Bronchial brushings for investigating airway inflammation and remodelling

Respirology

Volumn 16, Issue 5, 2011, Pages 725-737

  Looi, Kevin ^a   Sutanto, Erika N ^b,c   Banerjee, Balarka ^a   Garratt, Luke ^a   Ling, Kak Ming ^b   Foo, Clara J ^a   Stick, Stephen M ^a,b,c   Kicic, Anthony ^a,b,c  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

Author keywords

Airway; Airway inflammation; Cytology brushing; Epithelium; Functional study

Indexed keywords

AIRWAY REMODELING; ASTHMA; BRONCHOSCOPY; BRONCHUS BIOPSY; INFLAMMATION; LUNG LAVAGE; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; REVIEW;

AIRWAY REMODELING; ASTHMA; AUSTRALIA; BIOPSY; BRONCHI; BRONCHOALVEOLAR LAVAGE; BRONCHOSCOPY; EPITHELIAL CELLS; HUMANS;

EID: 79959894244     PISSN: 13237799     EISSN: 14401843     Source Type: Journal    
DOI: 10.1111/j.1440-1843.2011.02001.x     Document Type: Review

References (122)

1. Global Strategy for Asthma Management and Prevention. Global Initiative for Asthma (GINA); 2010. [Accessed 9 Jun 2011.] Available from URL: http://www.ginasthma.org/
2. Braman SS. The global burden of asthma. Chest 2006; 130: 4-12S.
3. Australian Centre for Asthma Monitoring 2008. Asthma in Australia 2008. AIHW Asthma series no. 3. Cat. no. ACM 14. Canberra: AIHW.
4. Anderson GP. Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 2008; 372: 1107-19.
5. Erjefält JS, Erjefält I, Sundler F et al. In vivo restitution of airway epithelium. Cell Tissue Res. 1995; 281: 305-16.
6. White SR, Tse R, Marroquin BA. Stress-activated protein kinases mediate cell migration in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2005; 32: 301-10. (Pubitemid 40478305)
7. Vignola AM, Mirabella F, Costanzo G et al. Airway remodeling in asthma. Chest 2003; 123: 417-22S.
8. Kraft M, Martin Richard J, Wilson S et al. Lymphocyte and eosinophil influx into alveolar tissue in nocturnal asthma. Am. J. Respir. Crit. Care Med. 1999; 159: 228-34. (Pubitemid 29036528)
9. 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: 122-33.
10. Hackett TL. Characterization of side population cells from human airway epithelium. Stem Cells 2008; 26: 2576-85.
11. Prakash U, Mehta A. Newer and miscellaneous applications of bronchoscopy. In: Prakash U (ed.) Bronchoscopy. Raven Press Ltd, New York, 1994; 433-41.
12. Prakash UB. Bronchoscopy in North America: the ACCP survey. Chest 1991; 100: 1668-75.
13. Burns DM, Shure D, Francoz R et al. The physiologic consequences of saline lobar lavage in healthy human adults. Am. Rev. Respir. Dis. 1983; 127: 695-701. (Pubitemid 13101548)
14. Ettensohn DB. Bronchoalveolar lavage in the normal volunteer subject. 2. Safety and results of repeated BAL and use in the assessment of intra-subject variability. Chest 1988; 94: 281-5.
15. Jarjour NN, Calhoun WJ. Bronchoalveolar lavage in stable asthmatics does not cause pulmonary inflammation. Am. Rev. Respir. Dis. 1990; 142: 100-3. (Pubitemid 20224585)
16. Krug N. Safety aspects of local endobronchial allergen challenge in asthmatic patients. Am. J. Respir. Crit. Care Med. 1996; 153: 1391-7. (Pubitemid 26112607)
17. Nussbaum E. Pediatric fiberoptic bronchoscopy: clinical experience with 2,836 bronchoscopies. Pediatr. Crit. Care Med. 2002; 3: 171-6.
18. Pue CA. Complications of fiberoptic bronchoscopy at a university hospital. Chest 1995; 107: 430-2.
19. Wood R, Daines C. Bronchoscopy and bronchoalveolar lavage in pediatric patients. In: Chernick V, Boat T, Wilmott R et al. (eds) Kendig's Disorders of the Respiratory Tract in Children, 7th edn. Elsevier, Philadelphia, PA, 2006; 94-109.
20. Veeraraghavan S, Latsi PI, Wells AU et al. BAL findings in idiopathic nonspecific interstitial pneumonia and usual interstitial pneumonia. Eur. Respir. J. 2003; 22: 239-44. (Pubitemid 36986991)
