EGF shifts human airway basal cell fate towarda smoking-Associated airway epithelial phenotype

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 29, 2013, Pages 12102-12107

  Shaykhiev, Renat ^a   Zuo, Wu Lin ^a   Chao, IonWa ^a   Fukui, Tomoya ^a   Witover, Bradley ^a   Brekman, Angelika ^a   Crystal, Ronald G ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Airway Epithelial Barrier; Cigarette Smoking; Progenitor Cell

Indexed keywords

CLAUDIN 3; CLAUDIN 8; CYTOKERATIN 14; CYTOKERATIN 16; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 4; INVOLUCRIN; OCCLUDIN; PARD3 PROTEIN; PARD6B PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN ZO1; PROTEIN ZO2; STRATIFIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BASAL CELL; CELL DIFFERENTIATION; CELL FATE; CILIATED EPITHELIUM; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; SMOKING;

AIRWAY EPITHELIAL BARRIER; CIGARETTE SMOKING; PROGENITOR CELL;

BLOTTING, WESTERN; CELL DIFFERENTIATION; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SMOKING;

EID: 84880337808     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303058110     Document Type: Article

References (52)

1. Crystal RG, Randell SH, Engelhardt JF, Voynow J, Sunday ME (2008) Airway epithelial cells: Current concepts and challenges. Proc Am Thorac Soc 5(7):772-777.
2. Rawlins EL, Hogan BL (2006) Epithelial stem cells of the lung: Privileged few or opportunities for many? Development 133(13):2455-2465.
3. Rock JR, et al. (2009) Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA 106(31):12771-12775.
4. Hajj R, et al. (2007) Basal cells of the human adult airway surface epithelium retain transit-Amplifying cell properties. Stem Cells 25(1):139-148.
5. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR (2004) Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 164(2): 577-588.
6. Wistuba II, Gazdar AF (2006) Lung cancer preneoplasia. Annu Rev Pathol 1:331-348.
7. Auerbach O, Stout AP, Hammond EC, Garfinkel L (1961) Changes in bronchial epithelium in relation to cigarette smoking and in relation to lung cancer. N Engl J Med 265:253-267.
8. Leopold PL, et al. (2009) Smoking is associated with shortened airway cilia. PLoS ONE 4(12):e8157.
9. Sisson JH, et al. (1994) Smoke and viral infection cause cilia loss detectable by bronchoalveolar lavage cytology and dynein ELISA. Am J Respir Crit Care Med 149(1): 205-213.
10. Heijink IH, Brandenburg SM, Postma DS, van Oosterhout AJ (2012) Cigarette smoke impairs airway epithelial barrier function and cell-cell contact recovery. Eur Respir J 39(2):419-428.
11. Kennedy SM, Elwood RK, Wiggs BJ, Paré PD, Hogg JC (1984) Increased airway mucosal permeability of smokers: Relationship to airway reactivity. Am Rev Respir Dis 129(1): 143-148.
12. Shaykhiev R, et al. (2011) Cigarette smoking reprograms apical junctional complex molecular architecture in the human airway epithelium in vivo. Cell Mol Life Sci 68(5): 877-892.
13. Lumsden AB, McLean A, Lamb D (1984) Goblet and Clara cells of human distal airways: Vidence for smoking induced changes in their numbers. Thorax 39(11):844-849.
14. Peters EJ, et al. (1993) Squamous metaplasia of the bronchial mucosa and its relationship to smoking. Chest 103(5):1429-1432.
15. Hogg JC, et al. (2004) The nature of small-Airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 350(26):2645-2653.
16. Araya J, et al. (2007) Squamous metaplasia amplifies pathologic epithelial-mesenchymal interactions in COPD patients. J Clin Invest 117(11):3551-3562.
17. Ooi AT, et al. (2010) Presence of a putative tumor-initiating progenitor cell population predicts poor prognosis in smokers with non-small cell lung cancer. Cancer Res 70(16):6639-6648.
18. Nettesheim P, et al. (1990) Pathways of differentiation of airway epithelial cells. Environ Health Perspect 85:317-329.
19. Citri A, Yarden Y (2006) EGF-ERBB signaling: Towards the systems level. Nat Rev Mol Cell Biol 7(7):505-516.
20. Polosa R, et al. (1999) Expression of c-erbB receptors and ligands in human bronchial mucosa. Am J Respir Cell Mol Biol 20(5):914-923.
21. Hackett NR, et al. (2011) The human airway epithelial basal cell transcriptome. PLoS ONE 6(5):e18378.
22. Voynow JA, Fischer BM, Roberts BC, Proia AD (2005) Basal-like cells constitute the proliferating cell population in cystic fibrosis airways. Am J Respir Crit Care Med 172(8):1013-1018.
23. Takeyama K, et al. (1999) Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci USA 96(6):3081-3086.
24. Cohen S (1965) The stimulation of epidermal proliferation by a specific protein (EGF). Dev Biol 12(3):394-407.
25. Rheinwald JG, Green H (1977) Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature 265(5593):421-424.
