Animal models of cigarette smoke-induced lung disease

Minerva Pneumologica

Volumn 42, Issue 3, 2003, Pages 85-99

  Wright, J L ^a   Churg, A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Bronchitis, chronic; Hypertension, pulmonary; Pulmonary emphysema; Smoking

Indexed keywords

ALPHA 1 ANTITRYPSIN; CIGARETTE SMOKE; COLLAGEN; COLLAGENASE 3; CYTOKINE; ELASTIN; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FIBROBLAST GROWTH FACTOR RECEPTOR 4; FIBULIN; GAMMA INTERFERON; GELATINASE A; GELATINASE B; INTERLEUKIN 11; INTERLEUKIN 6; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE 14; PLATELET DERIVED GROWTH FACTOR A; PROTEINASE; PROTEINASE INHIBITOR; TOBACCO SMOKE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANIMAL MODEL; APOPTOSIS; BRONCHIOLITIS; CHRONIC BRONCHITIS; CIGARETTE SMOKING; COR PULMONALE; DISEASE COURSE; DNA MODIFICATION; EXPERIMENTAL ANIMAL; EXPERIMENTAL MODEL; EXPOSURE; GENE TARGETING; GOBLET CELL; HUMAN; LUNG BLOOD VESSEL; LUNG EMPHYSEMA; METAPLASIA; NONHUMAN; PATHOGENESIS; PULMONARY HYPERTENSION; RESPIRATORY TRACT INFLAMMATION; REVIEW; SPONTANEOUS MUTATION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

EID: 0344442330     PISSN: 00264954     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (139)

1. National Heart Lung and Blood Institute, World Health Organization. Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Pulmonary Disease: NHLBI/WHO Workshop. 201.
2. D'Ambrosio D, Mariani M, Panini-Bordignon P, Sinigaglia F. Chemokines and their receptors guiding T lymphocyte recruitment in lung inflammation. Am J Respir Crit Care Med 2001:164:1266-75.
3. Zhu Z, Lee CG, Zheng T, Chupp G, Wang J, Homer RJ et al. Airway inflammation and remodeling in asthma. Am J Respir Crit Care Med 2001;164:567-70.
4. Kawakami M, Paul JK, Thurlbeck WM. The effect of age on lung structure in male BLALB:cNNia inbred mice. Am J Anat 1984;170:1-21.
5. Wright JL, Churg A. Cigarette smoke causes physiologic and morphologic changes of emphysema in the guinea pig. Am Rev Respir Dis 1990;142:1422-8.
6. Morris DG, Huang X, Kaminski N, Wang Y, Shapiro SD, Dolganov G et al Loss of integrin αvβ6-mediated TGF-β activation causes Mmp12-dependent emphysema. Nature 2003;422:169-73.
7. Lundblad LKA, Irvin CG, Adler A, Bates JHT. A reevaluation of the validity of unrestrained plethysmography in mice. J Appl Physiol 2002;93:1198-207.
8. Thurlbeck WM, Wright JL. Thurlbeck's chronic airflow Obstruction. Hamilton: B.C. Decker; 1999.
9. Medical Research Council. Definition and classification of chronic bronchitis for clinical and epidemiological purposes. Lancet 1965;1:775-9.
10. American Thoracic Society. Chronic bronchitis, asthma and pulmonary emphysema. A statement by the Committee on Diagnostic Standards for Nontuberculosis Respiratory Disease. Am Rev Respir Dis 1962;85:762-8.
11. Snider GL, Kleinerman J, Thurlbeck WM, Bengali ZH. The definition of emphysema: Report of a National Heart, Lung, and Blood Institute. Division of lung diseases workshop, Am Rev Respir Dis 1985;132:182-5.
12. March TH, Barr EB, Finch GL, Hahn FF, Hobbs CH, Méache MG et al. Cigarette smoke exposure produces more evidence of emphysema in BGC3FI mice than in F344 rats. Toxicol Sci 1999;51:289-99.
13. Heckman CA, Dalbey WE. Pathogenesis of lesions induced in rat lung by chronic tobacco smoke inhalation. Natl Cancer Inst 1982;69:117-29.
14. Huber GL, Davies P, Zwilling GR, Pochay VE, Hinds WC, Nicholas HA et al. A morphologic and physiologic bioassay for quantifying alterations in the lung following experimental chronic inhalation of tobacco smoke. Clin Resp Physiol 1981;17:269-327.