21. Casale TB. Direct evidence of a role for mast cells in the pathogenesis of antigen-induced bronchoconstriction. J. Clin. Invest. 1987; 80: 1507-11. (Pubitemid 18027799)
22. Callister ME. Extracellular thioredoxin levels are increased in patients with acute lung injury. Thorax 2006; 61: 521-7. (Pubitemid 43901523)
23. Crohns M, Saarelainen S, Laine S et al. Cytokines in bronchoalveolar lavage fluid and serum of lung cancer patients during radiotherapy - association of interleukin-8 and VEGF with survival. Cytokine 2009; 50: 30-6.
24. Striz I, Wang YM, Svarcova I et al. The phenotype of alveolar macrophages and its correlation with immune cells in bronchoalveolar lavage. Eur. Respir. J. 1993; 6: 1287-94. (Pubitemid 23329544)
25. Ishii H. High serum concentrations of surfactant protein A in usual interstitial pneumonia compared with non-specific interstitial pneumonia. Thorax 2003; 58: 52-7. (Pubitemid 36135359)
26. Ward C. Evaluation of albumin as a reference marker of dilution in bronchoalveolar lavage fluid from asthmatic and control subjects. Thorax 1993; 48: 518-22. (Pubitemid 23160168)
27. De Jong PM, Van Sterkenburg MAJA, Kempenaar JA et al. Serial culturing of human bronchial epithelial cells derived from biopsies. In Vitro Cell Dev. Biol. Anim. 1993; 29A: 379-87. (Pubitemid 23187757)
28. Ackerman V. Detection of cytokines and their cell sources in bronchial biopsy specimens from asthmatic patients. Relationship to atopic status, symptoms, and level of airway hyperresponsiveness. Chest 1994; 105: 687-96. (Pubitemid 24088441)
29. Laitinen LA, Laitinen A, Altraja A et al. Bronchial biopsy findings in intermittent or "Early" asthma. J. Allergy Clin. Immunol. 1996; 98: S3-6.
30. Bradley BL, Azzawi M, Jacobson M et al. Eosinophils, T-lymphocytes, mast cells, neutrophils, and macrophages in bronchial biopsy specimens from atopic subjects with asthma: comparison with biopsy specimens from atopic subjects without asthma and normal control subjects and relationship to bronchial hyperresponsiveness. J. Allergy Clin. Immunol. 1991; 88: 661-74.
31. Bayram H. Comparison of ciliary activity and inflammatory mediator release from bronchial epithelial cells of nonatopic nonasthmatic subjects and atopic asthmatic patients and the effect of diesel exhaust particles in vitro. J. Allergy Clin. Immunol. 1998; 102: 771-82.
32. Devalia JL, Bayram H, Abdelaziz MM et al. Differences between cytokine release from bronchial epithelial cells of asthmatic patients and non-asthmatic subjects: effect of exposure to diesel exhaust particles. Int. Arch. Allergy Immunol. 1999; 118: 437-9. (Pubitemid 29195594)
33. Campbell AM, Chanez P, Vignola AM et al. Functional characteristics of bronchial epithelium obtained by brushing from asthmatic and normal subjects. Am. Rev. Respir. Dis. 1993; 147: 529-34. (Pubitemid 23072637)
34. Vignola AM, Chanez P, Campbell AM et al. Quantification and localization of HLA-DR and intercellular adhesion molecule-1 (ICAM-1) molecules on bronchial epithelial cells of asthmatics using confocal microscopy. Clin. Exp. Immunol. 1994; 96: 104-9. (Pubitemid 24213806)
35. Ketterer MR. Infection of primary human bronchial epithelial cells by Haemophilus influenzae: macropinocytosis as a mechanism of airway epithelial cell entry. Infect. Immun. 1999; 67: 4161-70. (Pubitemid 29357042)
36. Lordan JL, Bucchieri F, Richter A et al. Cooperative effects of Th2 cytokines and allergen on normal and asthmatic bronchial epithelial cells. J. Immunol. Methods 2002; 169: 407-14. (Pubitemid 34686162)
37. Bucchieri F. Asthmatic bronchial epithelium is more susceptible to oxidant-induced apoptosis. Am. J. Respir. Cell Mol. Biol. 2002; 27: 179-85. (Pubitemid 34780797)
38. Doherty GM, Christie SN, Skibinski G et al. Non-bronchoscopic sampling and culture of bronchial epithelial cells in children. Clin. Exp. Allergy 2003; 33: 1221-25. (Pubitemid 37108525)
