Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-β1

American Journal of Respiratory and Critical Care Medicine

Volumn 180, Issue 2, 2009, Pages 122-133

  Hackett, Tillie Louise ^a,b   Warner, Stephanie Mary ^a   Stefanowicz, Dorota ^a   Shaheen, Furquan ^a   Pechkovsky, Dmitri V ^a,b   Murray, Lynne A ^c   Argentieri, Rochelle ^c   Kicic, Anthony ^d,e,f   Stick, Stephen M ^d,e,f   Bai, Tony R ^a   Knight, Darryl A ^a,b  

^a ST PAUL S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c CENTOCOR INC   (United States)

^d PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Asthma; Epithelial mesenchymal transition; Epithelium; Transforming growth factor 1

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; ECTODYSPLASIN A; FIBRONECTIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MONTELUKAST; OCCLUDIN 1; OSTEOGENIC PROTEIN 1; SALBUTAMOL; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; RECOMBINANT PROTEIN; SCLEROPROTEIN; SIGNAL PEPTIDE;

ADOLESCENT; ADULT; ARTICLE; ASTHMA; CELL STRUCTURE; CELL TYPE; CHILD; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIUM BASAL CELL; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VIVO STUDY; MALE; MESENCHYME CELL; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; CASE CONTROL STUDY; CELL DEDIFFERENTIATION; CULTURE TECHNIQUE; DRUG EFFECT; MESENCHYMAL STEM CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADOLESCENT; ASTHMA; CASE-CONTROL STUDIES; CELL CULTURE TECHNIQUES; CELL DEDIFFERENTIATION; CHILD; CHILD, PRESCHOOL; EPITHELIAL CELLS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MESENCHYMAL STEM CELLS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; YOUNG ADULT;

EID: 67650752133     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200811-1730OC     Document Type: Article

References (57)

