Trachea epithelium as a "Canary" for cigarette smoking-induced biologic phenotype of the small airway epithelium

Clinical and Translational Science

Volumn 2, Issue 4, 2009, Pages 260-272

  Turetz, Meredith L ^a   O'Connor, Timothy P ^a   Tilley, Ann E ^a   Strulovici Barel, Yael ^a   Salit, Jacqueline ^a   Dang, David ^a   Teater, Matthew ^a   Mezey, Jason ^b   Clark, Andrew G ^b   Crystal, Ronald G ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Cornell University Ithaca ^*  (United States)

Author keywords

Airway; Epithelium; Gene expression

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME;

ADULT; ARTICLE; BODY MASS; CIGARETTE SMOKING; CONSCIOUS SEDATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FORCED EXPIRATORY VOLUME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; LUNG DIFFUSION CAPACITY; LUNG FUNCTION; MALE; MINIMALLY INVASIVE PROCEDURE; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT EXAMINATION; SAMPLING; SMOKING HABIT; TISSUE MICROARRAY; TISSUE PREPARATION; TOTAL LUNG CAPACITY; TRACHEA MUCOSA; UPREGULATION;

ADULT; EPITHELIUM; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; SMOKING; TOBACCO; TRACHEA; TRANSLATIONAL RESEARCH;

EID: 77953455002     PISSN: 17528054     EISSN: 17528062     Source Type: Journal    
DOI: 10.1111/j.1752-8062.2009.00129.x     Document Type: Article

References (74)