39. Wallace JM, Deutsch AL, Harrell JH et al. Bronchoscopy and transbronchial biopsy in evaluation of patients with suspected active tuberculosis. Am. J. Med. 1981; 70: 1189-94. (Pubitemid 11072111)
40. Sarkar SK. Fiberoptic bronchoscopy in the diagnosis of pulmonary tuberculosis. Tubercle 1980; 61: 97-9. (Pubitemid 10122360)
41. Lane C. The use of non-bronchoscopic brushings to study the paediatric airway. Resp. Res. 2005; 6: 53-63.
42. 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: 1110-18. (Pubitemid 44772081)
43. Trapnell BC, Chu CS, Paakko PK et al. Expression of the cystic fibrosis transmembrane conductance regulator gene in the respiratory tract of normal individuals and individuals with cystic fibrosis. Proc. Natl Acad. Sci. USA 1991; 88: 6565-69. (Pubitemid 21914988)
44. Hamosh A. Severe deficiency of cystic fibrosis transmembrane conductance regulator messenger RNA carrying nonsense mutations R553X and W1316X in respiratory epithelial cells of patients with cystic fibrosis. J. Clin. Invest. 1991; 88: 1880-5.
45. Sutanto EN, Kicic A, Foo CJ et al. Innate inflammatory responses of pediatric cystic fibrosis airway epithelial cells: effects of non-viral and viral stimulation. Am. J. Respir. Cell Mol. Biol. 2011; 44: 761-7.
46. Campbell AM. Low-affinity receptor for IgE on human bronchial epithelial cells in asthma. Immunology 1994; 82: 506-8. (Pubitemid 24263373)
47. Guo FH. Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis. J. Immunol. 2000; 164: 5970-80. (Pubitemid 30389845)
48. McNamara PS, Kicic A, Sutanto EN et al. Comparison of techniques for obtaining lower airway epithelial cells from children. Eur. Respir. J. 2008; 32: 763-8.
49. Banerjee B, Kicic A, Musk M et al. Successful establishment of primary small airway cell cultures in human lung transplantation. Respir. Res. 2009; 10: 99-108.
50. 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: 1901-10.
51. Lopez-Souza N, Favoreto S, Wong H et al. In vitro susceptibility to rhinovirus infection is greater for bronchial than for nasal airway epithelial cells in human subjects. J. Allergy Clin. Immunol. 2009; 123: 1384-90.
52. McDougall CM. Nasal epithelial cells as surrogates for bronchial epithelial cells in airway inflammation studies. Am. J. Respir. Cell Mol. Biol. 2008; 39: 560-8.
53. Lopez-Souza N, Dolganov G, Dubin R et al. Resistance of differentiated human airway epithelium to infection by rhinovirus. Am. J. Physiol. Lung Cell Mol. Physiol. 2004; 286: L373-81.
54. Kicic A. Decreased fibronectin production significantly contributes to dysregulated repair of asthmatic epithelium. Am. J. Respir. Crit. Care Med. 2010; 181: 889-98.
55. Devalia JL. Culture and comparison of human bronchial and nasal epithelial cells in vitro. Respir. Med. 1990; 84: 303-12. (Pubitemid 20271049)
56. Devalia JL. Human nasal and bronchial epithelial cells in culture: an overview of their characteristics and function. Allergy Asthma Proc. 1991; 12: 71-9.
57. Mosler K, Coraux C, Fragaki K et al. Feasibility of nasal epithelial brushing for the study of airway epithelial functions in CF infants. J. Cyst. Fibros. 2008; 7: 44-53.
58. Calderón MA, Devalia JL, Prior A et al. A comparison of cytokine release from epithelial cells cultured from nasal biopsy specimens of atopic patients with and without rhinitis and nonatopic subjects without rhinitis. J. Allergy Clin. Immunol. 1997; 99: 65-76. (Pubitemid 27074899)
59. Chanez P, Vignola Antonio M, Vic P et al. Comparison between nasal and bronchial inflammation in asthmatic and control subjects. Am. J. Respir. Crit. Care Med. 1999; 159: 588-95. (Pubitemid 29084885)