1. Martinez FD. Asthma treatment and asthma prevention: a tale of 2 parallel pathways. J Allergy Clin Immunol 2007;119:30-33. (Pubitemid 46037818)
2. Bai TR, Knight DA. Structural changes in the airways in asthma: observations and consequences. Clin Sci (Lond) 2005;108:463-477. (Pubitemid 40827554)
3. Gizycki MJ, Adelroth E, Rogers AV, O'Byrne PM, Jeffery PK. Myofibroblast involvement in the allergen-induced late response in mild atopic asthma. Am J Respir Cell Mol Biol 1997;16:664-673. (Pubitemid 127498942)
4. Barbato A, Turato G, Baraldo S, Bazzan E, Calabrese F, Panizzolo C, Zanin ME, Zuin R, Maestrelli P, Fabbri LM et al. Epithelial damage and angiogenesis in the airways of children with asthma. Am J Respir Crit Care Med 2006;174:975-981. (Pubitemid 44684445)
5. Payne DN, Rogers AV, Adelroth E, Bandi V, Guntupalli KK, Bush A, Jeffery PK. Early thickening of the reticular basement membrane in children with difficult asthma. Am J Respir Crit Care Med 2003;167:78-82. (Pubitemid 36015921)
6. Fedorov IA, Wilson SJ, Davies DE, Holgate ST. Epithelial stress and structural remodelling in childhood asthma. Thorax 2005;60:389-394. (Pubitemid 40685821)
7. Nihlberg K, Larsen K, Hultgardh-Nilsson A, Malmstrom A, Bjermer L, Westergren-Thorsson G. Tissue fibrocytes in patients with mild asthma: a possible link to thickness of reticular basement membrane? Respir Res 2006;7:50.
8. Holgate ST, Davies DE, Lackie PM, Wilson SJ, Puddicombe SM, Lordan JL. Epithelial-mesenchymal interactions in the pathogenesis of asthma. J Allergy Clin Immunol 2000;105:193-204.
9. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-1784. (Pubitemid 38063698)
10. Liu Y. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 2004;15:1-12. (Pubitemid 38020692)
11. Greenburg G, Hay ED. Epithelia suspended in collagen gels can lose polarity and express characteristics of migrating mesenchymal cells. J Cell Biol 1982;95:333-339.
12. Nawshad A, Lagamba D, Polad A, Hay ED. Transforming growth factor-beta signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs 2005;179:11-23.
13. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-454.
14. Forino M, Torregrossa R, Ceol M, Murer L, Vella MD, Prete DD, D'Angelo A, Anglani F. TGFbeta1 induces epithelial-mesenchymal transition, but not myofibroblast transdifferentiation of human kidney tubular epithelial cells in primary culture. Int J Exp Pathol 2006;87:197-208. (Pubitemid 43781685)
15. Kaimori A, Potter J, Kaimori JY, Wang C, Mezey E, Koteish A. Transforming growth factor-beta1 induces an epithelial-to-mesenchymal transition state in mouse hepatocytes in vitro. J Biol Chem 2007;282:22089-22101. (Pubitemid 47195788)
16. Willis BC, Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007;293:L525-L534.
17. 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 USA 2006;103:13180-13185. (Pubitemid 44338936)
18. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 2005;16:1987-2002. (Pubitemid 40471965)
19. Saika S, Kono-Saika S, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Flanders KC, Yoo J, Anzano M, Liu CY, et al. Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 2004;164:651-663. (Pubitemid 38364679)
20. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 2003;112:1486-1494. (Pubitemid 38056275)
21. Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z. TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 2005;6:56. (Pubitemid 41410179)
22. Zavadil J, Cermak L, Soto-Nieves N, Bottinger EP. Integration of TGFbeta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J 2004;23:1155-1165. (Pubitemid 38436879)
23. Pechkovsky DV, Scaffidi AK, Hackett TL, Ballard J, Shaheen F, Thompson PJ, Thannickal VJ, Knight DA. Transforming growth factor beta1 induces alphavbeta3 integrin expression in human lung fibroblasts via a beta3 integrin-, c-Src-, and p38 MAPK-dependent pathway. J Biol Chem 2008;283:12898-12908.
24. Yu L, Hebert MC, Zhang YE. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J 2002;21:3749-3759. (Pubitemid 34787048)
25. Davies M, Robinson M, Smith E, Huntley S, Prime S, Paterson I. Induction of an epithelial to mesenchymal transition in human immortal and malignant keratinocytes by TGF-beta1 involves MAPK, Smad and AP-1 signalling pathways. J Cell Biochem 2005;95:918-931. (Pubitemid 41420140)
26. Kojima T, Takano K, Yamamoto T, Murata M, Son S, Imamura M, Yamaguchi H, Osanai M, Chiba H, Himi T, et al. Transforming growth factor-beta induces epithelial to mesenchymal transition by down-regulation of claudin-1 expression and the fence function in adult rat hepatocytes. Liver Int 2008;28:534-545.
27. Gal A, Sjoblom T, Fedorova L, Imreh S, Beug H, Moustakas A. Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 2008;27:1218-1230. (Pubitemid 351294691)
28. Hackett T-L, Warner SM, Shaheen F, Pechkovsky DV, Argenteri R, Murray L, Kicic A, Stick S, Knight DA. TGF-beta-induces epithelial-mesenchymal-transition in primary human bronchial epithelial cells from normal and asthmatic subjects [abstract]. Am J Respir Crit Care Med 2008;177:A97.
29. Hackett TL, Shaheen F, JohnsonA,Wadsworth S, PechkovskyDV, Jacoby DB, Kicic A, Stick SM, Knight DA. Characterization of side population cells from human airway epithelium. Stem Cells 2008;26:2576-2585.