15. Escolar JD, Martinez MN, Rodriquez FJ, Gonzalo C, Escolar MA, Roche PA. Emphysema as a result of involuntary exposure to tobacco smoke: morphometrical study of the rat. Exp Lung Res 1995;21:255-73.
16. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD. Macrophage elastese is required for cigarette smoke-induced emphysema in mice. Science 1997;277:2002-4.
17. Selman M, Montano M, Ramos B, Vanda C, Beccerril C, Delgado J et al. Tobacco smoke-induced lung emphysema in guinea pigs is associated with increased interstitial collagenase. Am J Physiol 1996;271:L734-L43.
18. Ayre D, Keast DJ, Papadimitriou JM. A survey of pathological changes associated with long-term high tar tobacco smoke exposure in a murine model. J Pathol 1981;135:249-57.
19. Selman M, Cisneros-Lira J, Gaxiola M, Ramirez R, Kudlacz EM, Mitchell PG et al. Matrix metalloproteinases inhibition attenuates tobacco smoke-induced emphysema in guinea pigs. Chest 2003;123:1633-41.
20. Hoidal JR, Niewoehner DE. Cigarette smoke inhalation potentiates elastase-induced emphysema in hamsters. Am Rev Respir Dis 1983;127:478-81.
21. Diamond L, Kimmel EC, Lai Y-L, Winsett DW. Augmentation of elastase-induced emphysema by cigarette smoke. Am Rev Respir Dis 1988;138:1201-6.
22. Hernandez JA, Anderson AE, Holmes WL, Foraker AG. Pulmonary parenchymal defects in dogs following prolonged cigarette smoke exposure. Am Rev Respir Dis 1966;93:78-83.
23. Cavarra E, Bartalesi B, Lucattelli M, Fineschi S, Lunghi B, Gambelli F et al. Effects of cigarettes smoke in mice with different levels of α1-proteinase inhibitor and sensitivity to oxidants. Am J Respir Crit Care Med 2001;164:886-90.
24. Meshi B, Vitalis TZ, Ionescu D, Elliott WM, Liu C, Wang Z-D et al. Emphysematous lung destruction by cigarette smoke. Am J Respir Cell Mol Biol 2002;26:52-7.
25. Frasca JM, Auerbach O, Carter HW, Parks VR. Morphologic alterations induced by short-term cigarette smoking. Am J Pathol 1983;111:11-27.
26. Wright JL. The importance of ultramicroscopic emphysema in cigarette smoke induced lung disease. Lung 2001;179:71-81.
27. Belton JC, Crise N, McLaughlin RF, Tueller EE. Ultrastructural alterations in collagen associated with microscopic foci of human emphysema. Hum Pathol 1977;8:66-77.
28. Cardoso W, Sekhon H, Hyde DM, Thurlbeck WM. Collagen and elastin in human pulmonary emphysema. Am Rev Respir Dis 1993;147:975-81.
29. Lang MR, Fiaux GW, Gillooly M, Stewart JA, Hulmes DJS, Lamb D. Collagen content of alveolar wall tissue in emphysematous and non-emphysematous lungs. Thorax 1994;49:319-26.
30. Lang MR, Fiaux GW, Hulmes DJS, Lamb D, Miller A. Quantitative studies of human lung airspace wall in relation to collagen and elastin content. Matrix 1993;13:471-80.
31. Akers S, Kucich U, Swartz M, Rosen G, Glass M, Rosenbloom J et al. Specificity and sensitivity of the assay for elastin-derived peptides in chronic obstructive pulmonary disease. Am Rev Respir Dis 1992;145:1077-81.
32. Schriver EE, Davidson JM, Sutcliffe MC, Swindell BB, Bernard GR. Comparison of elastin peptide concentrations in body fluids from healthy volunteers, smokers, and patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1992;145:762-6.
33. Betsuyaku T, Nishimura M, Yoshioka A, Takeyabu K, Miyamoto K, Kawakami Y. Elastin-derived peptides and neutrophil elastase in bronchoalveolar lavage fluid. Am J Respir Crit Care Med 1996;154:720-4.
34. Fukuda Y, Masuda Y, Ishizaki M, Masugi Y, Ferrans VJ. Morphogenesis of abnormal elastic fibers in lungs of patients with panacinar and centriacina emphysema. Hum Pathol 1989;20:652-9.