60. Vignola AM, Campbell AM, Chanez P et al. HLA-DR and ICAM-1 expression on bronchial epithelial cells in asthma and chronic bronchitis. Am. Rev. Respir. Dis. 1993; 148: 689-94. (Pubitemid 23263781)
61. Gibson PG. Chronic cough resembles asthma with IL-5 and granulocyte-macrophage colony-stimulating factor gene expression in bronchoalveolar cells. J. Allergy Clin. Immunol. 1998; 101: 320-6. (Pubitemid 28146349)
62. Hilty M, Burke C, Pedro H et al. Disordered microbial communities in asthmatic airways. PLoS One 2010; 5: e8578-86.
63. Huang YJ, Nelson CE, Brodie EL et al. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J. Allergy Clin. Immunol. 2011; 127: 372-81.
64. Borthwick LA, Parker SM, Brougham KA et al. Epithelial to mesenchymal transition (EMT) and airway remodelling after human lung transplantation. Thorax 2009; 64: 770-7.
65. Romagnoli M, Vachier I, Vignola AM et al. Safety and cellular assessment of bronchial brushing in airway diseases. Respir. Med. 1999; 93: 461-6. (Pubitemid 29364060)
66. Vega-Carrascal I, Reeves EP, Niki T et al. Dysregulation of TIM-3 Galectin-9 pathway in the cystic fibrosis airways. J. Immunol. 2011; 186: 2897-09.
67. Bonfield TL, Konstan MW, Berger M. Altered respiratory epithelial cell cytokine production in cystic fibrosis. J. Allergy Clin. Immunol. 1999; 104: 72-8. (Pubitemid 29364482)
68. Carson JL, Collier AM, Gambling TM et al. Ultrastructure of airway epithelial cell membranes among patients with cystic fibrosis. Hum. Pathol. 1990; 21: 640-7. (Pubitemid 20204953)
69. Dannhoffer L, Blouquit-Laye S, Regnier A et al. Functional properties of mixed cystic fibrosis and normal bronchial epithelial cell cultures. Am. J. Respir. Cell Mol. Biol. 2009; 40: 717-23.
70. Blouquit S, Regnier A, Dannhoffer L et al. Ion and fluid transport properties of small airways in cystic fibrosis. Am. J. Respir. Crit. Care Med. 2006; 174: 299-5.
71. + i-dependent hyperinflammatory response in human cystic fibrosis airway epithelia. J. Biol. Chem. 2005; 280: 17798-806.
72. Terajima M, Yamaya M, Sekizawa K et al. Rhinovirus infection of primary cultures of human tracheal epithelium: role of ICAM-1 and IL-1β. Am. J. Physiol. 1997; 273: L749-59.
73. Wojnarowski C, Frischer T, Hofbauer E et al. Cytokine expression in bronchial biopsies of cystic fibrosis patients with and without acute exacerbation. Eur. Respir. J. 1999; 14: 1136-44.
74. Perez A, Issler AC, Cotton CU et al. CFTR inhibition mimics the cystic fibrosis inflammatory profile. Am. J. Physiol. Lung Cell Mol. Physiol. 2007; 292: L383-95.
75. 2+ of airway epithelia. Am. J. Physiol. Lung Cell Mol. Physiol. 2007; 293: L1250-60.
76. Heeckeren A, Walenga R, Konstan MW et al. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J. Clin. Invest. 1997; 100: 2810-15. (Pubitemid 28007550)
77. Gosselin D. Impaired ability of CFTR knockout mice to control lung infection with Pseudomonas aeruginosa. .Am. J. Respir. Crit. Care Med. 1998; 157: 1253-62.
78. Gavilanes X, Huaux F, Meyer M et al. Azithromycin fails to reduce increased expression of neutrophil-related cytokines in primary-cultured epithelial cells from cystic fibrosis mice. J. Cyst. Fibros. 2009; 8: 203-10.
79. Kube D, Sontich U, Fletcher D et al. Proinflammatory cytokine responses to P. aeruginosa infection in human airway epithelial cell lines. Am. J. Physiol. Lung Cell Mol. Physiol. 2001; 280: L493-502.
80. Stecenko AA, King G, Torii K et al. Dysregulated cytokine production in human cystic fibrosis bronchial epithelial cells. Inflammation 2001; 25: 145-55. (Pubitemid 32493687)
81. Aldallal N, McNaughton EE, Manzel LJ et al. Inflammatory response in airway epithelial cells isolated from patients with cystic fibrosis. Am. J. Respir. Crit. Care Med. 2002; 166: 1248-56. (Pubitemid 35222603)
82. Verbeek E. Chloride transport in cultured nasal epithelium of cystic fibrosis patients. Pflügers Archiv 1990; 415: 540.