30. Kicic A, Sutanto EN, Stevens PT, Knight DA, Stick SM. Intrinsic biochemical and functional differences in bronchial epithelial cells of asthmatic children. Am J Respir Crit Care Med 2006;174:1110-1118. (Pubitemid 44772081)
31. Hartsough MT, Mulder KM. Transforming growth factor beta activation of p44mapk in proliferating cultures of epithelial cells. J Biol Chem 1995;270:7117-7124.
32. Zavadil J, Bitzer M, Liang D, Yang YC, Massimi A, Kneitz S, Piek E, Bottinger EP. Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 2001;98:6686-6691. (Pubitemid 32538277)
33. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL. p38 mitogen-activated protein kinase is required for TGFb-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 2002;115:3193-3206. (Pubitemid 34905902)
34. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003;9:964-968. (Pubitemid 36889942)
35. Davies DE, Wicks J, Powell RM, Puddicombe SM, Holgate ST. Airway remodeling in asthma: new insights. J Allergy Clin Immunol 2003;111:215-225. (quiz 226).
36. Ward C, Forrest IA, Murphy DM, Johnson GE, Robertson H, Cawston TE, Fisher AJ, Dark JH, Lordan JL, Kirby JA, et al. Phenotype of airway epithelial cells suggests epithelial to mesenchymal cell transition in clinically stable lung transplant recipients. Thorax 2005;60:865-871. (Pubitemid 41475217)
37. Molloy EL, Adams A, Moore JB, Masterson JC, Madrigal-Estebas L, Mahon BP, O'Dea S. BMP4 induces an epithelial-mesenchymal transition-like response in adult airway epithelial cells. Growth Factors 2008;26:12-22.
38. Wu Z, Yang L, Cai L, Zhang M, Cheng X, Yang X, Xu J. Detection of epithelial to mesenchymal transition in airways of a bleomycin induced pulmonary fibrosis model derived from an alpha-smooth muscle actin-Cre transgenic mouse. Respir Res 2007;8:1.
39. Ando S, Otani H, Yagi Y, Kawai K, Araki H, Fukuhara S, Inagaki C. Proteinase-activated receptor 4 stimulation-induced epithelial-mesenchymal transition in alveolar epithelial cells. Respir Res 2007;8:31.
40. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000;2:76-83. (Pubitemid 30785917)
41. Carver EA, Jiang R, Lan Y, Oram KF, Gridley T. The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 2001;21:8184-8188. (Pubitemid 33051806)
42. Woods AJ, White DP, Caswell PT, Norman JC. PKD1/PKCμ promotes avb3 integrin recycling and delivery to nascent focal adhesions. EMBO J 2004;23:2531-2543.
43. Knox P, Crooks S, Rimmer CS. Role of fibronectin in the migration of fibroblasts into plasma clots. J Cell Biol 1986;102:2318-2323. (Pubitemid 16052172)
44. Turley EA. Hyaluronan and cell locomotion. Cancer Metastasis Rev 1992;11:21-30.
45. Greiling D, Clark RA. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci 1997;110:861-870. (Pubitemid 27196785)
46. Leir SH, Baker JE, Holgate ST, Lackie PM. Increased CD44 expression in human bronchial epithelial repair after damage or plating at low cell densities. Am J Physiol Lung Cell Mol Physiol 2000;278:L1129-L1137.
47. Huebener P, Abou-Khamis T, Zymek P, Bujak M, Ying X, Chatila K, Haudek S, Thakker G, Frangogiannis NG. CD44 is critically involved in infarct healing by regulating the inflammatory and fibrotic response. J Immunol 2008;180:2625-2633.
48. Ellenrieder V, Hendler SF, Boeck W, Seufferlein T, Menke A, Ruhland C, Adler G, Gress TM. Transforming growth factor beta1 treatment leads to an epithelial-mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signal-regulated kinase 2 activation. Cancer Res 2001;61:4222-4228. (Pubitemid 32720992)
49. Bates RC, Mercurio AM. Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Mol Biol Cell 2003;14:1790-1800.
50. Ross KR, Corey DA, Dunn JM, Kelley TJ. SMAD3 expression is regulated by mitogen-activated protein kinase kinase-1 in epithelial and smooth muscle cells. Cell Signal 2007;19:923-931. (Pubitemid 46436433)
51. Schramek H, Feifel E, Marschitz I, Golochtchapova N, Gstraunthaler G, Montesano R. Loss of active MEK1-ERK1/2 restores epithelial phenotype and morphogenesis in transdifferentiated MDCK cells. Am J Physiol Cell Physiol 2003;285:C652-C661. (Pubitemid 37022064)
52. Zeisberg M, Bottiglio C, Kumar N, Maeshima Y, Strutz F, Muller GA, Kalluri R. Bone morphogenic protein-7 inhibits progression of chronic renal fibrosis associated with two genetic mouse models. Am J Physiol Renal Physiol 2003;285:F1060-F1067. (Pubitemid 37421041)
53. Murray LA, Hackett TL, Warner SM, Shaheen F, Argentieri RL, Dudas P, Farrell FX, Knight DA. BMP-7 does not protect against bleomycin-induced lung or skin fibrosis. PLoS One 2008;3:e4039.
54. Hajj R, Lesimple P, Nawrocki-Raby B, Birembaut P, Puchelle E, Coraux C. Human airway surface epithelial regeneration is delayed and abnormal in cystic fibrosis. J Pathol 2007;211:340-350. (Pubitemid 46172710)
55. 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)
56. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008;68:989-997. (Pubitemid 351272216)
57. McDowell N, Gurdon JB, Grainger DJ. Formation of a functional morphogen gradient by a passive process in tissue from the early Xenopus embryo. Int J Dev Biol 2001;45:199-207. (Pubitemid 32267252)