1. Doll R, Peto R. Mortality in relation to smoking: 20 years' observations on male British doctors. Br Med J. 1976; 2: 1525-1536.
2. Shopland DR. Tobacco use and its contribution to early cancer mortality with a special emphasis on cigarette smoking. Environ Health Perspect. 1995; 103(Suppl 8): 131-142.
3. Rennard SI. COPD: Overview of definitions, epidemiology, and factors influencing its development. Chest. 1998; 113: 235S-41S.
4. Hecht SS. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat Rev Cancer. 2003; 3: 733-744.
5. Cigarette smoking among adults-United States, 2007. MMWR Morb Mortal Wkly Rep 2008; 57: 1221-1226.
6. Pauwels RA, Buist AS, Calverley PM, Jenkins CR, Hurd SS. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop summary. Am J Respir Crit Care Med. 2001; 163: 1256-1276.
7. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin. 2008; 58: 71-96.
8. Fletcher C, Peto R. The natural history of chronic airflow obstruction. Br Med J. 1977; 1: 1645-1648.
9. Cigarette smoking and health. American Thoracic Society. Am J Respir Crit Care Med. 1996; 153: 861-865.
10. Anthonisen NR, Connett JE, Murray RP. Smoking and lung function of Lung Health Study participants after 11 years. Am J Respir Crit Care Med. 2002; 166: 675-679.
11. Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, Postmus PE, Rusch V, Sobin L. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol. 2007; 2: 706-714.
12. Coxson HO, Rogers RM. Quantitative computed tomography of chronic obstructive pulmonary disease. Acad Radiol. 2005; 12: 1457-1463.
13. Bach PB, Jett JR, Pastorino U, Tockman MS, Swensen SJ, Begg CB. Computed tomography screening and lung cancer outcomes. JAMA. 2007; 297: 953-961.
14. Henschke CI, Yankelevitz DF, Libby DM, Pasmantier MW, Smith JP, Miettinen OS. Survival of patients with stage I lung cancer detected on CT screening. N Engl J Med. 2006; 355: 1763-1771.
15. Hogg JC, Macklem PT, Thurlbeck WM. Site and nature of airway obstruction in chronic obstructive lung disease. N Engl J Med. 1968; 278: 1355-1360.
16. Auerbach O, Hammond EC, Garfinkel L. Changes in bronchial epithelium in relation to cigarette smoking, 1955-1960 vs. 1970-1977. N Engl J Med. 1979; 300: 381-385.
17. Cosio MG, Hale KA, Niewoehner DE. Morphologic and morphometric effects of prolonged cigarette smoking on the small airways. Am Rev Respir Dis. 1980; 122: 265-321.
18. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, Pare PD. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004; 350: 2645-2653.
19. Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet. 2004; 364: 709-721.
20. Mercer RR, Russell ML, Roggli VL, Crapo JD. Cell number and distribution in human and rat airways. Am J Respir Cell Mol Biol. 1994; 10: 613-624.
21. Weibel ER. Design and morphometry of the pulmonary gas exchanger. In: Crystal RG, West JB, Weibel ER, Barnes PJ, eds. The Lung Scientific Foundations. 2nd ed. Philadelphia: Lippincott-Raven, 2009, 1147-1157.
22. Barnes PJ, Chowdhury B, Kharitonov SA, Magnussen H, Page CP, Postma D, Saetta M. Pulmonary biomarkers in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2006; 174: 6-14.
23. Cazzola M, MacNee W, Martinez FJ, Rabe KF, Franciosi LG, Barnes PJ, Brusasco V, Burge PS, Calverley PM, Celli BR, Jones PW, Mahler DA, Make B, Miravitlles M, Page CP, Palange P, Parr D, Pistolesi M, Rennard SI, Rutten-van Molken MP, Stockley R, Sullivan SD, Wedzicha JA, Wouters EF. Outcomes for COPD pharmacological trials: From lung function to biomarkers. Eur Respir J. 2008; 31: 416-469.
24. Hackett NR, Heguy A, Harvey BG, O'Connor TP, Luettich K, Flieder DB, Kaplan R, Crystal RG. Variability of antioxidant-related gene expression in the airway epithelium of cigarette smokers. Am J Respir Cell Mol Biol. 2003; 29: 331-343.
25. Spira A, Beane J, Shah V, Liu G, Schembri F, Yang X, Palma J, Brody JS. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc Natl Acad Sci USA. 2004; 101: 10143-10148.
26. Beane J, Sebastiani P, Liu G, Brody JS, Lenburg ME, Spira A. Reversible and permanent effects of tobacco smoke exposure on airway epithelial gene expression. Genome Biol. 2007; 8: R201.
27. Harvey BG, Heguy A, Leopold PL, Carolan BJ, Ferris B, Crystal RG. Modification of gene expression of the small airway epithelium in response to cigarette smoking. J Mol Med. 2007; 85: 39-53.