83. Carrabino S, Carpani D, Livraghi A et al. Dysregulated interleukin-8 secretion and NF-κB activity in human cystic fibrosis nasal epithelial cells. J. Cyst. Fibros. 2006; 5: 113-19.
84. Norez C, Antigny F, Noel S et al. A cystic fibrosis respiratory epithelial cell chronically treated by miglustat acquires a noncystic fibrosis-like phenotype. Am. J. Respir. Cell Mol. Biol. 2009; 41: 217-25.
85. Machen TE. Innate immune response in CF airway epithelia: hyperinflammatory? Am. J. Physiol. Cell Physiol. 2006; 291: C218-30.
86. Moeller A, Horak F Jr, Lane C et al. Inducible NO synthase expression is low in airway epithelium from young children with cystic fibrosis. Thorax 2006; 61: 514-20. (Pubitemid 43901522)
87. Verkman AS. Development and biological applications of chloride-sensitive fluorescent indicators. Am. J. Physiol. 1990; 259: C375-88.
88. Galietta LV, Jayaraman S, Verkman AS. Cell-based assay for high-throughput quantitative screening of CFTR chloride transport agonists. Am. J. Physiol. Cell Physiol. 2001; 281: C1734-42.
89. Li W, Zhang L, Johnson JS et al. Generation of novel AAV variants by directed evolution for improved CFTR delivery to human ciliated airway epithelium. Mol. Ther. 2009; 17: 2067-77.
90. Granio O. Improved adenovirus type 5 vector-mediated transduction of resistant cells by piggybacking on coxsackie B-adenovirus receptor-pseudotyped baculovirus. J. Virol. 2009; 83: 6048-66.
91. Kwilas AR, Yednak MA, Zhang L et al. Respiratory syncytial virus engineered to express the cystic fibrosis transmembrane conductance regulator corrects the bioelectric phenotype of human cystic fibrosis airway epithelium in vitro. J. Virol. 2010; 84: 7770-81.
92. Cigana C, Assael BM, Melotti P. Azithromycin selectively reduces tumor necrosis factor alpha levels in cystic fibrosis airway epithelial cells. Antimicrob. Agents Chemother. 2007; 51: 975-81. (Pubitemid 46355283)
93. Ribeiro CM, Hurd H, Wu Y et al. Azithromycin treatment alters gene expression in inflammatory, lipid metabolism, and cell cycle pathways in well-differentiated human airway epithelia. PLoS One 2009; 4: e5806-21.
94. Kukafka DS, O'Brien GM, Furukawa S et al. Surveillance bronchoscopy in lung transplant recipients. Chest 1997; 111: 377-81. (Pubitemid 27096954)
95. Matsuo T, Colt HG. Evidence against routine scheduling of surveillance bronchoscopy after stent insertion. Chest 2000; 118: 1455-9.
96. Forrest IA, Murphy DM, Ward C et al. Primary airway epithelial cell culture from lung transplant recipients. Eur. Respir. J. 2005; 26: 1080-85. (Pubitemid 41829940)
97. Ward C, Forrest IA, Murphy DM et al. Phenotype of airway epithelial cells suggests epithelial to mesenchymal cell transition in clinically stable lung transplant recipients. Thorax 2005; 60: 865-71. (Pubitemid 41475217)
98. Hodge S, Holmes M, Banerjee B et al. Posttransplant bronchiolitis obliterans syndrome is associated with bronchial epithelial to mesenchymal transition. Am. J. Transplant. 2009; 9: 727-33.
99. Christie JD, Edwards LB, Kucheryavaya AY et al. The registry of the international society for heart and lung transplantation: twenty-seventh official adult lung and heart-lung transplant report - 2010. J. Heart Lung Transplant. 2010; 29: 1104-18.
100. Borger P, Kauffman HF, Timmerman JAB et al. Cyclosporine, FK506, mycophenolate mofetil and prednisolone differentially modulate cytokine gene expression in human airway-derived epithelial cells. Transplantation 2000; 69: 1408-13. (Pubitemid 30238733)
101. Elssner A, Jaumann F, Dobmann S et al. Elevated levels of interleukin-8 and transforming growth factor-b in bronchoalveolar lavage fluid from patients with bronchiolitis obliterans syndrome: proinflammatory role of bronchial epithelial cells1. Transplantation 2000; 70: 362-7. (Pubitemid 30602758)