26. Filosto S, Becker CR, Goldkorn T (2012) Cigarette smoke induces aberrant EGF receptor activation that mediates lung cancer development and resistance to tyrosine kinase inhibitors. Mol Cancer Ther 11(4):795-804.
27. Takeyama K, et al. (2001) Activation of epidermal growth factor receptors is responsible for mucin synthesis induced by cigarette smoke. Am J Physiol Lung Cell Mol Physiol 280(1):L165-L172.
28. Dempsey PJ, Meise KS, Yoshitake Y, Nishikawa K, Coffey RJ (1997) Apical enrichment of human EGF precursor in Madin-Darby canine kidney cells involves preferential basolateral ectodomain cleavage sensitive to a metalloprotease inhibitor. J Cell Biol 138(4):747-758.
29. Vermeer PD, et al. (2003) Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422(6929):322-326.
30. Karp PH, et al. (2002) An in vitro model of differentiated human airway epithelia: Methods for establishing primary cultures. Methods Mol Biol 188:115-137.
31. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119(6):1420-1428.
32. Clark AB, et al. (1995) Regulation of ciliated cell differentiation in cultures of rat tracheal epithelial cells. Am J Respir Cell Mol Biol 12(3):329-338.
33. Mani SA, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133(4):704-715.
34. Schneeberger EE, Lynch RD (2004) The tight junction: A multifunctional complex. Am J Physiol Cell Physiol 286(6):C1213-C1228.
35. Aida S, Tamai S, Sekiguchi S, Shimizu N (1994) Distribution of epidermal growth factor and epidermal growth factor receptor in human lung: Immunohistochemical and immunoelectron-microscopic studies. Respiration 61(3):161-166.
36. Casalino-Matsuda SM, Monzón ME, Forteza RM (2006) Epidermal growth factor receptor activation by epidermal growth factor mediates oxidant-induced goblet cell metaplasia in human airway epithelium. Am J Respir Cell Mol Biol 34(5):581-591.
37. Takeyama K, et al. (2000) Oxidative stress causes mucin synthesis via transactivation of epidermal growth factor receptor: Role of neutrophils. J Immunol 164(3):1546-1552.
38. Filosto S, et al. (2011) EGF receptor exposed to oxidative stress acquires abnormal phosphorylation and aberrant activated conformation that impairs canonical dimerization. PLoS ONE 6(8):e23240.
39. Hübner RH, et al. (2009) Coordinate control of expression of Nrf2-modulated genes in the human small airway epithelium is highly responsive to cigarette smoking. Mol Med 15(7-8):203-219.
40. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2004) Tobacco smoke and involuntary smoking. IARC Monogr Eval Carcinog Risks Hum 83: 161-274.
41. Løkke A, Lange P, Scharling H, Fabricius P, Vestbo J (2006) Developing COPD: A 25-year follow up study of the general population. Thorax 61(11):935-939.
42. Van Winkle LS, Isaac JM, Plopper CG (1997) Distribution of epidermal growth factor receptor and ligands during bronchiolar epithelial repair from naphthalene-induced Clara cell injury in the mouse. Am J Pathol 151(2):443-459.
43. Hirsch FR, Scagliotti GV, Langer CJ, Varella-Garcia M, Franklin WA (2003) Epidermal growth factor family of receptors in preneoplasia and lung cancer: Perspectives for targeted therapies. Lung Cancer 41(Suppl 1):S29-S42.
44. You Y, et al. (2004) Role of f-box factor foxj1 in differentiation of ciliated airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 286(4):L650-L657.
45. Guichard C, et al. (2001) Axonemal dynein intermediate-chain gene (DNAI1) mutations result in situs inversus and primary ciliary dyskinesia (Kartagener syndrome). Am J Hum Genet 68(4):1030-1035.
46. Sharma P, et al. (1998) MUC5B and MUC7 are differentially expressed in mucous and serous cells of submucosal glands in human bronchial airways. Am J Respir Cell Mol Biol 19(1):30-37.
47. Buisson AC, et al. (1996) Wound repair-induced expression of a stromelysins is associated with the acquisition of a mesenchymal phenotype in human respiratory epithelial cells. Lab Invest 74(3):658-669.
48. Martin-Belmonte F, et al. (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128(2):383-397.
49. Lu Z, Ghosh S, Wang Z, Hunter T (2003) Down-regulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 4(6):499-515.
50. Solic N, Davies DE (1997) Differential effects of EGF and amphiregulin on adhesion molecule expression and migration of colon carcinoma cells. Exp Cell Res 234(2): 465-476.
51. Chang TH, et al. (2011) Slug confers resistance to the epidermal growth factor receptor tyrosine kinase inhibitor. Am J Respir Crit Care Med 183(8):1071-1079.
52. Hackett NR, et al. (2012) RNA-Seq quantification of the human small airway epithelium transcriptome. BMC Genomics 13:82.