35. Dalbey WE, Nettesheim P, Griesemer R, Caton JE, Guerin MR. Chronic inhalation of cigarette smoke by F344 rats. J Natl Cancer Inst 1980;64:383-90.
36. Zwicker GM, Filipy RE, Park JF, Loscutoff SM, Ragan HA, Stevens DL. Clinical and pathological effects of cigarette smoke exposure in beagle dogs. Arch Pathol Lab Med 1978;102:623-8.
37. Haag HB, Larson PS, Weatherby JH. The effect on rats chronic exposure to cigarette smoke. Ann N Y Acad Sci 1960;60:227-38.
38. Wright JL, Churg A. Smoke-induced emphysema in the guinea pig is associated with morphometric evidence of collagen breakdown and repair. Am J Physiol 1995;268:L17-L20.
39. Keil M, Lungarella G, Cavarra E, vanEven P, Martorana PA. A scanning electron microscopic investigation of genetic emphysema in tight-skin, pallid, and beige mice, three different C57 BL/6J mutants. Lab Invest 1996;74:353-62.
40. Tuder RM, McGrath S, Neptune E. The pathobiologial mechanism of emphysema models: what do they have in common? Pulm Pharmacol Ther 2003;16:68-78.
41. Ray P, Tang W, Wang P, Homer R, Kuhn C, Flavell RA et al. Regulated overexpression of interleukin 11 in the lung. J Clin Invest 1997;100:2501-11.
42. Kuhn C, Homer RJ, Zhu Z, Ward N, Flavell RA, Geba GP et al. Airway hyperresponsiveness and airway obstruction in transgenic mice: morphologic correlates in mice overexpressing interleukin (IL)-11 and IL-6 in the lung. Am J Respir Cell Mol Biol 2000;22:289-95.
43. Zheng T, Zhu Z, Wang Z, Homer RJ, Ma B, Riese RJ et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J Clin Invest 2000;106:1081-93.
44. Lanone S, Zheng T, Zhy Z, Liu W, Lee CG, Ma B et al. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling J Clin Invest 2002;110:63-74.
45. Wang Z, Zheng T, Zhu Z, Homer RJ, Riese RJ, Chapman HA et al. Interferon y induction of pulmonary emphysema in the adult murine lung. J Exp Med 2000;192:1587-99.
46. Lucey EC, Keane J, Kuang P-P, Snider GL, Goldstein RH. Severity of elastase-induced emphysema is decreased in tumor necrosis factor-α and interleykin-1β receptor-deficient mice. Lab Invest 2000;82:79-85.
47. Gross P, Pfitzer EA, Tolker E, Babyak MA, Kaschak M. Experimental emphysema: its production in normal and silicotic rats. Arch Environ Health 1965;11:50-80
48. Janoff A. Elastases and emphysema. Am Rev Respir Dis 1985;132:417-33.
49. Churg A, Zay K, Shay S, Zie C, Shapiro SD, Hendricks R et al. Acute cigarette smoke induced connective tissue breakdown requires both neutrophils and macrophage metalloelastase in mice. Am J Respir Cell Mol Biol 2002;27:368-74.
50. Takubo Y, Guerassimov A, Ghezzo H, Triantafillopoulos A, Bates JHT, Hoidal JR et al. α-antitrypsin determines the pattern of emphysema and function in tobacco smoke-exposed mice. Parallels with human disease. Am J Respir Crit Care Med 2002;166:1596-603.
51. Churg A, Dai J, Zay K, Karsan A, Hendricks R, Yee C el al. Alpha-1-antitrypsin and a broad spectrum metal-loprotease inhibitor, RS113456, have similar acute anti-inflammatory effects. Lab Invest 2001;81:119-31.
52. Churg A, Wang RD, Xie C, Wright JL. Alpha-l-antitrypsin ameliorates cigarette smoke-induced emphysema in the mouse. Am J Respir Crit Care Med 2003;168:199-207.
53. Churg A, Dai J, Tai H, Xie V, Wright JL. Tumor necrosis factor-α is central to acute cigarette smoke induced inflammation and connective tissue breakdown. Am J Respir Crit Care Med 2002;166:849-54.
54. Wright JL, Farmer SG, Churg A. Synthetic serine elastase inhibitor reduces cigarette smoke induced emphysema in guinea pigs. Am J Respir Crit Care Med 2002;166:954-60.