102. Elssner A, Jaumann F, Wolf WP et al. Bronchial epithelial cell B7-1 and B7-2 mRNA expression after lung transplantation: a role in allograft rejection? Eur. Respir. J. 2002; 20: 165-9. (Pubitemid 34822939)
103. Murphy DM. Effect of azithromycin on primary bronchial epithelial cells derived from stable lung allografts. Thorax 2007; 62: 834-5.
104. Murphy DM, Forrest IA, Corris PA et al. Simvastatin attenuates release of neutrophilic and remodelling factors from primary bronchial epithelial cells derived from stable lung transplant recipients. Am. J. Physiol. Lung Cell Mol. Physiol. 2008; 294: L592-9.
105. Biernacki WA, Kharitonov SA, Barnes PJ. Increased leukotriene B4 and 8-isoprostane in exhaled breath condensate of patients with exacerbations of COPD. Thorax 2003; 58: 294-8. (Pubitemid 36411413)
106. Kharitonov SA, Barnes PJ. Exhaled biomarkers. Chest 2006; 130: 1541-6. (Pubitemid 44786751)
107. Fabbri LM, Romagnoli M, Corbetta L et al. Differences in airway inflammation in patients with fixed airflow obstruction due to asthma or chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2003; 167: 418-24. (Pubitemid 36216426)
108. Rutgers SR, Postma DS, ten Hacken NHT et al. Ongoing airway inflammation in patients with COPD who do not currently smoke. Thorax 2000; 55: 12-18. (Pubitemid 30248773)
109. Powell CA. Loss of heterozygosity in epithelial cells obtained by bronchial brushing: clinical utility in lung cancer. Clin. Cancer Res. 1999; 5: 2025-34. (Pubitemid 29399254)
110. Wistuba II. Molecular damage in the bronchial epithelium of current and former smokers. J. Natl Cancer Inst. 1997; 89: 1366-73. (Pubitemid 27418028)
111. Franklin WA. Widely dispersed p53 mutation in respiratory epithelium. A novel mechanism for field carcinogenesis. J. Clin. Invest. 1997; 100: 2133-7. (Pubitemid 27459370)
112. Guo M. Promoter hypermethylation of resected bronchial margins. Clin. Cancer Res. 2004; 10: 5131-6.
113. Miyazu YM. Telomerase expression in noncancerous bronchial epithelia is a possible marker of early development of lung cancer. Cancer Res. 2005; 65: 9623-7. (Pubitemid 41541435)
114. Spira A. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc. Natl Acad. Sci. USA 2004; 101: 10143-8. (Pubitemid 38891209)
115. Schulz C, Kratzel K, Wolf K et al. Activation of bronchial epithelial cells in smokers without airway obstruction and patients with COPD. Chest 2004; 125: 1706-13. (Pubitemid 38648401)
116. Takizawa H, Tanaka M, Takami K et al. Increased expression of inflammatory mediators in small-airway epithelium from tobacco smokers. Am. J. Physiol. Lung Cell Mol. Physiol. 2000; 278: L906-13.
117. Harvey BG, Heguy A, Leopold PL et al. Modification of gene expression of the small airway epithelium in response to cigarette smoking. J. Mol. Med. 2007; 85: 39-53. (Pubitemid 46020941)
118. Hackett NR, Heguy A, Harvey BG et al. Variability of antioxidant-related gene expression in the airway epithelium of cigarette smokers. Am. J. Respir. Cell. Mol. Biol. 2003; 29: 331-43.
119. Zhang X, Sebastiani P, Liu G et al. Similarities and differences between smoking-related gene expression in nasal and bronchial epithelium. Physiol. Genomics 2010; 41: 1-8.
120. Spira A, Beane JE, Shah V et al. Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat. Med. 2007; 13: 361-6. (Pubitemid 46376687)
121. Voss JS, Kipp BR, Halling KC et al. Fluorescence in situ hybridization testing algorithm improves lung cancer detection in bronchial brushing specimens. Am. J. Respir. Crit. Care Med. 2010; 181: 478-85.
122. Crystal RG. Future research directions in idiopathic pulmonary fibrosis: summary of a national heart, lung, and blood institute working group. Am. J. Respir. Crit. Care Med. 2002; 166: 236-46. (Pubitemid 34765460)