. (Pubitemid 34979286)
85. Powdrill JG, Ellis R, Wattie JN, Inman MD. Effects of inhaled allergen on epithelial permeability and hypersensitivity. Am J Respir Crit Care Med 2009;2009:A6041.