55. Kuraki T, Ishibashi M, Takayama M, Shiraishi M, Yoshida M. A novel oral neutrophil elastase inhibitor (ONO-6818) inhibits human neutrophil elastase-induced emphysema in rats. Am J Respir Crit Care Med 2002;166:496-500.
56. Shapiro SD. Evolving concepts in the pathogenesis of chronic obstructive pulmonary disease. Clin Chest Med 2000;21:621-32.
57. Churg A, Wang RD, Tai H, Wang X, Xie C, Dai J et al. Macrophage metalloelastase mediates acute cigarette smoke-induced inflammation via tumor necrosis factor-α release. Am J Respir Cell Mol Biol 2003;167:1083-9.
58. D'Armiento J, Dalal SS, Okada Y, Berg RA, Chada K. Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell 1992;71:955-61.
59. Foronjy RF, Okada Y, Cole R, D'Armiento J. Progressive adult-onset emphysema in transgenic mice expressing human MMP-1 in the lung. J Appl Physiol 2003;284: L727-J37.
60. Leco KJ, Waterhouse P, Sanchez OH, Gowing KL, Poole AR, Wakeham A et al. Spontaneous ari space elargement in the lungs of mice lacking tissue inhibitor of metalloproteinases-3 (TIMP-3). J Clin Invest 2001;108:817-29.
61. Fujita M, Shannon JM, Irvin CG, Fagan KA, Coll C, Augustin A et al. Overexpression of tumor necrosis factor-α produces an increase in lung volumes and pulmonary hypertension. Am J Physiol 2002;280:L39-L49.
62. Feinberg MW, Jain MK, Werner F, Sibinga NE, Wiesel P, Wang H et al. Trasforming growth factor-beta 1 inhibits cytokine-mediated induction of human metalloestase in macrophages. J Biol Chem 2000;18:25766-73.
63. Yosida M, Korfhagen TR, Whitsett JA. Surfactant protein D regulates NF-kappa B and matrix metalloproteinase production in alveolar macrophages via oxidant-sensitive pathways. J Immunol 2001;166:7514-9.
64. Macklin CC. Alveolar pores and their significance in the human lung. Arch Pathol Lab Med 1936;21-203-16.
65. Liebow AA. Pulmonary emphysema with special reference to vascular changes. Am Rev Respir Dis 1959;80:67-91.
66. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK et al. Inhibitors of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 2000;106:1311-9.
67. Tuder RM, Zhen L, Cho CY, Taraseviciene-Stewart L, Kasahara Y, Salvemini D et al. Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. Am J Respir Crit Care Med 2003;29:88-97.
68. Aoshiba K, Yokohori N, Nagai A. Alveolar wall apoptosis causes lung destruction and emphysematous changes. Am J Respir Cell Mol Biol 2003;28:555-62.
69. Kasahara Y, Tuder RM, Cool CD, Lynch DA, Flores SC, Voelkel NF. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. Am J Respir Crit Care Med 2001;163:737-44.
70. Majo F, Ghezzo H, Cosio MG. Lymphocyte population and apoptosis in the lungs of smokers and their relation to emphysema. Eur Respir J 2001;17:946-53.
71. Reid LM. Measurement of the bronchial mucous gland layer: a diagnostic yardstick in chronic bronchitis. Thorax 1960;15:132-41.
72. Thurlbeck WM. Bronchial mucous gland size. Review. Unpublished 1997.
73. Bedrossian CWM, Anderson AE, Foraker AG. Comparison of methods for quantitating bronchial morphology. Thorax 1971;26:406-42.
74. Wright JL, Lawson LM, Kennedy S, Wiggs B, Hogg JC. The detection of small airways disease. Am Rev Respir Dis 1984;129:989-94.
75. Muller JBM, Wright JL, Wiggs BR, Pare PD, Hogg JC. Structure of central airways in current smokers and ex-smokers with and without mucus hypersecretion: relationship to lung function. Thorax 1987;42:843-8.
76. Jones R, Bolduc P, Reid LM. Goblet cell glycoprotein and tracheal gland hypertrophy in rat airways: the effect to tobacco smoke with and without the antiinflammatory agent phenylmethyloxadiozole. Br J Exp Pathol 1973;54:229-39.