28. Pierrou S, Broberg P, O'Donnell RA, Pawlowski K, Virtala R, Lindqvist E, Richter A, Wilson SJ, Angco G, Moller S, Bergstrand H, Koopmann W, Wieslander E, Stromstedt PE, Holgate ST, Davies DE, Lund J, Djukanovic R. Expression of genes involved in oxidative stress responses in airway epithelial cells of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007; 175: 577-586.
29. Ammous Z, Hackett NR, Butler MW, Raman T, Dolgalev I, O'Connor TP, Harvey BG, Crystal RG. Variability in small airway epithelial gene expression among normal smokers. Chest. 2008; 133: 1344-1353.
30. Zhang LI, Lee J, Tang H, Fan YH, Xiao L, Ren H, Kurie J, Morice RC, Hong WK, Mao H. Impact of smoking cessation on global gene expression in the bronchial epithelium of chronic smokers. Cancer Prev Res. 2008; 1: 112-118.
31. Suratt PM, Smiddy JF, Gruber B. Deaths and complications associated with fiberoptic bronchoscopy. Chest. 1976; 69: 747-751.
32. Pereira W Jr, Kovnat DM, Snider GL. A prospective cooperative study of complications following flexible fiberoptic bronchoscopy. Chest. 1978; 73: 813-816.
33. Pue CA, Pacht ER. Complications of fiberoptic bronchoscopy at a university hospital. Chest. 1995; 107: 430-432.
34. Lu BS, Yu AD, Zhu X, Garrity ER Jr, Vigneswaran WT, Bhorade SM. Sequential gene expression profiling in lung transplant recipients with chronic rejection. Chest. 2006; 130: 847-854.
35. Heguy A, Harvey BG, Leopold PL, Dolgalev I, Raman T, Crystal RG. Responses of the human airway epithelium transcriptome to in vivo injury. Physiol Genomics. 2007; 29: 139-148.
36. Kramer EL, Deutsch GH, Sartor MA, Hardie WD, Ikegami M, Korfhagen TR, Le Cras TD. Perinatal increases in TGF-{alpha} disrupt the saccular phase of lung morphogenesis and cause remodeling: Microarray analysis. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L314-L327.
37. Tilley AE, Harvey BG, Heguy A, Hackett NR, Wang R, O'Connor TP, Crystal RG. Down-regulation of the notch pathway in human airway epithelium in association with smoking and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2009; 179: 457-466.
38. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Royal Statist Soc. 2009; 57: 289-300.
39. Spira A, Beane JE, Shah V, Steiling K, Liu G, Schembri F, Gilman S, Dumas YM, Calner P, Sebastiani P, Sridhar S, Beamis J, Lamb C, Anderson T, Gerry N, Keane J, Lenburg ME, Brody JS. Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat Med. 2007; 13: 361-366.
40. Thompson AB, Robbins RA, Romberger DJ, Sisson JH, Spurzem JR, Teschler H, Rennard SI. Immunological functions of the pulmonary epithelium. Eur Respir J. 1995; 8: 127-149.
41. MacNee W. Oxidative stress and lung infl ammation in airways disease. Eur J Pharmacol. 2001; 429: 195-207.
42. Barnes PJ. Genetics and pulmonary medicine. 9. Molecular genetics of chronic obstructive pulmonary disease. Thorax. 1999; 54: 245-252.
43. Silverman EK, Chapman HA, Drazen JM, Weiss ST, Rosner B, Campbell EJ, O'Donnell WJ, Reilly JJ, Ginns L, Mentzer S, Wain J, Speizer FE. Genetic epidemiology of severe, early-onset chronic obstructive pulmonary disease. Risk to relatives for airfl ow obstruction and chronic bronchitis. Am J Respir Crit Care Med. 1998; 157: 1770-1778.
44. Molfino NA. Current thinking on genetics of chronic obstructive pulmonary disease. Curr Opin Pulm Med. 2007; 13: 107-113.
45. Mastrangeli A, Crystal RG. Alpha 1-antitrypsin deficiency. In: Crystal RG, editor. Alpha 1-Antitrypsin Deficiency. New York: Marcel Dekker, Inc, 1996, 3-18.
46. Jones PW, Agusti AG. Outcomes and markers in the assessment of chronic obstructive pulmonary disease. Eur Respir J. 2006; 27: 822-832.
47. Tzortzaki EG, Tsoumakidou M, Makris D, Siafakas NM. Laboratory markers for COPD in "susceptible" smokers. Clin Chim Acta. 2006; 364: 124-138.
48. Gan WQ, Man SF, Senthilselvan A, Sin DD. Association between chronic obstructive pulmonary disease and systemic inflammation: A systematic review and a meta-analysis. Thorax. 2004; 59: 574-580.
49. Karadag F, Karul AB, Cildag O, Yilmaz M, Ozcan H. Biomarkers of systemic infl ammation in stable and exacerbation phases of COPD. Lung. 2008; 186: 403-409.
50. Lomas DA, Silverman EK, Edwards LD, Miller BE, Coxson HO, Tal-Singer R. Evaluation of serum CC-16 as a biomarker for COPD in the ECLIPSE cohort. Thorax. 2008; 63: 1058-1063.
51. Sin DD, Man SF, Marciniuk DD, Ford G, FitzGerald M, Wong E, York E, Mainra RR, Ramesh W, Melenka LS, Wilde E, Cowie RL, Williams D, Gan WQ, Rousseau R. The effects of fluticasone with or without salmeterol on systemic biomarkers of inflammation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008; 177: 1207-1214.
52. Keatings VM, Collins PD, Scott DM, Barnes PJ. Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am J Respir Crit Care Med. 1996; 153: 530-534.
53. Brightling CE, Monteiro W, Ward R, Parker D, Morgan MD, Wardlaw AJ, Pavord ID. Sputum eosinophilia and short-term response to prednisolone in chronic obstructive pulmonary disease: A randomised controlled trial. Lancet. 2000; 356: 1480-1485.
54. Tsoumakidou M, Tzanakis N, Chrysofakis G, Kyriakou D, Siafakas NM. Changes in sputum T-lymphocyte subpopulations at the onset of severe exacerbations of chronic obstructive pulmonary disease. Respir Med. 2005; 99: 572-579.
55. Yamamoto C, Yoneda T, Yoshikawa M, Fu A, Tokuyama T, Tsukaguchi K, Narita N. Airway inflammation in COPD assessed by sputum levels of interleukin-8. Chest. 1997; 112: 505-510.
56. Hill AT, Bayley D, Stockley RA. The interrelationship of sputum inflammatory markers in patients with chronic bronchitis. Am J Respir Crit Care Med. 1999; 160: 893-898.
57. Vernooy JH, Lindeman JH, Jacobs JA, Hanemaaijer R, Wouters EF. Increased activity of matrix metalloproteinase-8 and matrix metalloproteinase-9 in induced sputum from patients with COPD. Chest. 2004; 126: 1802-1810.
58. Franciosi LG, Page CP, Celli BR, Cazzola M, Walker MJ, Danhof M, Rabe KF, Della Pasqua OE. Markers of disease severity in chronic obstructive pulmonary disease. Pulm Pharmacol Ther. 2006; 19: 189-199.
59. Luisetti M, Ma S, Iadarola P, Stone PJ, Viglio S, Casado B, Lin YY, Snider GL, Turino GM. Desmosine as a biomarker of elastin degradation in COPD: Current status and future directions. Eur Respir J. 2008; 32: 1146-1157.
60. Montuschi P, Collins JV, Ciabattoni G, Lazzeri N, Corradi M, Kharitonov SA, Barnes PJ. Exhaled 8-isoprostane as an in vivo biomarker of lung oxidative stress in patients with COPD and healthy smokers. Am J Respir Crit Care Med. 2000; 162: 1175-1177.
61. Kostikas K, Papatheodorou G, Psathakis K, Panagou P, Loukides S. Oxidative stress in expired breath condensate of patients with COPD. Chest. 2003; 124: 1373-1380.
62. Kharitonov SA, Barnes PJ. Exhaled biomarkers. Chest. 2006; 130: 1541-1546.
63. Sung HJ, Cho JY. Biomarkers for the lung cancer diagnosis and their advances in proteomics. BMB Rep. 2008; 41: 615-625.
64. Danel C, Erzurum SC, McElvaney NG, Crystal RG. Quantitative assessment of the epithelial and inflammatory cell populations in large airways of normals and individuals with cystic fibrosis. Am J Respir Crit Care Med. 1996; 153: 362-368.
65. Heguy A, Harvey BG, O'Connor TP, Hackett NR, Crystal RG. Sampling-dependent up-regulation of gene expression in sequential samples of human airway epithelial cells. Mol Med. 2003; 9: 200-208.
66. Chari R, Lonergan KM, Ng RT, MacAulay C, Lam WL, Lam S. Effect of active smoking on the human bronchial epithelium transcriptome. BMC Genomics. 2007; 8: 297.
67. Barnes PJ, Shapiro SD, Pauwels RA. Chronic obstructive pulmonary disease: Molecular and cellular mechanisms. Eur Respir J. 2003; 22: 672-688.
68. Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, van de Rijn M, Rosen GD, Perou CM, Whyte RI, Altman RB, Brown PO, Botstein D, Petersen I. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA. 2001; 98: 13784-13789.
69. Smith RV, Schlecht NF, Childs G, Prystowsky MB, Belbin TJ. Pilot study of mucosal genetic differences in early smokers and nonsmokers. Laryngoscope. 2006; 116: 1375-1379.
70. Spivack SD, Hurteau GJ, Jain R, Kumar SV, Aldous KM, Gierthy JF, Kaminsky LS. Gene-environment interaction signatures by quantitative mRNA profiling in exfoliated buccal mucosal cells. Cancer Res. 2004; 64: 6805-6813.
71. Sridhar S, Schembri F, Zeskind J, Shah V, Gustafson AM, Steiling K, Liu G, Dumas YM, Zhang X, Brody JS, Lenburg ME, Spira A. Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC Genomics. 2008; 9: 259.
72. Nagai K, Betsuyaku T, Suzuki M, Nasuhara Y, Kaga K, Kondo S, Nishimura M. Dual oxidase 1 and 2 expression in airway epithelium of smokers and patients with mild/moderate chronic obstructive pulmonary disease. Antioxid Redox Signal. 2008; 10: 705-714.
73. Lee NH, Saeed AI. Microarrays: An overiview. In: Hilario E, Mackay J, eds. Methods in Molecular Biology. 2nd ed. Totowa: Humana Press Inc, 2007, 265-300.
74. Peano C, Severgnini M, Cifola I, De BG, Battaglia C. Transcriptome amplification methods in gene expression profiling. Expert Rev Mol Diagn. 2006; 6: 465-480.