77. Hayashi M, Sornberger GC, Huder GL. Morphometric analysis of tracheal gland secretion and hypertrophy in male and female rats after exprimental exposure to tobacco smoke. Am Rev Respir Dis 1979;119:67-73.
78. Walker D, Wilton LV, Binnis R. Inhalation toxicity studies on cigarette smoke (VII) 6-week comparative experiment using modified flue-cured cigarettes: Histopathology of the coducting airways. Toxiol 1978;10:241-59.
79. Park SS, Kikkawa Y, Goldring IP, Daly MM, Zelefsky M, Shim C et al. An animal model of cigarette smoking in beagle dogs. Am Rev Respir Dis 1977;115:971-9.
80. Lamb D, Reid L. Goblet cell increase in rat bronchial epithelium after exposure to cigarette and cigar tobacco smoke, Br Med J 2001;1:33-5.
81. Rogers DF, Jeffery PK, Inhibition by oral N-acetylcysteine of cigarette smoke-induced "bronchitis" in the rat. Exp Lung Res 1986;10:267-83.
82. Rogers DF, Godfrey RW, Majumdar S, Jeffery PK. Oral N-acetylcysteine speeds reversal of cigarette smoke-induced mucous cell hyperplasia in the rat. Exp Lung Res 1988;14:19-35.
83. Jones R, Dolduc P, Reid K, Protection of rat bronchial epithelium against tobacco smoke. Br Med J 1972;2:142-4.
84. Hayashi M, Sornberger GC, Huber GL. Differential response in the male and female tracheal epithelium following chronic tobacco smoke inhalation. Chest 1978;4:515-8.
85. Bernfeld P, Homburger F, Soto E, Pai KJ. Cigarette smoke inhalation studies in inbred Syrian Golden hamsters. J Natl Cancer Inst 1979;63:675-89.
86. Wright JL, Ngai T, Churg A. Effect of long-term exposure to cigarette smoke on the small airways of the guinea pig. Exp Lung Res 1992;18:105-14.
87. Wright JL, Churg A. Smoking cessation decreases the number of metaplastic secretory cells in the small airways of the guinea pig. Inhal Toxicol 2002;14:101-7.
88. Leikauf GD, Borchers MT, Prows DR, Simpson LG. Mucin apoprotein expression in COPD. Chest 2002;121:166S-82S.
89. Voynow JA, Youn LR, Want Y, Horger T, Rose MC, Fischer BM. Neutrophil elastase increases. MUC5AC mRNA and protein expression in respiratory epithelial cells. Am J Physiol 1999;276:L835-L43.
90. Takeyama K, Jung B, Shim JJ, Burget P-R, Dao-Pick T, Ueki IF et al. Activation of epidermal growth factor receptors is responsible for mucin synthesis induced by cigarette smoke. Am J Physiol 2002;280:L165-L72.
91. Richter A, O'Donnell RA, Powel RM, Sanders MW, Holgate ST, Djukanovic R et al. Autocrine ligands for the epidermal growth factor receptor mediate interleukin-8 release from bronchial epithelial cells in response to cigarette smoke. Am J Respir Cell Mol Biol 2002;27:85-90.
92. Takeyama K, Agusti C, Ueki I, Lausier JA, Cardel LO, Nadel JA. Neutrophil-dependent globet cell degranulation: role of membrane-bound elastase and adhesion molecules. Am J Physiol 1998;275:L294-L302.
93. 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;24:176-9.
94. Carlile A, Edwards C. Structural variation in the named bronchi of the left lung: a morphometric study. Br J Dis Chest 1983;77:344-8.
95. Ngai A, West WW, Paul JL, Thurtbeck WM. The national institutes of health intermittent positive-pressure breathing trial: pathology studies. 1. Interrelationship between morphologic lesions. Am Rev Respir Dis 1985;132:937-45.
96. Hossain S, Heard BE. Hyperplasia of bronchial muscle in chronic bronchitis. J Pathol 1970;101:171-84.
97. Rubio ML, Sanchez-Cifuentes MV, Ortega M, Peces-Barbe G, Escolar JD, Verbanck S et al. N-acetylcysteine prevents cigarette smoke induced small airways alteration in rats Eur Respir J 2000;15:505-11.
98. Wright JL, Sun J-P. Dissociation of chronic vascular cell proliferation and vascular contractility after chronic cigarette smoke exposure. Eur Respir J 1999;14:832-8.
99. Sekhon HS, Wright JL, Churg A. Cigarette smoke causes rapid cell proliferation in small airways and associated pulmonary arteries. Am J Physiol 1994;267:L557-L63
100. Dadmanesh F, Wright JL. Endothelin-A receptor antagonist BQ-610 blocks cigarette smoke-induced mitogenesis in rat airways and vessels. Am J Physiol 1997;272:L614-L8.
101. Wright JL, Sun J-P, Churg A. Glutathione levels play a role in cigarette smoke induced cell proliferation in the rat lung. Inhal Toxicol 1998;10:969-94.
102. Saetta M, Di Stefano A, Maestrelli P, Ferraresso A, Drigo R, Potena A et al. Activated T-lymphocytes and macrophages in bronchial mucosa of subjects with chronic bronchitis. Am Rev Respir Dis 1993;147:301-6.
103. O'Shaughnessy TC, Ansari TW, Barnes NC, Jeffery P. Inflammation in bronchial biopsies of subjects with chronic bronchitis: inverse relationship of CD8+ T lymphocytes with FEVI. Am J Respir Crit Care Med 1997;155:852-7.
104. Di Stefano A, Turato G, Maestrelli P, Mapp CE, Ruggieri MP, Roggeri A et al. Airflow limitation in chronic bronchitis in associated with T-lymphocyte and macrophage infiltration of the bronchial mucosa. Am J Respir Crit Care Med 1996;153:629-32.
105. Mueller R, Chanez P, Champbell AM, Bousquet J, Heusser C, Bullock GR. Different cytokine patterns in bronchial biopsies in asthma and chronic bronchitis. Resp Med 1996;90:79-85.
106. Lams BEA, Sousa AR, Rees PJ, Lee TH. Subepithelial immunopathology of the large airways in smokers with and without chronic obstructive pulmonary disease. Eur Respir J 2000;15:512-6.
107. Saetta M, Turato G, Facchini FM, Corbino L, Lucchini RE, Casoni G et al. Inflammatory cells in the bronchial glands of smokers with chronic bronchitis. Am J Respir Crit Care Med 1997;156:1633-9.
108. Bosken CH, Hards J, Gatter K, Hogg JC. Characterization of the inflammatory reaction in the peripheral airways of cigarette smokers using immunocytochemistry. Am Rev Respir Dis 1992;145:911-7.
109. Saetta M, Di Stefano A, Turato G, Facchini FM, Corbino L, Mappa CE et al. CD8+ T-lymphocytes in peripheral airways of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998;157:822-6.
110. Lams BEA, Sousa AR, Rees PJ, Lee TH. Immunopathology of the small-airway submucosa in smokers with ant without chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999;158:1518-23.
111. Niewoehner DE, Kleinerman J, Rice DB. Pathologic changes in the peripheral airways of young cigarette smokers. N Engl J Med 1974;291:755-8.
112. Mosmann TR, Coffman RL. Heterogeneity of cytokine secretion patterns and functions of helper T cells. Adv Immunol 1989;46:111-47.
113. Del Prete G, Maggi E, Romagnani S. Human Th1 and Th2 cells: function properties, mechanisms of regulation, and role in disease. Lab Invest 1994;70:299-306.
114. Tollerud DJ, Weiss ST, Leung DY. Elevated soluble interleukin-2 receptors in young healthy cigarette smokers: lack of association with atopy or airways hyperresponsiveness. Int Arch Allergy Immunol 1992;97:25-30.
115. Turato G, Di Stefano A, Maestrelli P, Mapp CE, Ruggieri MP, Roggeri A et al. Effect of smoking cessation on airways inflammation in chronic bronchitis. Am J Respir Crit Care Med 1995;152:1262-7.
116. Sun G, Stacey MA, Vittori E, Marini M, Bellini A, Kleimberg J et al. Cellular and molecular characteristics of inflammation in chronic bronchitis. Eur J Clin Invest 1998;28:364-72.
117. Vitalis TZ, Kern I, Croome A, Behzad H, Hayashi S, Hogg JC. The effect of latent adenovirus 5 infection on cigarette smoke-induced lung inflammation. Eur Respir J 1998;11:664-9.
118. Matsumoto K, Aizawa H, Inoue H, Koto H, Takata S, Shigyo M et al. Eosinophilic airway inflammation induced by repeated exposure to cigarette smoke. Eur Respir J 1998;12:387-94.
119. Nishikawa M, Kakemizu N, Ito T, Kudo M, Kaneko T, Suzuki M el al. Superoxide mediates cigarette smoke-induced infiltration of neutrophils into the airways through nuclear factor-kB activation and IL-8 mRNA expression in guinea pig in vivo. Am J Respir Cell Mol Biol 1999;20:189-98.
120. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J el al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 1999;103;779-88.
121. Lee CG, Homer RJ, Zhu Z, Lanone S, Wang X, Koteliansky V et al. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor β1. J Exp Med 2001;194:809-21.
122. Lee CG, Homer RJ, Cohn L, Link H, Jung S, Craft JE et al. Transgenic overexpression of interleukin (IL)-10 in the lung causes mucus metaplasia, tissue inflammation, and airway remodeling via IL-13-dependent and-independent pathways. J Biol Chem 2002;277:35466-74.
123. Kessler R, Faller M, Weitzenblum E, Chaquat A, Aykut A, Ducolone A et al. "Natural history" of pulmonary hypertension in a series of 131 patients with chronic obstructive lung disease. Am J Respir Crit Care Med 2001;164:219-24.
124. Hale KA, Niewoehner DE, Cosio MG. Morphologic changes in the muscular pulmonary arteries: relationship to cigarette smoking, airway disease, and emphysema. Am Rev Respir Dis 1980;122:273-8.
125. Hale KA, Ewing SL, Gosnell BA, Niewoehner DE. Lung disease in long-term cigarette smokers with and without chronic air-flow obstruction. Am Rev Respir Dis 1984;130:716-21.
126. Santos S, Peinado VI, Ramirez J, Morales-Blanhir J, Bastos R, Roca J et al. Enhanced expression of vascular endothelial growth factor in pulmonary arteries of smokers and patients with moderate chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003;167:1250-6.
127. Wright JL, Churg A. Effect of long-term cigarette smoke exposure on pulmonary vascular structure and function in the guinea pig. Exp Lung Res 1991;17:997-1009.
128. Wright JL. The relationship of increased pulmonary artery pressure and airflow obstruction to emphysema. J Appl Physiol 1993;74:1320-4.
129. Wright JL, Sun J-P. The effect of smoking cessation on pulmonary and cardiovascular function and structure. J Appl Physiol 1994;76:2163-8.
130. Yamato H, Sun J-P, Churg A, Wright JL. Cigarette smoke-induced emphysema in guinea pigs is associated with diffusely decreased capillary density and capillary narrowing. Lab Invest 1996;75:211-9.
131. Yamato H, Sun J-P, Churg A, Wright JL. Guinea pig pulmonary hypertension caused by cigarette smoke cannot be explained by capillary bed destruction. J Appl Physiol 1997;82:1644-53.
132. Wright JL, Tai H, Dai J, Churg A. Cigarette smoke induces rapid changes in gene expression in pulmonary arteries. Lab Invest 2002;82:1391-8.
133. Voelkel NF, Cool C, Taraceviene-Stewart L, Geraci MW, Yeager M, Bull T et al. Janus face of vascular endothelial growth factor: the obligatory survival factor for lung vascular endothelium controls precapillary artery remodeling in severe pulmonary hypertension. Crit Care Med 20200;30:S251-S6.
134. Wilson Do, Rogers RM, Hoffman RM. Nutrition and chronic lung disease. Am Rev Respir Dis 1985;132:1347-65.
135. Wilson DO, Rogers RM, Wright EC, Anthonisen NR. Body weight in chronic obstructive pulmonary disease. Am Rev Respir Dis 1989;139:1435-8.
136. Gray-Donald K, Gibbson L, Shapiro SH, Macklem PT, Martin JG. Nutritional status and mortality in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996;153:961-6.
137. Sahebjami H, Wirman JA. Emphysema-like changes in the lungs of starved rats. Am Rev Respir Dis 1981;124:619-24.
138. Sahebjami H. Effects of postnatal starvation and refeeding on rat lungs during adulthood. Am Rev Respir Dis 1986;133:769-72.
139. Massarella GR, Radaeva S, Clerch LB, Massaro D. Lung alveoli: endogenous programmed destruction and regeneration. Am J Physiol 2003;283:L305-L9.